Reproductive Biology: The Natural History of the Crustacea, Volume 6 0190688556, 9780190688554

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Reproductive Biology

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The Natural History of the Crustacea Series SERIES EDITOR Martin Thiel EDITORIAL ADVISORY BOARD Geoff Boxshall, Natural History Museum, London, UK Emmett Duffy, Virginia Institute of Marine Sciences, Gloucester, USA Darryl Felder, University of Louisiana, Lafayette, USA Gary Poore, Victoria Museum, Melbourne, Australia Bernard Sainte-​Marie, Fisheries and Oceans Canada, Mont-​Joli, Canada Gerhard Scholtz, Humboldt University Berlin, Berlin, Germany Fred Schram, Friday Harbor Marine Laboratory, Seattle, USA Les Watling, University of Hawaii, Hawaii, USA Functional Morphology and Diversity (Volume 1) Edited by Les Watling and Martin Thiel Lifestyles and Feeding Biology (Volume 2) Edited by Martin Thiel and Les Watling Nervous Systems and Control of Behavior (Volume 3) Edited by Charles Derby and Martin Thiel Physiology (Volume 4) Edited by Ernest S. Chang and Martin Thiel Life Histories (Volume 5) Edited by Gary Wellborn and Martin Thiel Reproductive Biology (Volume 6) Edited by Rickey D. Cothran and Martin Thiel

Reproductive Biology The Natural History of The Crustacea Volume 6

EDITED BY RICKEY D. COTHRAN AND MARTIN THIEL

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1 Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide. Oxford is a registered trade mark of Oxford University Press in the UK and certain other countries. Published in the United States of America by Oxford University Press 198 Madison Avenue, New York, NY 10016, United States of America. © Oxford University Press 2020 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, by license, or under terms agreed with the appropriate reproduction rights organization. Inquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above. You must not circulate this work in any other form and you must impose this same condition on any acquirer. CIP data is on file at the Library of Congress ISBN 978–​0–​19–​068855–​4 9 8 7 6 5 4 3 2 1 Printed by Integrated Books International, United States of America

PREFACE

This is the sixth volume of a 10-​volume series on The Natural History of the Crustacea. Our volume examines Reproductive Biology, and it follows Volume 1:  Functional Morphology and Diversity, Volume 2: Life Styles and Feeding Biology, Volume 3: Nervous Systems and Control of Behavior, Volume 4:  Physiology, and Volume 5:  Life Histories. The remaining four volumes will explore additional aspects of crustacean natural history, including developmental biology and larval ecology, evolution and biogeography, fisheries and aquaculture, and ecology and conservation biology. Chapters in this volume synthesize our current understanding of diverse topics in crustacean reproductive biology. The first five chapters of the volume address allocation strategies to reproduction, gamete production, brooding behavior, and other components of parental care in crustaceans. Jared Goos and Punidan Jeyasingh lead off the volume with an exploration of the diverse reproductive strategies observed in crustaceans, highlighting the critical role this group has played in understanding life history evolution and the promise of crustaceans as model systems for exploring how life will respond to rapid environmental change in the Anthropocene. The next two chapters focus on gamete production taking a comparative approach to surveying gametogenesis. Mariusz Jaglarz and Szczepan Bilinkski provide a detailed overview of ultrastructural aspects and patterns of oogenesis in various crustaceans. This chapter is followed by a chapter by Mika Tan and colleagues exploring similar ultrastructural aspects of spermatogenesis and patterns of sperm allocation in crustaceans. The volume then moves to the post-​fertilization challenges of brooding offspring and parental care. Miriam Fernández and colleagues provide patterns of brooding behavior in decapods, where there is a clear association between extended brooding behavior and terrestial life styles and a paucity of studies addressing the cost of brooding along relevant environmental gradients. The first section of the volume is bookended by a chapter on parental care in crustaceans by Alexandre Palaoro and Martin Thiel. The authors highlight the fact that among invertebrates, crustaceans are some of the most caring animals, tending to juveniles more often than many other groups, making them a great model system for exploring the evolutionary ecology of parental care. The second part of the volume centers on sexual systems in crustaceans. Günter Vogt opens the section with an overview of sexual systems in crustaceans, discussing the multiple independent origins of hermaphroditism and parthenogenesis from ancient gonochoristic ancestors. Kota Sawada and Sachi Yamaguchi follow the overview chapter with a review of empirical and theoretical work on sex allocation and sex determination, highlighting the need to integrate theoretical frameworks and provide a phylogenetic context to the diverse patterns observed in crustaceans. Chiara Benvenuto and Stephen Weeks explore patterns of the evolution of hermaphroditism in

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vi Preface crustaceans by comparing this sexual system to gonochorism within an ecological context. They discuss patterns of when such “unusual” sexual systems are found in nature and champion crustaceans as a model group for exploring the ecological constraints and implications of evolving a hermaphroditic sexual system. David Innes and France Dufresne complete the section on sexual systems with an exploration of patterns of parthenogenesis in crustaceans. They highlight that parthenogens tend to have wider distributions and are more common in marginal habitats at higher latitudes and longitudes. The diversity of asexual species and a wealth of information about their ecology and growing understanding of their genomes place crustaceans at the forefront of understanding evolutionary transitions between sexual and asexual lineages. The third section of the volume covers crustacean mating systems and sexual selection. Alexandre Palaoro and Jan Beermann lead off the section, highlighting the diversity of mating systems found in crustaceans—​probably owing to the tremendous variation in body plans, habitats, and lifestyles observed in the group. These features make crustaceans an attractive group for studying the evolution of reproductive strategies and social behavior. Rickey Cothran follows with a chapter that discusses how sexual selection and sexual conflict interact to shape the evolution of crustacean weapons and ornaments. Carola Becker and Raymond Bauer provide a chapter on multiple mating and sperm competition, covering factors that affect the intensity of sperm competition, and how this affects the evolution of male and female traits; they note the need for a more integrative and comprehensive set of studies to ascertain the full power of this evolutionary force in crustaceans. Along the same lines, Colin McLay and Stefan Dennenmoser explore the evidence for cryptic female choice in crustaceans and find that much of the supposed evidence for this evolutionary mechanism is equivocal; the authors provide a framework to guide future research in this area. Alison Dunn and colleagues provide a review of how environment, parasitism, and pollution shape crustacean sex determination and sex ratios and the consequences of these effects for crustacean reproduction. Shawn Garner and Bryan Neff review the tremendous diversity of alternative mating tactics observed in crustaceans, along with the morphological and behavioral adaptations that accompany these different mating strategies. In the final chapter of the section, Matthias Galipaud and colleagues take on the potential role that sexual selection has played as an engine of cryptic species diversification in crustaceans. The volume ends with three chapters covering diverse topics including reproductive rhythms, crustacean personality research, and record-​breaking crustaceans with respect to reproductive characters. Stefan Dennenmoser and colleagues review the causes and consequences of reproductive rhythms in crustaceans, providing insights into environmental cues that trigger such rhythms, external and internal processes that control rhythms, and sources of selection that maintain rhythms in crustacean populations. Mark Briffa then introduces readers to research on crustacean personalities, focusing on work done on the European hermit crab, Pagurus bernhardus. He concludes that while many of the key signatures of animal personality have been uncovered, there is a need for more work on how personality variation contributes to outcomes of mating interactions, as well as work focusing on female behaviors. Günter Vogt and colleagues finish the volume with a fun chapter on record breakers in the Crustacea when it comes to reproductive biology. Collectively, these 19 chapters provide an integrative and comprehensive treatment of crustacean reproductive biology from gamete formation to mating and reproductive strategies and their evolutionary and ecological consequences. We expect this volume will be valuable to scholars and students who are interested in a wide range of topics in reproductive biology. We hope that the synthesis and future research directions in the volume provided by expert biologists thrust forward research on reproductive biology and highlight the important role these amazing animals have played in our understanding of the most critical component of evolutionary fitness.

ACKNOWLEDGMENTS

We thank our contributors for graciously sharing their time, energy, knowledge, and insights to make this volume possible—​it has been both a pleasure and honor to work with each of them. Our editorial assistants, Annie Mejaes, Mika Tan, Tim Kiessling, Miles Abadilla and Miguel Angel Penna-​Díaz, were impeccably skilled and organized, and always kept us moving forward. We thank our external reviewers for their valuable and generous feedback. Finally, we express our appreciation to our publisher, Oxford University Press, for their commitment to this project. Editing of this book was generously supported by Universidad Católica del Norte, Chile.

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CONTRIBUTORS

EDITORS Rickey D. Cothran Department of Biological Sciences Southwestern Oklahoma State University 100 Campus Drive Weatherford, OK 73096, USA

Jan Beermann Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research Department of Functional Ecology Am Handelshafen 12, 27570 Bremerhaven, Germany

Martin Thiel Facultad de Ciencias del Mar Universidad Católica del Norte Larrondo 1281 1781421, Coquimbo, Chile

Chiara Benvenuto University of Salford Peel Building Room 317 The Crescent, Salford M5 4WT, Manchester, UK

AUTHORS Simone Baldanzi Facultad de Ciencia del Mar y Recursos Naturales, Universidad de Valparaiso, Av. Borgoño 16344, Viña del Mar, Chile

Szczepan M. Bilinski Department of Developmental Biology and Invertebrate Morphology Institute of Zoology and Biomedical Research, Faculty of Biology Jagiellonian University Gronostajowa 9 30-​387 Krakow, Poland

Raymond T. Bauer Department of Biology University of Louisiana, Lafayette 300 E. St. Mary Blvd. Lafayette, Louisiana, 70504-​3602, USA Carola Becker Queen’s University Marine Laboratory 12-​13 The Strand Portaferry, Co. Down BT22 1PF, Australia

Loïc Bollache Chrono-​environnement, UMR 6249 CNRS Université Bourgogne Franche-​Comté 16 Route de Gray, 25000 Besançon, France Antonio Brante Universidad Católica de la Santísima Concepción Facultad de Ciencias, Campus San Andrés Alonso de Ribera 2850, Concepción, Chile

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x Contributors Mark Briffa School of Biological and Marine Sciences Plymouth University Plymouth PL4 8AA, UK John H. Christy Smithsonian Tropical Research Institute Luis Clement Avenue, Bldg. 401 Tupper Balboa Ancon Panama, Republic of Panama

Matthias Galipaud Department of Evolutionary Biology and Environmental Studies University of Zürich Winterthurerstrasse 190, 8057 Zürich, Switzerland Department of Evolutionary Biology Bielefeld University Konsequenz 45 33615 Bielefeld, Germany

Rickey D. Cothran Department of Biological Sciences Southwestern Oklahoma State University 100 Campus Drive Weatherford OK 73096, USA

Shawn Garner Department of Biology Western University 1151 Richmond Street London, Ontario, N6A 5B7, Canada

Stefan Dennenmoser Carl von Ossietzky University Oldenburg Institute for Biology and Environmental Sciences Carl von Ossietzky Str. 9-​11 26111 Oldenburg, Germany

Jared M. Goos Department of Integrative Biology Oklahoma State University Stillwater, OK 74078, USA

France Dufresne Département de Biologie, Chimie et Géographie Université du Québec à Rimouski Campus de Rimouski 300, allée des Ursulines, C.P. 3300, succ. A Rimouski, Québec G5L 3A1, Canada Alison M. Dunn School of Biology Faculty of Biological Sciences University of Leeds LS2 9JT, UK Miriam Fernández Pontificia Universidad Católica de Chile Estación Costera de Investigaciones Marinas Departamento de Ecología, Facultad de Ciencias Biológicas Av. Libertador Bernardo OHiggins 340 Santiago, Chile Alex T. Ford University of Portsmouth Institute of Marine Sciences School of Biological Sciences Ferry Road Portsmouth PO4 9LY

David J. Innes Department of Biology Memorial University St. John’s, NL, A1B 3X9, Canada Mariusz K. Jaglarz Department of Developmental Biology and Invertebrate Morphology Institute of Zoology and Biomedical Research, Faculty of Biology Jagiellonian University Gronostajowa 9 30-​387 Krakow, Poland Punidan D. Jeyasingh Departament of Integrative Biology Oklahoma State University Stillwater, OK 74078, USA Clément Lagrue Department of Zoology University of Otago 340 Great King Street PO Box 56 Dunedin 9054, New Zealand Department of Biological Sciences University of Alberta Edmonton, Alberta, T6G 2E9, Canada

Contributors Colin L. McLay Biological Sciences Canterbury University Christchurch 4800 New Zealand Bryan Neff Department of Biology Western University 1151 Richmond Street London, Ontario, N6A 5B7, Canada

Mika M. J. Tan ASEAN Centre for Biodiversity Domingo M. Lantican Avenue University of the Philippines Los Baños College Laguna Philippines 4031, Philippines Martin Thiel Facultad de Ciencias del Mar Universidad Católica del Norte Larrondo 1281 1781421, Coquimbo, Chile

Alexandre V. Palaoro LUTA do Departamento de Ecologia e Biologia Evolutiva Universidade Federal de São Paulo Rua Artur Riedel, 275, Eldorado, 09972-270, Diadema, Brazil

Christopher Tudge Deparment of Biology American University 4400 Massachusetts Avenue, NW Washington, DC 20016, USA

Miguel A. Penna-​Díaz Facultad de Ciencias del Mar Universidad Católica del Norte Larrondo 1281 1781421, Coquimbo, Chile

Günter Vogt Faculty of Biosciences University of Heidelberg Im Neuenheimer Feld 234 69120 Heidelberg, Germany

Thierry Rigaud UMR CNRS 6282 Biogéosciences Equipe Ecologie Evolutive Université Bourgogne Franche-​Comté 6 boulevard Gabriel 21000 Dijon, France

Stephen C. Weeks Department of Biology The University of Akron Akron, OH 44325-​3908, USA

Kota Sawada Oceanic Ecosystem Group National Research Institute of Far Seas Fisheries Fisheries Research and Education Agency 2-​12-​4 Fukuura, Kanazawa, Yokohama 236-​8648, Japan

Sachi Yamaguchi KYOUSEI Science Center for Life and Nature Nara Women’s University Kitauoyahigashi-machi, Nara 630-8506, Japan

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CONTENTS

Preface • v Acknowledgments • vii Contributors • ix

1. Allocation of Reproductive Efforts  •  1 Jared M. Goos and Punidan D. Jeyasingh



2. Oogenesis in Crustaceans: Ultrastructural Aspects and Selected Regulating Factors • 29 Mariusz K. Jaglarz and Szczepan M. Bilinski



3. Fertilization Success in Crustaceans from the Male Perspective: Sperm Ultrastructure and Sperm Economy  •  60 Mika M. J. Tan, Christopher Tudge, Miguel A. Penna-​Díaz, and Martin Thiel



4. Costs and Benefits of Brooding among Decapod Crustaceans: The Challenges of Incubating in Aquatic Systems  •  86 Miriam Fernández, Antonio Brante, and Simone Baldanzi



5. “The Caring Crustacean”: An Overview of Crustacean Parental Care  •  115 Alexandre V. Palaoro and Martin Thiel



6. An Overview of Sexual Systems  •  145 Günter Vogt



7. An Evolutionary Ecological Approach to Sex Allocation and Sex Determination in Crustaceans • 177 Kota Sawada and Sachi Yamaguchi



8. Hermaphroditism and Gonochorism  •  197 Chiara Benvenuto and Stephen C. Weeks

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9. Parthenogenesis • 242 David J. Innes and France Dufresne



10. Overview of the Mating Systems of Crustacea  •  275 Alexandre V. Palaoro and Jan Beermann



11. Sexual Selection and Sexual Conflict in Crustaceans  •  305 Rickey D. Cothran



12. Multiple Matings and Sperm Competition  •  332 Carola Becker and Raymond T. Bauer



13. Detecting Cryptic Female Choice in Decapod Crustaceans  •  364 Colin L. McLay and Stefan Dennenmoser



14. Environmental Influences on Crustacean Sex Determination and Reproduction: Environmental Sex Determination, Parasitism, and Pollution  •  394 Alison M. Dunn, Thierry Rigaud, and Alex T. Ford



15. Alternative Reproductive Tactics  •  429 Shawn Garner and Bryan Neff



16. Cryptic Diversity and Sexual Selection  •  447 Matthias Galipaud, Loïc Bollache, and Clément Lagrue



17. Rhythms and Reproduction  •  472 Stefan Dennenmoser, John H. Christy, and Martin Thiel



18. Animal Personality and Investment in Reproduction: Hermit Crabs and Other Crustaceans as Model Organisms  •  503 Mark Briffa



19. Crustacean Reproductive Records  •  526 Günter Vogt, Rickey D. Cothran, Mika M. J. Tan, and Martin Thiel Index • 555

1 ALLOCATION OF REPRODUCTIVE EFFORTS

Jared M. Goos and Punidan D. Jeyasingh

Abstract The allocation of resources is a fundamental component of all life history models. Inherent in these models is the concept of allocation trade-​offs, where finite resources must be allocated to certain life history traits at the expense of others. Reproduction is thought to be a costly trait in most organisms, and thus allocation to reproduction could drive the evolution of other life history traits. Much research has examined patterns of resource allocation to reproduction and the resulting trade-​offs with other life history traits, both within and among taxa. In many respects, empirical work on crustaceans has pioneered our understanding of life history evolution. In this chapter, we examine the great diversity in allocation of resources to reproduction among crustaceans. For many years, crustaceans have served as important models in understanding the importance of a variety of resources (e.g., energy, inorganic nutrients, organic nutrients) to reproduction. Diversity in allocation to reproduction is evident regardless of the resource under investigation. Because of the interconnectedness among such resource parameters, and the rapid change in the availability of such resources in the Anthropocene, frameworks integrating variation in multiple resource axes have much promise in discovering general rules underlying reproductive allocation in natural populations. Given the diverse allocation strategies employed, and the rich history of studies exami­ ning reproductive allocation, crustaceans will continue to be an important taxon for such work.

INTRODUCTION Life is predicated on an organism’s ability to survive, grow, and reproduce. Organismal life history—​ that is, growth, development, and reproduction—​is extremely variable, both among and within species. Selection favors strategies that maximize the chance of specific genotypes contributing to the next generation (Fisher 1930). While the most extreme strategy to maximize fitness would be Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology to allocate all resources to reproduction, such a strategy is not possible and is constrained by the central life history theory concept of trade-​offs between traits (Stearns 1989). With trait trade-​offs, organisms must allocate their finite resources to reproduction, often at the expense of other traits. As such, the allocation of resources to reproduction is determined both by genetically determined mechanisms underlying life history strategies and environmental factors such as the availability of resources. Much research has sought to elucidate the broad patterns of variation in the allocation of resources to reproduction, as well as the mechanisms of such allocation. Additionally, theoretical models of life history have hypothesized generalizable mechanisms for the evolution of reproductive allocation patterns, and the genetic and environmental influences on reproduction-​driven life history trade-​offs. A tight link between Crustacea and life history theory is evident in the literature, as research utilizing crustacean models has spurred the development of many important theoretical models, which have in turn been empirically tested using such models. In this chapter, we highlight the various ways in which resource allocation to reproduction has been studied in a more resource-​explicit manner. First, we outline the key theoretical models used to explain patterns of reproductive allocation, and the mechanisms underlying trade-​offs driven by these allocation patterns. Next, we address the fundamental question: “What is a resource?” While researchers have highlighted many potential resources that may be allocated to reproduction in various species, here we focus on the allocation of various nutritional resources that are known to play important roles in the reproductive effort among crustacean taxa. We address the role of nutrition on reproduction by examining the effects of both food quantity and quality on reproductive allocation. Finally, we examine how resource-​explicit studies of reproductive allocation can illuminate our understanding of the mechanisms of allocation, the trade-​ offs inherent in this allocation, and the links between allocation and processes at the community and ecosystem level. We highlight some new avenues of such resource-​explicit research that will provide a mechanistic understanding of resource allocation to reproduction in an era of global change.

THEORETICAL BACKGROUND OF RESOURCE ALLOCATION TO REPRODUCTION Inherent in the idea of trade-​offs, and thus life history, is that resources must be allocated to various traits to maximize an organism’s fitness. Because reproductive effort is assumed to be costly, trade-​ offs between reproduction and other life history traits, such as survival, are thought to be strong (Cody 1966, Reznick 1985). As such, acquired resources must be allocated to various life history traits at the expense of others, a concept suggested by Levins (1968) and later Sibly and Calow (1986) as the Principle of Allocation. This idea, that resource allocation to life history traits is a zero-​sum process, suggests that when resources are in limited supply, trade-​offs are more likely to be stronger between resource-​intensive traits. Variation exists among individuals in the amount of resources available to allocate toward traits at both the inter-​and intra-​population level, contributing to variation among members of the same species in reproductive allocation. As such, the resources available to allocate toward reproduction are a function of both the environmental conditions in which an organism lives and genetically determined mechanisms that allow organisms to exploit finite resources in their environment. While there are many theoretical models attempting to explain general patterns of resource allocation and life history trade-​offs, we will focus on, arguably, the two more influential general theoretical frameworks: the r/​K selection theory and the acquisition-​ allocation model, or Y-​model.



Allocation of Reproductive Efforts

The r/​K Selection Theory The “zero-​sum” view of resource allocation to reproduction has been well studied, particularly with respect to trade-​offs between reproductive output and survival between taxa or populations. Perhaps the most well-​known framework of these broad patterns in resource allocation to reproduction is MacArthur and Wilson’s r/K -​selection theory (1967). Briefly, this theory describes two kinds of selection acting on populations driven by the stability of their habitats, and thus, resource availability. Populations in unstable habitats rarely achieve densities in which competition for resources is a factor, and thus are selected for greater allocation to reproduction (high r). In contrast, stable environments often harbor populations with densities close to carrying capacity (K), and thus such populations encounter density-​dependent selection where decisions on allocating resources toward non-​reproductive traits or reallocating resources from reproductive tissues may be common and prioritized. Consequently, density-​dependent effects are the main selective forces determining where a species falls on the r/​K continuum. Generally, it has been suggested that there is a trade-​off between r-​ and K-​selection (Gadgil and Bossert 1970), although this hypothesis has been supported in some systems (e.g., Mueller et al. 1991), but not in others (Kerfoot 1977). Pianka (1970) further developed r/​K selection theory to include predictions of specific life history traits expected in stable or unstable environments. In this interpretation, r-​selected organisms are selected for fast growth rates, early reproduction, smaller body size, and greater fecundity, while K-​selection should favor the opposite characteristics, with lower allocation to reproduction in favor of competitive ability and survival. Within crustaceans, there seems to be some evidence for predicted K-​strategy traits in relatively stable environments such as the poles (Clarke 1979) and the deep sea (Eckelbarger and Watling 1995). Additionally, patterns of trait variation roughly following predicted r/​K strategies have been observed across crustacean populations (Sainte-​Marie 1991, Quadros et  al. 2009), although these patterns have proven difficult to definitively attribute to r-​ and K-​selection, as the roles of density-​ dependent competition and population demography have not been rigorously studied. The r/​ K selection theory has been historically used as a framework to view broad patterns of life history trade-​offs. However, a lack of clear associations between life history traits and r-​ and K-​selection has led to suggestions that it cannot explain the majority of variation within populations in life history trade-​offs that occur in natural systems due to environmental fluctuations (Stearns 1992, Giangrande et al. 1994, Roff 2002). Specifically, while r/​K selection theory attempts to provide an explanation for the variation in body size and life history across species and populations, empirical studies have shown that body size itself may be a strong determinant of variation in life history (Stearns 1983, Peters 1986). As such, observed body-​size independent life history trait associations have led to the concept of a “slow-​fast continuum” of life history (Stearns 1983, Read and Harvey 1989, Promislow and Harvey 1990). This concept is very similar to the r/​K selection theory concept, except variation in life histories is not density dependent but is instead determined by differences in mortality and lifespan. Organisms can exhibit life histories anywhere along the continuum from the fast end, in which individuals breed earlier and reproduce more frequently, to the slow end, where individuals mature later and reproduce less frequently. Selection favors fast life history strategies when the mortality rate in adulthood outweighs that in juvenility, necessitating accelerated reproduction to ensure that the chance to contribute to the next generation is not forfeited. Conversely, slow strategies are favored when juvenile mortality is greater than adult mortality, necessitating greater investment in each juvenile, to ensure survival to adulthood. This reimagining of r/​K selection to account for some of the realities of selective forces at play in natural populations has contributed substantially to our understanding of variation in life history, and the “slow-​fast continuum” is often the basis for comparative analyses of life history variation in many taxa (Bielby et al. 2007).

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Reproductive Biology Resource allocation to life history traits and the trade-​off relationships between those traits are largely a function of the timing of resource investments. In r/​K selection theory and slow-​fast continuum theory, different selective environments shape the timing of reproductive investment, such that populations either invest in reproduction early at the cost of longevity or invest in longevity at the cost of lower reproductive output over a longer period. Similarly, organismal growth characteristics shape allocation patterns, particularly as individuals age. Animals can either be determinate or indeterminate growers, and Crustacea includes both groups (Maszczyk and Brzeziński, 2018). Many crustaceans exhibit indeterminate growth and continually molt throughout their lives. As such, growth in these species continues even after maturity, placing a constraint on reproduction as allocation of resources must be divided between both life history traits (Heino and Kaitala 1999). In contrast, determinate growers cease molting and growth after a certain size is attained. Allocation to reproduction is thus concentrated after determinate growers reach maturity. In general, models have suggested that determinate growth should be the optimal strategy, as determinate growers do not have to divide their resources between growth and reproduction, therefore diverting more resources toward reproduction. Despite this prediction, the occurrence of indeterminate growth strategies is widespread (Kozlowski 1992, Perrin and Sibly 1993). Much like the selective forces driving r/​K strategies, indeterminate growth is thought to be favored when organisms live in unpredictable environments, where organisms hedge their bets, sacrificing current reproductive effort to increase survival probability or future reproductive output. Acquisition-​Allocation Model (the Y-​model) Much of the research on life history and resource allocation to traits concerns the evolution of specific traits and the trade-​offs that constrain them. A thorough knowledge of resource allocation, therefore, must consider the underlying genetic architecture of life history traits. If trade-​offs between reproduction and other life history traits occur, negative correlations between these traits are predicted. As we highlighted earlier, these predicted negative correlations are often observed across taxa or populations within a species. Positive correlations, however, are often found within populations, rather than the expected negative correlations that indicate trade-​offs between life history traits (e.g., van Dijk 1979, Allan 1984, reviewed in Roff 2000). Motivated by this observation, van Noordwijk and de Jong (1986) developed the acquisition-​allocation model (or Y-​model) to help explain why positive correlations between traits are observed when negative correlations are expected. A key assumption when considering life history trade-​offs is that the pool of resources available to traits is limited such that allocation to one trait results in fewer resources that are allocable to other traits. As the pool of resources available to traits is a function of the organism’s ability to acquire resources, it follows that resource allocation to reproduction is not independent from resource acquisition. Van Noordwijk and de Jong (1986) suggested that, while trade-​offs are expected to occur when individuals within a population are all similarly constrained by resource availability, in reality, individuals vary in their abilities to acquire the resources needed for the expression of traits. Briefly, their model advances the idea that an understanding of the degree of variation in acquisition of resources relative to that of allocation allows for clear predictions on the directionality of the relationship between traits. Specifically, if variation in acquisition is greater than the variation in allocation, one should expect positive correlations to occur (graph a in Fig. 1.1), because individuals that acquire more resources will have a larger pool of resources to allocate to all traits, while resource-​poor individuals will have fewer resources available for traits. When there is less variation in acquisition than allocation, that is, when all individuals in a population have similar resources available to them, trade-​offs and negative correlations between traits should arise (graph b in Fig. 1.1). Importantly, this model only applies to observed trade-​offs on the population level, and



Allocation of Reproductive Efforts (B)

Allocation to Traits Pool of Resources

Trait 2

(A)

Trait 1

Trait 1

Fig. 1.1. The van Noordwijk and de Jong (1985) model. Solid lines radiating from the origin correspond to the relationship of allocation to Trait 2 vs. Trait 1, while the dotted lines located at distances from the origin correspond to different levels of resource acquisition. In the first scenario (a), variation in acquisition is greater than variation in allocation, and a positive correlation between Traits 1 and 2 is predicted. Conversely, when variation in allocation is greater than acquisition (b), a trade-​off between Traits 1 and 2 is expected to occur.   

within-​individual trade-​offs are expected to always occur, regardless of the relationship between acquisition and allocation. While the initial Y-​model only applied to phenotypic correlations, later efforts expanded the model to include explicit predictions on the role of genetic covariances in trade-​offs (Houle 1991, de Jong and van Noordwijk 1992). This model, however, only allows for comparisons between two traits, and more complex models have been developed that consider resource allocation to multiple traits in a hierarchical manner (de Laguerie et al. 1991, de Jong 1993, Worley et al. 2003). For example, organisms may allocate resources to growth or reproduction, at which point subdivisions of allocation will be made within reproduction between traits such as gamete number and gamete size. This allocation hierarchy has been hypothesized to be a principal factor, masking trade-​offs, as high variation in early levels of the hierarchy influence later levels of allocation (de Laguerie et al. 1991, de Jong 1993). Together, these models suggest that resource allocation to life history traits is a product of both environmental supply of resources and genetically determined differences in the ability to acquire and allocate resources to traits, and the interaction between these two sources of variation. Despite its influence, rigorous empirical tests of the Y-​model are surprisingly scarce. Chief among the reasons for this lack of empirical testing over the past 30 years is the fact that an operational definition of “acquisition” or “allocation” does not exist, and simply measuring these two processes has proven difficult (Roff and Fairbairn 2007, King et al. 2011a). Resource acquisition, for example, has been measured in a number of ways such as body size (Festa-​Bianchet et al. 1998, Glazier 1999, Bashir-​Tanoli and Tinsley 2014), the storage of important macromolecules like lipids (Chippindale et al. 1996, Bashir-​Tanoli and Tinsley 2014), and the rate of foraging (Schütz et al. 2002, Boggs and Freeman 2005). While these various methods for estimating acquisition have produced high-​quality empirical data, often these measures are not resource-​explicit, making it difficult to assess the contribution of resource environments to life history trade-​offs. For example, body size is a complex trait that is shaped by many factors, such as resource availability and genetically determined physiological factors such as assimilation efficiency. Additionally, foraging rate is

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Reproductive Biology similarly coarse, as foods vary in their compositions, and organisms vary in their abilities to assimilate different food components. Thus, this approach hinders our ability to determine the resources that may limit organismal traits (Raubenheimer et al. 2009). Allocation is similarly difficult to estimate in a way that is resource explicit. As a result, allocation to traits is often estimated by simply measuring the trait value, with resource allocation assumed to be tightly correlated with trait value. Patterns of resource allocation, however, are complex and encompass many processes that may not be reflected by simply measuring a single trait. Importance of Studying Sex-​Specific Resource Allocation to Reproduction When examining resource allocation to reproduction and the trade-​offs that result from this allocation, the previously described models are overwhelmingly used to understand reproduction in females. Arguably, the greatest driver of this study bias is due to the extreme costs of egg production. While the costs of primary reproductive traits are not as great in males as in females, males often still likely incur large costs of reproduction in the form of secondary sexual traits such as weapons and ornaments (Zahavi 1975, Andersson 1994, Cotton et al. 2004, discussed in depth in Chapter 11 of this volume). A key principle in sexual selection research is the idea that these traits serve as some honest signal of male quality and, thus, the development of these traits is highly dependent on the quality or condition of the individual male (i.e., heightened condition dependence; Cotton et al. 2004). As in general life history theory, resource acquisition and allocation are central to theories on the evolution of condition-​dependent traits. Specifically, in most models and studies of condition dependence, “condition” and “quality” are often synonymous with the acquisition of resources (Rowe and Houle 1996, Hunt et al. 2004). Because all organisms must allocate resources to reproduction, and the sexes often have different and sometimes conflicting selection pressures that drive sex-​specific evolution, more attention must be paid to sex-​specific patterns of allocation to reproduction (Chapman et al. 2003, Maklakov et al. 2008, Cornwallis and Uller 2010).

WHAT RESOURCES ARE ALLOCATED TO REPRODUCTION? Broadly applicable empirical studies examining the mechanisms of resource allocation are often hindered by the fact that there are no widely accepted methods for estimating “acquisition” or “allocation.” Precisely what constitutes a “resource” to be acquired and allocated to reproduction is often an open-​ended question with many answers. In the context of resource allocation to reproduction, if studies on acquisition and allocation of resources are not resource-​explicit, it is nearly impossible to determine under what conditions organisms are resource-​limited, making extrapolations to wild populations difficult. To be sure, reproduction requires the allocation of many resources at any given time, and organisms are limited by multiple resources in nature. Regardless, examining resource allocation in a resource-​explicit manner allows for a greater understanding of the roles of genetic and environmental sources of variation in resource allocation within populations, and the mechanisms underlying allocation patterns and trade-​offs. Additionally, resource-​explicit studies have the potential for facilitating the scaling implications of allocation to reproduction on the individual level up to higher orders of biological organization (e.g., community and ecosystem level). Throughout the years, ecologists have studied the allocation of numerous resources to reproductive efforts. The models described above are most closely associated with nutritional resources derived from food. While some resources such as time, space, and the availability of mates have been noted as essential resources organisms may allocate to reproduction, such resources are often tightly linked to one another and many other resources such as nutrients.



Allocation of Reproductive Efforts

Additionally, the theoretical models described in the preceding have generally not formally integrated these resources. Such integration is beyond the scope of this chapter. Within this volume (and see Krebs and Davies 1997 for a more thorough overview), however, the allocation of time, space, and mate availability is discussed in more depth in the context of parental care (see Chapter 5 in this volume), density-​dependent mating strategies (see Chapters 10 and 15 in this volume), mate selection (see Chapters 11–​13 and 18 in this volume), and reproductive rhythms (see Chapter 17 in this volume). As such, in this section, we specifically focus on highlighting nutritional resources commonly studied in an explicit manner in crustaceans, and some empirical frameworks that researchers are utilizing to build mechanistic predictions for resource allocation to reproduction in both males and females. Food Quantity and the Allocation of Energy By far, the resource most often associated with allocation to reproduction is food quantity, and thus energy. Energy is a common currency for all taxa that is controlled by the laws of thermodynamics, thus allowing studies on energetic allocation to apply across multiple levels of biological organization (Nisbet et al. 2000). Nearly all models of life history and, by extension, of resource allocation either explicitly or implicitly treat “resources” as synonymous with energy. In these models, energy is the single currency from which life history, from acquisition to allocation, is charted. Because growth is limited by metabolism, energy is often thought to be the limited resource that must be allocated to various traits. Such energy limitation may be environmentally driven, as food resources may be in limited supply or competition for resources is particularly high. Additionally, reproductive energy limitation may be driven by shifts in behavior, particularly when behaviors such as parental care (e.g., Thiel 1999, 2001, Baeza and Fernández 2002) and mate pairing ( Jormalainen 1998, Jormalainen et al. 2001) come at a cost of acquiring resources (i.e., foraging). In recent years, efforts have been made to assess organismal energy budgets and the effects of food quantity on reproduction and patterns of life history trade-​offs. Recently, King et al. (2011a, 2011b) empirically tested the Y-​model, explicitly using energy as a resource, in the cricket Gryllus firmus. In their studies, King and colleagues manipulated the energy available to crickets (by altering food quantity) and estimated energy acquisition and allocation to both flight and reproduction. Their findings suggested strong support for the Y-​model when using energy as the currency. They also found evidence suggesting that acquisition and allocation of resources are not independent from one another, as the Y-​model assumes, suggesting that allocation to reproduction is a function of the acquisition of resources (King et al. 2011a, 2011b, Robinson and Beckerman 2013). Olijnyk and Nelson (2013) further tested the Y-​model in Daphnia pulicaria, and found that, contrary to the predictions of the Y-​model, positive correlations between life history traits, such as growth and reproduction, remained even when genetic variation and variation in resource acquisition is absent. These results suggest that an intermediate step between resource acquisition and allocation, the assimilation of resources, should also drive relationships between life history traits. Specifically, just as genetic variation may exist in the acquisition and allocation of food resources, genetic variation in the efficiency with which acquired resources are digested and incorporated into organismal tissue potentially represents a third source of variation in life history traits. While the Y-​model is implicitly about energy allocation to various pools, it does not account for the complexities of energetics in most systems. Any energetics framework employs the concept of organismal energy budgets, in which organisms have set energetic demands for growth, maintenance, and reproduction (Karasov and Martinez del Rio 2007). Due to differences in organismal size between species and energy availability in different environments, however, generalizable energetics models of allocation are often difficult to attain. The recently developed dynamic energy

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Fig. 1.2. Diagram of basic dynamic energy budget (DEB) model of allocation, highlighting the κ-​rule of allocation. The total pool of organismal resource reserves are first allocated to the combination of somatic maintenance and growth in a fixed proportion κ. The remainder of the total budget, 1–​κ, is allocated to the maturation of reproductive tissues and reproductive effort. The proportion of energy allocated to reproduction is then allocated to various reproductive traits such as gamete quality and number. Solid gray arrows indicate allocation nodes in which direct competition for resources is occurring, whereas the dashed gray arrow indicates an example of indirect resource competition.   

budget (DEB) model has provided a framework from which general patterns of energy allocation to reproduction can be elucidated (Kooijman 2000). Simply put, this model relates patterns of growth, reproduction, and survival to feeding and maintenance requirements of organisms. Within this model, energy budgets are state-​dependent, accounting for body scaling when determining energy allocation to various pools (Kooijman 2000, Kooijman and Lika 2014). Figure 1.2 shows the basic energy fluxes within the DEB model. A central aspect of DEB is the concept of the so called κ-​rule, which states that a fixed proportion κ of energy acquired is first allocated to growth and maintenance, while the remaining 1–​κ is allocated to maturity development and reproduction (Kooijman 2000). Central to this rule is the idea that allocation to maintenance and growth directly compete, where growth slows or ceases at larger body sizes because somatic maintenance is assumed to be proportional to body volume and energy is being directly diverted from growth to maintenance (Lika and Kooijman 2003). Similarly, allocation to reproduction and maturity development directly compete for resources, and reproduction ceases when the entire fraction of energy 1–​κ is needed to meet maturity maintenance requirements. In energy-​limited environments, allocation to maintenance and growth is always prioritized, but individuals may change the proportion κ of energy allocated such that allocation to reproduction may cease (Kooijman 2000, Lika and Kooijman 2003). Because of the κ-​rule, maintenance and growth do not directly compete with either reproduction or maturity development. Instead these pools indirectly compete on a higher level of hierarchical allocation, a concept similar to the hierarchical allocation models described earlier in this chapter (de Laguerie et al. 1991, de Jong 1993). Empirical Examples of Energy Allocation in Crustacea Invertebrates, and particularly crustaceans, were among the first organisms in which energetic models of allocation were studied. Many of the energetics studies have used Daphnia as a model



Allocation of Reproductive Efforts

organism. Indeed, Daphnia energy budgets have been extensively studied, making it a model organism for the development of the DEB models (Gurney et al. 1990, McCauley et al. 1990, Kooijman 2000, Nisbet et al. 2004, 2010). Some of the earliest examples of energetic studies in Daphnia are those that examined carbon budgets as a proxy for energy (Lampert 1977a, 1977b, Lynch et  al. 1986, Lynch 1989). These studies explored the various environmental conditions that shape carbon budgets and the allocation of energy to growth, maintenance, and reproduction. A key finding in these studies, as it pertains to reproduction, was the realization that energy allocation is a function of organismal size (Lampert 1977a, 1977b), and the proportion of energy allocated to reproduction increases in a hyperbolic fashion as a function of body size (Lynch et al. 1986, Lynch 1989). Additionally, energy allocation to reproduction, as a proportion of the total energy budget, was shown to be independent of the food quantity. Allocation of net assimilated energy (i.e., the energy not allocated to maintenance and respiration) to reproduction in Daphnia increased with Daphnia body size toward an asymptote of ~89%, a pattern that has been shown to be largely conserved across daphniid species (Fig. 1.3; Dudycha and Lynch 2005). Together, these results suggest that, after energy is allocated to maintenance, adult Daphnia are allocating nearly all of their available energy toward reproduction. In another study, He and Wang (2006) utilized 14C radiotracers to estimate the allocation of assimilated energy to various pools under different food quantities. Their results indicated that Daphnia mothers transfer a significant portion of assimilated carbon to egg production, comparable to the carbon losses due to dissolved organic carbon excretion. As in the previous studies, this allocation to reproduction was not influenced by food quantity. While on an individual level food quantity does not seem to affect the proportion of assimilated energy allocated to reproduction in Daphnia, energy limitation may still carry life history consequences. In fact, studies have shown that Daphnia fed low food quantities will reduce or cease allocation to reproduction entirely in favor of growth and maintenance (McCauley et al. 1990, Bradley et al. 1991, Glazier and Calow 1992). Life history traits such as age at maturity, size at maturity, fecundity, and egg size are often influenced by energy limitation (Lynch 1989, McCauley et al. 1990, Tessier and Consolatti 1991, Taylor and Gabriel 1992, Ebert 1994), although it has been suggested that many of these traits are more influenced by the reduction in growth due to energy limitation than a direct allocation penalty toward reproduction (Lynch 1989, Dudycha and Lynch 2005). While Daphnia have been an important model organism for many energetic studies, examples of energy allocation to reproduction in other crustaceans also exist. For example, in a study examining whether energy reserves in the form of fat deposits influenced the fecundity of females in multiple populations of the amphipod species Gammarus minus, Glazier (2000) found evidence that fatter females have higher fitness than their thinner counterparts. Specifically, somatic investment, in terms of body size and fat content, was positively correlated with reproductive investment, likely due to variation among individuals in the acquisition of energetic resources (Glazier 2000), a key prediction of the van Noordwijk and de Jong model (1986). Gorokhova and Hansson (2000) examined energy content of gravid females in the mysid Mysis mixta and estimated energetic costs of egg production ranged between 8% and 17% of the total energy budget of adult females. Additionally, their results indicated low energy contents in post-​copulatory males relative to precopulatory males and gravid females, suggesting that male energetic allocation to either spermatogenesis or copulation is likely energetically costly as well. Similarly, in the prawn Palaemon adspersus non-​ reproductive females possessed higher growth rates than reproductive females, allowing them to escape fish predation (Berglund and Rosenqvist 1986). This suggests that egg production often is twofold, manifesting in both somatic growth and survival. Male reproductive allocation of energy has been studied in a few crustacean species, although it has generally received less attention compared to the larger energetic costs of egg production in females. Often, male reproductive success is limited by access to mates. In all organisms, there is a trade-​off between current and future reproduction, and this trade-​off is often influenced by

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Fig. 1.3. The phylogenetically conserved relationship between proportional allocation of energy to reproduction and body size across multiple daphniid species. To the left are the linearized phylogenetic relationships between daphniid species, based on 12S ribosomal DNA. On the right are approximated fit lines for the amount of energy allocated to reproduction as a function of body size. Adapted from Dudycha and Lynch 2005, with permission from John Wiley and Sons ©.   



Allocation of Reproductive Efforts

mate competition (Stearns 1992, Reznick et al. 2000, Scharf et al. 2013). This trade-​off may manifest in allocation to ejaculate quantity and quality, as males may invest more energetic resources to first copulation at the expense of future copulations (Wedell et al. 2002, Kelly and Jennions 2011). Nevertheless, this trade-​off has been most extensively studied in insect species, with little evidence in crustaceans (see examples in Scharf et al. 2013). Although evidence for such trade-​offs between ejaculate quantity and quality are lacking, it is possible that selection for these traits is relatively weak in crustaceans, as many species of crustaceans fertilize externally, resulting in weak sperm competition in these species (but see Chapter 12 of this volume for further discussion). As such, exclusionary behaviors such as mate guarding are more likely to be the dominant male-​male competition strategy in many crustacean species, as monopolization of fertile eggs ensures paternity. Some evidence for such interplay between sperm competition and mate guarding exists in the rock shrimp Rynchocinetes typus, where male ontogenetic stages correspond to the economics of their allocation to sperm (Hinojosa and Thiel 2003). Specifically, small female-​like “typus” males allocate their energy resources to increased sperm quantity during the first mating opportunity due to their inability to monopolize females over a dominant male. In contrast, the dominant “robustus” males allocate their resources to sperm production more economically, spreading out allocation among multiple matings due to their ability to monopolize females and reduce the chance of sperm competition. Although mate guarding ensures monopolization of females, this strategy, particularly amplexus, can be a costly behavior for males, imposing substantial energetic costs. Such energetic costs may be due to reduction in foraging effort during amplexus, the increasing expense of carrying a female, and/​or inter-​individual conflict over the initiation of amplexus. For example, multiple studies have shown evidence for a sex-​specific energetic cost to mate guarding driven by a reduction in male foraging capability during mate guarding (Robinson and Doyle 1985, Sparkes et  al. 1996). Alternately, in a study of energetic costs of precopulatory mate guarding in Gammarus pulex, Plaistow et al. (2003) observed that energetic costs of mate guarding were strongly influenced by female size, but not duration of guarding or food availability, suggesting that the initiation of mate guarding and not amplexus itself is energetically costly. Specifically, males in that study guarding larger females exhibited a reduction in energy reserves relative to those guarding smaller females. Additionally, energetic reserves in paired males were much higher than in unpaired males, providing evidence that males with insufficient energetic reserves cannot bear the substantial energetic cost of precopulatory mate guarding. Further evidence of an energetic cost of mate guarding was observed in wild G. pulex and G. fossarum populations studied by Becker et al. (2013). In that study, male energy reserves (as triglycerides and glycogen) decreased throughout the reproductive period, and replenished in the fall and winter after cessation of mate guarding, providing further evidence that males require sufficient energy reserves to compensate for energetically costly mate guarding behavior. Further study has found that direct male-​male competition for females already in precopula is also energetically costly (Prenter et al. 2006), suggesting that the cost of initiating precopulatory mate guarding is potentially the result of both male-​female and male-​male conflict in some species. These studies show that different aspects of mate guarding behavior are energetically costly for males and could explain some of the variation in mating success among males. Energy allocation to reproduction may also manifest in males in the context of costly secondary sexual traits, such as exaggerated ornamental traits or courtship behaviors. There are numerous examples of energy allocation patterns to sexual traits, with mate calling efforts (reviewed in Kotiaho 2001) and secondary sexual trait morphology in insects (Emlen and Nijhout 2000) representing the largest portion of such studies. The cost of such exaggerated traits is a central aspect of theory on the evolution of sexual trait exaggeration (e.g., Zahavi 1975, Andersson 1994), and such costs likely manifest in the allocation of energetic resources to such traits. Recently described general mechanisms for the determination of condition and, thus, exaggeration of sexual traits have focused primarily

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Reproductive Biology on regulatory pathways related to energy metabolism. Specifically, Hill (2011, 2014) has proposed a general framework for determining condition focusing specifically on cellular respiration, where an organism’s genotype, somatic state, and epigenetics determine the efficiency of cellular respiration. In turn, sexual trait exaggeration is a function of an organism’s ability to maintain minimum cellular functionality while also possessing such costly traits. Additionally, a specific mechanism linking nutrition and male trait exaggeration, the insulin/​insulin-​like signaling pathways, has been identified in multiple insect species (Emlen et al. 2012, Warren et al. 2013). Briefly, exaggerated traits possess greater sensitivity to insulin signaling, allowing for heightened growth when nutrition is good. While the role of energy in the development of sexual traits has been examined in insects, and general mechanisms for such development have been outlined, few examples exist of studies examining such energy allocation in crustaceans. In the freshwater amphipod genus Hyalella, food quantity and quality may play a role in the allocation of resources to, and thus the condition dependence of, posterior gnathopods in males, a trait with strong sexual dimorphism being 15 times larger in males than females (Cothran and Jeyasingh 2010, Goos et al. 2016). More evidence is needed to understand whether any of these patterns of energy allocation to male sexual traits result in trade-​offs with other traits or underlie the variation in fitness among males in natural populations. Food Quality and the Allocation of Materials An energetics view of resource allocation has certainly contributed much to our understanding of trade-​offs related to allocation to reproduction in crustaceans. While these research endeavors have been illuminating, this single currency approach fails to consider that organisms are often limited by nutrients in their food more so than the quantity of food (i.e., energy; Sterner and Hessen 1994). In many organisms, in fact, it is thought that material costs may be more important for the development of certain reproductive traits than simply energetic costs (Morehouse et al. 2010). Variation in food quality can represent many things, from coarse differences in the types of food available to, more explicitly, variation in the biochemical composition of foods. Current literature on the nutritional ecology of reproductive allocation often utilizes two frameworks from which acquisition and allocation to traits may be examined: the Geometric Framework (GF) and Ecological Stoichiometry (ES). Both of these frameworks have been useful in research that looks toward a more nutritionally explicit view of allocation and the fitness consequences of these allocation patterns. Introduced by Raubenheimer and Simpson (Raubenheimer and Simpson 1993, Simpson and Raubenheimer 1993, 1995), GF is a framework that seeks to understand interactions between organisms and their environments through the lens of nutrient intake in a three-​dimensional nutrient space. Central to this framework is the idea that organisms have an intake target in nutritional space that maximizes their overall fitness. When two or more nutrients are plotted on different axes, this intake target represents a single point in nutritional space. Foods of differing nutritional quality are then illustrated as “nutritional rails,” representing the ratio of resource A to resource B (and so on). Presented with foods that are imbalanced relative to the organismal intake target, organisms must either (a) regulate the amount of certain food eaten, or (b) choose among multiple foods to reach their target. Intake decisions made by the organisms when fed different foods are then related to allocation to various fitness-​conferring traits to understand the role of nutrition in influencing organismal fitness. While this framework can be used to understand any number of nutrients within foods, often complex biomolecules such as lipids, proteins, and carbohydrates are used as the nutrients under examination. Recently, some researchers have applied the statistical approaches of GF to other nutrients, such as the macroelements phosphorus (P) and nitrogen (N), although these efforts represent a small fraction of work using the GF (Harrison et al. 2014, Cease et al. 2016).



Allocation of Reproductive Efforts

The supply of nutrient elements (e.g., C, N, P) have been carefully quantified at various spatial scales ranging from microhabitats to continents, and temporal scales ranging from days to millennia (e.g., Schlesinger 1997). As such, an elemental perspective may improve our ability to predict responses of life history evolution across a large spatiotemporal scale. This approach is perhaps best achieved within the framework of Ecological Stoichiometry (ES; Sterner and Elser 2002). Research in ES is based on the following axioms: (i) elements are the fundamental building blocks of the living cell and are involved in every organismal process; (ii) organisms must take up all elements from the environment; (iii) despite vast differences in environmental supply, species maintain their elemental composition to some degree; (iv) individuals acquire and assimilate elements from the local environment, allocate them to develop and maintain fitness-​enhancing traits, and this is orchestrated by the genome; and, (v) because of vast trait diversity there is inter-​and intra-​specific variation in elemental composition and thus elemental demand. Alfred Lotka (1925) used these axioms to argue that to understand the evolutionary play on the ecological stage, equal attention should be paid to both, because they are all made of the same materials (i.e., atoms). The supply of the ~25 elements involved in biology represents a fundamental, and quantifiable eco-​space. The elemental composition of an individual is determined by acquisition of elements, assimilation, and allocation within the individual (Fig. 1.4). The byproducts (e.g., metabolic waste) and unused materials are returned back to the environment. ES has largely been applied to understand ecosystem and community-​level processes, such as nutrient cycling (e.g., Elser and Urabe 1999) and trophic dynamics (e.g., Sterner et al. 1992, Elser et al. 2000a). Redfield (1958) most famously demonstrated the advantages of using elements to integrate processes across vast spatiotemporal scales. Briefly, he noted the remarkable tendency of oceans in disparate regions of the globe to converge on similar C:N:P stoichiometry, and ascribed it to biological processes causing such trends. Ecosystem ecologists since have used information on elemental supply and elemental content of biomass (i.e., demand) to predict fluxes of nutrients between the abiotic and biotic realms, as well as through the food web, with associated effects on key ecological parameters such as productivity (Reiners 1986, Sterner and Elser 2002). For example, Elser et al. (1988) found that primary production was limited by P when P-​rich daphniids were the predominant grazer in lakes, but shifted to N limitation when N-​rich copepods became dominant. The immutability of elements makes ES a useful, yet underutilized approach toward understanding resource allocation. Much like energetic models of allocation, the approach of ES is bound by the principles of conservation of mass and energy. All organismal traits have an elemental basis. As such, it follows that elemental variation between traits within individuals should underlie similar variation in morphology, physiology, and structure of such traits (Kay et al. 2005, Morehouse et al. 2010, Snell-​Rood et al. 2015). Because trait demand is variable within individuals, traits likely compete for elemental resources, driving trade-​offs. As such, elements in high demand within organisms are those that are likely used by many pools within the organism (e.g., tissues, metabolites, etc.). Of particular interest is the growth rate hypothesis (GRH; Elser et al. 1996, 2003), which posits that phosphorus-​intensive ribosome biogenesis is the primary mechanism by which P limits growth. Indeed, there is ample evidence, especially in crustacean taxa like Daphnia, indicating that fast-​ growing taxa contain higher amounts of P (Elser et al. 2000b, 2003, Makino et al. 2003), and also unique ribosomal DNA (rDNA) structure (Weider et  al. 2004). Such patterns enable a genes-​ to-​ecosystem understanding of growth and associated diversification in elemental content (e.g., Quigg et al. 2003, Elser and Hamilton 2007). The patterns described by the GRH—​specifically, that organisms possessing greater rates of growth should also have higher somatic P content—​are generally consistent when comparing vast differences in growth and organismal P content (Elser et al. 2003).

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Fig. 1.4. Schematic representation of the stoichiometric framework. Organisms must acquire all of their elemental resources from the supply in their environment. Based on first principles, those acquired resources must then be assimilated into the body and allocated to various processes and traits. All unused elemental resources must then be excreted in the form of waste. These organism-​level elemental processing strategies underlie all organismal traits that confer fitness. By studying the fitness consequences of these processes, we can understand biological processes on higher levels of organization that, in turn, influence the total environmental pool of elemental resources available to all organisms.   

Empirical Examples in Crustacea of the Allocation of Materials The effects of food quality on reproduction in crustaceans has been studied in a diverse array of taxa. Central to all studies assessing food quality effects on life history traits is the concept of imbalances between food composition and consumer nutritional demands. Effects of food quality on life history are often tested by comparing organismal responses to different food types (e.g., animal vs. algal) or different prey species. In one such study, Cruz-​Rivera and Hay (2000a) assessed food quality effects on fitness parameters in four species of marine amphipods: the sedentary tube-​ builders Ampithoe marcuzzii, A.  valida, and Cymadusa compta and the more motile Gammarus mucronatus. The researchers fed amphipods multiple single-​species algal foods, a single animal food (Artemia), a mixed algal diet, and a mixed algal and animal diet. This experimental design allowed the researchers to assess whether different species of marine amphipods may prefer different algal species or mixed diets in the wild. Their results indicated significant growth and reproduction differences between the single species algal foods, indicating variation in food quality between such foods. Additionally, all amphipod species exhibited increased fecundity when fed a mixed algal diet over single species foods, suggesting that such diets may represent less of a dietary imbalance. Interestingly, only one species of amphipod tested, the more motile G. mucronatus, exhibited heightened growth and reproduction when fed the assumedly high-​quality animal food,



Allocation of Reproductive Efforts

suggesting some association with activity level and optimal diets in marine amphipods. Further study has shown that such motile amphipod species may be more susceptible to variation in food quality, as sedentary species may be able to alleviate negative effects of poor food quality by compensatory feeding activity (Cruz-​Rivera and Hay 2000b). Effects of differing quality diets have also been shown to affect allocation to alternate reproductive phenotypes in males. In the marine amphipod Jassa marmorata, males exhibit minor and major morphs that reflect sneaking and fighting reproductive strategies, respectively (Clark 1997). Kurdziel and Knowles (2002) demonstrated that these two male morphs are likely nutritionally determined, as major males were essentially only present when fed a high-​quality diet consisting of a mix of algal and animal foods vs. a low-​quality diet consisting of just algal foods. Using a parent-​ offspring regression, the researchers were also able to determine that reproductive phenotype is not determined by genetic differences between males. These results largely follow theory on the heightened condition dependence of sexual traits, as it is clear that allocation to expensive reproductive traits is substantially limited by imbalances between consumers and their food. Although coarse manipulations of food quality via differing diets has provided much to our understanding of how reproductive efforts are often as much the function of food quality as quantity, such manipulations are often not explicit in assessing the effects of specific material resources on life history traits. The importance of the allocation of macromolecular resources to reproduction has been extensively studied in crustaceans. For example, multiple studies have highlighted the importance of polyunsaturated fatty acids (PUFAs), especially eicosapentaenoic acid (EPA), for reproduction in Daphnia, where higher concentrations of EPA in algal foods significantly increase egg production (Becker and Boersma 2005, Wacker and Martin-​Creuzburg 2007, Martin-​Creuzburg et al. 2009). Additionally, these studies found evidence for co-​limitation of reproduction by PUFAs and other resources like sterols and phosphorus. EPA concentrations in Daphnia eggs are 2.5 times higher than in maternal somatic tissues, suggesting substantial EPA allocation to eggs relative to other tissues (Wacker and Martin-​Creuzburg 2007). Although researchers have used crustacean model organisms to understand the effects of some macromolecular resources on reproduction, these studies have not utilized the analytical tools and inferential abilities afforded by the Geometric Framework of Nutrition (GF). Multiple GF studies have examined the effects of nutrient intake on reproductive allocation in other taxa, particularly insects. Often, such studies have explicitly examined sex-​specific nutrient regulation strategies. For example, Maklakov et  al. (2008) examined the effects of carbohydrate and protein content in food on sex-​specific patterns of reproduction and aging in the cricket species Teleogryllus commodus. Their results indicated that males and females have different dietary intake targets, where males prefer food intake that optimizes reproduction. Female reproduction and lifespan trade off under different diets, with higher protein diets conferring optimal reproduction and higher carbohydrate diets conferring longer lifespan. Males, however, optimized both lifespan and reproductive effort under high-​carbohydrate diets. Additionally, the researchers found evidence of sexual conflict in their nutritional regulation when crickets were given a choice between diets, where both sexes were unable to optimize their diets to their respective intake targets. Clearly, GF is consistent with general acquisition-​allocation models, where organismal processes are largely driven by intake of food resources. Integrating GF into the study of crustacean model species is substantially limited by the difficulty of tightly controlling food resources and measuring food intake accurately. However, development of artificial diets that are stable in aquatic environments, or the utilization of terrestrial crustacean models, can spur such integration. While GF increases our knowledge of the role of multiple nutritional components in shaping life history trade-​offs, the focus on molecular nutrients hinders the amenability of this powerful framework in generating predictions using information at larger spatiotemporal scales, as such resources do not retain their forms across trophic levels.

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Reproductive Biology Elemental resources are immutable across both taxa and levels of biological organization. As such, examining the allocation of elemental resources to reproduction using ES has the potential to bridge individual-​level effects to higher levels of organization, as well as providing general mechanisms for allocation across taxa. There is much work, particularly in plants, that indicate preferential allocation of nutrient elements to various tissue types and organ systems (e.g., Yang et al. 2014). Evidence that the GRH is relevant at the intra-​individual level, however, is still sparse. In its simplest form, fast-​growing tissues can be expected to be P-​rich, and thus more sensitive to environmental (dietary) P supply (e.g., Moen and Pastor 1998, Elser et al. 2007). The pervasive relationship between P supply, P content, and ribosome biogenesis predisposes growth to be a P-​intensive process. The relationship between reproduction and P, however, is less clear. In some crustaceans, especially females, reproduction has been previously thought to be C-​intensive, as eggs have been observed to be high in C content, likely due to their high concentration of proteins and lipids (Tessier et al. 1983, Sterner and Elser 2002). However, there is evidence that reproduction may be affected similarly to growth by dietary P supply, as egg and embryo development are also thought to be dependent on RNA for biosynthesis of proteins and other macromolecules (Markow et al. 1999, 2001, Faerovig and Hessen 2003, Visanuvimol and Bertram 2010). Reproduction affects intraspecific variation in female P content in natural populations of Daphnia, and Daphnia females may store P for use in later reproductive efforts (Ventura and Catalan 2005). Indeed, consistent with these observations, Scavia and McFarland (1982) found that the reproductive cycle of Daphnia has a major effect on P release, with individuals carrying more mature embryos excreting P at slower rates. External stresses, such as temperature, predation, and water quality, may also drive allocation of specific elemental resources to reproduction in crustaceans. In a study examining the effects of temperature and predation on somatic composition in Daphnia, Zhang et al. (2016) observed that the two stresses drove independent compositional responses. Both stresses have been previously hypothesized to drive shifts in metabolic activity, with higher temperatures and predation risk associated with an increase in metabolic rates, resulting in increased C:N ratios (Hawlena and Schmitz 2010, Schmitz 2013). Interestingly, predation and temperature drove independent changes in Daphnia C:N, with predation risk driving a decrease in C:N ratios. Zhang et al. (2016) attributed this unexpected shift to a large increase in protein allocation to egg production, suggesting that adjustments in fecundity driven by size-​selective predation pressure fundamentally alter allocation of resources in Daphnia. Such understanding of the role of elemental resources in limiting female egg production in various crustacean taxa provides valuable information toward a greater understanding of the environmental factors limiting such reproductive efforts and the potential role of rapid environmental changes in affecting fitness-​conferring traits. In addition to the effects of elemental resources on female reproductive allocation, secondary sexual traits in males should also be limited by elemental resources. Many male secondary sexual traits take the form of exaggerated morphology or costly behaviors. While few studies have used ES to examine allocation to male secondary sexual traits, there is compelling evidence in the amphipod genus Hyalella that exaggerated trait development is limited by elemental resources. As mentioned earlier, amphipods in the genus Hyalella possess exaggerated second gnathopods. Males with larger gnathopods are generally more successful at acquiring mates (Wellborn 2000, Wellborn and Bartholf 2005, Cothran et  al. 2010). When fed a P-​depleted diet, males develop smaller gnathopods, relative to their bodies, as males cannot allocate resources to both overall growth and gnathopod growth (Cothran et al. 2012, 2014). Indeed, variation in dietary P supply induces sex-​specific shifts in nutrient processing (i.e., acquisition, assimilation, allocation), with preferential allocation of elemental resources to gnathopod development (Goos et al. 2016). In addition, Hyalella species possessing faster growth and larger gnathopods also exhibit greater plasticity in P content than species with smaller gnathopods and slower growth under differing dietary P supply, a pattern that may be driven by the differences in sexual selection for overall



Allocation of Reproductive Efforts

size and gnathopod size between these species (Goos et al. 2014b). Dietary P content has also been shown to influence mating interactions and male mating success, independent of shifts in relative gnathopod size (Goos et al. 2014a). These results suggest that allocation to reproductive behaviors in crustaceans may also be driven by elemental resources, a phenomenon that has also been observed in crickets (Bertram et al. 2006). Although these studies in Hyalella amphipods highlight the importance of elemental resources in the development and maintenance of exaggerated male traits and mating behavior, this line of research is very much in its infancy. Clearly, because of the potential for secondary sexual traits to drive differences between the sexes in nutritional demands and allocation patterns, more studies must focus on the material basis of such traits to understand variation across ecological gradients.

FUTURE DIRECTIONS We end the chapter by highlighting emerging ideas in nutritional ecology that may advance our understanding of the mechanisms underlying life history trade-​offs and reproductive allocation in crustacean species. While the aforementioned studies employing ES have shown some clear patterns of elemental resource allocation, more research is still warranted that explicitly integrates acquisition and assimilation of elemental resources into examinations of allocation of such resources to reproduction. Additionally, much of the focus of ES research, when it comes to allocation to reproduction in crustaceans, has been on the allocation of just one elemental resource, P, to various life history traits. The utility of examining resource allocation in the context of elemental resources is precisely because it allows for a more complete understanding of relationship between dietary resource supply and the allocation of those resources to traits. The importance of such approaches are perhaps magnified in the Anthropocene, when the supplies of key biogenic elements have been dramatically altered with potentially distinct impacts on the evolution of life histories (Snell-​Rood et al. 2015). While the focus on the supplies of key elements (e.g., P) is necessary, understanding the subsequent impact of such altered supply on allocation decisions to reproduction based on the supply of other elements may be particularly rewarding. There are approximately 25 elemental resources with known nutritional functions in biology (Williams and Frausto da Silva 2006). It is clear that a focus on just one or a few elements can mask important interactive effects between multiple elemental resources that may drive allocation to reproductive traits. Recent advances in a rapidly growing area of research termed ionomics, largely restricted to plants (Salt et al. 2008), have made it increasingly clear that various ecological factors such as temperature, nutrient availability, and salinity have unique effects on the uptake and processing of multiple elements (Norton et al. 2009, Baxter 2010, Sánchez-​Rodríguez et al. 2010, Quadir et al. 2011, Baxter and Dilkes 2012, Wu et al. 2013). Such shifts in nutrient utilization should, in turn, affect the entire stoichiometry of an individual (i.e., the ionome). Whether (and to what extent) such shifts affect life history trade-​offs remains to be seen. Nevertheless, contrary to single-​ currency approaches (e.g., van Noordwijk and de Jong 1986, Reznick et al. 2000, Kooijman and Lika 2014), it is not hard to imagine a situation where positive correlations among life history traits are common. Specifically, the Y-​model of van Noordwijk and de Jong (1986) assumes that the energetic (not material) costs of all traits are equal, and thus allocation to one trait necessarily results in a trade-​off with another trait. One of the axioms of ecological stoichiometry is that all traits are not equal. In Chapter 2 of their treatise on ES, Sterner and Elser (2002) elaborate on the vast stoichiometric diversity among biomolecules. Although correctly considered an axiom for illuminating broader scale patterns, understanding the nature of ionomic architecture at the intraspecific level should provide important insights into the materials underlying life history trade-​offs. While ecological stoichiometry, predominantly, has focused on N:P, owing largely to their high mass-​specific

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Reproductive Biology abundance in living systems (e.g., N-​rich amino acids, P-​rich nucleic acids), molecules and tissues vary considerably in other elements as well. Within the context of sexually selected exaggerated traits, such an ionomic perspective has provided insights into the allocation of elemental materials to such traits, and the role of this allocation in shaping sexual dimorphism on the elemental level. Goos et al. (2017) examined sexual dimorphism on the elemental level in Hyalella amphipods and found significant sexual dimorphism in elemental composition beyond C, N, and P. Sexual differences within this undescribed species of amphipod were primarily driven by greater concentrations of Ca, Sr, and Li in males than females. Additionally, this study compared elemental compositions of the exaggerated male gnathopod and a similarly sized homologous trait, the fifth pereopod, to assess whether sexual traits may be greater sinks for particular elemental resources. The results of this comparison revealed substantial trait-​ specific elemental compositions, indicating that the demands for the building and maintenance of exaggerated traits are fundamentally different than those for non-​sexually selected traits. Although this study found such within-​individual variation in elemental composition, there was no evidence that the possession of exaggerated traits itself contributed to the observed differences between the sexes in overall elemental composition, as intersexual differences in elemental composition exhibited similar patterns when male gnathopods were removed. Further, there was no relationship between exaggerated trait value and trait-​specific elemental composition, suggesting that variation in trait value may not be the result of greater allocation of elemental resources, contrary to predictions suggesting that exaggerated traits represent substantial resource sinks (Andersson 1994, Kay et al. 2005, Morehouse et al. 2010). Indeed, other studies in other crustacean species have observed clear element-​trait functional value relationships, particularly in claw coloration (Katsikini 2016) or hardness (Schofield et al. 2009), but such studies have generally not examined whether such trait-​specific elemental allocation is a significant driver of overall variation in organismal nutritional demand. Together, these results highlight the value of utilizing high-​throughput multidimensional analyses such as ionomics to empirically test fundamental questions in the allocation of resources to the development and maintenance of sexually selected ornaments and weapons. Such an ionomic perspective of resource allocation can also provide insights into the role of the co-​limitation of growth and reproduction by macroelements and trace elements. Although trace metals contribute a minor percentage to individual mass, often these micronutrients are pivotal during development, ensuring proper growth of a cell or tissue because they orchestrate a variety of pathways as cofactors of metalloenzymes (McArdle and Ashworth 1999, MacDonald 2000, Alloway 2013). For example, iron-​containing proteins (e.g., transferrins) play a key role in oogenesis (Bottke 1982, Kurama et al. 1995, Dunkov et al. 2002, Georgieva et al. 2002). Zhou et al. (2007) found that the mosquito (Aedes aegypti) allocated ~80% of transferrin-​bound iron to eggs. Although the precise role of transferrins in oogenesis is not yet known, it appears that its function as an intra-​as well as intercellular iron carrier is important (Kurama et al. 1995, Briggs et al. 1999). As such, these observations indicate that variation in the supply of iron could disrupt oogenesis. As an example, to illustrate such potentially pivotal roles of trace metals in altering allocation to life history traits, Jeyasingh and Pulkkinen (2019) examined how Fe availability influences crustacean growth and maturity. Their results indicate a strong impact of dietary iron on reproduction and a negligible impact on growth. This is in stark contrast to dietary phosphorus supply, which is known to invoke a striking growth penalty (Elser et al. 2003). In their study, Jeyasingh and Pulkkinen supplied Daphnia magna with the same quantity of Scenedesmus algae differing in the amount of iron. They found no differences in juvenile growth rate between the low-​and high-​iron treatments (F1,15 = 3.392, p = 0.085; graph a in Fig. 1.5), while age at first reproduction was strongly affected (F1,15 = 359.23, p < 0.001; graph b in Fig. 1.5). While much work remains, particularly



Allocation of Reproductive Efforts (B) 30

1.4 Age at First Reproduction (days)

Juvenile Growth Rate (mm day–1)

(A) 1.2 1.0 0.8 0.6 0.4 0.2 0

High Fe

Low Fe

25 20 15 10 5 0

High Fe

Low Fe

Fig. 1.5. Effects of Fe levels on (a) juvenile growth rate, and (b) age at first reproduction in Daphnia magna. Dietary iron content did not have an effect on juvenile growth rate, but did have a strong effect on age at first reproduction, suggesting that iron may play a role in D. magna reproduction independent of growth. Bar values represent means, while error bars represent 95% confidence intervals. Data from Jeyasingh and Pulkkinen (2019).   

to understand whether the role of iron in oogenesis is as pervasive as the role of P in growth (Elser et al. 2003), phosphorus and iron appear to have distinctive effects on growth and reproduction, respectively. If these linkages are strictly genetic, then individuals that possess superior P use can grow rapidly, while those with superior Fe use can reproduce faster. On the other hand, if these effects are strictly environmental, then habitats with higher P supply should promote rapid growth, while habitats with higher Fe supply should promote earlier reproduction. It is perhaps a combination of both (i.e., genotype-​by-​environment interactions), as is common in most studies in ES at the intraspecific level (Frisch et al. 2014, Roy Chowdhury and Jeyasingh 2016). How such potential genotype-​by-​environment interactions are related to other selective forces such as predation should further illuminate the material basis of divergent life history strategies. While it is well established that size-​selective predation has strongly influenced the evolution of life histories in freshwater crustaceans (Wellborn 1994, Wellborn et al. 1996), we know little about the material demands that are associated with such life history shifts, perhaps with striking ecological consequences. In summary, while it is clear that the framework of ES offers a unique approach to understanding life history evolution with a high degree of ecological realism, it is also clear that the current focus on only a few elements dampens its scope. An ionome-​wide understanding of the material basis of life history strategies as discussed here may mechanistically resolve the paradoxes of positive correlations encountered in single-​currency frameworks that are commonly employed to understand life history evolution. Efforts to integrate the various nutritional ecology frameworks are emerging as potentially powerful analytical tools to study the complex links between life history strategies on the organism level and processes at higher and lower levels of biological organization. One such approach is an effort to integrate nutrient-​based frameworks with the energetically based DEB approach. By combining these approaches, researchers have generated important insights into the efficiency with which crustacean taxa such as copepods utilize elemental resources like C and N for reproduction and somatic maintenance (Kuijper et al. 2004). Additionally, researchers are similarly integrating GF principles with the DEB to more accurately predict nutrient ratios that are most efficient for optimal reproduction (Kearney et al. 2010). Most recently, researchers are beginning to utilize such integrative approaches to predict how organismal processes such as homeostasis influence higher order phenomena like consumer nutrient recycling or food web dynamics (Sperfeld et al. 2016a,

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Reproductive Biology 2016b). While these approaches to integrate the various frameworks of nutritional allocation of resources are still in their infancy, successful integration will provide for higher resolution predictions for the consequences of environmental challenges on organismal fitness outcomes. Such efforts will be valuable tools in the search for a mechanistic understanding of nutritional demands, allocation decisions, organismal behavior, and, ultimately, variation in reproduction within and across populations.

SUMMARY AND CONCLUSIONS Resource allocation to reproduction is central to any model of life history evolution. This centrality is clearly evident by the sustained efforts of researchers to understand what selective pressures drive reproductive patterns and what important life history trade-​offs occur when allocation to reproduction is high. Several models have been developed to understand patterns of allocation to reproduction, such as the r/​K selection theory, which explains broad patterns of resource allocation to reproduction in terms of habitat stability, or the van Noordwijk and de Jong (1986) model, which explains allocation patterns and trade-​offs as a function of acquisition of resources. Resource allocation patterns vary, however, depending on the resources limiting reproduction and the ecology of organisms. As such, resource-​explicit research into allocation to reproduction is important to understand the mechanisms driving life history trade-​offs. Crustacean species have been important model organisms in the development of many of the allocation models presented in this chapter. Such work examining allocation of nutritional resources has provided much to our understanding of the costs of reproduction in many crustacean species. For example, studies using crustacean species have assessed the complex allocation rules governing resource trade-​offs between growth and reproduction, as well as the role of environmental variation in material resources (e.g., elements, molecules) in determining reproductive decisions in both males and females. Additionally, recent ES studies utilizing crustacean species as model organisms have discovered the importance of examining allocation patterns in a context that considers entire elemental composition beyond C, N, and P, as allocation patterns may be more complex than single-​currency models suggest. It seems likely that crustaceans will continue to be valuable model organisms in the effort to expand allocation models to include multiple, interacting resources, and complex life history trait resource demands.

ACKNOWLEDGMENTS We thank Oklahoma State University and the University of Texas at Arlington for providing support during the development of this chapter.

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Reproductive Biology Worley, A. C., D. Houle, and S. C. H. Barrett. 2003. Consequences of hierarchical allocation for the evolution of life-​history traits. The American Naturalist 161:153–​167. Wu, D., Q. Shen, S. Cai, Z.-​H. Chen, F. Dai, and G. Zhang. 2013. Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant and Cell Physiology 54:1976–​1988. Yang, X., Z. Tang, C. Ji, H. Liu, W. Ma, A. Mohhamot, Z. Shi, W. Sun, T. Wang, X. Wang, X. Wu, S. Yu, M. Yue, and C. Zheng. 2014. Scaling of nitrogen and phosphorus across plant organs in shrubland biomes across Northern China. Scientific Reports 4:5448. Zahavi, A. 1975. Mate selection: a selection for a handicap. Journal of Theoretical Biology 53:205–​214. Zhang, C., M. Jansen, L. De Meester, and R. Stoks. 2016. Energy storage and fecundity explain deviations from ecological stoichiometry predictions under global warming and size-​selective predation. Journal of Animal Ecology 85:1431–​1441. Zhou, G., P. Kohlhepp, D. Geiser, M. del Carmen Frasquillo, L. Vazquez-​Moreno, and J. J. Winzerling. 2007. Fate of blood meal iron in mosquitos. Journal of Insect Physiology 53:1169–​1178.

2 OOGENESIS IN CRUSTACEANS: ULTRASTRUCTURAL ASPECTS AND SELECTED REGULATING FACTORS

Mariusz K. Jaglarz and Szczepan M. Bilinski

Abstract This chapter explores ultrastructural aspects of crustacean oogenesis. It focuses on various cellular processes associated with female germline development in selected crustacean groups. Oogenesis in crustaceans comprises four stages:  proliferation of germline cells, previtellogenesis, vitellogenesis, and formation of egg coverings. The greater part of oogenesis occurs in the ovary. In Crustacea, two structurally and functionally distinct types of ovary are recognized: panoistic and meroistic. In panoistic ovaries, all germline cells differentiate into oocytes, and this type of ovarian organization occurs in a great majority of crustaceans, including Malacostraca. In contrast, in the meroistic ovaries, oogonial cells are connected by intercellular bridges and form characteristic linear cysts. Within each cyst, only one cell becomes an oocyte, and the remaining cells differentiate into nurse cells. Meroistic ovaries are typical for Branchiopoda and Ostracoda: Podocopida. Ultrastructural studies reveal that the nucleus and cytoplasmic organelles of the oocyte are highly synthetically active in the panoistic ovary, whereas in the meroistic type, oocyte development is supported, to some extent, by accompanying nurse cells. During previtellogenesis, oocytes accumulate large numbers of various organelles, e.g. ribosomes, mitochondria, and cisternae of endoplasmic reticulum. The oocyte cytoplasm also contains characteristic disc-​shaped bodies and cortical granules. A comparative analysis of the proteinaceous yolk formation in different crustaceans reveals two distinct types of vitellogenesis (autosynthesis and heterosynthesis), and indicates that a mixed type prevails in these arthropods. In most crustacean species, germline cells associate with somatic follicle cells that may fulfill several functions during oogenesis.

This chapter is dedicated to our friend, the late Prof. Janusz Kubrakiewicz, an enthusiast for arthropod oogenesis. Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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INTRODUCTION With an estimated 50,000–​70,000 extant species, crustaceans exhibit a tremendous disparity of form, size, lifestyle, and ecology, far exceeding that of other arthropod groups (Brusca and Brusca 2003, VanHook and Patel 2008, Schram 2013). Despite this exceptional diversity, the ovarian morphology and various aspects of oogenesis have only been comprehensively studied in one crustacean subgroup, the Malacostraca. Likewise, the ultrastructural aspect of the female germline development is particularly well characterized in several lineages of malacostracans. This is probably justified by the economic importance of this crustacean group and the relative ease of collection of the research material. However, the few studies of ovarian structure and female gametogenesis in other crustacean groups indicate that malacostracan oogenesis cannot be considered the paradigm of crustacean oogenesis. Recently, a renewed interest in all aspects of crustacean morphology has been ignited by a new phylogenetic concept, which nests Hexapoda/​Insecta within Crustacea and advocates the creation of a new taxon, the Pancrustacea or Tetraconata, comprising both groups (reviewed in Regier et al. 2005, von Reumont and Edgecombe, 2020). The postulated close relationship between hexapods and crustaceans allows a novel interpretation of some morphological features of these invertebrates and also provides a new perspective of crustacean oogenesis. Comparative analysis of the female germline development in various crustacean lineages not only unveils existing diversity, but also promotes a more comprehensive understanding of how ovarian structure and oogenesis were modified during arthropod evolution. In this review, we concentrate on the ultrastructural aspects of oogenesis in select groups of crustaceans, in which the processes associated with female gametogenesis are best characterized or most informative.

GENERAL REMARKS ON CRUSTACEAN OOGENESIS Oogenesis in crustaceans, as in other arthropods, can be arbitrarily divided into four stages: (1) proliferation of the germline cells, (2) previtellogenesis, (3) vitellogenesis, and (4) the formation of the oocyte/​egg coverings. Each stage has its distinct structural and functional characteristics and most frequently takes place in a discrete compartment of the female reproductive system. The main part of oogenesis occurs in the female gonad, the ovary (Fig. 2.1). The proliferative stage, i.e., multiplication of oogonial cells by mitotic divisions, usually takes place in a more or less morphologically distinct ovarian region, termed the germarium. However, both the size and position of the germarium within the ovary may vary among different crustacean groups. In Remipedia, for instance, the germarium is located in the anterior region of the body (the cephalothorax) and is clearly separated from the remaining part of the ovary (Kubrakiewicz et al. 2012). But such an arrangement seems rather exceptional. More frequently, the germinal zone is not clearly demarcated and occupies either a peripheral (e.g., some decapods) or central region (e.g., brachyuran crabs) of the ovary (for review, see Adiyodi and Subramoniam 1983, Jaglarz et al. 2014a). Also, in several malacostracan species, the germarium invades ovarian lobes and forms so-​called germinal nests (Adiyodi and Subramoniam 1983). As a gen­eral rule, both previtellogenesis and vitellogenesis proceed within the ovary. Only the final stage of oogenesis, i.e., the formation of the oocyte/​egg coverings, can also take place in the oviduct (a distal part of the female reproductive ducts), or in other specialized body regions, such as the ovisac in some branchiopods. The general features of ovarian morphology in crustaceans have been recently reviewed and will not be covered in this chapter (see Lopez Greco 2013, Jaglarz et al. 2014a). It is worth emphasizing that oogenesis in crustaceans, as in other animal groups, is tightly linked with meiosis, and the most significant part of oocyte differentiation takes place during the extended meiotic prophase. As a rule, it is during the diplotene stage that the most intensive (previtellogenic and vitellogenic) growth of the oocytes occurs. Subsequently, oocyte development is arrested in



Oogenesis in Crustaceans

Fig. 2.1. Ovaries within a partially transparent body of a clam shrimp (Branchiopoda). Note ovarian follicles (arrows) protruding from the ovary. A living specimen photographed in a stereoscopic microscope with side illumination. See color version of this figure in the centerfold. Abbreviations: an = antenna; c = carapace; e = eye; g = gut; ov = ovary; tl = trunk limb.   

the first meiotic metaphase, and meiosis resumes after successful fertilization (reviewed in Adiyodi and Subramoniam 1983, Meusy and Payen 1988). In an overwhelming majority of crustacean species, germline cells associate early with mesodermal, somatic cells of the ovary, forming functional ovarian units termed ovarian follicles. The germline cells/​oocytes developing inside the follicles are typically surrounded or enveloped by a layer of somatic cells, termed follicle or follicular cells (FCs). Such somatic cells have not been reported in Ostracoda: Myodocopida, nor in highly specialized parasitic species of Branchiura and Pentastomida. In these crustaceans, developing oocytes protrude from the ovary into the hemocoel and are covered exclusively by a thin acellular layer of the basement membrane of the ovarian wall (Böckeler 1984, Walldorf and Riehl 1985, Kubrakiewicz and Klimowicz 1994, Ikuta and Makioka 1997, 1999, 2004).

PROLIFERATION OF GERMLINE CELLS In the ovary, germline (oogonial) cells increase in number through mitotic divisions. Cytokinesis following each division may either be complete or incomplete, which has important consequences for the further course of oogenesis. Complete mitotic divisions generate a population of separate germline cells, all of which differentiate into oocytes, enter meiosis, and subsequently become fertilizable eggs. In contrast, incomplete mitotic divisions result in the formation of syncytial cysts consisting of sibling oogonial cells, termed cystocytes, which are connected by intercellular bridges, at least through the initial phase of oogenesis (A and B in Fig. 2.2). The most characteristic feature of the germline cysts in crustaceans is a linear (chain-​like) arrangement of the cystocytes (A in Fig. 2.2). As a rule, within each cyst only one cell differentiates into an oocyte and the remaining cells become nurse cells, also called trophocytes (C and D in Fig. 2.2). The number of the nurse cells is species-​specific and depends on the ultimate size of the germline cyst, which in turn is defined by the number of consecutive mitotic divisions. On the extreme low end, only one nurse

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Fig. 2.2. Germline cysts or young oocytes in different crustacean groups. (A)  Artemia salina (Branchiopoda, Anostraca). Intercellular bridges (arrows) connecting cystocytes (c) in the linear ovarian germline cell cyst. Note that intercellular bridges are lined with electron-​dense material. Transmission electron microscope, scale bar  =  1 μm. cm  =  cell membrane; m  =  mitochondria; n  =  cystocyte nucleus. Micrograph courtesy of Dr. Izabela Jedrzejowska, University of Wroclaw, Poland. (B) Triops australensis (Branchiopoda, Notostraca). Germline cell cysts in a developing ovary. Each cyst consists of four germline cells (cystocytes) connected by ring-​like intercellular bridges (arrows) lined with filamentous actin. Stained with rhodamine conjugated



Oogenesis in Crustaceans

cell has been reported in two-​cell germline cysts of Cyprinotus uenoi (Ostracoda: Podocopida; Ikuta et al. 2007). In contrast, each oocyte is accompanied by three nurse cells in ovarian follicles of many branchiopods, including Triops (Notostraca), Daphnia (Anomopoda), Cyzicus (Spinicaudata), and Lynceus (Laevicaudata) (C and D in Fig. 2.2; reviewed in Rossi 1980, Martin 1992, Jaglarz et  al. 2014b). The presence of the germline cysts, comprising four cells connected by intercellular bridges, suggests that they are generated by two consecutive and incomplete mitotic divisions of a stem cell. It appears, however, that the relatively small number of nurse cells in the ovarian follicles is not typical for all branchiopods because many more nurse cells (up to 70) have been reported in multicellular, linear germline cysts in species representing the subgroup Anostraca:  Artemia salina and Siphonophanes grubei (Criel 1989, Kubrakiewicz et  al. 1991, Jaglarz et  al. 2014a). It should be mentioned that an entirely different origin of the female germline cells from a plasmodium-​like structure has been suggested in the branchiopod Eoleptestheria ticinensis (Spinicaudata: Leptesteridae; Scanabissi Sabelli and Tommasini 1990). However, in our view, this unorthodox mode of female gametogenesis is a matter of controversy and requires further investigation. There are no comprehensive reports on the formation of ovarian cysts in crustaceans; however, the presence, structure, and spatial distribution of stable intercellular bridges is a good indication that they originate by the same cytological mechanisms operating in the ovaries in other arthropods and animals (for the latest review, see Greenbaum et al. 2011). Based on what is known about animal gametogenesis (for further discussion, see Pepling et al. 1999), it is also conceivable that the syncytial phase of oogenesis in crustaceans might be a widespread phenomenon. The presence of exclusively linear ovarian germline cysts in crustaceans is interesting from a phylogenetic perspective. Linearly arranged germline cysts have been reported in other arthropod groups, including entognathans (Collembola and Diplura/​Campodeina), certain insects, e.g., mayflies (Ephemeroptera) and lacewings (Neuroptera), and even non-​arthropod groups (for review, see Büning 1998, Jaglarz et al. 2014a). Therefore, it has been recently postulated that linear cysts arose independently in several lineages of arthropods as a reduction of the plesiomorphic condition, i.e., branched germline cysts ( Jaglarz et al. 2014a). In insects, the formation of the germline cyst and subsequent developmental fate of the cystocytes are well characterized in the fruit fly Drosophila melanogaster (for the latest review, see Ong and Tan 2010). In contrast to insects, the molecular mechanisms of cystocyte differentiation in the crustacean germline cysts are completely unknown. In this context, it is of interest that a transient assembly of mitochondria and electron-​dense, granular material, termed nuage (see the following section, “The Panositic vs. Meroistic Ovary”), occurs in the perinuclear region in the

phalloidin to reveal distribution of actin filaments. Confocal microscope, scale bar  =  2 μm. (C, D) Triops australensis (Branchiopoda, Notostraca). Fragment of an early (C) and late (D) vitellogenic ovarian follicles. Each follicle consists of an oocyte (o) and three nurse cells (nc) only two of which are visible. Semithin section, methylene blue; light microscope, scale bars = 200 μm. fe = follicular epithelium; n = oocyte nucleus; nn = nurse cell nucleus. (E) Daphnia magna (Branchiopoda, Anomopoda). Fragment of a previtellogenic oocyte. The nucleus (n) contains a prominent nucleolus (nu) and is surrounded by a regular nuclear envelope (ne). Perinuclear ooplasm contains a Balbiani body-​like aggregate of organelles consisting of nuage material (encircled), mitochondria (m), and a centriole (black arrowhead). Transmission electron microscope, scale bar = 0.5 μm. (F) Cherax quadricarinatus (Malacostraca: Decapoda). Fragment of the oocyte nucleus (n) and perinuclear ooplasm containing a microtubule network. Transmission electron microscope, scale bar = 1 μm. White arrowheads = microtubules; np = nuclear pores; nu = nucleolus; v = vesicle. See color version of this figure in the centerfold.   

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THE PANOISTIC VS. MEROISTIC OVARY Because the proliferative stage of oogenesis has not been studied extensively in crustaceans, information on the origin of the oocytes is not always available. Nevertheless, based on the final cellular architecture of the female gonads, two structurally and functionally different types of ovaries can be distinguished: panoistic and meroistic. In the panoistic ovaries, the germline is represented only by oocytes (and the female gonial cells, the oogonia), whereas in the meroistic ovaries the oocytes are accompanied by their sister cells, the nurse cells (C and D in Fig. 2.2). Ovaries with the canonical panoistic grade of organization appear more widespread among the Crustacea and have been reported in Remipedia, Cephalocarida, Mystacocarida, Copepoda, and Malacostraca: Amphipoda, Isopoda, and Decapoda (reviewed in Adiyodi and Subramoniam 1983, Boxshall 1992, Krol et al. 1992, Wägele 1992). The meroistic ovaries have been reported, so far, in only two groups: Branchiopoda (reviewed in Rossi 1980, Martin 1992, Jaglarz et  al. 2014a) and Ostracoda:  Podocopida (Ikuta et al. 2007). Obviously, the functioning of the ovarian follicles in crustaceans differs markedly depending on ovarian organization. In panoistic ovaries, the oocyte is solely responsible for synthesis of macromolecules and reserve materials necessary for proper development of the embryo. Therefore, both the oocyte nucleus and cytoplasm (ooplasm) are highly synthetically active. The ultrastructural architecture of the oocyte nucleus, traditionally called the germinal vesicle, has been best characterized in freshwater calanoid copepods (Cuoc et al. 1993), a representative of Cephalocarida, Hutchinsoniella macracantha (Hessler et al. 1995), Remipedia (Kubrakiewicz et al. 2012), as well as in several groups of malacostracans (reviewed in Krol et al. 1992). In these crustacean lineages, the oocyte nucleus is usually large, spherical, and surrounded by a regular nuclear envelope, perforated by numerous nuclear pores (F in Fig. 2.2). The nucleoplasm contains mostly dispersed chromatin and only occasional inconspicuous clumps of heterochromatin. The most prominent nuclear domain of the germinal vesicle is undoubtedly the nucleolus. Both its large size (e.g., 25–​35 μm in diameter in the oocyte nucleus of Acanthocelops vernalis, Copepoda) and ultrastructural morphology indicate active involvement in the biosynthesis of ribosomal subunits (Standiford 1988, Krol et al. 1992). As oogenesis progresses, the nucleolus often becomes vacuolated, which signifies rapid and massive transport of ribosomal subunits from this nuclear domain into the ooplasm. The perinuclear cytoplasm of germline cells (both the oocytes and nurse cells) often contains characteristic accumulations of dense granular material, the nuage (E in Fig. 2.2). Such accumulations were reported in a variety of crustaceans, including branchiopods, cephalocarids, copepods, amphipods, isopods, and decapods (Beams and Kessel 1963, 1980, Bilinski 1979, Zerbib 1980, Blades-​Eckelbarger and Youngbluth 1984, Krol et al. 1992, Cuoc et al. 1993, Hessler et al. 1995, Jaglarz et al. 2014b). In crustaceans, the nuage material is usually described, based solely on morphological criteria, as of nucleolar origin. However, because detailed molecular composition of the nuage in crustaceans is unknown, its homology to similar material well characterized in insect germline cells and its putative functions remain speculative (for the latest review on nuage and related structures in animal germline cells, see Kloc et al. 2014). Nevertheless, the characteristic distribution of nuage material strongly indicates that intensive nuclear-​cytoplasmic exchanges take place during crustacean oogenesis.



Oogenesis in Crustaceans

In some crustacean species, the perinuclear cytoplasm may also contain other specific structures. In Cherax quadricarinatus (Decapoda) oocytes, the nucleus is surrounded by an intricate network of microtubules, which is best visible after a special extraction method used prior to fixation of the ovary (F in Fig. 2.2). This microtubule network may be involved in maintaining a central position of the oocyte nucleus. Another function of the network, based on the association of electron-​dense aggregates with this network, may be to transport macromolecular complexes from the perinuclear region toward the oocyte periphery ( Jaglarz et al. 2016). Functioning of the meroistic ovary differs significantly from that of the panoistic ovary. The development of the oocyte is supported to a certain extent by nurse cells that actively synthesize various organelles (primarily ribosomes) and macromolecules and subsequently transfer them via existing intercellular bridges into the oocyte. Therefore, these intercellular bridges represent an indispensable component of the functioning of the meroistic ovary. In crustaceans, the intercellular bridges have a rather simple and uniform structure. The inner rim of the bridges is lined with an electron-​dense layer (A in Fig. 2.2). Staining with fluorescently labeled phalloidin revealed that this layer contains filamentous actin in several species of branchiopods (B in Fig. 2.2; Jaglarz et al. 2014a,b). Actin filaments have also been demonstrated inside the intercellular bridge connecting a nurse cell and an oocyte in Cyprinotus uenoi (Ostracoda: Podocopida; Ikuta et al. 2007). In the immediate vicinity of the intercellular bridges, cell membranes of the connected cystocytes run parallel and are usually fastened by adherens junctions (Durfort et al. 1980, Jaglarz et al. 2014b). It is well established in different animal systems that intercellular bridges may participate in (1)  transferring cues responsible for synchronization of the cystocyte divisions; (2)  cystocyte differentiation or oocyte determination, or both; and (3)  transport of various cytoplasmic constituents between connected cells of the fully formed cyst (reviewed in Greenbaum et al. 2011). In crustacean ovaries, compelling evidence exists for only transport of cytoplasmic constituents between connected cells. Ultrastructural studies revealed that the bridges have a diameter large enough (2 µm or more) for passage of organelles. Moreover, various organelles were frequently found within the cytoplasm filling the lumen of the bridges, including ribosomes, mitochondria, cisternae of the endoplasmic reticulum, and various vesicular structures (Criel 1989, Jaglarz et al. 2014a, 2014b). In addition, some circumstantial evidence exists for other functions of the intercellular bridges in crustacean oogenesis. In the ovaries of Artemia salina (Branchiopoda) and Mytilicola intestinalis (Copepoda), two types of bridges were reported: open and closed (Anteunis et al. 1966, Durfort et al. 1980). The lumen of the closed bridges is apparently obstructed by elongated cisternae of the endoplasmic reticulum (Durfort et al. 1980). It is conceivable that such structural modification of the bridges may be responsible for the differential diffusion of molecular cues or the transfer of organelles across the cyst, or both. In crustaceans, not all meroistic ovaries are equal, and group-​specific differences exist, especially in the morphological distinction between the oocyte and nurse cells. In Cyprinotus uenoi ovaries, nurse cells are much smaller than the oocytes throughout oogenesis, while in Artemia, Leptestheria, Cyzicus, and Lynceus, nurse cells are roughly the size of the oocyte, at least until mid-​vitellogenesis when the oocyte volume increases considerably (Criel 1989, Zeni and Zaffagnini 1989, Ikuta et al. 2007, Jaglarz et al. 2014b). In contrast, nurse cells in the ovarian follicles of Triops cancriformis and T. australiensis are initially larger than the oocyte, but diminish as oogenesis progresses (C and D in Fig. 2.2; Scanabissi Sabelli and Trentini 1979). In branchiopods, nurse cell ultrastructure highly resembles that of the oocyte, and the nurse cell cytoplasm contains the same set of organelles as reported in the ooplasm (Trentini and Scanabissi Sabelli 1978, Jaglarz et al. 2014b). In ovarian follicles of Triops, Leptestheria, Cyzicus, and Lynceus, nurse cells even synthesize yolk spheres, apparently in the same manner as the oocyte (Trentini and Scanabissi Sabelli 1978, Zeni and Zaffagnini 1989, Jaglarz et al. 2014a, 2014b). A prominent single nucleolus (e.g., Cyzicus, Lynceus) or many nucleoli (Triops) develop both in the oocyte and nurse

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Reproductive Biology cell nuclei, suggesting active involvement of both germline cell types in biogenesis of the ribosomes (C and D in Fig. 2.2; Trentini and Scanabissi Sabelli 1978, Jaglarz et al. 2014b). Ultimately the nurse cells degenerate after passing most of their cytoplasm into the oocyte ( Jaglarz et al. 2014b). All the aforementioned observations suggest that nurse cells in branchiopods are abortive oocytes, which suppress their own development for the benefit of just one of their siblings, the ultimate oocyte (Trentini and Scanabissi Sabelli 1978, Zeni and Zaffagnini 1989, Jaglarz et al. 2014b). Meroistic ovaries of crustaceans are not as advanced in “meroism” as ovaries of certain insects. It is well established that in insect meroistic ovaries, nurse cells are highly polyploid and provide the oocyte with a variety of macromolecules, including proteins and different classes of RNAs: ribosomal, protein-​coding, and regulatory/​noncoding (for review, see Büning 1998). The situation is less clear in crustaceans. It was suggested that crustacean nurse cells might become polyploid (for further discussion, see Adiyodi and Subramoniam 1983, Criel 1989); however, to our knowledge, the level of ploidy of these cells in crustacean ovaries has not been rigorously investigated. One study showed that in Cyprinotus uenoi, nurse cell nuclei gave a visibly stronger signal than oocyte nuclei in Hoechst-​33342-​staining, which is indicative of higher ploidy of these cells (Ikuta et al. 2007).

PREVITELLOGENESIS The stage of oogenesis after oocyte determination and prior to the onset of reserve material (yolk) accumulation is designated previtellogenesis. The previtellogenic growth of the oocyte is characterized by a marked increase in transcription of ribosomal genes (see earlier discussion) as well as activity of the cytoplasmic organelles. It is at this stage of oogenesis that a variety of organelles, including ribosomes, mitochondria, annulate lamellae, cisternae of endoplasmic reticulum, and stacks of Golgi complexes, are gradually accumulated in large numbers within the oocyte cytoplasm (A and B in Fig. 2.3; for review, see Krol et al. 1992, Martin 1992, Cuoc et al. 1993 and references therein). As a result, the ooplasm expands and the oocyte volume increases noticeably. In the ooplasm of some crustacean species, conspicuous accumulations of particular organelles have been described. For instance, in the remipede Godzilliognomus frondosus and certain branchiopods, oocytes contain characteristic whorls of concentrically arranged endoplasmic reticulum cisternae, while in Artemia oocytes, multivesicular bodies, dense bodies, free ribosomes, and microvesicles form large aggregates, traditionally referred to as the vitelline nucleus (Criel 1989, Kubrakiewicz et  al. 2012, Jaglarz et al. 2014b). There is no doubt that the most characteristic ultrastructural feature of previtellogenesis in crustaceans is the formation of disc-​shaped bodies:  electron-​dense, roughly spherical granules present inside cisternae or vesicles of the rough endoplasmic reticulum (E in Fig. 2.3). Originally described by Beams and Kessel (1963) in oocytes of several crayfish species (Cambarus, Orconectes, and Procambarus spp.), disc-​shaped bodies have been reported in oocytes of various crustaceans including branchiopods, copepods, and decapods (reviewed in Adiyodi and Subramoniam 1983 and Krol et al. 1992). Morphologically similar structures have also been described in the oocytes of other invertebrates, e.g., polychaetes, entognathous insects, and pycnogonids (for review, see Bilinski et al. 2008). The function of disc-​shaped bodies in crustaceans remains controversial. They have been usually interpreted as precursors of the yolk spheres (e.g., Cuoc et al. 1993). Recently, however, several authors suggested that these bodies may be related to cortical granules (see later discussion) and are involved in the formation of the fertilization membrane (Goudeau and Lachaise 1980, Goudeau and Becker 1982, Pillai and Clark 1990, Blades-​Eckelbarger and Marcus 1992, Cuoc et al. 1993, Eckelbarger and Blades-​Eckelbarger 2005). Unfortunately, the molecular composition of the disc-​shaped bodies in crustaceans is unknown, and hence their role in oogenesis remains obscure. Based on the ubiquitous occurrence of disc-​shaped bodies in oocytes of various arthropod species,

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Fig. 2.3. Ultrastructure of vitellogenesis. (A) Lynceus brachyurus (Branchiopoda, Laevicaudata). Early vitellogenic oocyte. The ooplasm contains numerous Golgi complexes (Gc), rough endoplasmic reticulum cisternae (rer) and nascent yolk spheres (asterisks) indicating autosynthetic mode of vitellogenesis. Transmission electron microscope, scale bar = 0.5 μm. m = mitochondria. (B, C) Godzilliognomus frondosus (Remipedia). (B) Fragment of ooplasm (oo) with a prominent Golgi complex (Gc) surrounded by rough endoplasmic reticulum cisternae (rer). db = dense body. (C) Nascent yolk spheres (asterisks) within the lumen of the rough endoplasmic reticulum cisternae (rer). Transmission electron microscope, scale bars  =  400  nm. (D, E) Porcellio scaber (Malacostraca, Isopoda). (D)  The peripheral ooplasm during micropinocytotic uptake of yolk precursors. The oocyte surface is covered with microvilli (mv). Note micropinocytotic pits (arrowheads) and vesicles (mpv) pinching off the oocyte membrane. The ooplasm contains mitochondria (m), endoplasmic reticulum cisternae (er), nascent (asterisk), and more mature (y) yolk spheres. Transmission electron microscope, scale bars  =  0.5 μm. (E) Fragment of ooplasm (oo) with a nascent yolk sphere (asterisk) and endoplasmic reticulum cisternae (er) filled with disc-​shaped bodies. Transmission electron microscope, scale bars  =  0.5 μm. m = mitochondrium.   

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Reproductive Biology it has been proposed that these structures may represent a ground-​plan condition (plesiomorphic character) of arthropods inherited from their common ancestor (Bilinski et al. 2008). Ultrastructural studies have also revealed the presence of distinct cytoplasmic vesicles, termed cortical granules, in the peripheral, i.e., cortical, region of the oocytes in several crustacean groups. They have been identified so far in amphipods (Zerbib 1980), decapods (reviewed in Krol et al. 1992), and copepods (Blades-​Eckelbarger and Marcus 1992, Santella and Ianora 1992). Cortical granules are electron-​dense, membrane-​bound organelles. Although the origin of cortical granules is still debated (see earlier discussion), their function appears clear: after fertilization, they release their contents by exocytosis and participate in the formation or modification of the fertilization membrane (or both), preventing polyspermy (reviewed in Rosati 1995).

VITELLOGENESIS Crustaceans, similarly to other oviparous animals, load their eggs with large amounts of diverse reserve substances collectively called yolk (reviewed in Meusy and Payen 1988, Tsukimura 2001, Wilder et  al. 2002). Because these substances significantly differ structurally and biochemically, they are usually divided into at least three groups: proteinaceous yolk (yolk spheres or platelets), lipid droplets, and glycogen particles. Little is known about the origin of lipid and glycogen yolk in crustacean oocytes; therefore, we will focus only on yolk protein synthesis. The ultrastructure of yolk spheres deposited within the ooplasm is remarkably uniform among the Crustacea: they are contained inside vesicles surrounded by a smooth (i.e., devoid of ribosomes) limiting membrane (A, D–​E in Fig. 2.3; A in Fig. 2.4). A comparative analysis of the course of vitellogenesis in different crustacean species reveals two distinct mechanisms for the formation of these vesicles and the synthesis of their contents. In some crustaceans (e.g., certain branchiopods), yolk proteins are produced by the oocyte cytoplasmic machinery in a process called autosynthesis (or intra-​oocytic yolk synthesis). In this scenario, yolk proteins are synthesized within the lumen of the rough endoplasmic reticulum and subsequently are transferred via transport vesicles into the dictiosome/​Golgi apparatus for further sorting and modifications (Beams and Kessel 1963, 1980, Blades-​Eckelbarger and Youngbluth 1984, Cuoc et al. 1993, Jaglarz et al. 2014b, some authors, however, question the role of the Golgi apparatus in yolk formation). Accordingly, the oocyte cytoplasm contains a well-​developed network of endoplasmic reticulum and a prominent Golgi apparatus (A–​C in Fig. 2.3). The vesicles containing modified yolk proteins bud off from the cisternae of the Golgi apparatus and are therefore surrounded by a smooth membrane. Nascent yolk spheres first appear in the central cytoplasm, in the vicinity of the oocyte nucleus, where the Golgi apparatus usually resides. Initially small, the yolk-​containing vesicles fuse with each other, forming larger, electron-​dense, mature yolk spheres. During these processes, yolk spheres gradually translocate toward the peripheral ooplasm and fill up the ooplasm. A different mode of vitellogenesis, termed heterosynthesis (or extra-​oocytic yolk synthesis), is typically found in malacostracans. It has been demonstrated that female-​specific yolk precursors, termed vitellogenins, are synthesized outside the oocyte in the hepatopancreas, subepidermal adipose tissue (fat body), or in somatic cells of the ovary (reviewed in Tsukimura 2001, Subramoniam 2011). Gene expression analyses have demonstrated that in some penaeid decapods, vitellogenin is synthesized in both the hepatopancreas and the ovary (Tsutsui et al. 2000, Avarre et al. 2003, Raviv et  al. 2006, Xie et  al. 2009). Biochemically, crustacean vitellogenin was identified as a lipoglycocarotenoprotein; it serves as the major large lipid transfer protein (reviewed in Wilder et al. 2010, Subramoniam 2011). The vitellogenins released to the hemolymph are subsequently taken up specifically by the oocytes (for review, see Meusy and Payen 1988, Krol et al. 1992, Tsukimura 2001,



Oogenesis in Crustaceans (A)

(B)

(C)

(D)

Fig. 2.4. Somatic (follicle) cells accompanying oocytes. (A) Cyzicus tetracerus (Branchiopoda, Spinicaudata). Highly extended follicular epithelium (fe) covering a vitellogenic oocyte (o). The oocyte cytoplasm is filled with yolk spheres (y), lipid droplets (l), and cisternae of the rough endoplasmic reticulum (rer) some of which contain nascent yolk spheres (asterisks). Transmission electron microscope, scale bar = 1 μm. al = annulate lamellae; bm = basement membrane; m = mitochondrium. (B) Godzilliognomus frondosus (Remipedia). Follicle cells (fc) surrounding previtellogenic oocyte (o). Transmission electron microscope, scale bar = 2 μm. bm = basement membrane; db = dense body; n = follicle cell nucleus. (C, D) Cherax quadricarinatus (Malacostraca: Decapoda). (C) Fractured ovarian follicle with the exposed: oocyte membrane (om), egg envel­ope (en), and a layer of follicle cells (fc). (D) Fragment of a vitellogenic oocyte with a partially removed oocyte membrane (om) to reveal yolk spheres (y). Scanning electron microscope, scale bars = 200 μm.   

Wilder et al. 2010, Subramoniam 2011). The internalized yolk protein is traditionally referred to as vitellin or lipovitellin. At the ultrastructural level, heterosynthesis is associated with the formation of abundant microvilli on the oocyte surface as well as the presence of coated pits (small plasma membrane invaginations with a distinctive electron-​dense protein coat on the cytosolic surface), and microvesicles distributed within the cortical ooplasm (D in Fig. 2.3; Hinsch and Cone 1969, Bilinski

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Reproductive Biology 1979, Beams and Kessel 1980, Zerbib 1980, Okumura et al. 2004). Such ultrastructural characteristics have been interpreted as the morphological manifestation of ongoing micropinocytosis or receptor-​ mediated endocytosis of externally produced yolk precursors. Recently, vitellogenin receptors have been characterized molecularly in the mud crab Scylla serrata and the tiger prawn Penaeus monodon (Warrier and Subramoniam 2002, Tiu et  al. 2008). Exactly how the vitellogenins access the oocyte surface in crustaceans is a matter of debate (see also the following section, “Follicle Cells”), but there is no contention that in the heterosynthetic type of vitellogenesis, nascent yolk spheres form in the peripheral/​cortical region of the oocyte by endocytotic vesicle fusions followed by coalescence of their contents. The mature, electron-​dense, and membrane-​enclosed yolk spheres, or platelets, disperse ultimately throughout the ooplasm (D in Fig. 2.4). The two principal modes of vitellogenesis in Crustacea are schematically represented in Fig. 2.5. Older and more recent literature on vitellogenesis in crustaceans indicates that yolk spheres are generated by a combination of auto-​and heterosynthetic mechanisms in a great majority of crustaceans (see Table 2.1). Such a mixed mode of vitellogenesis has been described in branchiopods, copepods, amphipods, decapods, and isopods (Zerbib 1977, Komm and Hinsch 1987, Zeni and Zaffaganini 1989, Cuoc et al. 1993). Furthermore, a comparative analysis of vitellogenesis in malacostracans living in different habitats (aquatic or terrestrial) reveals no significant differences in the ultrastructural characteristics of this process (reviewed in Krol et al. 1992, Wägele 1992). This suggests that there is no apparent correlation between the type of living environment and the course of oogenesis in crustaceans (Bilinski 1979). Likewise, the type of development in

(A)

(B) fc

hp

fc mv n

mv

rer

cp Ga n

o

o

y

y

Fig. 2.5. Schematic representation of autosynthetic (A) and heterosynthetic (B) modes of yolk synthesis (vitellogenesis) in crustaceans. In autosynthesis, oocytes internalize low molecular weight precursors from hemolymph (non-​selective transport) to synthetize vitellin (yolk) with the help of their own membranous organelles: the rough endoplasmic reticulum (rer) and Golgi apparatus (Ga). In heterosynthesis, oocytes incorporate selectively high molecular weight yolk proteins (vitellogenins) produced by cells outside the ovary, e.g., cells of the hepatopancreas (hp). A combination of auto-​and heterosynthesis, called mixed vitellogenesis, is also reported in some crustaceans (see text for further details). Abbreviations: cp = coated pits; fc = follicle cell; mv = microvilli; n = nucleus; o = oocyte; y = yolk spheres.   

1

3 or several dozen

Number of Nurse Cells in Germline Cysts

heterosynthesis/​mixed heterosynthesis/​mixed heterosynthesis/​mixed

? ? ? mixed? mixed ? absent absent present in some species

? ? absent present present absent

Type  of   Vitellogenesis Prominent Assemblages of RER* and Golgi Complexes in Oocytes autosynthesis? present autosynthesis? absent autosynthesis/​mixed present

Notes: ? indicates characters that are uncertain or unknown; * RER = rough endoplasmic reticulum.

panoistic panoistic panoistic

meroistic panoistic panoistic panoistic panoistic panoistic

panoistic panoistic meroistic

Remipedia Cephalocarida Branchiopoda

Ostracoda: Podocopida Myodocopida Branchiura Pentastomida Copepoda Mystacocarida Malacostraca Amphipoda Isopoda Decapoda

Type of Ovary

Group

Table 2.1.  Selected Ovarian Characters in Crustaceans.

polarized polarized polarized

? FCs absent FCs absent FCs absent ? unpolarized

unpolarized unpolarized unpolarized

Type of Follicle Cells (FCs)

absent absent absent/​present in Palaemonidae

present absent

?

Tubular Network Penetrating Follicle Cells absent absent present

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Reproductive Biology amphipods and certain reproductive traits in tropical caridean shrimps show no difference between marine and freshwater species (Steele and Steele 1991, Anger and Moreira 1998). Finally, in some crustacean groups such as Cephalocarida and Remipedia, the mode of vitellogenesis remains uncertain, although based on ultrastructural features of the ooplasm, it has been speculated that yolk proteins might be synthesized by the oocyte in the autosynthetic manner (B and C in Fig. 2.3; Hessler et al. 1995, Kubrakiewicz et al. 2012, Jaglarz et al. 2014a, 2014b). Regardless of the vitellogenesis scenario, the volume of the oocytes increases tremendously as the yolk spheres, lipid droplets, and other reserve substances are deposited within the ooplasm. It is also well established that crustacean vitellogenesis is regulated by endocrine factors. The intricacies of hormonal regulation of vitellogenesis in crustaceans, as well as structural and biochemical characterization of yolk in various species, are beyond the scope of this review (for details, see Tsukimura 2001, Wilder et al. 2002, Tiu et al. 2009, Nagaraju 2011, Subramoniam 2011).

FOLLICLE CELLS There is a great deal of confusion in the terminology of the somatic cells accompanying the germline cells in the ovaries of crustaceans. In our opinion, the term follicle cells (FCs) should be restricted only to the somatic, mesodermally derived cells that (1) reside beneath the basement membrane covering the ovarian follicle or ovary (A and B in Fig. 2.4), (2) contact the germline cells directly by apposition of the cell membranes or by specialized intercellular junctions (termed heterocellular gap junctions), and (3) actively participate in some aspects of oogenesis, e.g., formation of an egg envelope (for further discussion, see Jaglarz et al. 2014a). The progenitors of the FCs, called pre-​ FCs, multiply via mitosis and are scattered among the germline cells in the germarial region of the ovary (reviewed in Adiyodi and Subramonian 1983). Once divisions of the germline cells are completed, pre-​FCs penetrate between the gonial cells, separate individual oogonia or germline cysts (in meroistic ovaries) from one another, and, in cooperation with germline cells, form ovarian follicles. At this stage they usually stop dividing; however, mitotic divisions of these cells were reported in more advanced follicles in some decapods (reviewed in Krol et al. 1992). Initially, FCs form an unstratified multilayer around the germline cells, but they subsequently rearrange into a single cell layer as oogenesis progresses and oocytes increase in size (C and D in Fig. 2.2). There are, however, numerous deviations from this general characteristic. In crustacean ovarian follicles, at least two types of FC arrangements can be distinguished, roughly corresponding to the traditional division into lower and higher crustaceans. In branchiopods, FCs form a simple continuous layer around germline cells that flattens and expands greatly during vitellogenic growth of the oocyte (C and D in Fig. 2.2; A in Fig. 2.4). These somatic cells are morphologically unpolarized ( Jaglarz et al. 2014a). In ovaries of Remipedia and Cephalocarida, there is no typical follicular epithelium either (B in Fig. 2.4). Instead, somatic ovarian cells extend thin cytoplasmic projections that penetrate between oocytes and separate neighboring oocytes from one another (Hessler et al. 1995, Kubrakiewicz et al. 2012, Addis et al. 2013). Recent ultrastructural analysis revealed that in the remipede Godzilliognomus frondosus, these somatic cells form very fine elongated cytoplasmic processes, which penetrate the oocyte cytoplasm and maintain connection with the oocyte by means of heterocellular gap junctions ( Jaglarz et al. 2014a). This strongly indicates that the somatic cells directly associated with the oocytes can be regarded as canonical FCs, at least in Remipedia (for further discussion, see Kubrakiewicz et al. 2012, Jaglarz et al. 2014a). In malacostracan ovaries, FCs surrounding the oocytes are connected via specialized junctions such as adherens junctions or desmosomes and form a proper epithelium on the oocyte surface (for review, see Jaglarz et al. 2014a and references therein). During oogenesis, FCs become clearly polarized into a basal region adjacent to the basal lamina and an apical region equipped with numerous



Oogenesis in Crustaceans

microvilli facing the germline cells. Morphogenesis of the follicular epithelium accompanying the progression of oogenesis was well characterized in the ovaries of a marine isopod Idothea balthica (Souty 1980). At the onset of vitellogenesis, intercellular junctions disintegrate, and large spaces arise between neighboring FCs. These processes apparently facilitate access of the hemolymph, and consequently vitellogenins, to the oocyte surface (Souty 1980). This is also very much reminiscent of the patency formation occurring during vitellogenesis in the vast majority of insect species (reviewed in Büning 1994). In other crustaceans, penetration of hemolymph to the surface of the oocyte is secured in another way: a characteristic tubular network develops within FCs at the onset of vitellogenesis and disappears once yolk acquisition is completed. The tubules of this network are continuous with both apical and basal plasma membranes of the FCs, connecting otherwise isolated compartments: the hemolymph and the perioocytic space, i.e., the space between FCs and the oocyte surface (Arcier and Brehelin 1982, Jugan and Zerbib 1984, Criel 1989, Jaglarz et  al. 2014b). Experiments with electron-​dense tracers demonstrated that the tubular network is permeable and may indeed facilitate transfer of substances (e.g., vitellogenins and other yolk precursors) from the hemolymph into the growing oocytes ( Jugan and Zerbib 1984, Criel 1989). Such morphological specializations of the FCs were described in branchiopods (Artemia, Cyzicus, Lynceus), copepods, and several species of decapods from the family Palaemonidae (Arcier and Brehelin 1982, Blades-​Eckelbarger and Youngbluth 1984, Jugan and Zerbib 1984, Meusy and Payen 1988, Criel 1989, Jaglarz et al. 2014b). Interestingly, similar tubular networks were also reported in the basal hexapod bristletails from the order Diplura/​Campodeina (Bilinski 1983). Taken together, the available data suggest that structurally similar “epithelial transformations” that ensure uptake of yolk precursors during vitellogenesis might have evolved multiple times in distinct lineages of Pancrustacea/​Tetraconata. A comprehensive survey of the literature shows that FCs of crustaceans may fulfill several functions. For instance, ultrastructural studies in certain malacostracans revealed that FC cytoplasm contains, apart from numerous free ribosomes and mitochondria, a well-​developed endoplasmic reticulum and Golgi apparatus, indicating involvement of these cells in the active synthesis of secreted proteins (Souty 1980, Talbot and Goudeau 1988). Hence, it has been proposed that FCs contribute to the formation of the oocyte/​egg extracellular envelope, for example, in the marine isopod Idothea balthica (Souty 1980)  and in decapods Carcinus maenas, Palaemon serratus, and Homarus americanus (Goudeau and Lachaise 1980, Arcier and Brehelin 1982, Talbot and Goudeau 1988, Rosati 1995). In contrast to many hexapod groups, egg envelopes in crustaceans are usually morphologically simple and free of any surface specializations (C in Fig. 2.4). It is not surprising, therefore, that the FCs are morphologically uniform and are not diversified into distinct subpopulations. More elaborate external ornamentation is characteristic for resting eggs (or cysts) produced by many branchiopods. However, an outer shell (also termed a tertiary envelope) covering the resting eggs is secreted not by FCs but by specialized cells of an oviduct or shell glands (reviewed in Martin 1992). In addition, it has been suggested that FCs in crustaceans may fulfill endocrine functions by producing ovarian hormones or secreting vitellogenins (e.g., in Orchestia gammarella and Penaeus japonicus; reviewed in Charniaux-​Cotton 1985, Yano and Chinzei 1987). Crustacean FCs have also been implicated in a process of oosorption (see the following). Finally, it should be mentioned that the ultimate fate of FCs following ovulation might be different depending on the crustacean group: in some amphipods and decapods, FCs are retained in the ovary and are reused by joining fully grown primary follicles (so-​called secondary folliculogenesis), while in isopods, they degenerate altogether (for review, see Lopez Greco 2013 and references therein). Charniaux-​Cotton (1985) suggested that the secondary folliculogenesis is a general reproductive strategy in Malacostraca that allows accumulation of primary follicles during the period of ovarian rest and synchronization of oocyte development.

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Reproductive Biology

OOSORPTION Oosorption is defined as the interruption of the course of oogenesis, usually during the vitellogenic stage, which ultimately leads to the death of the oocytes. During oosorption, cytoplasmic constituents of oocytes are degraded and usually are absorbed by the ovarian tissue or transferred into the hemolymph. Typically, this specific reproductive strategy occurs while the oocyte or egg is still in the ovary, surrounded by follicle cells, and it may affect some or all reproductive cells in the ovary. Oocytes, which fail to leave the ovary at the time of spawning, are particularly prone to oosorption. Much of what is known on oosorption comes from the studies of oogenesis in insects (reviewed in Bell and Bohm 1975, Hinton 1981). In these arthropods, oosorption may even occur in eggs covered with chorion and already in the oviducts. Moreover, a low level of oosorption always accompanies regular oogenesis, at least in some insect species (Huebner 1981a, 1981b). It has been demonstrated that oosorption is under hormonal control and can be induced by a lack of juvenile hormone. In crustaceans, cytological aspects of oosorption are poorly understood. Studies in the crab Paratelphusa hydrodromous revealed that different yolk components undergo resorption in a reverse sequence of their appearance during yolk formation: carbohydrates are dissociated from the yolk granules (platelets) first, followed by lipids, and finally proteins (Adiyodi and Subramoniam 1983). Carayon (1941) reported that hemocytes may enter oocytes and take part in the oocyte resorption in hermit crabs. Also, phagocytes and follicle cells have been implicated in this process (Adiyodi and Subramoniam 1983, Erdman and Blake 1988, Krol et al. 1992). However, a more recent study confirmed involvement of neither hemocytes nor phagocytes in oosorption in the golden crab Chaceon fenneri (Hinsch 1992). In this species, resorption of unspawned eggs occurs by autolysis of the individual oocytes. This is also in line with the results of ultrastructural analyses of oosorption in certain insects (Bell and Bohm 1975, Asplen and Byrne 2006). It appears, therefore, that digestion of the oocytes by the lysosome-​derived enzymes and the release of the degraded components into the hemolymph may be the principle mechanism of oosorption in Pancrustacea. Studies in both insects and crustaceans indicate that various ecological and physical factors may initiate or control oosorption, including poor nutritional quality of food, starvation, absence of males, seasonal fluctuations in temperature and changes in other environmental factors, e.g., photoperiod (reviewed in Bell and Bohm 1975, Hinton 1981). Also, parasites and the aging of a female may favor increased rates of oocyte resorption. Even though oosorption inevitably reduces fecundity, it seems to present selective value by preventing loss of precious reserves normally used during oogenesis. Moreover, oosorption may enable females to better tolerate environmental stresses such as a lack of food or a suitable site for oviposition, or low temperatures. More importantly, the surviving females may still lay eggs when more favorable conditions occur. Obviously, this would be only beneficial to species with longer adult lifespans.

ENVIRONMENTAL FACTORS INFLUENCING OOGENESIS Although crustaceans are among the most widespread animals on Earth, we know surprisingly little about their reproductive biology. For instance, no reliable data exist regarding the total number of eggs produced by an individual female from various crustacean groups. Nevertheless, it has been estimated that copepods lay from a few to 50 eggs, up to several hundred eggs are brooded in terrestrial isopods, and decapods produce fewer than 50 to as many as 3 million eggs per spawn (Hines 1982, 1991, Harrison 1990). Factors influencing egg number have been well characterized in fiddler crabs. The number of eggs produced by these crustaceans may vary widely in relation to



Oogenesis in Crustaceans

latitudinal range, type of habitat, and food availability (Koga et al. 2000, Hemni 2003). The number is not only species-​specific but also varies between populations (Colpo and Negreiros-​Fransozo 2003, Castiglioni and Negreiros-​Fransozo 2005). Similar results were reported for amphipods of the genus Gammarus (Sutcliffe 1993). In crustaceans, the number of eggs produced by a female usually increases with her size, i.e., available body cavity space for egg storage, but a marked inverse correlation exists between egg size and the number of eggs per brood (Hines 1982, 1986, Glazier 2018). It has long been recognized that there is a trade-​off between the number of eggs a female can produce and egg quality, as well as the quality of offspring (Smith and Fretwell 1974, Glazier 2018). An important parameter of eggs is their size, and crustacean eggs differ considerably in size among species (Hines 1982). It is well established that egg size can be affected by factors associated with the condition of a mother (so-​called maternal effect), including the mother’s size, nutritional status, and age (reviewed in Harrison 1990, Marshall et al. 2008, Moran and McAlister 2009). In amphipods, the structure of the brood pouch constrains egg size, and species with broad oostegites produce smaller eggs than those with narrow oostegites (Steele and Steele 1991). In shrimp, egg size may vary with consecutive ovipositions (Hancock et al. 1998, Arcos et al. 2003, Racotta et al. 2003, Calado et  al. 2005). Significant intraspecific variability in egg size among broods was also found in some saltwater species of Gammarus (Sutcliffe 1993), the freshwater prawn Macrobrachium amazonicum (Odinetz-​Collart and Rabelo 1996), and the estuarine crab Chasmagnathus granulata (Giménez and Anger 2001). A positive correlation between female size and various egg traits has been shown for American and European lobsters (Homarus americanus and H. gammarus) (Attard and Hudon 1987, Wickins et al. 1995, Tully et al. 2001), the spiny lobster Jasus edwardsii (Smith and Ritar 2007), several species of crabs (Rabalais 1991, Giménez and Anger 2001, Fischer et al. 2009), three species of caridean shrimp (Clarke 1993), and the cladoceran Daphnia spp. (Lampert 1993). However, the female size–​ egg size relation cannot be extended to all crustaceans because no apparent correlation exists between these parameters in the New Zealand crab Ovalipes catharus (Haddon 1994), giant crabs Pseudocarcinus gigas (Gardner 2001), spiny lobster Panulirus marginatus (DeMartini et  al. 2003), and the blue crab Callinectes sapidus (Koopman and Siders 2013). One possible explanation for these differences might be that the observed variation in crustacean egg traits are not directly related to female size, but rather may be associated with less frequent molting cycles of larger females, which allows the investment of more energy into egg production (Ouellet and Plante 2004). It is also possible that egg formation and development in some species may be more sensitive to genetic and environmental factors than to female size. Interestingly, studies of the blue crab Callinectes sapidus showed that over reproductive lifespans, even though larger females produce larger egg clutches, smaller females produce more clutches, and the overall individual reproductive output was similar across all egg size classes (Dickinson et al. 2006). Egg size strongly correlates with a mode of embryonic development and appears to significantly influence later life history of crustaceans. For instance, several studies showed that the egg developmental time increases with egg size in related species of copepods (McLaren et al. 1969, Corkett and McLaren 1970, Corkett 1972, Vijverberg 1980). In lobsters, larger eggs with higher lipid contents yield larger larvae with better prospects of survival to adulthood (Wickins et al. 1995, Sibert et al. 2004). As a general rule, in crustaceans with small and few yolk eggs, embryogenesis is relatively short and usually leads to free-​living and planktotrophic larval stage (nauplius). In contrast, in crustacean species with larger and yolk-​rich eggs, the embryonic development is extended and the larval stage is relatively short-​lived, non-​feeding (lecitotrophic), or completely absent (Thorson 1950, Mileikovsky 1971, Steele and Steele 1975, Strathmann 1985, Wray and Raff 1991, Fischer et al. 2009). The size of the eggs has been frequently used as a good and convenient measure of energy content in marine invertebrates (McEdward and Morgan 2001). However, the estimation of energy and maternal investment based solely on egg size can be error-​prone and appears as a rather poor predictor

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Reproductive Biology of energetic capacity both across species and among taxa (reviewed in Moran and McAlister 2009). It is well established that the volume of eggs in various crustaceans may change due to the absorption of water or growth of the embryo and the expansion of the egg shell (Pandian 1970, Babu 1987, Giménez and Anger 2001, Anger et al. 2002, Figueiredo et al. 2008, Ravi and Manisseri 2013). Hence, it is not the size of the egg that matters, but its quality or composition, i.e., protein, carbohydrate and lipid content, which in turn defines the egg energy content. Vitellogenesis in crustaceans encompasses production of vitellogenin (the proteinaceous egg yolk precursor), lipovitellin (the major yolk lipoprotein), and the accumulation of various organic and inorganic components of yolk by the oocytes (for review, see Tsukimura 2001, Wilder et al. 2010, Subramoniam 2011). There is no doubt that the rate of yolk biosynthesis depends on the capacity of the oocyte and supporting somatic cells to convert yolk precursors into mature yolk. And this, in turn, is heavily dependent on the overall structure of the ovary and environmental factors (see later discussion). Proteins are considered to be the primary component of marine invertebrate eggs (Holland 1978, Pond et  al. 1996). But it is estimated that the most significant source of energy are lipids, which account for at least 60% of the total energy expenditure of developing crustacean embryos (Herring 1974, Holland 1978, Amsler and George 1984, Anger et al. 2002, Figueiredo et al. 2008). It is well documented that the level of egg energy provision affects later life history stages in decapods (reviewed in Giménez 2006). However, only a few studies have determined the energy content of individual crustacean eggs and examined the relationships among egg size, composition, and energy content. As far as chemical composition is concerned, crustacean eggs appear highly variable both intraspecifically (Attard and Hudon 1987, Anger et  al. 2002)  and interspecifically (Herring 1974, Shakuntala and Reddy 1982, Anger et al. 2002). For instance, eggs of equal size have been reported to differ in their lipid content in the Atlantic blue crab Callinectes sapidus (Amsler and George 1984). Also, intraspecific and even interpopulational variability regarding egg energy concentration have been reported in some invertebrates, including crustaceans (Mashiko 1983, Jaeckle 1995, Odinetz-​Collart and Rabelo 1996, Wehrtmann and Kattner 1998, Anger et al. 2002). Presumably, such phenotypic variation reflects adaptation to variable environmental conditions and may allow for the optimization of reproductive effort (Hadfield and Strathmann 1996, Anger et al. 2002). On the other hand, a comparison of the dry weight egg energy content value in the blue crab and American lobster reveals that the value is within a similar range (24–​27 kJ/​g dry weight) (Amsler and George 1984, Attard and Hudon 1987). This rather surprising find may suggest that egg energy content may be more uniform despite egg size differences. Such results, however, should be interpreted cautiously because the amount and ratios of different biochemical egg constituents and the role they play in embryonic and larval development are rather poorly characterized. Furthermore, underlying mechanisms that are responsible for intraspecific variation in egg size and energy investment among females remain unclear. Although the rate of vitellogenesis is affected by the genetic make-​up of an individual, it can be significantly modulated by environmental variables such as food availability (influencing maternal nutrient status), temperature, water salinity, and seasonality (reviewed in Nagaraju 2011). A comprehensive review on metazoan ovaries and vitellogenic mechanisms revealed that reproductive response to food varied greatly among species and was correlated with interspecific differences in food type, digestive kinetics, and mechanisms regulating yolk production (Eckelbarger 1994). These sources of variation may be particularly important in crustaceans which have a wide range of diets and use a tremendous variety of feeding strategies, including suspension feeding, selective deposit feeding, scavenging, herbivory, carnivory, and omnivory. However, it is the food quality, rather than type or quantity, that is important from the perspective of vitellogenesis. Much of what is known about the relationship between nutrition and reproduction comes from aquaculture studies and artificial diets formulated for panaeid shrimp. Results from these studies show that the



Oogenesis in Crustaceans

efficiency of utilizing different food components (proteins, lipids, and carbohydrates) varies enormously among species (reviewed in Harrison 1990). This is probably not surprising considering that species (or even individuals) have different capacities to respond to the same food levels and to convert food into reserve materials stored in eggs. Interspecific differences in response to food were also observed in a study of three species of amphipods reared on artificially formulated foods of varying nutritional quality (Cruz-​Rivera and Hay 2000). The study revealed that low-​nutrient foods caused a decline in the female gonad size/​fecundity in more mobile species Gammarus mucronatus and Elasmopus levis. In contrast, fecundity was not reduced in the more sedentary species Ampithoe longimana, apparently by compensatory feeding (Cruz-​Rivera and Hay 2000). Surprisingly, similar compensatory feeding behavior was ineffective to circumvent the effects of low-​quality diet in the two other mobile amphipod species studied. An intriguing question remains on how pelagic species respond to food levels in the marine environment. Copepods are the only crustaceans for which reliable data are available. It has been reported that copepods may show significant differences in their response to temporal and spatial variations in food supply. In some copepod species, egg production starts within hours after food ingestion, while in others the response may take days (reviewed in Tester and Turner 1990). Unfortunately, there is no comparative ultrastructural study of oogenesis in these species. The only study of oogenesis in pelagic copepods concerns Labidocera aestiva, which is a fast egg producer. In this species, ultrastructural analysis revealed that the oocytes accumulate yolk precursors from the hemolymph by the endocytotic mechanism (Blades-​Eckelbarger and Youngbluth 1984). Copepods have been reported to exhibit seasonal changes in egg production in response to changes in food levels (Ohman 1987). Winter females of the oceanic subantarctic copepod Neocalanus tonsus, inhabiting mesopelagic depths, store substantial lipid reserves in their bodies and use them to produce eggs, irrespective of the current food availability. Spring females, on the other hand, have only limited lipid reserves and must rely on exogenous food sources for egg production. Apart from food, temperature and light are frequently considered to be major exogenous factors affecting the breeding cycles of crustaceans, especially in terrestrial and freshwater species of the temperate zones (reviewed in Meusy and Payen 1988). Indeed, higher temperature and longer photoperiods increase reproductive activity in North American freshwater amphipods (Kruschwitz 1978). Photoperiod is known to influence ovarian development also in the crayfish Orconectes nais (Rice and Armitage 1974). However, light may have variable effects depending on the environmental context and a species pattern of reproduction. Steele and Steele (1986) reported that photoperiod had different effects on vitellogenesis in various Gammarus species. Vitellogenesis is induced by short-​day photoperiods in Gammarus setosus, a species living in high latitude and producing only one brood at the beginning of the year. In contrast, it is the longer photophase that stimulates yolk production in another species, Gammarus lawrencianus, which produces several broods throughout spring and summer. It is well established that crustacean females exposed to either low or high sublethal temperatures have decreased fertility and/​or fecundity, and many studies have indicated that temperature may affect oogenesis as well as embryonic and larval development (McLaren et al. 1969, Wear 1974, Steele and Steele 1975, Vijverberg 1980, Herzig 1983, Maier 1989, Giménez 2006). Unfortunately, there is no detailed information on how temperature influences particular stages of oogenesis. Research usually concentrates on the effect of different temperatures on egg size and the rate of development. Nonetheless, there is no doubt that ambient temperature experienced by a female may influence physiological processes associated with oogenesis (e.g., food conversion into reserve materials, rate of yolk synthesis) in ectotherm animals (reviewed in Moran and McAlister 2009). The temperature-​ mediated plasticity in egg production is well documented in insects. Studies in Drosophila revealed that temperature influences both daily and total fecundity and there is an optimal temperature range in which fecundity is highest (David et al. 1983). An investigation of the ovarian dynamics in

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Reproductive Biology butterflies indicated that stages of oogenesis may respond differently to temperature, and oocyte differentiation is more sensitive to temperature than oocyte growth (i.e., vitellogenesis) (Steigenga and Fischer 2007). As a result, a lower number of larger eggs are produced at lower temperatures. In many crustaceans (e.g., the barnacle Balanus balanoides, brachyuran crab Romaleon setosum, several species of caridean shrimps, gammarid amphipods), egg size (both dry mass and volume) increases with increasing latitude, and the factor responsible appears to be latitudinal changes in temperature (Patel and Crisp 1960, Clarke 1979, Clarke et al. 1991, Sainte-​Marie 1991, Gorny et al. 1992, Wehrtmann and Kattner 1998, Kyomo 2000, Lardies and Castilla 2001, Brante et al. 2003, 2004, Fischer et al. 2009, Baldanzi et al. 2015). It was also demonstrated that seasonal and interannual changes in temperature may affect size and chemical composition of the eggs (e.g., Sutcliffe 1993, Sibert et al. 2004, Urzúa et al. 2012). For instance, the caridean shrimp Crangon crangon produces large eggs during the winter months, while “summer” eggs are substantially smaller (Urzúa et al. 2012). Also, the total energy content of larger “winter” eggs was significantly larger than that of the small “summer” eggs. Urzúa et al. (2012) estimated that oogenesis takes substantially longer for eggs produced during the winter season than for “summer” eggs. In general, at lower temperatures, crustaceans produce larger yolk-​rich eggs, which yield larger larvae with a shorter development time. This adaptive strategy can be related to low or unpredictable food availability for larva developing in low-​temperature waters (Yampolsky and Schreiner 1996). On the other hand, at higher temperature and more favorable feeding conditions for larvae, female fecundity can be maximized by producing many small eggs (Yampolsky and Schreiner 1996). However, as studies in insects and certain crustaceans indicate, the female physiological response to temperature may be a crucial factor responsible for temperature-​egg size relationships. Also, the correlation between egg size and temperature is not universal because no such correlation has been found among populations of a sand crab Emerita analoga, collected along the coast of California (Dugan et al. 1991). Similarly, Bas et al. (2007) found no clear temperature effects on egg size in the grapsoid crab Chasmagnathus granulatus, and suggested that food quality or salinity may determine size and energy content of eggs in this species. It appears, therefore, that more experimental data are needed to better assess the effects of temperature on oogenesis and egg production in crustaceans. When considering vitellogenesis, the frequency of breeding must also be taken into account. Generally, two main strategies are adopted by animals. Some species, called semelparous or monotelic, breed only once during their lifetime, while others, called iteroparous or polytelic, breed several times, either on an annual basis (annual iteroparity) or continuously (continuous iteroparity) (reviewed in Eckelbarger 1994). Most small crustaceans are semelparous, whereas iteroparous species are found primarily among large decapod crustaceans, such as crabs and lobsters. The frequency of reproductive episodes and the pace of oogenesis are very much dependent on the type of the habitat. Long-​lived crustacean species, inhabiting relatively stable marine environments, e.g., shallow waters in temperate zones, have adopted mechanisms for slower production of eggs, relying on continuous or predictable food supplies. They have panoistic ovaries and a mixed type of vitellogenesis. In contrast, a rapid rate of oogenesis is favorable in ephemeral habitats, with alternating periods of flooding and desiccation. As a rule, the dry conditions are passed in the egg stage. Interestingly, crustaceans that live in such habitats (e.g., tadpole shrimps, clamp shrimps, freshwater fairy shrimps) have meroistic ovaries, suggesting that this type of ovary organization is advantageous in temporary habitats. It is tempting to speculate that owing to the synthetic activity of supporting nurse cells, the oocyte growth rate could be significantly accelerated in favorable environmental conditions. As has been mentioned previously, nurse cells accompanying oocytes in some crustacean species share many similarities with the oocyte and are considered to be abortive oocytes. Most importantly, nurse cells are connected to oocytes by intercellular bridges large enough to facilitate transport of macromolecules (yolk precursors) and organelles (lipid droplets, ribosomes, mitochondria) to the ooplasm. It is worth adding, in this context, that studies



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in insects have demonstrated that species with meroistic ovaries and the heterosynthetic mode of vitellogenesis have shorter oogenesis and usually produce eggs more rapidly (Büning 1994). On the other hand, oogenesis/​vitellogenesis is relatively long in insects with panoistic ovaries, and may take several months (Büning 1994). Based on what is known in insects and other animal groups, it appears that species with an autosynthetic mode of vitellogenesis usually have a slow rate of egg production and require longer periods between subsequent reproductive episodes. In contrast, species employing heterosynthesis rely on external ovary sources (e.g., hepatopancreas, fat body), accumulate yolk reserves faster, and their reproductive intervals are relatively short (for a review, see Eckelbarger 1994). Finally, it should be emphasized that the distribution of the vitellogenic strategies within Metazoa indicates that yolk precursors are delivered to developing oocytes from outside the ovary in evolutionarily more advanced animal taxa. This appears to be true also for crustaceans.

FUTURE DIRECTIONS Research on oogenesis in crustaceans suffers severely from inadequate sampling of species. In most crustacean lineages, the ultrastructural aspect of oogenesis has been studied only in a handful of species. Therefore, the pending question remains to what extent the available data can be considered representative for a particular group of Crustacea. The example of Ostracoda shows convincingly that even within a single crustacean subgroup, considerable differences may exist regarding overall ovarian organization and functioning (panoistic vs. meroistic ovaries). The necessity of expanding species coverage cannot be overemphasized. Certain aspects of oogenesis in crustaceans await clarification or reinterpretation in the light of modern understanding of cellular processes and their underlying mechanisms. Nuage material is a good example in this respect. The conventional view is that nuage participates in germline cell specification; however, it is now clear that the term nuage is applied, somewhat freely, to various accumulations of proteins and ribonucleoproteins involved in distinct cellular pathways (for review, see Voronina et al. 2011, Kloc et al. 2014). A precise analysis of the molecular composition of nuage present in the crustacean germline cells is required to sensibly relate these cytoplasmic constituents to morphologically similar structures in insects and other invertebrates. Disc-​shaped bodies are another component of developing crustacean oocytes arousing controversy. Although the origin of these characteristic structures is well-​established, their ultimate fate and role in oogenesis are still debated. To clarify the contentious issues, reliable markers are needed, which should provide researchers the ability to follow the disc-​shaped body constituents throughout oogenesis. There are also important questions left unanswered regarding female germline development, in particular, in crustacean lineages. For instance, what is the mechanism of oocyte determination in the linear germline cyst in branchiopods? How important is nurse cell contribution to oocyte development in these crustaceans? Recent research of oogenesis in various invertebrate and vertebrate species revealed that germ cells can be replenished by stem cells residing in a specific somatic microenvironment termed the germline stem cell niche (reviewed in Fuller and Spradling 2007, Hubbard 2007, Morrison and Spradling 2008, Tworzydło et al. 2010). Nothing is known on ovarian stem cells or their niche in crustaceans, although they are likely to exist, especially in species with a long reproductive lifespan. Another interesting aspect of oogenesis worth studying, but unfortunately currently completely neglected in crustaceans, is the presence of local asymmetries in the distribution of organelles (e.g., mitochondria), and macromolecules such as specific proteins and

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Reproductive Biology classes of RNAs within the ooplasm, which in other systems have been demonstrated to be vital for proper embryonic development. Standard ultrastructural research has its limitations, as does any other method. In particular, static images provided by electron micrographs should be used cautiously in the functional interpretation of cellular events. Therefore, it would be beneficial to combine electron microscopic studies with modern biochemical and molecular methods to gain a more comprehensive understanding of female gonad functioning in crustaceans. One may also expect that significant insight into the mechanisms of crustacean oogenesis could be gained by tracking various processes of oogenesis with antibodies or fluorescent-​tagged proteins, provided such markers become available. Recent innovations in biological microscopy as well as advances in imaging technology provide a new opportunity to further explore oogenesis in Crustacea. Modern methods of microscopy, such as high-​resolution confocal microscopy or transmission electron microscopy tomography, combined with computer data processing, allow us to create three-​dimensional (3D) reconstructions of cell constituents and to gain a better insight into the cytoarchitecture of germline cells. We expect that the application of novel microscopy methods to ovarian tissue analyses in crustaceans will substantially improve our understanding of important aspects of their oogenesis, such as: spatial organization of the germline cysts; relationships between various organelles participating in the process of vitellogenesis (in particular, the relationship of enigmatic disc-​shaped bodies to other organelles); mutual interactions between somatic follicle cells and germline cells; as well as 3D organization of the tubular networks penetrating the follicular epithelium in ovaries of certain crustaceans. Applying the cytoplasm extraction method combined with immuno-​labeling techniques will help to uncover the distribution of different cytoskeleton elements and elucidate their role in subsequent stages of oogenesis.

SUMMARY AND CONCLUSIONS Crustaceans are greatly diversified arthropods, and this is reflected in the variety of general ovarian architecture, as well as in certain aspects of oogenesis observed in the group (see Table 2.1). This diversity clearly manifests in the initial stages of germline development and the organization of the ovarian somatic tissue, including its interaction with the germline cells. However, striking as such morphological differences may be, they somewhat mask the fact that at least some basic aspects of crustacean oogenesis, such as a previtellogenic growth of the oocytes, are highly uniform at the ultrastructural level and conform to the general pattern of such processes in other arthropods. Also, the available data suggest that a mixed mode of yolk deposition, i.e., combined auto-​and heterosynthesis, prevails in vitellogenesis in crustacean oocytes, although the relative ratio of the two processes may differ depending on the group. There are two types of oogenesis in crustaceans:  panoistic and meroistic, each with distinct characteristics. However, crustacean meroistic ovaries appear less structurally and functionally advanced when contrasted with insect ovaries of the same type. In crustaceans, both the oocyte cytoplasmic organelles and the germinal vesicle are highly synthetically active, despite the presence of nurse cells. Recently, ovarian architecture of selected crustacean groups attracted more attention in view of the Pancrustacea/​Tetraconata hypothesis. It is becoming increasingly realized that studies of female gonads in crustaceans provide a valuable contribution to more comprehensively understand the evolutionary changes in the structure of the ovary and patterns of oogenesis in the entire Arthropoda. This may also have important phylogenetic ramifications. It is of interest in this context that a recent comparative analysis revealed significant similarities between the basal hexapods



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(Protura, Collembola, Diplura: Campodeina) and Xenocarida (Remipedia + Cephalocarida) in the gross morphology of the ovary and the structure of follicle cells ( Jaglarz et al. 2014a). Finally, it is important to emphasize that the ultrastructure of the ovary and oogenesis have been investigated comprehensively only in a rather limited number of crustacean species; therefore, the current review should be regarded as exemplifying rather than typifying particular crustacean lineages.

ACKNOWLEDGMENTS We are grateful to Rickey Cothran and Martin Thiel for providing thoughtful criticism and advice on an earlier version of the manuscript. We thank Dr. Ali Halajian (University of Limpopo, Rep. South Africa) for providing Cherax specimens, Ms. Ada Jankowska for excellent technical assistance, and the late Ms. Elżbieta Kisiel for helping with the figures. The research on crustacean oogenesis was supported by grants from the National Science Centre (NCN) (DEC-​2011/​01/​B/​ NZ4/​00595) and N18/DBS/000013.

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Reproductive Biology Tiu, S. H. K., H. L. Hui, B. Tsukimura, S. S. Tobe, J. G. He, and S. M. Chan. 2009. Cloning and expression study of the lobster (Homarus americanus) vitellogenin: conservation in gene structure among decapods. General and Comparative Endocrinology 160:36–​46. Trentini, M., and F. Scanabissi Sabelli. 1978. Ultrastructural observations on the oogenesis of Triops cancriformis (Crustacea, Notostraca). I: Origin and differentiation of nurse cells. Cell and Tissue Research 194:71–​77. Tsukimura, B. 2001. Crustacean vitellogenesis: its role in oocyte development. American Zoologist 41:465–​476. Tsutsui, N., I. Kawazoe, T. Ohira, S. Jasmani, W. J. Yang, M. N. Wilder, and K. Aida. 2000. Molecular characterization of a cDNA encoding vitellogenin and its expression in the hepatopancreas and ovary during vitellogenesis in the kuruma prawn, Penaeus japonicus. Zoological Science 17:651–​660. Tully, O., V. Roantree, and M. Robinson. 2001. Maturity, fecundity and reproductive potential of the European lobster (Homarus gammarus) in Ireland. Journal of the Marine Biology Association of United Kingdom 81:61–​68. Tworzydło, W., M. Kloc, and S. M. Bilinski. 2010. Female germline stem cell niches of earwigs are structurally simple and different from those of Drosophila melanogaster. Journal of Morphology 271:634–​640. Urzúa, A., K. Paschke, P. Gebauer, and K. Anger. 2012. Seasonal and interannual variations in size, biomass and chemical composition of the eggs of North Sea shrimp, Crangon crangon (Decapoda: Caridea). Marine Biology 159:583–​599. VanHook, A. M., and N. H. Patel. 2008. Crustaceans. Current Biology 18:R547–​R550. Vijverberg, J. 1980. Effect of temperature in laboratory studies on development and growth of Cladocera and Copepoda from Tjeukemeer, The Netherlands. Freshwater Biology 10:317–​340. von Reumont, B. M., and G. D. Edgecombe. 2020. Crustaceans and insect origins. In G. Poore, and M. Thiel, editors. The Natural History of the Crustacea, Volume 8: Evolution and Biogeography. Oxford University Press, New York. Voronina, E., G. Seydoux, P. Sassone-​Corsi, and I. Nagamori. 2011. RNA granules in germ cells. Pages 85–​111 in P. Sassone-​Corsi, M. T. Fuller, and R. Braun, editors. Germ Cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. Wägele, J. W. 1992. Isopoda. Pages 529–​617 in A. G. Humes and F. W. Harrison, editors. Microscopic Anatomy of Invertebrates, Volume 9: Crustacea. Wiley-​Liss, New York. Walldorf, V., and R. Riehl. 1985. Oogenesis in the pentastomid Raillietiella aegypti (Cephalobaenida). I: Previtellogenic and vitellogenic stages. Zeitschrift für Parasitenkunde 71:113–​124. Warrier, S., and T. Subramoniam. 2002. Receptor-​mediated yolk protein uptake in the crab Scylla serrata: crustacean vitellogenin recognizes related mammalian serum lipoproteins. Molecular Reproduction and Development 61:536–​548. Wear, R. G. 1974. Incubation in British decapod Crustacea and the effects of temperature on the rate and success of embryonic development. Journal of the Marine Biology Association of United Kingdom 54:745–​762. Wehrtmann, I. S., and G. Kattner. 1998. Changes in volume, biomass, and fatty acids of developing eggs in Nauticaris magellanica (Decapoda: Caridea): a latitudinal comparison. Journal of Crustacean Biology 18:413–​422. Wickins, J. F., T. W. Beard, and A. R. Child. 1995. Maximizing lobster, Homarus gammarus (L.), egg and larval viability. Aquaculture Research 26:379–​392. Wilder, M. N., T. Subramoniam, and K. Aida. 2002. Yolk proteins of Crustacea. Pages 131–​174 in A. S. Raikhel and T. W. Sappington, editors. Reproductive Biology of Invertebrates, Volume 12: Recent Progress in Vitellogenesis. Science, Plymouth, UK. Wilder, M. N., T. Okumura, and N. Tsutsui. 2010. Reproductive mechanisms in Crustacea focusing on selected prawn species: vitellogenin structure, processing and synthetic control. Aqua-​BioScience Monographs 3:73–​110. Wray, G. A., and R. A. Raff. 1991. The evolution of developmental strategy in marine invertebrates. Trends in Ecology and Evolution 6:45–​50. Xie, S., L. Sun, F. Liu, and B. Dong. 2009. Molecular characterization and mRNA transcript profile of vitellogenin in Chinese shrimp, Fenneropenaeus chinensis. Molecular Biology Reports 36:389–​397.



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Yampolsky, L. J., and S. M. Schreiner. 1996. Why larger offspring at lower temperatures? A demographic approach. The American Naturalist 147:86–​100. Yano, I., and Y. Chinzei. 1987. Ovary is the site of vitellogenin synthesis in kuruma prawn, Penaeus japonicus. Comparative Biochemistry and Physiology B 86:213–​218. Zeni, C., and F. Zaffagnini, 1989. Electron microscopic study on oocytes, nurse cells and yolk formation in Leptestheria dahalacensis (Crustacea, Conchostraca). Invertebrate Reproduction and Development 15:119–​129. Zerbib, C. 1977. Endocytose ovocytaire chez le Crustace Amphipode Orchestia gammarellus Pallas. Demonstration par la peroxydase. Comptes Rendus de l Academie des Sciences. Serie III, Sciences de la Vie, Paris 284:757–​760. Zerbib, C. 1980. Ultrastructural observation of oogenesis in the crustacea amphipoda Orchestia gammarellus (Pallas). Tissue and Cell 12:47–​62.

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3 FERTILIZATION SUCCESS IN CRUSTACEANS FROM THE MALE PERSPECTIVE: SPERM ULTRASTRUCTURE AND SPERM ECONOMY

Mika M. J. Tan, Christopher Tudge, Miguel A. Penna-​Díaz, and Martin Thiel

Abstract The morphology and ultrastructure of spermatozoa are very diverse among the classes of the Crustacea, but how this diversity relates to sperm production and sperm economy has been little studied. A brief description of major forms and shapes of crustacean spermatozoa is provided and an overview of sperm ultrastructure is updated. Spermatogenesis is a costly process for males, as it requires considerable energy and time to achieve the required quality and quantity to guarantee success in fertilizing the eggs of females. Sperm are embedded in seminal fluids to preserve stored sperm and/​or counteract the risk of sperm competition, which contributes significantly to the energy budget and sperm economy. In general, sperm are transferred in spermatophores of very diverse sizes and shapes within the different crustacean groups. Strategies related to sperm economy depend on the physical size of the partner, mating history, and perception of future mating opportunities. The mechanics involved in spermatogenesis and production of seminal fluids vary among the different crustacean classes and between different taxa. Sperm economy has direct links to sperm limitation in several male-​centered fisheries. To better understand the evolutionary processes and to design suitable applied strategies (e.g., fisheries management or aquaculture), better knowledge is required about sperm histochemistry and functional morphology; furthermore, a wider taxonomic coverage is recommended by including commercial and non-​commercial crustaceans beyond the decapods.

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Sperm Ultrastructure and Sperm Economy

INTRODUCTION Studies of spermatozoa began more than three centuries ago. It started in 1676 by Anton Leeuwenhoek, who inspected his own spermatozoa with a self-​constructed optical lens (Birkhead et al. 2009). Later, when optical light microscopy technologies improved, a wide diversity of taxa was studied and new hypotheses about the evolution of sperm structure and function emerged (Birkhead and Montgomery 2009). Research on crustacean spermatozoa took off in the previous century (see Klaus et al. 2009, Tudge 2009), and over the past half-​century, with modern microscopy techniques, enormous progress in our knowledge of sperm ultrastructure has been made (Pochon-​Masson 1983, Jamieson 1987, 1991a, 1991b). Sperm morphology in Crustacea is highly diverse, but the common “aquasperm,” found in many aquatic organisms, is very rare in arthropods (Mann 1984, Jamieson 1986, Jamieson and Rouse 1989, Vogt 2016). The majority of the Crustacea have introsperm, which generally are non-​motile because spermatozoa in most groups are aflagellate (Mann 1984, Jamieson 1991a). The production of spermatophores (sperm packages with variable amounts of seminal fluids produced by the vas deferens; Bauer 1991, Hinsch 1991, Subramoniam 1991, 1993, López Greco 2013) is common across the Crustacea. Spermatophores have diverse functionality that goes beyond the mere packaging of spermatozoa (Mann 1984). Some aflagellate sperm can be motile due to contractile elements in their ultrastructure, resulting in longitudinal rotation of the entire sperm (Matzke-​Karasz et al. 2017), which may compensate for the lack of the flagellum and contribute to mechanical penetration of the egg (Vogt 2016). Particular record holders are found among the crustaceans, such as the largest sperm in relation to body size in the class Ostracoda, or the particularly unusual explosive-​ like spermatozoa in the Decapoda (Vogt 2016). It is not easily understood why so many different and exotic sperm morphologies have evolved, especially when these are energetically costly to produce, e.g., the enormously large (and predictably) costly sperm in ostracods (Vogt 2016); but it is possible that these diverse morphologies are related to the post-​copulatory sperm-​selection process (Snook 2005). Traditional knowledge about spermatogenesis generalized the process as cheap for the males, but arthropods are very different in comparison with other taxa. In the case of the Crustacea, spermatogenesis and production of seminal fluids differ between classes and genera (Subramoniam 1991, López Greco 2013), and recovery of sperm reserves depends directly on the mating history (Hinojosa and Thiel 2003), the size of the male or his mate (Rubolini et al. 2007, Smith et al. 2016a, 2016b), competition (Sato and Goshima 2007a), future mating opportunities ( Jivoff 2003, Hinojosa and Thiel 2003), and sperm competition (Parker and Pizzari 2010). Spermatogenesis and the conformation of spermatophores are not necessarily related to the intermolt cycle and seem to be continuous even in captive males under intensive culture (Heitzmann and Diter. 1993). The generation of spermatophores can take several months depending on the species (Heitzmann and Diter et  al. 1993). For others, the regeneration time is significantly less (e.g., Homarus americanus; Waddy et al. 2017), but also depends on environmental conditions that can influence sperm quality (Heitzmann et al. 1993, Harlıoğlu et al. 2018). How the shape and size of sperm are linked to the production of sperm in crustaceans is not well known. In this chapter we make a first attempt to relate sperm morphology and ultrastructure to the processes of spermatogenesis and spermatophore production. We also review how males exercise sperm economy to maximize lifetime reproductive success.

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SPERMATOZOAL ULTRASTRUCTURE AND DIVERSITY The phylum Arthropoda has incredible somatic morphological diversity, in size, segmentation, and appendage development and use (e.g., Schram 2013, Bauer 2013). The sperm cell types in this phylum are equally diverse, with atypical and aflagellate spermatozoa being common and convergently evolved in many disparate groups of arthropods. Fully flagellate (free-​swimming) spermatozoa are actually rare, even though the flagellate spermatozoon is considered to be plesiomorphic for the Arthropoda (Baccetti 1979, Jamieson 1987, 1991a). This plesiomorphic flagellate sperm cell (the “aquasperm” of Jamieson 1986 and Jamieson and Rouse 1989) occurs in only six chelicerate orders at the base of the arthropod phylogenetic tree (as both ect-​aquasperm and ent-​aquasperm), being replaced in all other parts of the tree by highly modified introsperm. Crustacean spermatozoa have been studied for more than 100 years (Klaus et al. 2009, Tudge 2009), and sperm diversity within this subphylum rivals that of the phylum Arthropoda. Crustacean sperm cells are so baffling in their diversity of form that Jamieson wrote in his seminal work on insect spermatozoa ( Jamieson 1987, p. 16): “Although the sperm of the Crustacea reflect very well the distinctness and internal unity of its major subgroups, they give no clear indication of relationship of Crustacea with uniramians nor, in fact, do they provide clues as to relationships with any other phylum.” This great diversity in sperm morphology in crustaceans makes it difficult, in fact practically impossible, to describe a typical crustacean sperm cell. As with the other arthropods, the plesiomorphic state was most likely a flagellate and motile sperm cell, but not a simple aquasperm. With the exception of the xiphosurans (horseshoe crabs), a flagellate spermatozoon broadcast into seawater for external fertilization does not exist in the arthropods, but many other examples of flagellate swimming sperm delivered into the female via insemination or spermatophore (externally or internally deposited) occur. Such directly deposited spermatozoa, especially inside spermatophores, would have pre-​adapted many arthropod groups, including crustaceans, for their later move to freshwater and terrestrial environments. Derivatives of this basal aquasperm form have led in nearly all crustacean classes to more derived flagellate or pseudo-​flagellate introsperm, and even to highly modified aflagellate and immotile introsperm in several classes, including the Branchiopoda and Malacostraca. Of all crustacean groups, the decapods have been most extensively studied, with the majority of the spermatozoal literature published in the last two decades covering 100% of the decapod infraorders, 50% of the families, and approximately 10% of the extant genera, though this represents only 2%–​3% of the described, extant decapod species (last reviewed by Tudge 2009). Within particular crustacean groups, though, characteristic spermatozoal forms can be identified (Fig. 3.1). For example, decapod sperm lack a true flagellum, are non-​motile, have large, spherical, or oblong-​ovoid, often concentrically arranged, acrosome vesicles and diminutive decondensed nuclei with reduced and unique nuclear proteins (Tudge 2009). On the other hand, mystacocaridans, branchiurans, ascothoracidans, and cirripedes have distinctive, elongate flagellate sperm (Grygier 1982) while all branchiopods thus far described for spermatozoal morphology have often large, amorphous, amoeboid sperm cells, sometimes with radiating spines, rods, or axopods (Wingstrand 1978). As previously mentioned, the use of sealed packages of spermatozoa (= spermatophores) is fairly common in the animal kingdom (Mann 1984), more dominant in the Arthropoda, and the principal form of sperm transfer in the Crustacea. As with any arthropod, the spermatophores of crustaceans are not only pre-​adaptive for habitat expansion into freshwater and terrestrial environments, but also allow for storage of viable sperm cells for short or long periods, both in the external environment or on or inside the female reproductive system. This allows some groups to retain external sperm deposition and fertilization even in challenging terrestrial or freshwater environments. In general, spermatophores serve multiple functions in animals, and many of these roles are



Sperm Ultrastructure and Sperm Economy Spermatozoa morphology

Miracrustacea

Introsperm

Altocrustacea

Ent - Aquasperm Ect - Aquasperm

+

Hexapoda Xenocarida

Aflagellate

Communocostraca Multicrustacea Vericrustacea

Remipedia Cephalocarida Thecostraca Malacostraca

+

Copepoda

Pancrustacea

Branchiopoda Ichthyostraca

Pentastomida Branchiura

Oligostraca

Mystacocarida Ostracoda

Mandibulata

Myodocopa Podocopa

Arthropoda

Myriapoda Chelicerata

+

Euchelicerata Pycnogonida

Fig. 3.1. Phylogeny of the main groups of the Crustacea related to the characteristic spermatozoa morphology. Summary diagram of higher-​level arthropod relationships. Based on Regier et al. (2010).   

documented for arthropods and crustaceans. The multiple functions include providing a transport mechanism for groups of spermatozoa, protecting sperm cells, minimizing sperm cell loss, and providing a storage container for both short-​term and long-​term holding of spermatozoa, either inside the female reproductive system, on the outside of the female body, or on the substratum or a spun web (the latter is common in terrestrial arthropods). Additional roles attributed to spermatophores are:  as copulatory plugs preventing further male insemination of a female, as aphrodisiacs for stimulating female egg laying and insemination, as a nutritional source for the female for later egg development, and even a sperm cell maturation or capacitation role much like the function of a male epididymis (Mann 1984). The diversity of spermatophore size and form in the Crustacea is very impressive, and in some cases can be phylogenetically informative (for example, Tudge 1991, 1999a, 1999b, Tudge and Jamieson 1996a, 1996b). It is possible that the great sperm cell diversity in the Crustacea, and also the Arthropoda, could be the result of a relaxation of the functional evolutionary constraint placed on swimming aquasperm, by the packaging into distinct spermatophores. This then possibly shifted the evolutionary pressure onto the somatic morphology associated with sperm transfer and the subcellular ultrastructure and biochemistry, both of which are equally diverse in the arthropods and crustaceans, and in the latter case could drive development of bizarre sperm cells. It can be imagined that simple swimming aquasperm, common to many animal groups such as sponges, cnidarians, some polychaetes, and even fishes ( Jamieson, 1991b), have engineering and hydrodynamic constraints on the shape and function of the sperm cell. These aquasperm often have small spherical to ovoid sperm heads composed of a compact nucleus with a small apical acrosome vesicle and a set of basal mitochondria to drive the posterior axoneme or flagellum. This design is adapted for fast swimming motion through the relatively “thin” liquid medium of seawater as they

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Reproductive Biology are broadcast into this aquatic environment to seek out the often free-​floating eggs. Any modification in fertilization biology that moves the fertilization event inside the body of the female, whether into a brood chamber, coelom, or inside the female reproductive system, requires the sperm cells to swim in a changed, often more viscous, environment and to be delivered in close proximity to the eggs. This change in environment now requires a change in sperm cell morphology, often necessitating the development of a more elongate, fibrillar, more-​streamlined flagellate spermatozoon, i.e., the introsperm. The sperm cell usually has a thin, elongate nucleus, capped by a thin, close-​ fitting acrosome vesicle, and the mitochondria are similarly extended into a sheath-​like mid-​piece, tapering to a long flagellum. The more viscous medium constrains the sperm cell to a different swimming motion, whereby the cell undulates gently along its entire length (sperm head and mid-​piece included), slowly corkscrewing around its central axis. This is in contrast to the rapid thrashing of simpler aquasperm, where a shorter flagellum beats exaggeratedly from side to side, driving the immobile head in front of it. This progression of sperm cell morphology from aquasperm to introsperm is well demonstrated for several invertebrate groups, such as the Polychaeta ( Jamieson and Rouse 1989) and Gastropoda (Healy 1988). The development of bundles of these elongate introsperm being aggregated together and bound and delivered as a unit into the female system, the spermatozeugmata (sperm bundles) and spermatophores of Mann (1984), further relieved the functional constraint of swimming to fertilize eggs. This would allow for the loss of sperm motility, and consequently, the loss of the engine (the axoneme) and the power source (the mitochondria) and perhaps exaggerate the nucleus and acrosome vesicle components. These spermatophore-​enclosed sperm cells now cannot swim to meet the egg, but must be delivered to the site of fertilization, either on the outside of or inside the female. The immotile spermatozoa, lacking flagella and functional mitochondria, are essentially just sperm heads, and the selection pressure is switched to the egg recognition organelle (acrosome) and the fertilizing nucleus, sometimes driving extreme morphological and biochemical evolution. Some cases in point in the Arthropoda include the bizarre sperm cells described for the chelicerate ticks and mites, the myriapod millipedes ( Jamieson 1987), and in the Crustacea the branchiopods, copepods, and decapods ( Jamieson 1991a, Jamieson and Tudge 2000). In the decapod Crustacea, for example, the acrosome vesicle has increased in size to dominate the mass of the sperm cell, and the nucleus has been reduced in size and complexity, and all other organelles, like the flagellum, mitochondria, and the rest of the cytoplasm, have virtually disappeared (Tudge 2009). The spermatozoon is essentially a non-​swimming acrosome carrying a trimmed-​down package of chromatin. These compact sperm cells are efficiently packaged into complex spermatophores and are delivered to the external simple receptacles recessed into the ventral surface of the female, or completely internalized into the female reproductive system, which is highly modified to receive and store the spermatophores and spermatozoa. At ovulation the immotile sperm cells are exposed to the passing eggs inside the female system or as they emerge from the female system and are externalized. Apart from egg membrane and acrosome membrane interaction and the penetration of the egg by the sperm cell and accompanying chromatin, no other activity is required of the immotile spermatozoa. This remarkably inert interaction between sperm cell and egg is likely the reason for the drastic reduction of sperm cell function and morphology, and the consequent increase in acrosome complexity, in this fascinating crustacean group. This unique sperm cell morphology of the Decapoda does appear to be largely constrained by phylogeny, though, as the complex acrosome vesicles retain plenty of phylogenetic signal at the ultrastructural level (for fine examples of modern spermiotaxonomy, see Braga et al. 2013, Tudge et al. 2014, Assugeni et al. 2017, Camargo et al. 2018). One mystery left to be explained in decapod spermatozoa is the common development of multiple microtubular or nuclear arms, emerging laterally from the spermatozoon, and being highly variable in number across the major groups (Tudge 2009, Antunes et al. 2018). These lateral arms can



Sperm Ultrastructure and Sperm Economy

be made of thin extensions of the nucleus, bundles of microtubules, or a combination of both. The microtubular bundles are not arranged in the typical axonemal pattern for motility, and in fact, no definitive motility has ever been described for any decapod sperm cell lateral arm. So, it is obvious that the sperm cells do not swim or crawl with them. What function can be ascribed to these conspicuous organelles of decapod sperm? When tightly packed inside the decapod spermatophore, in its many forms, the lateral arms of the sperm cells are usually wrapped around each cell, and only extend out straight, and laterally, when the sperm cells are exposed to seawater, secretions of the female reproductive system, or are generally released from the spermatophore into any more liquid medium. The three or more conspicuous lateral arms when fully extended away from the main body of the spermatozoon give the cell a star-​like or stellate appearance (see also G in Fig. 3.2), prompting them to be labeled as such by early spermatologists (Kolliker 1841, Retzius 1909), and this descriptive terminology remains in use today (Braga et al. 2013). But, irrespective of their multi-​spined C D

B E

K

A L

F G J

H

M I O

P Q N

Fig. 3.2. Diagrammatic representations of general sperm morphology in various crustacean groups. (A)  Giant ostracod sperm. (B) “Umbrella” sperm of caridean shrimp Rhynchocinetes. (C) Branchiopod sperm. (D) Mysid sperm. (E) Stomatopod sperm. (F) Cephalocarid sperm. (G) Copepod sperm. (H) Sicyonid shrimp sperm. (I)  Lithodid crab sperm. ( J)  Paleomonid shrimp sperm. (K)  Dromiid crab sperm. (L)  Tanaid sperm. (M)  Astacid crayfish sperm. (N)  Potamonautid crab sperm. (O)  Mole crab Emerita sperm. (P)  Sergestid shrimp sperm. (Q) Remipede sperm. Sperm cells not to scale. Figures D, E, F, G, L and Q are modified after Jamieson (1991a); H and P are modified after Jamieson and Tudge (2000). Figures A, B, C, I, J, K, M, N, and O are original.   

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Reproductive Biology beauty (Fig. 3.2), what function do they serve? The loss of the functional flagellum and mitochondrial mid-​piece from a swimming sperm cell also robs the cell of any directionality or polarity. On a swimming cell, the acrosomal end or pole will always be projected in front of the swimming cell and will contact the egg membrane first. This polarity is lost when the cell becomes spheroidal to ovoid and immotile. The inert spermatozoon can randomly contact an adjacent egg membrane at any point on the surface area of the cell, and probability suggests that the contact would not occur at the apical point of the acrosome, the operculum, which is designed for this initial contact and recognition. The opercular surface area for egg attachment is therefore very small and, in many cases, would miss being the first to contact the egg surface. But, the development of large, long, lateral arms on the spheroidal or ovoid sperm cells, and especially projecting these from the midpoint of the sperm cell where the large, concentrically zoned, complex acrosome vesicle meets the meager cytoplasmic and nuclear material, would impose a simple bipolarity to the cell. The stellate sperm cell now has an acrosomal pole, capped by the reactive operculum, and an anacrosomal pole, where the nucleus dominates (Fig. 3.2). The chances of the operculum randomly meeting the egg membrane have now been increased to 50%, much higher than the previous small chance of a tiny operculum on the outer surface of a spherical cell. If the lateral arms are long, as well, then they may contact the egg first and bring the main body of the sperm into contact with the egg membrane. There is no empirical evidence to support this hypothesis, but there must be multiple ways that one could test it with decapod sperm cells. It is obvious that the lateral arms, although very common, are not critical to fertilization, because there are several groups of crustaceans that have spherical sperm cells with small acrosome vesicles, which achieve fertilization adequately without any arms or extensions. These include stomatopods, euphausids, and even some dendrobranchiate shrimps ( Jamieson and Tudge 2000).

SPERM MORPHOLOGY, GENERATION TIME, AND FERTILIZATION ENVIRONMENT In spite of the volumes of literature published on crustacean spermatology over the past 100 years, there are still several important areas of investigation that remain as yet underexplored, and in some instances unexplored. This is surprising considering the impact that answers to the following questions would have on commercial crustacean aquaculture, crustacean fisheries management, and even conservation and recovery of threatened crustacean species. For example, is there a link between spermatozoal complexity, size, and ultrastructure and regeneration time in males after deposition or insemination, and the availability of adequate sperm cell reserves for multiple matings? Similarly, do more complex sperm cells (ultrastructurally), or larger sperm cells, affect male sperm economy and perhaps promote earlier sperm limitation? More basically, is there a cost to males if they invest in larger or morphologically complex spermatozoa? Do larger males invest in larger sperm cells, or do they simply invest in many more sperm cells of the same size and complexity to out-​compete rivals? If the size and morphology of spermatozoa are phylogenetically constrained within a crustacean group, do the males then have to rely on other anatomical, physiological, or behavioral adaptations (e.g., spermatophores with large quantities of seminal fluids) to gain the upper hand, and achieve more fertilizations? The incredible sperm cell diversity recorded in the Crustacea, and outlined in the preceding, would necessitate that investigations into such questions would need to be done within specific groups of crustaceans and not compared across different groups. For example, questions of sperm cell regeneration times after depletion could be investigated in three species of commercial shrimp with males of the same age and body mass but with different sperm cell sizes and morphology/​ ultrastructural complexity. Other commercial crustacean species, with well-​known reproductive



Sperm Ultrastructure and Sperm Economy

biology, could also be investigated to look at sperm economy and sperm limitation after multiple mating opportunities. Some of this research has already been addressed for several commercial decapods, including brachyurans (Hines et  al. 2003, Xuan et  al. 2014, Pardo et  al. 2015), spiny lobsters (MacDiarmid and Butler 1999, Robertson and Butler 2013), and anomurans (Sato 2011, Sato and Goshima 2006, 2007a, 2007b, 2007c, Sato et al. 2006, 2008, 2010), but the connection to sperm cell size and complexity has not been directly investigated. In some ostracod species, which produce giant sperm, variability in sperm length is high, and it has been suggested that sperm of different sizes belong to different age groups (Smith et al. 2016a, 2016b). Similarly, large males, which have a higher potential for copulation, might produce more short sperm than small males; and small males might produce large sperm advantageous in sperm competition given their limi­ ted mating opportunities. Since in ostracods the production of giant sperm requires substantial resources, each male (or species) is expected to optimize the sperm length that offers the best return for the given resource investment (Smith et al. 2016a, 2016b). In general, though, spermatozoa are of a remarkably consistent size and ultrastructure within a single male ejaculate and within all males of a species (e.g., Paschoal and Zara 2018), and one does not start to see differences in these two parameters until species within genera are compared (Vogt 2016, Guinot et al. 1997, Benetti et al. 2008) or more significantly when comparisons are made between different genera (Tudge et al. 1998, 1999). Crustacean sperm are packaged in spermatophores that often contain large amounts of seminal fluids (López Greco 2013, Vogt 2018). Seminal secretions are formed in the vas deferens, where sperm are packaged in dense layers of seminal fluids (e.g., Zara et al. 2012, Antunes et al. 2018, Feng et al. 2018, Garcia Bento et al. 2018). The seminal fluids contain mainly glycoproteins, proteins, lipids, and mucopolysaccharides (Subramoniam 1991, Feng et al. 2018, De Oliveira and Zara 2018, Bento et al. 2018). These substances are important in sperm maintenance and activation (e.g., Alfaro-​Montoya et al. 2017); additionally, the seminal fluids have accessory uses by providing nutrients for sperm storage inside or on the female (Hinton 1974) and additional compounds, such as phenols, that may have antibacterial functions (Subramoniam 1991, Jayasankar and Subramoniam 1999, López Greco 2013 and references therein). Seminal fluids may also displace rival sperm in the female’s reproductive tract (Parker and Pizzari 2010, see also “Recent Mating History and Mating Order” section later in this chapter), and it has been proposed that the seminal plasma forms part of the sperm plug that helps retain sperm transferred to a female, as well as preventing other males from depositing more sperm (Hartnoll 1969). In the penaeid Litopenaeus vannamei, important changes in the spermatozoa occur after spermatophore transfer to the female, which may be media­ted by the seminal fluids (Alfaro-​Montoya et al. 2017). In the free-​swimming spermatozoa of the Ostracoda, the giant spermatozoa are immotile when they are produced in the male but release a coat that is thought to dissolve inside the female’s seminal receptacles in order for the sperm to gain motility (Matzke-​ Karasz et al. 2017). These motile spermatozoa can then penetrate the egg and fertilize them during oviposition (Vogt 2018).

INCREASING FERTILIZATION SUCCESS THROUGH SPERM ECONOMY Since spermatogenesis involves non-​trivial energetic costs, and sperm competition and other factors affect optimal ejaculate expenditure, many males exercise sperm economy to maximize overall lifetime reproductive success (Wedell et al. 2002). In other words, males adjust their ejaculate allocation according to various factors, such as female size, risk of sperm competition, and recent mating history, so that they will have the highest chances of inseminating the greatest number of eggs. Moreover, ejaculation of sperm not only carries energetic costs of production, but also of lost opportunity (MacDiarmid and Butler IV 1999). Especially in species with short or limited breeding

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Reproductive Biology seasons (e.g., blue crab Callinectes sapidus; Kendall et al. 2001), costs to males associated with lost mating opportunities due to insufficient time to recharge sperm stores can be high; hence, it is more prudent for males to exercise sperm economy to inseminate the greatest number of females. The ability of males to regulate the size of their ejaculate according to social circumstances has been demonstrated in species as diverse as humans, rats, insects, birds, and crustaceans (MacDiarmid and Butler IV 1999, and references therein). Theories of ejaculate economics are extensive and predict sperm-​allocation strategies of males in given conditions at the individual (e.g., recent mating history) and population level (e.g., sperm competition; for a review of models of sperm competition games, see Parker and Pizzari 2010). Herein, we review the often-​interrelated factors that affect sperm allocation and economy in crustaceans. Male Size and Sperm Competition Sperm competition is a widespread phenomenon that occurs when sperm from two or more males compete for a given set of ova (Parker 1998). Crustaceans have been shown to modulate their sperm allocation based on risk of sperm competition (e.g., Rondeau and Sainte-​Marie 2001, Hinojosa and Thiel 2003, Jivoff 2003, Pardo et  al. 2018). In the presence of potential rivals, males increase the number of ejaculated sperm (Sato and Goshima 2007a) and also guard females longer ( Jivoff 1997a, Rondeau and Sainte-​Marie 2001, see Chapter 12 in this volume). Larger males tend to face lower risk of sperm competition, as they are better able to attract and guard mates than smaller males, and in some species may be socially dominant with greater access (and possibly exclusivity) to reproductive females (e.g., Sainte-​Marie et al. 1999, Goshima et al. 2000, Jivoff 2003, Sainte-​Marie 2007). Moreover, during any given reproductive period, smaller males may, at the expense of sperm production, allocate surplus energy to somatic growth to increase body size for greater reproductive success at subsequent reproductive periods (Hinojosa and Thiel 2003). Therefore, one might expect larger males to produce more sperm than smaller males. Indeed, there is evidence that larger males pass more sperm to females than smaller males (e.g., Jivoff 2003, Sato et al. 2010). For example, in the crab Metacarcinus edwardsii the ejaculates transferred to females by larger males were larger than those by smaller males, but this difference was due to relatively large amounts of seminal fluids, rather than sperm (Pardo et al. 2018). However, precisely because mating opportunities afforded to smaller males are often limited due to the actions of larger, more competitive males, they allocate relatively more sperm during each mating opportunity to win fertilizations. Hinojosa and Thiel (2003) found that in rock shrimp Rhynchocinetes typus, dominance status and the imminent risk of sperm competition have strong effects on sperm investment of a given male during a single mating. Subordinate males that face a high risk of sperm competition invested substantial amounts of sperm in a single mating to dilute sperm investments of potential competitors, whereas larger robustus males (that face lower sperm competition) invested a relatively small number of spermatophores during the first mating opportunity (graph a in Fig. 3.3). The subordinate R. typus males, however, greatly diminished their sperm reserves after the first mating and transferred significantly fewer spermatophores at subsequent mating opportunities, or completely failed to mate (graph a in Fig. 3.3). It is also worth noting that, in absolute terms, larger males may still transfer more sperm than smaller males do, but these often represent a smaller share of their total sperm reserves (Gosselin et al. 2003). Larger males in some species are also capable of replenishing sperm reserves more quickly than smaller males (Sato and Goshima 2006, Lemaître et al. 2009, Sato et al. 2010, Fig. 3.4). However, these larger, more attractive males tend to mate more frequently, and multiple copulations in rapid succession without sufficient time for sperm recovery may ultimately result in them being in a constant state of sperm depletion compared to their subordinate peers (e.g., Rondeau and Sainte-​Marie 2001, see also later in this chapter).



Sperm Ultrastructure and Sperm Economy (A) Number of spermatophores per mating opportunity

12 10 8 6 4 2 ab

bb

bb

bb

bb

1

2

3

4

5

0 Successive matings

Multiple matings realized

(B)

6 5 4 3 2 1 0

Typus

Robustus

Fig. 3.3. Rhynchocinetes typus. (a)  Number of spermatophores transferred by subordinate typus (○) and dominant robustus (●) males during five consecutive mating opportunities. Data points marked with a cross were not included in statistical analysis, because females did not produce viable offspring; two-​way ANOVA with unequal replication, followed by post-​hoc Tukey, treatments that did not differ significantly are marked by the same letters. (b) Average number (±SE) of multiple matings realized by subordinate typus and dominant robustus males that were offered the opportunity to mate five times consecutively. From Hinojosa and Thiel (2003) with permission from © Elsevier.   

An interesting case with opposing evidence occurs in the freshwater crayfish Austropotamobius italicus, a species with external fertilization and a coercive mating system (i.e., males force females to copulate; Rubolini et al. 2007). Rubolini et al. (2006, 2007) found that ejaculate size decreased with increasing male size, and that larger males also mated with fewer females compared to smaller males. In this case, larger, and hence older, males may experience age-​related decline in reproductive performance. Female Size and Fecundity Female size, condition, and size at maturity affect fecundity and the maximum number of eggs that can be produced (MacDiarmid and Butler IV 1999). In many decapod species, larger females are capable of producing more and larger eggs, and these females often receive more sperm than their smaller counterparts (e.g., spiny lobster Panulirus argus: MacDiarmid and Butler IV 1999, snow crab

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70

12

9 CL 9–10 mm

10

CL 13–14 mm

b 6

8 6

10

a 5

4 2 0

6 unmated

5 0

a 5

a 5 5 5

10

5 20

Number of days after depletion

Fig. 3.4. Hapalogaster dentata. Recovery rate of sperm in males of different carapace lengths (CL). Number of sperm in the vasa deferentia of males differing in body size, and number of sperm in the vasa deferentia of unmated males. Different letters and numbers above columns indicate significant differences and sample size, respectively. From Sato and Goshima (2006) with permission.   

Chionoecetes opilio:  Rondeau and Sainte-​Marie 2001, Sainte-​Marie et  al. 2002, American lobster Homarus americanus: Gosselin et al. 2003). This pattern suggests that males alter their sperm allocation according to female size because it is often a good indicator of relative fecundity (Wedell et al. 2002). Moreover, larger females may also provide greater fertilization returns per unit sperm passed to the female, as evidenced by Hapalogaster dentata females, where egg-​to-​sperm ratio significantly increases with female body size (Sato and Goshima 2007c). In that study, large males also did not mate when presented with small females (with low egg-​to-​sperm ratio) even though smaller males did mate, indicating that large males were selective about mate choice, preferring larger females to efficiently make use of limited sperm reserves. It has been shown, however, that in some cases sperm allocation is only weakly correlated with female size in smaller males (e.g., MacDiarmid and Butler IV 1999, Hinojosa and Thiel 2003, Sato and Goshima 2007a), even though larger males in the respective investigations proportionately allocated sperm according to female size (Fig. 3.5). This indicates that small males may have limited capacity to increase the amount of sperm to match the size (and perceived fecundity) of their partner. Recent Mating History and Mating Order Whether a partner has recently mated can have direct effects on sperm allocation and fertilization chances for the choosing individual, as well as the chosen individual ( Jivoff 2003, Mellan et al. 2014). This applies to both males and females; for a female, a male’s recent mating history may indicate his ability or willingness to provide sperm, especially if males mate more frequently than reproductive resources can be replenished; for a male, signs of prior mating in a female partner (e.g., presence of attached spermatophores) provide clues about the level of sperm competition and his chances of fertilization success. The number of times a male has mated in succession, as well as the time between matings, significantly affects the number of sperm passed to a female in many crustaceans. In general, if sperm ejaculated per mating represents a significant proportion of sperm reserves (e.g., 47% in blue crab Callinectes sapidus:  Jivoff 1997b, and ~50% in Gammarus pulex:  Lemaître et  al. 2009), and if the time between consecutive copulations is insufficient for adequate sperm recovery, males cannot

Sperm Ultrastructure and Sperm Economy No. of ejaculated sperm (× 105)

6

10

Small male Large male

4 10

9

11

2

0

Small female

Large female

Fig. 3.5. Hapalogaster dentata. Effects of male and female size on the average number (± SE) of ejaculated sperm. Small males did not allocate more sperm to larger females, while large males did. Numbers above the bars indicate the number of replicates. Redrawn after Sato and Goshima (2007a) with permission from © Oxford University Press.   

equally inseminate subsequent females and deposit fewer sperm at successive matings. This has been documented in several decapod species (e.g., blue crab: Jivoff 2003, crayfish: Rubolini et al. 2007, Mellan et al. 2014, rock shrimp: Hinojosa and Thiel 2003, coconut crab: Sato et al. 2010), the amphipod Gammarus duebeni (Dunn et al. 2006), and the terrestrial isopod Armadillidium vulgare (Rigaud and Moreau 2004), among others (see Table 3.1). Smaller males with smaller sperm reserves hence inseminate fewer females over time than larger males (Hinojosa and Thiel 2003). The most sperm-​depleted males may not even attempt to mate (Carver et al. 2005). While sperm depletion after repeated mating has been reported for many crustaceans (Kendall et al. 2001, Sato et al. 2005), in the American lobster, Homarus americanus, males can fertilize impressive numbers of females (up to 54 females in 131 days) during a single reproductive season (Waddy et al. 2017). There was no indication of decreasing fertilization potential as females that were fertilized late in the season, after males had inseminated multiple other females, also had complete broods. How lobsters achieve this high fertilization potential and the mechanisms of continuing spermatogenesis throughout the reproductive season are not well known. That study also indicated that during the time of their molt, male lobsters dramatically reduced their mating activity (Waddy et al. 2017), possibly because their sperm reserves are depleted due to investment in growth. Also, in the shrimp Litopenaeus vannamei males reduce mating activity during their molt (Parnes et al. 2006). Interestingly, after a simulated mating, in Farfantepenaeus brasiliensis spermatophores were replaced much faster in males that molted than in those males that did not molt (Braga et al. 2014). Besides sperm, recently mated males may also provide less seminal fluid than those allowed time to recover reserves (Kendall et al. 2001, Carver et al. 2005). Seminal fluid is an important component of reproductive success; it is the medium in which sperm is transferred, and larger ejaculates with more accessory fluid can better displace rival sperm in a female’s reproductive tract. Hence, in most crustaceans recently mated males with depleted reserves are unable to provide large ejaculate volume (consisting of sperm and seminal fluid), leading to lower reproductive success. Indeed, the number of offspring produced by amphipod G. duebeni females significantly decreased when mated with males who had mated three times, as compared to males who had mated only once or twice (Dunn et al. 2006). Sato and Goshima (2006) also showed that male size interacted with mating history such that female reproductive success decreased with successive mating attempts, and this decrease was more pronounced with smaller males than with larger males (Fig. 3.6). It then stands to reason that females should favor virgin males (or males who have not recently mated) that would be able to provide them with the greatest number of sperm over recently

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LM > SM

LM > SM overall, but subordinate males provided more sperm at first mating

Rhynchocinetes typus

Male Size and Sperm Competition LM > SM Males provided more sperm and guarded females longer with increasing sperm competition Males provided more sperm and guarded females longer with increasing sperm competition LM > SM

Panulirus argus

Jasus edwardsii

Callinectes sapidus

Chionoecetes opilio

Species

LF > SF, but only from larger males

LF > SF, especially from larger males LF > SF, especially from larger males

LF > SF

LF > SF

Female Size

Typus males significantly exhausted sperm reserves, but not robustus males

ND

ND

Second inseminating males passed larger ejaculates than the first male

Recent Mating History Males expended more sperm with previously mated females than virgin females

Table 3.1  Examples of the Main Factors Affecting Male Sperm Allocation in Crustacea

Y

Sperm Limited

ND

ND

ND

ND

Y

(Y)

SF

Ejaculate size decreased over successive matings Ejaculate size decreased over successive matings Ejaculate size decreased over successive matings Recently mated males more successful than non-​mated 6 days

ND

>30 days

? “refill rate may be very slow”

?

ND

LF > SF

>20 days

ND

Larger females received more sperm, but only from larger males ND

ND

ND

LF > SF, especially from larger males

N

Y

(Y)

(Y)

Y

(Y)

ND

Lemaître et al. 2009

Rigaud and Moreau 2004

Galeotti et al. 2006, 2007, Rubolini et al. 2006, 2007 Sato et al. 2010

Sato and Goshima 2006, Sato and Goshima 2007a, 2007b, 2007c Pardo et al. 2015

Gosselin et al. 2003

Notes: LM > SM: large males provided more sperm than small males; SM > LM: small males provided more sperm than large males; LF > SF: large females received more sperm than small females; Y: Yes; (Y): Likely; ?: unknown; ND: no data.

Gammarus pulex

LM > SM

Birgus latro

LM > SM Larger males guarded females longer Hapalogaster dentata Males provided more sperm with increased sperm competition Metacarcinus edwardsii Large males had greater sperm reserves Austropotamobius SM > LM italicus

Homarus americanus

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Reproductive Biology mated males of similar size (Sato and Goshima 2007b, Mellan et  al. 2014). Similarly, resource-​ depleted males should be more stringent in mate choice (e.g., choosing a larger, more fecund female; see section “Female Size and Fecundity” earlier in this chapter) to maximize their chances of reproductive success given limited resources. Evidence for this hypothesis has been discovered in the fruit fly Drosophila melanogaster: sperm-​depleted males preferentially mated with larger females than smaller ones (Byrne and Rice 2006). On the other hand, sperm depletion through recent matings does not affect pairing decisions of male G. pulex individuals, and mated males were more successful at subsequent matings than non-​mated males (Lemaître et  al. 2009). In this species, although males invest a large proportion (~50%) of their sperm reserves in each mating, precopula duration exceeds the time needed for sperm reserves to recover (6  days). However, during precopula, males do not feed regularly (Robinson and Doyle 1985), which could potentially delay sperm recovery in mate-​guarding males. Therefore, recent mating history of males likely does not play a significant role in sperm allocation in this and other species that experience sufficient recovery time, e.g., during precopulatory mate guarding. On the other hand, if sperm ejaculated at each mating only represents a small fraction of total reserves (e.g., 2% in snow crab Chionoecetes opilio: Sainte-​Marie 2007), even if sperm recovery is slow, males can equally inseminate several females in rapid succession until reserves are depleted (Sainte-​Marie and Lovrich 1994). A female’s recent sexual history also affects sperm allocation by males. To a male, whether a female has recently mated may indicate the level of sperm competition he faces and hence the optimal amount of sperm to allocate to win more fertilizations. For example, in experiments with the blue crab, Jivoff (1997a) found that males pass larger ejaculates to an already-​mated female, suggesting that the presence of another male’s ejaculate on the female spermathecae may have provided a cue for rival males to increase their sperm allocation (as compared to first males, which did not have such a cue). As predicted by theory, the greater the proportion of a male’s sperm in the mix, or the

100 Female reproductive success (%)

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80 60 40

CL 6–7 mm CL 9–10 mm

20 0

CL 13–14 mm First

Second

Third

Fourth

Fifth

Male mating frequency

Fig. 3.6. Hapalogaster dentata. Reproductive success of different-​sized males that mated five consecutive times with different females. Relationship between mating frequency by males of various carapace lengths (CL) and average reproductive success (± SE) of females. The reproductive success variable is based on the female fertilization rate (number of viable eggs incubated by the collected female/​expected total number of eggs produced by a female) 100. From Sato and Goshima (2006) with permission.   



Sperm Ultrastructure and Sperm Economy

more rival sperm a male can displace with his own gametes on or inside the female, the greater the fertilization success (Parker and Pizzari 2010). In other species like the crayfish Austropotamobius italicus, second males did not necessarily allocate more sperm to already-​mated females. Instead, they removed parts of the first male’s sperm (an average of 77%) before depositing the same amount of sperm as they previously had to virgin females (Galeotti et al. 2007). In such cases of sperm removal and last-​male precedence, a male may ration sperm among the females he encounters (MacDiarmid and Butler IV 1999), heeding the warning that “the early bird may get the worm, but the second mouse gets the cheese.” Indeed, the order of mating can also play a role in sperm allocation decisions by males. Based on the life history (e.g., determinate vs. indeterminate growth) and structure of the seminal receptacles of females, sperm may have vastly different “playing fields” in which different allocation strategies result in the greatest chances of paternity. Sainte-​Marie (2007), in his review of sperm demand of decapods, described four female reproductive types based on life history and sperm-​storage mode, ranging from Type I females with indeterminate growth that need to mate each time before extruding eggs, to Type IV females with a terminal molt and long-​term sperm storage. McLay and Dennenmoser (see Chapter 13 in this volume) also describe different structural features of the seminal receptacle in females that could favor fertilization by earlier or later ejaculates in the mating sequence. In other words, in different species, female reproductive type and seminal receptacle morphology influence whether males should allocate more sperm in first or subsequent matings to maximize chances of fertilization (assuming the order of mating is assessable by the males). For example, first males would have greater precedence with Type I females if fertilization occurs and eggs are extruded soon after copulation, whereas with Type IV females, later males may have greater success if before fertilization, older, stored sperm from earlier males have degraded in quality over time or have been lost. In the Tanner crab Chionoecetes bairdi, Paul (1984) found that older sperm were not viable to fertilize a third clutch of eggs, and females must re-​mate to remain productive (but see Nagao and Munehara 2007). Thus, mating history plays an important role, and in species where males have multiple mating opportunities, spermatogenesis should comprise an important fraction of the male’s energy budget. Whether and how this is related to the evolution of particular sperm ultrastructure, complexity, and/​or size has not been explored. Perception of Future Mating Possibilities: Timing and Operational Sex Ratio Related to male size and the order of mating, a male’s perception of his future mating opportunities affects sperm allocation and economy. Galvani and Johnstone (1998) predicted with mathematical models that in species with a fixed reproductive season, early in the season there are higher prospects of future mating, and males should be more prudent with sperm allocation and female mate choice (e.g., only mating with larger, more fecund females). Later in the season, when mating opportunities become scarcer, males benefit from becoming less choosy and ejaculating more sperm to the partners they do find. Sato and Goshima (2007c) found that as the reproductive season progressed, stone crab males passed more sperm to medium-​sized females, and by the end of the season, large males mated with small females they typically reject early in the season. Male rock shrimps Rhynchocinetes typus that approached the end of their lives became more reluctant to engage in matings, but once they had seized a receptive female and transferred spermatophores they guarded females for longer than young males, most likely to ensure one of their last sperm investments (Ory et al. 2015). In this respect, operational sex ratio, the number of reproductive males to receptive females at any one time in a population, influences the perception of sperm competition and future chances of copulating. If males have access to many potential mates (few males to many females; female-​biased sex ratio), males face less competition and can prudently allocate sperm across multiple matings

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Reproductive Biology (Parker and Pizzari 2010). Conversely, if a male encounters very few potential mates (male-​biased sex ratio), either due to the presence of more rival males or as a function of low population density, it would be advantageous to allocate more sperm to the females that he does copulate with so as to displace competing gametes or make use of sperm reserves (Carver et al. 2005, Sato and Goshima 2007a, Pardo et al. 2018). In addition, larger males in general tend to have a greater probability of future mating, either through being more successful at displacing smaller males in competitions for females, or by nature of having more sperm reserves to mate multiply. Hence, for a small male with lower chances of another mating opportunity, he should invest more in present matings (Hinojosa and Thiel 2003), even if they are with smaller, less fecund females (Sato and Goshima 2007c).

SPERM ECONOMY, SPERM LIMITATION, AND FISHERIES With multiple factors affecting optimal and actual sperm allocation, a female runs the risk of sperm limitation if she receives fewer sperm than is sufficient to fertilize her brood (Paul 1984, MacDiarmid and Butler IV 1999, Rondeau and Sainte-​Marie 2001). Time between matings and rate of sperm regeneration also determine the capacity of males to sufficiently inseminate females. Hence, sperm limitation is predicted to occur when there are (i) insufficient males (or insufficient sperm reserves in smaller males) to inseminate all receptive females (or all the eggs in larger females); (ii) insufficient time between matings to recharge sperm reserves, which can be particularly exacerbated by a short reproductive window in some species (e.g., a few days after the pubertal-​terminal molt in Chionoecetes opilio: Sainte-​Marie and Lovrich 1994); and (iii) when males are too economical with sperm allocation (Rondeau and Sainte-​Marie 2001). Sperm limitation may result from male limitation in the population. This could be caused by parasite-​induced castration, or by higher predation risks of males (e.g., Forbes et al. 2006). In commercial species, male limitation is often caused or intensified by fisheries. Fishing skews the sex ratio to favor females, especially in fisheries where a minimum-​size catch limit is in effect, sexual dimorphism results in larger males than females, and ovigerous females are protected by management regulations (Kendall et al. 2001, Sato et al. 2010, Butler IV et al. 2015, Pardo et al. 2015). As discussed earlier, sperm count and quality provided to females generally increase with increasing male size, and number of sperm can even vary by up to two orders of magnitude from the smallest to the largest male (Sainte-​Marie 2007 and references therein). When larger males are constantly removed from a population through fishing, reproductive success is affected in several ways: (i) fewer large males with larger sperm reserves remain, and these males may be subject to constant sperm depletion through extensive mating; (ii) small males with smaller sperm reserves are left to inseminate the females in the population; and (iii) the sex ratio becomes more female-​biased and sperm competition decreases, leading to parsimonious sperm allocation by males that perceive more future mating opportunities. In particular, (iii) can be exacerbated by (ii). MacDiarmid and Butler IV (1999) reported that sperm transferred and clutch size were about 40% smaller when a Panulirus argus female was mated by a male of the mean size found in a fished population, rather than by a male of a size typically found in an unfished marine sanctuary nearby. Butler IV et al. (2015) further confirmed through experimental removal of sperm that sperm limitation reduces fertilization success (percent of viable eggs in a clutch), more so in smaller than larger females. By modeling the effects of reduced fertilization in the amphipod G. duebeni, Ford et al. (2012) found that mild reductions in brood size (5%) due to sperm reduction allowed the population to persist at critically low levels, but severe reductions of >10% resulted in population collapse within six to seven years. Of course, this model cannot be directly extrapolated to other taxonomic levels due to species-​specific population dynamics and reproductive biology; nonetheless,



Sperm Ultrastructure and Sperm Economy

it underscores the potential impacts of reduced reproductive success, through sperm limitation, on long-​term population survival. Implications of Sperm Limitation on Fisheries Research on reproductive performance of crustacean populations has largely focused on female fecundity with the assumption that male gametic resources are energetically inexpensive to produce (Kendall et al. 2001, Pérez-​Jar et al. 2007). As a result, many fisheries and aquaculture practices are based on protecting female spawning stocks while overharvesting (large) males (Kendall et al. 2001, Pardo et al. 2015, Sørdalen et al. 2018). Indeed, males make up over 80% to almost 100% of landed catch in spiny lobsters (Jasus spp.; MacDiarmid and Butler IV 1999 and references therein), and average male size in fished crustacean populations worldwide has decreased (e.g., Butler IV et al. 2015). Moreover, there is evidence of sperm depletion in males under male-​biased fishing pressure (Fig. 3.7; Pardo et al. 2015). Females in a heavily fished population of Metacarcinus edwardsii had lower sperm reserves and fecundity than females in unfished populations, highlighting the population consequences of selective harvesting of males (Pardo et al. 2017). Proper long-​term management of crustacean fisheries needs to take into account all aspects of reproductive performance, not just female fecundity. Male contributions (from spermatogenesis, seminal fluid production, packaging, and delivery) to reproductive success, modulated through sperm economy principles, should be considered in management decisions to determine optimal catch size limits and temporal restrictions. An interesting case of the swimming crab Portunus trituberculatus fishery in the East China Sea shows promising results of non-​selective fishing

0.18

Low High LAB

Vasa deferentia weight (g)

0.16 0.14 0.12 0.10 0.08 0.06 0.04 0.02 0.00

100

120

140

160

Carapace width (mm)

Fig. 3.7. Metacarcinus edwardsii. Relationship between carapace width and vasa deferentia weight of males during the mating season for individuals from contrasting fishery scenarios and recently mated males from the laboratory. (○) Sperm reserve in males under low or (●) high fishing intensity based on carapace width. (▼) Males from the laboratory that had mated recently. Data from localities with similar fishing intensity were pooled. Continuous line: linear fit from low fishing intensity sites; dashed line: linear fit from laboratory experiment; dotted line:  linear fit from high fishing intensity sites. Modified after Pardo et  al. (2015) under © Creative Commons license.   

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Reproductive Biology management:  females were found to be under low risk of sperm limitation under such fishing practices (Xuan et al. 2014), which differs from other exploited decapod species. In the European lobster H.  gammarus, females in a marine protected area preferentially mated with large males, whereas females in a nearby fished area, where males generally were smaller, had to mate with those small males; thus, selective extraction of large males not only may provoke sperm limitation in females, but also can result in fisheries-​induced sexual selection toward smaller male sizes (Sørdalen et al. 2018).

FUTURE DIRECTIONS Crustaceans feature a wide range of sperm morphology, and in most species these sperm are packaged in spermatophores that contain diverse secretions. Thus, male ejaculate investment involves production of sperm and seminal fluids. The differential costs of producing sperm and seminal fluids are not well known at present. Since many crustaceans, and in particular the Decapoda, have aflagellate introsperm, seminal fluids are fundamental for successful sperm delivery, survival, and fertilization. Consequently, it can be expected that the components and amounts of seminal fluids are exposed to intense intra-​and intersexual selection (Snook 2005). Whether production of spermatophores is limited by the maturation of new spermatocytes or by the secretion of seminal fluids requires future investigation. Male limitation can result in sperm limitation and reduced reproductive potential of females. This has been demonstrated in natural populations of amphipods (Forbes et al. 2006), and it is likely that severe male limitation, e.g., due to differential male predation risk, also occurs in other crustaceans. For example, Sudo and Azeta (1992) found that predatory fish exclusively preyed on mate-​searching males of the amphipod Byblis japonicus, which consequently were much less common in the benthic population than mature females. Future studies on male limitation in natural populations of diverse crustaceans are warranted. There is also evidence that sex-​selective harvesting of males can induce male limitation in fished populations. Some species (e.g., cancrid and portunid crabs) seem to be susceptible to these impacts, while others (e.g., H. americanus) appear to be more resistant to the effects of male-​selective fisheries. The causes for these species-​ specific impacts are not well known, but are likely related to differences in sperm replenishment and should be carefully investigated in future studies. Reproductive tract condition can be severely affected by temperature increases, affecting sperm quality and delaying the production and conformation of spermatophores (Pascual et  al. 1998). At high temperatures, spermatogenesis was suppressed in male crayfish Pontastacus leptodactylus (Farhadi and Harlıoğlu 2018), and in general, high temperatures have a negative effect on sperm quality in cultured decapods (Harlıoğlu et  al. 2018), similar to the temperature effects observed on oogenesis in female giant shrimp Macrobrachium rosenbergii (Mohamad et al. 2018). Reduced reproductive activity at high temperatures likely is a consequence of the trade-​off between energy required for maintenance and/​or growth and energy needed for gametogenesis. This is commonly reported for females (Ershova et al. 2016, Baliña et al. 2018), but has not received much attention for male crustaceans (for an exception, see Harlıoğlu et  al. 2018), and deserves attention, especially given the future prospects of rising ocean temperatures (Cane et al. 1997, Rayner et al. 2003, Reynolds et al. 2007). In addition, the impact of other environmental variables (e.g., pH, oxygen availability, or pollution) on spermatogenesis should be studied more intensively, considering current anthropogenic threats to the world’s oceans (Halpern et al. 2008). Genomics approaches are useful to distinguish between processes related to spermatogenesis versus the production of seminal fluids (Senarai et al. 2017, Zhang et al. 2018). Similarly, proteomic methods have been used to identify the proteins involved in spermatophore production (Niksirat



Sperm Ultrastructure and Sperm Economy

et al. 2014), which is a first step to estimate the associated costs. Also, the mobilization of sperm and processes related to fertilization could be investigated with these modern techniques (e.g., Niksirat et al. 2015). Furthermore, the nutritional requirements of males that are in the process of producing large amounts of spermatozoa and seminal fluid have been poorly studied, even though this information would be very useful in fisheries and aquaculture.

CONCLUSIONS Crustacean spermatogenesis is a topic that still needs attention due to the disparate morphologies found in this group and the variety of mechanisms involved in production, allocation, transfer, and storage of spermatocytes. The fact that most crustaceans have immotile sperm has placed more importance on seminal fluids, which serve as transfer, storage, or activation medium. In addition to sperm number or size, in crustaceans seminal fluid plays an important role in sperm competition. Regulating the volume of seminal fluid in spermatophores represents an opportunity to improve efficiency in sperm economy. The adjustment of ejaculation according to social conditions, operational sex ratio, body size or size of one’s mate, mating strategies and competition represents a mechanism for males to avoid sperm depletion. This is especially important in crustacean populations where males become limiting due to natural (e.g., predation) or anthropogenic (e.g., fishing and pollution) causes. Interestingly, how sperm morphology and ultrastructure are related to spermatogenesis and recovery of sperm reserves has rarely been studied in crustaceans, even though a better understanding of this relationship could be very useful in applied contexts (fisheries and aquaculture). Comparative approaches using closely related species with contrasting sperm morphology or with divergent mating behaviors might inform the relationship between sperm morphology/​ ultrastructure and sperm economy.

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Reproductive Biology Sato, T., K. Yoseda, K. Okuzawa, and N. Suzuki. 2010. Sperm limitation: possible impacts of large male-​ selective harvesting on reproduction of the coconut crab Birgus latro. Aquatic Biology 10:23–​32. Senarai, T., R. Vanichviriyakit, S. Miyata, C. Sato, P. Sretarugsa, W. Weerachatyanukul, and K. Kitajima. 2017. Alpha‐2 macroglobulin as a region‐specific secretory protein in male reproductive tract, and its dynamics during sperm transit toward the female spermatheca in the blue crab. Molecular Reproduction and Development 84:585–​595. Smith, R. J., R. Matzke-​Karasz, and T. Kamiya. 2016a. Sperm length variations in five species of cypridoidean non-​marine ostracods (Crustacea). Cell and Tissue Research 366:483–​497. Smith, R. J., R. Matzke‐Karasz, T. Kamiya, and P. De Deckker. 2016b. Sperm lengths of non‐marine cypridoidean ostracods (Crustacea). Acta Zoologica 97:1–​17. Snook, R. R. 2005. Sperm in competition: not playing by the numbers. Trends in Ecology and Evolution 20:46–​53. Sørdalen, T. K., K. T. Halvorsen, H. B. Harrison, C. D. Ellis, L. A. Vøllestad, H. Knutsen, E. Moland, and E. M. Olsen, 2018. Harvesting changes mating behaviour in European lobster. Evolutionary Applications 11:963–​977. Subramoniam, T. 1991. Chemical composition of spermatophores in decapod crustaceans. Pages 308–​321 in R. T. Bauer and J. W. Martin, editors. Crustacean Sexual Biology. Columbia University Press, New York. Subramoniam, T. 1993. Spermatophores and sperm transfer in marine crustaceans. Advances in Marine Biology 29:129–​214. Tudge, C. C. 1991. Spermatophore diversity within and among the hermit crab families, Coenobitidae, Diogenidae and Paguridae (Paguroidea, Anomura, Decapoda). Biological Bulletin 181:238–​247. Tudge, C. C. 1999a. Ultrastructure of the spermatophore lateral ridge in hermit crabs (Paguroidea, Anomura, Decapoda). Crustaceana 72:77–​84. Tudge, C. C. 1999b. Spermatophore morphology in the hermit crab families Paguridae and Parapaguridae (Paguroidea, Anomura, Decapoda). Invertebrate Reproduction and Development 35:203–​214. Tudge, C. C., and B. G. M. Jamieson. 1996a. Spermatophore and spermatozoal morphology in the Porcellanidae. I: Aliaporcellana suluensis and Pisidia longicornis (Decapoda, Anomura, Porcellanidae). Crustacean Research 25:73–​85. Tudge, C.C., and B. G. M. Jamieson. 1996b. Spermatophore and spermatozoal morphology in the Porcellanidae. II. The genera Petrolisthes and Polyonyx (Decapoda, Anomura, Porcellanidae). Journal of Crustacean Biology 16:535–​546. Tudge, C. C., B. G. M. Jamieson, M. Segonzac, and D. Guinot. 1998. Spermatozoal ultrastructure in three species of hydrothermal vent crab, in the genera Bythograea, Austinograea and Segonzacia (Decapoda, Brachyura, Bythograeidae) Invertebrate Reproduction and Development 34:13–​23. Tudge, C. C., D. M. Scheltinga, and B. G. M. Jamieson. 1999. Spermatozoal ultrastructure in the Hippoidea (Anomura, Decapoda). Journal of Submicroscopic Cytology and Pathology 31:1–​13. Tudge, C. C., D. M. Scheltinga, B.G. Jamieson, D. Guinot, and B. Richer de Forges. 2014. Comparative ultrastructure of the spermatozoa of the Majoidea (Crustacea, Decapoda, Brachyura) with new data on six species in five genera. Acta Zoologica 95:1–​20. Vogt, G. 2016. Structural specialties, curiosities, and record‐breaking features of crustacean reproduction. Journal of Morphology 277:1399–​1422. Vogt, G. 2018. Spermatogenesis and spermiogenesis in crustaceans. Pages 330–​335 in M. K. Skinner, editor. Encyclopedia of Reproduction, Volume 6. Academic Press, Elsevier, Cambridge, MA. Waddy, S. L., N. Feindel, N. Hamilton-​Gibson, D. E. Aiken, V. Merritt, and N. Leavitt. 2017. Reproductive cycles and mating capacity in male American lobsters (Homarus americanus). Fisheries Research 186:358–​366. Wedell, N., M. J. G. Gage, and G. A. Parker. 2002. Sperm competition, male prudence and sperm-​limited females. Trends in Ecology and Evolution 17:313–​320. Wingstrand, K. G. 1978. Comparative spermatology of the Crustacea Entomostraca. I: Subclass Branchiopoda. Kongelige Videnskabernes Selskab Biologiske Skrifter 22:1–​66. Xuan, F., W. Guan, C. Bao, F. Tang, B. Tang, and C. Zhou. 2014. Current fishing practices may induce low risk of sperm limitation in female swimming crab Portunus trituberculatus in the East China Sea. Aquatic Biology 20:145–​153.



Sperm Ultrastructure and Sperm Economy

Zara, F. J., M. H. Toyama, F. H. Caetano, and L. S. López-​Greco. 2012. Spermatogenesis, spermatophore, and seminal fluid production in the adult blue crab Callinectes danae (Portunidae). Journal of Crustacean Biology 32:249–​262. Zhang, J. S., X. J. Li, L. Yang, W. W. Li, and Q. Wang. 2018. Expression pattern and functional analysis of the two RING box protein RBX in spermatogenesis of Chinese mitten crab Eriocheir sinensis. Gene 668:237–​245.

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4 COSTS AND BENEFITS OF BROODING AMONG DECAPOD CRUSTACEANS: THE CHALLENGES OF INCUBATING IN AQUATIC SYSTEMS

Miriam Fernández, Antonio Brante, and Simone Baldanzi

Abstract This chapter discusses general patterns of brooding in decapod crustaceans from aquatic to terrestrial environments, addressing behavioral adaptations as well as costs and benefits. Brooding embryos is a common feature among decapods. However, brooding exhibits a wide range of modes that are highly dependent on the environment. Brooding is less common in marine systems, whereas there is a general pattern of extended brooding with terrestrialization. Exceptions are crabs that have invaded land directly via the seashore, i.e. land crabs that have indirect development like their marine ancestors. During terrestrialization, adaption to environmental stressors like desiccation, UV radiation, temperature variability, mechanical support, and osmolality seemed to generally favor decreasing larval development and increasing duration of brood care. Thus, crustaceans developed more complex brooding mechanisms as adaptive responses to the colonization of land (e.g., osmoregulation of the maternal fluids, marsupial fluid, sealed and specialized marsupium, provision of nutritious material, grooming and cleaning, ventilation of the embryo masses). However, clear brooding behaviors are also observed among several marine species (e.g. grooming and cleaning, oxygen provision). The major efforts to characterize general brooding patterns among decapod crustaceans and describe brooding behaviors were not accompanied by comprehensive studies to understand the costs and the benefits of brooding. Several studies have addressed the positive influence of the mother on embryo development, but the efforts to quantify the impact on embryo survival are still limited. This chapter identifies problems that need further consideration to reach a deeper understanding of the evolution of brooding in decapod crustaceans.

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Costs and Benefits of Brooding among Decapod Crustaceans

BROODING AMONG CRUSTACEANS: GENERAL PATTERNS Parental investment among crustaceans shows a wide diversity of strategies ranging from the total absence of embryo protection (e.g., euphausiids, penaeids), to active care of embryos in the brood pouch (e.g., freshwater amphipods, brachyuran crabs) and even to the extended care of juvenile stages (e.g., talitrid amphipods, bromeliad crabs, crayfishes; Clutton-​Brock 1991, Thiel 2000, Vogt 2013). Brooding also covers a wide range of modes that are highly dependent on the environment. Aquatic (marine and freshwater) and terrestrial systems show different and often contrasting physical, chemical, and biological characteristics that pose contrasting challenges for incubation and seem to have shaped brooding across taxa of crustaceans. In general, brooding, that extends to juvenile stages is more often observed among freshwater or terrestrial crustaceans. In the marine systems, a planktonic stage is often observed and brooding is less common, ceasing when larvae are released into the ocean. More often than not, the transition observed toward an extended brooding, when moving from the marine to terrestrial environment, includes a switch from an indirect to a direct developmental mode. Here, we define indirect development as the process in which an embryonic phase generates an intermediate planktonic larva that metamorphoses to a juvenile stage (Arenas-​Mena 2010). Direct development is defined here as an embryonic phase lacking a planktonic larval stage, in which juvenile offspring that are morphologically similar to the adults are released from the mother into the environment (Rabalais and Gore 1985, Anger 2001). This category may also include species that release juveniles as zoea larvae which are then brooded until the juvenile stage (Vogt 2013). We refer to the term brooding strictly as the behaviors exhibited by egg-laying animals during the incubation phase. Here, incubation is referred to as the process of maintaining uniform environmental conditions of the developing embryos. Abdominal flapping is an example of brooding behaviors exhibited by crustaceans to generate proper environmental conditions (oxygen) to developing embryos during the incubation period. Throughout this chapter, we refer to “eggs” as the organic receptacle containing the zygote that develops into an embryo after cell divisions. We will use “offspring” to refer to the young born of a reproductive event; collective offspring will also be referred to as a “brood.” This chapter first analyzes the patterns of brooding in decapod crustaceans in both aquatic and terrestrial environments, including references to other groups of crustaceans when discussing gen­ eral patterns. Second, we address the behavioral adaptations to incubate the brood in aquatic and terrestrial environments. Third, we examine the benefits and the cost of brooding, with a particular emphasis on the constraints of brooding in aquatic systems. Finally, we explore the possible consequences of global warming on brooding and problems that need further consideration to reach a deeper understanding of the evolution of brooding in decapod crustaceans. The topic of parental care will be extensively covered in Chapter 5.

BROODING IN DECAPODS: EXCEPTIONAL DIVERSITY, FROM MARINE TO TERRESTRIAL SYSTEMS Among decapods, incubation of the embryos is a common feature across environments (Strathmann and Strathmann 1982). Marine, freshwater, and terrestrial crabs incubate their embryos for variable periods, depending on the species, temperature, and other environmental conditions. A clear distinction in brooding patterns is observed between the two suborders of decapods, with Pleocyemata (crabs, lobster, crayfishes, stenopodidean, and caridean shrimps) showing higher levels of brooding and Dendrobranchiata (other shrimps and prawns) mostly shedding eggs directly into the water column (Anger 2001, Thiel 2007). This difference extends to the post-​embryonic phase: nauplius, zoea, and decapodid. After the embryonic phase, Dendrobranchiata species hatch as nauplii (Vogt

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Reproductive Biology 2013), while Pleocyemata as zoea (Anger 2001). Although the duration of the post-​embryonic developmental phase among decapods tends to be taxon-​specific, on average it lasts about five weeks (Pandian 1994). However, the extent of abbreviated development seems to vary in a consistent fashion as the environmental conditions become more stressing, such as in polar waters, deep sea, and terrestrialization (Anger 1995, Thatje et al. 2003, Bauer 2004). Abbreviated development has also been documented in other very specific conditions, such as symbiotic relationships of marine decapods with sessile invertebrates (e.g., tunicates or sponges) showing patchy distribution (Bolaños et al. 2004, Duffy and MacDonald 2010). Direct development (the highest degree of abbreviated development) is very rare in marine decapods, although present in some, such as the subtidal pilumnid crab Pilumnus vestitus (Wear 1967)  and the deep sea stenopodidean shrimps Spongicola japonicus Kubo, Spongicoloides koehleri Caullery, and Spongiocaris hexactinellicola Berggren (Goy 2010). Freshwater crabs (brachyurans) are a very large, polyphyletic group that show a broad range of incubation times, depending on whether the crabs originated from marine ancestors (hereafter, “secondary” crabs) or not (“primary” crabs) (Martin and Davis 2001, De Grave et al. 2009). Within these two broad categories also fall terrestrial crabs, for which water (either fresh-​or seawater) is still necessary for the brooding of the offspring (Vogt 2013). In primary freshwater crabs, brood care has been reported for all five families of the group, even though little information is available on the duration and behavior of post-​hatching brood care (Vogt 2013). Most of the examples of primary crabs come from the family Potamidae, in which several species were found to carry juveniles under the abdomen for days or weeks, allowing juveniles to develop through several stages before showing the adult form (Cumberlidge 1999, Wehrtmann et al. 2010). Fascinating examples of extended brooding are found in crabs that have colonized terrestrial environments, but for which water is still necessary for brooding the offspring. The Indian field crab Spiralothelphusa hydrodroma usually reproduces when temperatures are high and the fields are dry, but juveniles are brooded until the monsoon season (38–​100 days), when rainfall creates more suitable conditions for the juveniles to be released and survive (Pillai and Subramonian 1984). The arboreal crab Potamonautes raybouldi from closed canopy forests in Kenya and Tanzania raises its young in water-​filled holes found in tree branches (Cumberlidge and Vannini 2004, Bayliss 2011). Another important group of primary freshwater anomuran crabs belong to the family Aeglidae. All species show direct development: the hatching stage is a juvenile with an adult-​like form lacking pleopods and attached to their mothers through the chelae of their first pereopods (López Greco et al. 2004, Francisco et al. 2007). Extended brood care (3–​15 days) among anomuran crabs has been documented in a few species (Rodrigues and Hebling 1978, Swiech-​Ayoub and Masunari 2001, López Greco et al. 2004). In secondary freshwater crabs, the level of parental care, mode of development, and social organization is highly variable (Vogt 2013). Larvae of many secondary freshwater crabs develop in saltwater (such as the sesarmid Chiromantes haematocheir, Saigusa and Hidaka 1978, or the Chinese mitten crab Eriocheir sinensis, Anger 1991), others have abbreviated larval cycles, and some other species (particularly semi-​terrestrial and terrestrial Sesarmidae) exhibit direct development, often associated with post-​hatching brood care (Anger 1995, Ng and Tan 1995). Well-​developed juveniles are carried, attached to the pleon or carapace by females of the genus Geosesarma (A and B in Fig. 4.1) from a few days (four to five) to months (two to three; Diesel and Horst 1995). Another freshwater family of secondary crabs (Grapsidae) includes examples of exceptional brood care and sociality. This is the case of the well-​studied bromeliads crab Metopaulias depressus from Jamaica (C in Fig. 4.1), an indirect developer that colonized water reservoirs in epiphytic bromeliad plants (Diesel 1992, Diesel and Schuh 1993). Females release zoea stage larvae into the pool of water found in the leaf axils of the plants, which acts as a nursery area in which larvae develop into juveniles (González-​ Gordillo et al. 2010). Females contribute to their survival by supplying food and optimizing the



Costs and Benefits of Brooding among Decapod Crustaceans (A)

(B)

(C)

(D)

Fig. 4.1. Examples of brood care in secondary freshwater crabs. (A)  Mother of Geosesarma sp with juveniles. (B) Geosesarma notophorum with juveniles carried on dorsal carapace. (C) Metopauilias depressus within a water reservoir of a bromeliad plant protecting juveniles (arrow). (D) Female of Sesarma jarvisi inside a snail shell where she provides cares for her juveniles. Figure has been modified from Vogt (2013), with permission from John Wiley and Sons.   

water quality of the pool (oxygenation, removal of waste and detritus, pH and calcium balancing). The social organization of these crabs can be of a high level, especially in the case of habitat fragmentation and limited availability of plants, allowing juveniles to remain in the nursery pool long enough to favor the coexistence of more than one cohort in the same nursery (Diesel 1992, Diesel and Schubart 2007). Such form of eusociality is extremely well advanced and may resemble the level of sociality found in some insects (Vogt 2013). Another singular form of brood protection is found in the snail crab Sesarma jarvisi, which lives in the wet forests of western Jamaica’s limestone hills and mountains (Diesel and Horst 1995). These crabs look after the zoeas, decapodids, and juveniles in water-​filled snail shells and attend to them for a long period in the shell, normally up to two to three months (D in Fig. 4.1). Maternal care usually includes refilling the water in the shell and supplying food (Diesel and Horst 1995). The family Sesarmidae includes species that display the widest range of post-​embryonic development, varying from indirect (ocean-​type) development to the hatching of fully developed juveniles, followed by brood care (Anger and Schubart 2005, Gonzalez-​Gordillo et al. 2010). The transition from indirect to direct development following the process of terrestrialization of the family Sesarmidae is quite evident and more noticeable than across other crab taxa. A general pattern toward extended brooding (that includes protection of the embryos, larvae, and/​or juveniles) according to advanced terrestrialization can be found among crabs. However, the exceptions are those crabs that directly invaded land via the seashore, i.e., land crabs. These crabs mainly belong to the families Sesarmidae, Gecarcinidae, Ocypodidae and Coenobitidae (Bliss 1968, Hartnoll 1988, Anger 1995, Yeo et al. 2008). Land crabs are all indirect developers (as

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Reproductive Biology are their marine ancestors) and lack any form of extended brood care to juveniles (as performed by terrestrial and semi-​terrestrial decapods with freshwater origins). These crabs spend their entire life on land and only come in contact with seawater to release their larvae (Vogt 2013). An interesting behavior is observed in females of Coenobita clypeatus that live next to high cliffs that prevent the berried females from reaching the ocean. The females use their chelipeds to throw clumps of hatchlings off the cliffs and into the sea, allowing them to reach the ocean where larvae can develop (Hazlett 1983).

BROODING PATTERNS BEYOND CRABS: AQUATIC SHRIMPS AND CRAYFISHES Marine shrimps belonging to the order Dendrobranchiata mostly lack brooding mechanisms, and eggs embryos are usually released directly into the water column. Only one genus (Lucifer; Thompson 1829) is known to carry embryos. For instance, Lucifer faxoni brood the embryos until the nauplii emerge (Lee et al. 1992). The embryos are attached to the third pereopods and to each other by an adhesive substance on the embryo surface, though not very firmly, causing the embryos to be easily lost (Lee et  al. 1992, Naomi et  al. 2006). A  stronger and more complex attachment of embryos is found within the Pleocyemata shrimps, such as Cherax cainii and Austropotamobius pallipes (Thomas 1991, Burton et al. 2007). In these species, embryos are glued to oosetae that are kept together and are often twisted around each other, not only offering more stability but also facilitating embryos’ ventilation using the pleopods (Thomas 1991). The complexity and effectiveness of embryo attachment to the mother is considered to be the most important step in the evolution of abbreviated and direct development in Pleocyemata, with important consequences for their brooding mechanisms (Burkenroad 1963, Vogt 2013). Extension of brood care to post-​embryonic phases is known for only a few marine shrimps (Thiel 2000, 2007), such as the caridean shrimps Sclerocrangon ferox (Sars), S.  boreas, and S.  zenkevitchi (Makarov 1968, Haynes 1985, Guay et  al. 2011). Some sponge-​dwelling shrimps of the genus Synalpheus and the burrowing axiid Callichirus kraussi exhibit care for the free-​living offspring (Forbes 1973, Calado et al. 2006, Duffy and MacDonald 2010). An interesting brooding mechanism is shown by the burrowing axiid C. kraussi from South African estuaries. This shrimp has two non-​planktonic, but free-​living larval stages that stay in the protected environment of the maternal burrow for three to five days until metamorphosis (Forbes 1973). An extreme form of brooding among marine shrimps is achieved by six species of the genus Synalpheus, which exhibit eusocial brood protection (Duffy and MacDonald 2010). These shrimps form colonies, living within sponges and feeding on their secretions. Colonies can reach up to 350 genetically related, non-​breeding individuals organized in complex social structures that ensure offspring protection until they reach adult stages (Duffy 2007, Duffy and MacDonald 2010). Interestingly, Duffy and MacDonald (2010) found that eusociality in sponge-​dwelling shrimp is associated with small body-​ sized species, but this trend disappears after controlling for phylogeny. The authors concluded that the association of eusociality with small body size in sponge-​dwelling shrimps evolved in species that were already small-​bodied and not vice versa, suggesting that it may result because small-​bodied species more commonly have restricted larval dispersal (Duffy and MacDonald 2010). This may have fostered kin group formation and cooperation among relatives. However, all shrimps show the same basic embryonic development, characterized by restricted larval dispersal, suggesting that eusociality in the genus Synalpheus confers an advantage in saturated habitats, such as the colonized sponges (Wilson and Hölldobler 2005). In freshwater shrimps, extended brood care is documented for only two species, Dugastella valentina and D. marocana, both belonging to the family Atyidae (Rodríguez and Cuesta 2011). In these two species, brood care extends to the



Costs and Benefits of Brooding among Decapod Crustaceans

post-​embryonic development (decapodid stages) where females create movements of the maternal fluid with their pleopods, favoring water exchange between the incubation chamber and the environment (Dick et al. 1998, Fernández et al. 2002, Brante et al. 2003, Cuesta et al. 2011, Huguet et al. 2011, Rodríguez and Cuesta 2011). Freshwater crayfishes have been extensively studied for their brooding mechanisms and post-​ hatching brood care (Vogt and Tolley 2004, Vogt 2013). The embryos and juveniles are carried on the maternal pleopods, and juveniles are given protection in the brood pouch, formed by forward bending of the pleon. Brooding within freshwater crayfish shows complex dynamics and a strict relationship between mothers and juveniles. This is mainly due to the fact that juveniles lack the external sensory organs and masticatory structures that are necessary for orientation and feeding (Vogt and Tolley 2004). Juveniles have sufficient yolk reserves to allow them to boost their metabolism during the brooding period and even beyond. Brooding is highly variable in duration: it can vary from one to two weeks in Astacus astacus to five months in Paranephrops zealandicus (Andrews 1907, Whitmore and Huryn 1999). Exceptionally longer brooding (more than five months) has been reported for some burrowing terrestrial species (Richardson 2007, Duffy 2010). Truly terrestrial crayfish (the ones spending almost their entire life underground in burrows without connection to open bodies of water; Gherardi et al. 2010) and semi-​terrestrial ones (species that are active on land, but have their burrows close/​connected to open waters; Gherardi et al. 2010) have evolved brood protection even beyond the juvenile stages. The burrowing conditions have favored a complex form of sociality in the brooding mechanisms. Juveniles of the Tasmanian crayfish Ombrastacoides pulcher remain in the maternal burrow for at least 14 months before being totally independent from the mother (Richardson 2007). Juveniles of the semi-​terrestrial crayfish Parastacus pugnax from central Chile also cohabit with parents, but only during the dry period, establishing their own burrows during the wet season; this suggests that prolonged parent-​offspring cohabitation might have evolved in response to the predictable seasonal variations in the crayfish habitat (Palaoro et al. 2016). Among burrowing crayfish (Engaeus leptorhynchus), social systems have also been observed, with family groups consisting of one adult male, an embryo-​carrying female, a non-​ reproducing female, and 52 juveniles of two age classes (Horwitz et al. 1985).

BROODING AND TERRESTRIALIZATION OF CRUSTACEANS: GENERAL PATTERNS AND HYPOTHESIS The generalized pattern emerging from the preceding analysis is that most marine and some freshwater species have limited brooding of embryos (until larval hatching), and some of the freshwater and most of the terrestrial and semi-​terrestrial crustaceans exhibit extended brooding up to the newly hatched juveniles (Fig. 4.2). Nonetheless, terrestrialization has taken two alternative paths that appear to be associated with the degree of brooding. Terrestrial decapods that invaded land via the seashore, such as land crabs and terrestrial crayfish, do not show direct development or extended brood care. On the contrary, freshwater decapods and semi-​terrestrial/​terrestrial decapods that evolved from freshwater ancestors show mainly abbreviated development and extended brood care. The abundance of abbreviated/​direct development in freshwater decapods, in contrast with its scarcity in marine decapods, as well as the absence of direct development in terrestrial decapods that have invaded land via the seashore, links brooding to the process of terrestrialization, which involves massive changes in the biology, physiology, ecology, and behavior of crustaceans. It is worth mentioning that the independent evolution of abbreviated development with a reduction of larval stages to a level of complete absence of larvae (direct development) is found in several other groups of crustaceans, including Ostracoda, Cladocera, Leptostraca, and Peracarida that have undergone terrestrialization (Gruner 1993). Crustaceans living in aquatic systems (both marine and

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Terrestrial Habitats

Environmental Stress + +

Larval Development Brooding +

Fig. 4.2. Diagram showing the theoretical relationship between environment, developmental mode, and brooding. During terrestrialization, larval development of crustaceans tends to be reduced (from indirect to direct development), while brooding has been extended to post-​hatching juveniles. This trend seems to be an adaptation to the higher stress in terrestrial habitats compared to aquatic ones. In this perspective, brooding provides an important adaptive significance during the terrestrialization of crustaceans. Nonetheless, there are several examples that rule out such a pattern drawn among these three components (see examples in the text).   

freshwater) and those that colonized land experience physical forces that drastically differ in their intensity (Fig. 4.2; Martin and Strathmann 1999). During terrestrialization, stressors like desiccation, UV radiation, temperature variability, mechanical support, and osmolality represent physical challenges that crustaceans had to overcome in all aspects of their biology, reproduction included (Martin and Strathmann 1999). However, exceptions to such a trend are not rare in some families, genera, or even single species of crustaceans. As reported earlier, an extraordinary example comes from those groups that colonized land from freshwater sources, which maintained indirect development, but with exceptionally extended brood care and even complex forms of sociality (Vogt 2013). In an evolutionary context, the adaptation to harsh environments seems to have involved the strategy of decreasing larval development and increasing the duration of brood care. Thus, crustaceans developed more complex brooding mechanisms as an adaptive response to the colonization of land (Table 4.1). In terrestrial and semi-​terrestrial environments, and to some extent in freshwater systems, osmoregulation of the maternal fluids seems to be a critical brooding behavior (Spicer et al. 1987, Morritt and Spicer 1996a, 1996b, 1996c, Morritt and Richardson 1998, Surbida and Wright 2001, Table 4.1). Morritt and Spicer (1996a) were the first to provide support for the idea that mothers of amphipods, particularly semi-​terrestrial talitrids, can adjust the osmotic concentration of the maternal fluids in the pouches where offspring are brooded (see also Morrit and Richardson 1998, Surbida and Wright 2001). Amphipoda and Isopoda, the two crustacean orders showing both the greatest speciation and ecological radiation on land, have developed a highly specialized marsupium, which has likely been of a great adaptive significance in the colonization of land (Verhoeff 1917, 1920, Hoese 1984, Spicer et al. 1987, Hoese and Janssen 1989). On the other hand, in aquatic systems, ventilation of the embryos seems to be the most critical brooding behavior present in all groups (Table 4.1). Behaviors associated with the ventilation of the embryos occur regardless of embryo developmental stages, from small to large crustaceans in aquatic systems (Dick et al.

Taxon Amphipoda* Isopoda* Decapoda (**) Amphipoda Isopoda Decapoda Primary crabs* Secondary crabs* Crayfishes Shrimps Anomurans Amphipoda Isopoda Decapoda Mostly until hatching

Extended Mixed Extended Mixed Mostly extended

Direct Mixed Direct Mixed Mostly direct Mostly indirect

Brooding Extension Extended Extended Extended Extended Extended

Developmental Mode Direct Direct Indirect Direct Direct V; GC V; GC; NM V; ERR; NM; ES V; ERR V; ERR V; ERR; EEB V V; GC; ERR; ES

Brooding Strategy OB; MP; ERR; EEB MP; OB GC; ES V; ERR; EEB V; OB

Abbreviations: OB: Osmoregulatory Behavior; EEB: embryos elbowing (cycling of embryos); MP: Marsupial fluid provisioning; GC: Grooming and cleaning; V: Ventilation; ERR: Embryos Removal and Replacement; NM: Nursery Maintenance; ES: Eusociality. * This group includes semi-​terrestrial families or species. ** Includes truly terrestrial crabs and crayfishes.

Marine

Freshwater

Environment Terrestrial

Table  4.1. Description of the developmental mode, brooding extension and brooding strategies adopted by different taxa of crustaceans for each category of environment that have been colonized. 

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BEHAVIORAL MECHANISMS ASSOCIATED WITH BROODING: DESCRIPTIONS, COMPARISONS, AND BENEFITS Incubation of offspring requires not only parental morphological adaptations to carry offspring during development, but also specific female brooding behaviors to overcome physical and biological limitations of incubating in aquatic and terrestrial systems (Vogt 2013). In this section, we review the main behavioral adaptations related to incubating in aquatic and terrestrial brooding crustacean species. Avoiding Desiccation Unlike those of reptiles or birds, crustacean eggs lack an external protective layer and risk desiccation. Thus, in terrestrial systems, reproduction and incubation occur in aquatic environments, water reservoirs, or wetlands (Table 4.2). For example, the bromeliad crab Metopaulias depressus uses water reservoirs stored in the leaf axils of large bromeliads to incubate and care for its offspring (Diesel 1989, Diesel and Schuh 1993). Alternative morphological and behavioral mechanisms to incubate offspring and avoid desiccation are observed among semi-​terrestrial and terrestrial crustaceans. The evolution of a marsupium for incubation and female selection of breeding sites are viewed as key steps in the successful colonization of land by decapods, amphipods, and isopods (Morritt and Richardson 1998). For terrestrial and semi-​terrestrial crustaceans (mainly amphipods and isopods), incubation generally occurs in a marsupium that provides embryos with an aqueous microenvironment for development. In terrestrial species, the marsupium is completely sealed from the external environment to prevent extreme desiccation (terrestrial marsupial type). Terrestrial isopods excrete a marsupial fluid (hemolymph), which is derived from the female. In semi-​terrestrial and aquatic isopods and amphipods, the marsupium is semi-​closed and connected to the external environment, allowing constant water exchange to the marsupium through a water-​conducting system (amphibious and aquatic marsupial types, respectively). Osmoregulation Because decapods carry their embryos in an open incubation chamber, behaviors associated with osmotic regulation of the brood are less likely to evolve (Table 4.2). However, female isopods, amphipods, and mysids that incubate embryos in closed or semi-​closed marsupia are capable of osmotic regulation of the marsupial fluid, mainly by injecting hemolymph and urea in the marsupium (Table 4.2; Hoese and Janssen 1989, Spicer and Taylor 1994, Morritt and Spicer 1996c, Charmantier and Charmantier-​Daures 2001). These adaptations have allowed species to colonize environments across a wide variety of salinity conditions. For example, early and late stage embryos of the euryhaline isopod Sphaeroma serratum have little to no ability to osmoregulate and thus cannot survive outside of the marsupium (Charmantier and Charmantier-​Daures 1994). Brooding females of the semi-​terrestrial beachflea Orchestia gammarellus direct urine from the antennary gland to the brood chamber to regulate fluid osmolality (Moore et al. 1993, Spicer and Taylor 1994, Morritt and Spicer 1996c) (see Fig. 4.3; Morritt and Spicer 1996c). Some observations suggest that the marsupial fluid of mysid species, such as Neomysis integer and Praunus flexuosus, and some cladoceran species may also provide protection against environmental osmotic fluctuations (mysids: Ralph 1965, McLusky

Ventilation

Grooming and cleaning

Removal of unhealthy or dead embryos

Decapoda Grooming and Aquatic prawns cleaning and crayfishes

Decapoda Aquatic crabs

Ventilation

Behavior

Oxygen

ND

Oxygen

Factors

Insertion and movement of modify plepods with setae Water quality Insertion and movement of partially specialized chelipeds Use of modify plepods with setae Presence of non-​viable Use of partially embryos specialized chelipeds

Abdomen flapping

Pleopod beating

Use of the specialized 5th periopod

Direct and reverse gill ventilation

Abdomen flapping

Pleopod beating

Mechanism

(+/​+)

(–​/​+)

(–​/​+)

(–​/​+)

Relationship (Factor/​Behavior)

Schembri 1981, Wheatly 1981, de Vries et al. 1991, Naylor et al. 1997, Naylor and Taylor 1999, Fernández et al. 2000, Baeza and Fernández 2002, Fernández et al. 2002, Brante et al. 2003 Bauer 1981, Martin and Felgenhauer 1986, Pohle 1989, Fleischer et al. 1992, Försters and Baeza 2001

References

Tack 1941, Ameyaw-​Akumfi 1976, Kuris et al. 1991

Reduction of infection risk of healthy embryos

(continued)

Phillips 1971, Bauer 1981

Decrease of fouling

Increase of the oxygen availability Phillips 1971, Ameyaw-​Akumfi 1976 Reduction of metabolic wastes

Decrease of fouling

Increase of the oxygen availability and reduction of metabolic wastes

Benefits

Table 4.2.  Brooding Behaviors Adopted by Females of Crustacean Species in response to Different Limiting Factors: The Relationship between Factors and Behaviors, and the Benefits relative to the Behaviors.

Amphipoda Aquatic species

Isopoda Terrestrial marsupial species

Isopoda Aquatic marsupial species

Removal of unhealthy or dead embryos

Ventilation

“Elbowing of embryos” Replacement of lost embryos

Osmoregulatory behavior

Marsupial fluid provision

Osmoregulatory behavior

Oostegite movements

Ventilation

ND

Factors

Relationship (Factor/​Behavior)

Benefits

References

Increase of the oxygen White 1970, Janssen and Hoese 1993 availability Reduction of metabolic wastes Injection of Osmolality at Depending on Osmotic regulation Charmantier and Charmantier-​Daures hemolymph content the external external osmolality 1994, 2001 environment conditions Hemolymph supply BC Provision of an aqueous Akahira 1956, Hoese 1984, Hoese and via segmental matrix, nutrition and Janssen 1989 cotyledons oxygenation Modified integumental Osmolality at Depending on Osmotic regulation Hoese and Janssen 1989, Charmantier structures the external external osmolality and Charmantier-​Daures 2001 environment conditions Insertion of the first ND Rearrangement of Hurley 1968, Shillaker and Moore 1987 gnatopods embryos Insertion of the first Embryos (+/​+) Increase of the Borowsky 1983, Shillaker and Moore gnatopods dislodged reproductive success 1987 from the marsupium Pleopod beating Oxygen (–​/​+) Increase of the Borowsky 1980, Shillaker and Moore oxygen availability 1987, Dick et al. 1998, Tarutis et al. Oostogite flexure and reduction of 2005 Thorasic flexion metabolic wastes Use of mouthparts Presence of (+/​+) Reduction of the Dick et al. 1998 non-​viable infection risk of embryos healthy embryos

Mechanism

Behavior

Table 4.2. (Continued)

96

Osmoregulatory behavior

Osmoregulatory behavior

Osmoregulatory behavior

Hemolymph supply BC Provision of an aqueous Spicer et al. 1987, Morritt and Spicer via segmental matrix 1996 cotyledons Urine flux into the Osmolality at Depending on Osmotic regulation of Spicer and Taylor 1994, Morritt marsupium from the external external osmolality the marsupial fluid and Spicer 1996a, 1996b, 1996c, the antennary gland environment conditions Charmantier and Charmantier-​ exit duct Daures 2001 Urine flux into the Osmolality at Depending on Osmotic regulation of Ralph 1965, McLusky and Heard marsupium the external external osmolality the marsupial fluid 1971, Greenwood et al., 1989, environment conditions Charmantier and Charmantier-​ Daures 2001 Presence of brood Osmolality at Depending on Osmotic regulation of Review in Aladin and Potts 1995, and chamber fluid the external external osmolality the marsupial fluid Charmantier and Charmantier-​ environment conditions Daures 2001

Abbreviations: BC: Basal Condition for brooding; ND: Symbols + and – in the “Relationship” column refer to the magnitude of the factors considered and the intensity of the behaviors observed.

Cladocera Aquatic species

Mysida Aquatic species

Amphipoda Terrestrial/​ Semiterrestrial species

Marsupial fluid provision

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98

800 600 400 200

Marsupial Fluid

Female Hemolymph

Acclimation Medium

Fig. 4.3. Median osmolality (with 95% confidence interval) measured in the marsupial fluid (MF) and haemolymph (Haem) of ovigerous females of Orchestia gammarellus maintained at low salinity concentration (Medium). Redrawn from Morritt and Spicer (1996b), with permission from Elsevier.   

and Heard 1971, Cladocera: see Aladin and Potts 1995 for a review). Thus, the fluid of the incubating pouch plays an important role in embryo development, especially at early stages when the marsupial fluid is isosmotic compared to embryos (Charmantier and Charmantier-​Daures 1994). Embryonic Nutrition Provision of nutritious material to developing embryos ranges from yolk to other means of maternal provisions delivered during extended care (Lawlor 1976, Clarke 1985, Hoese and Janssen 1989, Helden and Hassall 1998). Embryos of some terrestrial isopods are capable of actively ingesting organic particles from the marsupial fluid (Hoese and Janssen 1989). For example, the dry weight gain during the marsupial phase of the isopod Armadillidium vulgare indicates that embryos use a significant amount of organic matter produced by the mother (Lawlor 1976, Helden and Hassall 1998). In addition, the depletion of maternal fat reserves during incubation and the association between the cotyledons and the maternal fat body reinforce the idea that mothers provide nutrients to the offspring (Hoese and Janssen 1989). In the Antarctic isopod Glyptonotus antarcticus, as in other Antarctic brooding species, females store enormous amounts of fat, allowing them to actively provide nutrients to their embryos during development ( Janssen and Hoese 1993). Sometimes mothers provide essential elements to the offspring during development. For instance, terrestrial isopod embryos need calcium for the formation of the cuticle in the brood pouch, and the marsupial fluid seems to be an important and sometimes unique source of calcium ions to offspring in this group (Ouyang and Wright 2005). In Armadillidium vulgare embryos, total calcium increases more than 17-​fold during development and up to 35-​fold in mancas (post-​larval juveniles) ingesting marsupial fluid (Ouyang and Wright 2005). Grooming and Cleaning Unviable embryos and embryos affected by infections and biofouling are potential sources of brood contamination and may lower the reproductive success of the females. Behavioral mechanisms



Costs and Benefits of Brooding among Decapod Crustaceans

associated with the removal of unviable or infected eggs and embryos from the brood, as well as the cleaning of the embryo masses observed among crustaceans, seem to support this hypothesis. Crabs, shrimps, and crayfish have specialized pereopods with setae that they introduce into the brood to groom and manipulate the embryo mass, reducing biofouling and preventing parasite and predator settlement (Phillips 1971, Bauer 1981, Martin and Felgenhauer 1986, Fleischer et al. 1992, Förster and Baeza 2001). For example, decapods from the genus Petrolisthes have specialized grooming setae on the carpus, propodus, and dactylus of the fifth pereopods (Förster and Baeza 2001). Experimental and observational data for P. violaceus suggest that individuals do not have specific mechanisms to seek, find, and selectively discard extraneous objects from the brood. However, females that manipulate and insert their pereopods in the embryo mass increased embryo survival compared to females whose pereopods had been experimentally removed (Förster and Baeza 2001). In decapods, the brush-​like form of the hairy grooming appendages aid in dislodging epibiotic organisms, detritus, and other kinds of debris from the mass, thereby reducing the risk of infection (Bauer 1989). The cleaning and grooming behavior observed among crabs and amphipods also results in the removal of dead embryos from the brood (Tack 1941, Ameyaw-​Akumfi 1976, Kuris et al. 1991). While most decapods do not have specific behaviors or mechanisms to selectively remove unviable embryos, observations suggest that the manipulation of the brood with grooming appendages and chelae incidentally discards nonviable embryos (Fleischer et al. 1992). In contrast, the amphipod Crangonyx pseudogracilis inserts its mouthparts into the brood to assess the condition of its embryos, and then selectively ejects unhealthy embryos (Dick et al. 1998). Similar behaviors have been identified in several crayfish species (Tack 1941, Ameyaw-​Akumfi 1976). Ventilation In aquatic systems, oxygen is one of the main limiting factors for brooding (Strathmann and Chaffee 1984). In some crustacean groups, oxygen supply to the embryos seems to be as important as other processes associated with providing proper environmental conditions to the brood among animals, such as thermoregulation in birds. For example, the marsupial fluid in isopods and amphipods provides embryos with not only nutrients and microelements, but also water and oxygen (Hoese and Janssen 1989). In other groups, diverse and specific ventilatory behaviors have been observed in brooding females. Laboratory experiments combining incubatory behavioral observations and oxygen measurements have demonstrated that abdominal flapping and pleopod beating by females during incubation is related to the ventilation and oxygenation of embryo masses in brachyuran crabs, prawns, and crayfishes (crabs: Schembri 1981, Wheatly 1981, de Vries et al. 1991, Naylor et al. 1997, Naylor and Taylor 1999, Fernández et al. 2000, Baeza and Fernández 2002, Fernández et  al. 2002, Ruiz-​Tagle et  al. 2002, Brante et  al. 2003, shrimps and crayfishes:  Phillips 1971, Ameyaw-​Akumfi 1976). Moreover, the frequency of such ventilatory behaviors is associated with the embryo oxygen demand (metabolic rate); therefore, oxygen demand increases as development advances and environmental temperature rises (Brante et al. 2003). Baeza and Fernández (2002) described behaviors associated with the provision of oxygen to the brood in the brachyuran crab Romaleon setosum: females engaged in abdominal flapping and inserted their pereopods and chelae into the embryo mass. Oxygen availability inside the brood is related to the frequency of these female behaviors that, in turn, are dependent on the developmental stage of the embryos (Baeza and Fernández 2002). Females carrying early-​stage embryos perform brooding behaviors cyclically and pulses of oxygen injection are observed, while continuous brooding behavior and relatively high oxygen concentrations are observed in females carrying late-​stage embryos (Baeza and Fernández 2002). These oxygen provision patterns were explained by the higher metabolic rates in late stage embryos. Moreover, the lower oxygen concentration at higher seawater temperature, combined with temperature-​dependent increase in

99

01

Reproductive Biology 00:00

Stage I

Stage II

Stage III

Stage IV

00:04 00:08 00:12 00:16 Time (min)

100

00:20 00:00 00:04 00:08 00:12 00:16 00:20 0

20

40 60 80 100 Mx St Flp Prp Ch

O2 availability (%)

Behavior

0

20

40

60

80 100 Mx St Flp Prp Ch

O2 availability (%)

Behavior

Fig. 4.4. Percentage of oxygen available in the center of the brood mass for females of Romaleon setosum (left side of each panel) incubating embryos at different embryonic stages (different panels). The right side of each panel depicts the timing of different brooding behaviors recorded simultaneously with oxygen over 20 min in laboratory during night. Mx = maxilliped beating; St = standing; Flp = abdominal flapping; Prp = pereiopod probing; Ch = chela probing. Bars represent behavioral states; arrows represent behavioral events. Redrawn from Baeza and Fernández (2002), with permission from John Wiley and Sons.   

embryo metabolic demand, induces females to ventilate more when temperature rises, generating a complex relationship among temperature, dissolved oxygen, and female/​embryo metabolism (Fig. 4.4). Despite ventilation behaviors, oxygen still seems to be limited in the center of the embryo mass of brachyuran crabs, as development of inner embryos is delayed, in comparison to outer embryos within a brood (Fernández et al. 2003). Similar ventilatory behaviors have been observed in amphipods. In the freshwater species Crangonyx pseudogracilis, brooding females flex and contract their body, expanding their interlocked oostegites to facilitate water exchange in the brood pouch (A in Fig. 4.5; Dick et al. 1998). Moreover, this species intensifies the ventilatory behaviors when the ambient temperature is high and/​or when oxygen availability is low to enhance oxygen conditions inside the embryo masses (B in Fig. 4.5; Dick et al. 1998). Similar behavioral patterns have reported in amphipod (e.g., Jakob et al. 2016) and decapod species (Fernández et al. 2002, Brante et al. 2003, Romero et al. 2010). In addition, time spent by the female engaged in this beating behavior increases with offspring development as embryo oxygen demand increases (Dick et al. 1998, Fernández et al. 2002, Brante et al. 2003). Although the vigorous body movements of the brooding females may result in the loss of embryos, some species (such as the amphipods Corophium bonnellii and Gammarus mucronatus) appear to account for the embryo loss due to beating by retrieving lost embryos with the use of their gnathopods



Costs and Benefits of Brooding among Decapod Crustaceans (A)

Coxal plate 3 pair of Pleopods

Embryos Brood pouch

Log mean time (s) actively brooding

(B)

Dissolved oxygen 7.2 mg/liter 1.0

71

5.2 mg/liter

0.8 0.6 71

71

0.4 71 0.2

20°C

10°C Temperature

Fig. 4.5. (A) Sequence showing the ventilatory behavior of a brooding female of Crangony pseudogracilis. CP = Coxal plate; BP = Brood pouch; P = Pleopods. (B) Time spent by brooding females of Crangony pseudogracilis ventilating their brood masses under four combined treatments of temperature and dissolved oxygen. (A, B) Redrawn from Dick et al. (1998), with permission from Elsevier.   

(Borowsky 1983, Shillaker and Moore 1987). Embryo losses, associated with ventilation, have also been reported in brachyuran crabs (Brante et al. 2003). In fact, the consistent patterns of increasing embryo loss toward lower latitudes could be linked to temperature-​dependent ventilation (Brante et al. 2003, 2004). Aquatic marsupial-​type isopods, such as those of the genera Idotea, Ligia, and Tylos, actively ventilate their embryo masses by moving their oostegites to circulate water through the special opening located at the posterior end of the marsupium (White 1970, Heinrich-​Janssen and Hoese 1993). In amphipods, oostogite movement is complemented with pleopod beatings and thoracic flexing. In amphibious marsupial type isopods from the Oniscidea group, broods are provided with oxygen via water drops from the external environment that are transported to the marsupium via a channel system (Hoese 1981, 1982, 1984). Conversely, oxygen is provided to the offspring of terrestrial marsupial type isopods through the hemolymph via the female’s cotyledons since the marsupium is hermetically sealed from the environment. Complementary to the ventilatory behaviors described in the preceding, some aquatic crabs oxygenate their embryo masses using the water current produced by the branchial chamber. Females of the decapod species Ebalia tuberosa ventilate their embryos by extending their telson to move water from the abdomino-​sternal chamber that encloses the brood to the branchial chamber. In

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Reproductive Biology

+1 Hydrostatic pressure (cm H2O)

102

0 –1 +1

O

S

0 –1

0

5

10

15 20 25

30 35

40 45

50 55

60 65 70 75

80 85

Time (s)

Fig. 4.6. Hydrostatic pressure profiles simultaneous measured in the (a) branchial chamber and the abdominosternal chamber of a female Ebalia tuberosa. Note that when the female opens the telson, the pressure in the abdominosternal chamber shows a perfect match with the pressure in the branchial chamber until the telson valve is closed. O = telson valve open; S = telson valve shut. Redrawn from Schembri (1981), with permission from John Wiley and Sons.   

this way, they can directly pump water to the embryos (Fig. 4.6; Schembri 1981). Brooding Cancer pagurus females use a similar mechanism of ventilation to oxygenate their embryo masses, but they do so with reversed gill flow (Naylor and Taylor 1999). The concurrent changes of patterns of oxygen availability in the embryo mass, female behav­ ior (abdominal flapping), and oxygen demand of the embryos of several brachyuran crab species (Baeza and Fernández 2002, Brante et al. 2003, Fernández et al. 2003, Fernández et al. 2006) suggest that females might be able to detect some cues related to the conditions of the brood. Experimental studies have shown the relative importance of environmental conditions in the embryo mass and physiological condition of the embryos as causal factors determining female behavior. Brooding females of the brachyuran crab Homalaspis plana carrying early-​stage embryos were experimentally exposed to (a)  low or high oxygen conditions and (b)  water with exudates from early and late-​stage embryos (and control, no embryos), pumping water from the different environmental conditions to the center of the embryo mass (Fernández et al. 2002). The results show that females carrying early-​stage embryos increased flapping frequency under low oxygen concentrations, suggesting that females, regardless of embryo development, detected and adjusted behaviorally to low oxygen levels inside the embryo mass (Fig. 4.7). The detection of environmental conditions and behavioral responses were also evident when 100% air-​saturated water was pumped to the embryo mass: females typically showed a low frequency of abdominal flapping. However, when 100% air-​saturated water containing waterborne substances from late-​stage embryos was pumped into the embryo mass of females carrying early-​stage embryos, females reacted by behaving as if they were carrying late-​stage embryos (Fig. 4.7; Fernández et al. 2002). Thus, both cues seem to be registered by females: environmental conditions (oxygen) and embryo condition (related to oxygen demand).



Costs and Benefits of Brooding among Decapod Crustaceans High oxygen

9 7 5 3 1

Late embryos

Early embryos

No embryos

Late embryos

–3

Early embryos

–1 No embryos

Mean difference in flapping frequency

Low oxygen

Fig. 4.7. Mean difference in abdominal flapping frequency when water containing no embryos, early stage embryos, or late stage embryos at low (15.9 mm Hg) or high (158.8 mm Hg) oxygen partial pressure was pumped into the embryo mass of females carrying early stage embryos. The difference was calculated between the application of a treatment and the control situation (no water pumped into the embryo mass). Vertical lines indicate SE. Redrawn from Fernández et al. (2002).   

WHAT ARE THE BENEFITS OF BROODING ON OFFSPRING DEVELOPMENT AND SURVIVAL? Embryos and larvae are the most vulnerable stages of the life cycles of individuals, and the evolution of parental care in different taxa and environments enhances survival and growth of their offspring (Clutton-​Brock 1991). However, it is a major challenge to effectively measure the benefits of parental care, especially for brooding, because of the difficulty of experimentally comparing embryo performance in the presence and absence of incubation. Thus, several claims of the benefits of brooding behavior are more or less speculative, and few studies have evaluated direct benefits of brooding on embryos in an experimentally comparative framework. Experimental studies have demonstrated that embryos of several crustacean species isolated from the mother show low survival rates or other negative effects on larval development (see examples in the following). Infection by bacteria and fungi is one of the main causes of embryo mortality, and most of the protocols of cultivation of isolated embryos include the use of antibiotics (e.g., Costlow and Bookhout 1960, Hartnoll and Paul 1982). For example, embryos of the marine crab Carcinus maenas are not viable when they are dislodged from the mother and reared in water (Hartnoll and Paul 1982). Similar results were obtained in embryos of the estuarine grapsid Cyrtograpsus angulatus and the freshwater shrimp Palaemonetes argentinus cultivated in vitro (Bas and Spivak 2000, Giovagnoli et al. 2014). In all these species, bacterial contamination is suggested as the potential cause of mortality. In the shrimp Heptacarpus pictus, ablation of the cleaning chelipeds of females produced an increase in microbial and sediment fouling of the brood mass, hindering embryo development (Bauer 1979). All this evidence suggests that cleaning and grooming

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Reproductive Biology behaviors exerted by females on their embryo mass increase embryo viability. In vitro cultivation of embryos has been achieved with greater success in semi-​terrestrial and terrestrial crustaceans (i.e., amphipods and isopods) than in aquatic ones, possibly due to the lower bacterial contamination (e.g., Morritt and Spicer 1996a, Surbida and Wright 2001). Crustaceans inhabiting coastal or brackish environments are exposed to high variability in salinity, with embryos and larvae experiencing stressful osmotic conditions. In this group, parental care seems to be essential for osmotic regulation, especially at early embryonic stages (Spicer et al. 1987, Hoese and Janssen 1989). In fact, embryos of some crustaceans extirpated from the brood pouch do not survive at low salinities (e.g., the isopod Sphaeroma serratum; Charmantier and Charmantier-​Daures 1994). Similar results have been observed in the semi-​terrestrial amphipod Orchestia gammarellus:  isolated embryos do not survive below 25% seawater, while embryos protected by the brood pouch may resist as low as 10% seawater (Morritt and Stevenson 1993). Very early stages of the marsupial development in the isopod Armadillidium vulgare showed a wide range of tolerance to osmolality, total ammonia, and pH (Surbida and Wright 2001), a key strategy that would allow early embryos to withstand high temporal variation in the marsupial environment. The female control over the marsupium fluid during incubation has a positive effect on offspring survival, particularly true for those that live in the transition from marine to freshwater and terrestrial habitats. The evolution of maternal fluid regulation represents a critical step that limits colonization of freshwater habitats, as demonstrated for copepods (Lee et al. 2011). Moreover, freshwater adaptations have broader implications for terrestrial invasions, given the many physiological challenges faced by crustaceans during saline-​to-​freshwater transitions that provided stepping-​ stones for the colonization of land (Wolcott 1992, Anger 2001, Morris 2001, Glenner et al. 2006). Oxygen can be a limiting factor in aquatic systems that affects embryo development (Strathmann and Chafee 1984). Some studies have shown that the viability of embryos isolated from the mother is lower under still water conditions (low oxygen availability) than under stirred water (e.g., the marine crab Carcinus maenas; Hartnoll and Paul 1982), which can be attributed to oxygen limitation. However, embryos of other species, such as the brachyuran crabs Callinectes sapidus, Hepatus epheliticus, Menippe mercenaria, Pilumnus sayi, Portunus gibbesii, and P.  sayi, show successful development in still water (Costlow and Bookhout 1960). Nevertheless, in nature, ventilation of the embryos enhances development (Fernández et al. 2003) and survivorship (Nebeker et al. 1992). Investment in maternal brooding activities when oxygen levels drop is therefore related to the maintenance of healthy embryos (Dick et al. 1998). Brooding females of the amphipod Crangonyx pseudogracilis increased the oxygenation of the brood when exposed to low/​limiting oxygen concentrations (Dick et  al. 1998), and similar observations were reported for brachyuran crabs (Fernández et al. 2002). These findings suggest that brooding enhances the survival of embryos during early development, compensating for the lack of independent uptake of oxygen by the embryo (Dick et al. 1998). When embryos reach independent stages of development (i.e., autonomous heartbeat, developed oxygen exchange system), the oxygenation of the brood by females ceases (e.g., amphipod C. pseudogracialis; Dick et al. 1998).

THE COST OF BROODING Investment in brooding is costly to the parents, and therefore trade-​offs between the costs and the benefits of parental care are important in shaping life history patterns throughout the animal kingdom (Clutton-​Brock 1991). Wilson (1975) defined several selective pressures that affect parental care in aquatic crustaceans, among them the risk of predation on the parent exerting the brood care and critical environmental conditions (e.g., temperature and oxygen availability). Information on the costs of parental care in crustaceans is still scarce, and even more limiting if we try to understand behaviors and costs associated with each selective pressure.



Costs and Benefits of Brooding among Decapod Crustaceans

Predation is considered an important selective force influencing parental brooding behavior and can substantially increase the costs of parental care. The risk of predation associated with brooding can occur during brooding, or subsequently as a result of a deteriorated condition of brooding mothers. In amphipods with active brood care, for example, the motion generated by active embryo ventilation may pose an increased predation risk (Lewis and Loch-​Mally 2010). Hence, the amount of brood care performed by females is likely to be the result of a trade-​off between maximizing reproductive success and avoiding predation. Arundell et  al. (2014) found evidence for changes in brood-​care behavior in response to increased risk of predation (i.e., chemical cues) in the amphipods Crangonyx pseudogracilis and Gammarus duebeni. A  reduction of brooding, with a subsequent earlier release of juveniles during a predation event, was a strategy adopted by the mother (Arundell et  al. 2014). The increase in flapping frequency in females carrying late-​stage embryos may increase visibility to predators. Migration of brooding females to open areas to release the larvae, such as in terrestrial, semi-​terrestrial, or marine burrowing crabs, may also expose them to higher predatory risk. To our knowledge, there are no experimental studies evaluating these hypotheses (see Hartnoll 2006 for a review of this topic). The risk of predation can also extend after brooding ends if the energy budget of brooding females has been decreased since the high costs of ventilation are not compensated for by higher feeding rates during brooding (Schultz and Shirley 1997, Ruiz-​Tagle et al. 2002). Direct costs of brooding can also be associated with embryo losses due mechanical actions during ventilation. In fact, Brante et al. (2003) showed that embryos are lost by females of R. setosum during brooding, and that losses increase as temperature increases (lower latitudes). Since consistent patterns of embryo losses associated with brooding behavior were not found (Brante et al. 2004), this potential cost needs to be further evaluated. There is, however, evidence of higher oxygen demand of brooding females in relation to female size, embryo development, and temperature (Fernández et al. 2000, Baeza and Fernández, 2002, Brante et al. 2003, Fernández et al. 2006). Oxygen demand of brooding females is higher than of non-​brooding females and increases as embryos develop (e.g., Fernández et  al. 2000, Baeza et al. 2002). Moreover, the oxygen demand of brooding females seems to be higher for larger species than in smaller species of crabs (Fernández et al. 2006), which is in line with the association between small body size and brooding that has been described across marine invertebrate taxa (Strathmann and Strathmann 1982). There are also several pieces of evidence that show the influence of temperature on the patterns of oxygen provision and the associated oxygen consumption rates of brooding females (Dick et al. 1998, Baeza and Fernández 2002, Brante et al. 2003, Fernández et  al. 2003, 2006). Increasing temperature and decreased oxygen concentration affected brooding of the amphipod Crangonyx pseudogracilis (a direct developer), inducing females to show a higher rate of putative brooding mechanisms, which could be a response to the interaction of embryonic development with temperature/​dissolved oxygen regime (Dick et al. 1998). In the brachyuran crab R. setosum (an indirect developer), oxygen demand of brooding females doubled as temperature increased from 10°C to 14°C (Brante et al. 2003). It is remarkable, however, that while the cost of embryo ventilation increases with temperature, investment in gonads increased with latitude, suggesting a trade-​off between investment in eggs and the cost of providing oxygen to the embryos at different temperatures (latitudes; Brante et al. 2003). This potential trade-​off needs to be further explored. Therefore, the influence of brooding on the subsequent survival of the mothers might not be uniform across body size, brooding time, and environmental factors. The variation in oxygen demand of brooding females in relation to temperature has been evaluated per unit of time. However, temperature also has an effect on the duration of embryo development (e.g., Wear 1974, Baldanzi et al. 2015, Horváthová et al. 2015, Tropea et al. 2015). Since higher temperatures speed up the development of embryos (Hartnoll 2001), they may also influence

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CONCLUSIONS AND FUTURE DIRECTIONS The broad range of environmental conditions, from marine to terrestrial ecosystems, that shape the extent and type of brooding behaviors among decapod crustaceans pose several questions regarding the evolution of brooding and trade-​offs between costs and benefits of brooding. Moreover, the changing global scenario opens new sets of questions regarding the distribution and extent of brooding in the ocean. In the ocean, the unprecedented climate change, mainly characterized by increasing temperatures, UV radiation, acidification, and hypoxic conditions (Kidwell 2015), may have severe impacts on planktonic stages of crustaceans (Brierley and Kingsford 2009, Storch et al. 2011, Byrne and Przeslawski 2013, Llabrés et al. 2013, Agustí et al. 2015, Carreja et al. 2016). Further research is needed to understand the interactions between these multiple stressors on larval survival and development (e.g., Carreja et al. 2016) and to predict the direction in which brooding patterns might evolve, including also in the equation the consequences of climate change on brooding adults to reach a better understanding of the effects of climate change on marine life histories. Thus, while increasing temperatures might shorten planktonic development and therefore reduce larval mortality, the cost of brooding might increase with temperature. Many questions emerge regarding brooding at higher temperatures: can females cope with a higher increase in brooding behaviors, which already seem to demand full attention and energy toward the end of the brooding period? Can higher ventilation frequency enhance embryo losses, thereby suppressing hatching success? How will changes in temperature impact the total cost of brooding of each reproductive event (e.g., will brooding costs be higher due to an increase in the frequency of behaviors, or lower because of shortened brooding duration)? We need to understand the responses of both brooders and larvae to environmental stressors to predict if the current patterns of low frequency of brooding toward low latitudes will stand (Astorga et  al. 2003, Fernández et  al. 2009, Pappalardo and Fernández 2014). Few studies have focused on these directions, and to our knowledge, none has analyzed multiple stressors on both parents and offspring. At the current rate of climate change, this represents an important and cutting-​edge area of research. We encourage future studies to examine the long-​ exposure effect (potentially multigenerational) of climate-​related stressors on the development of crustaceans, particularly directed at investigating the potential buffering effect of brooding against climate change. The analysis proposed in the preceding will be further enlightening if body size and sister species showing contrasting brooding patterns are compared. The hypothesis that the cost of brooding increases with adult size among marine invertebrates (Strathmann and Strathmann 1982) is supported by comparative studies in brachyuran crabs (Fernández et al. 2006), posing the question of whether changes in body size can be expected among brooders as the environmental factors that force brooding behaviors to generate proper conditions for embryo development change. The costs of brooding for the parents in a changing world need to be weighed against the benefits for the brood. We still need more and better designed studies to demonstrate that brooding will protect the embryos from changing environmental stressors and predation. Intuitively, we can predict positive effects, but currently, we lack effective experiments and ways to measure the benefits of brooding on the survival and development of embryos and larvae of crustaceans.



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5 “THE CARING CRUSTACEAN”: AN OVERVIEW OF CRUSTACEAN PARENTAL CARE

Alexandre V. Palaoro and Martin Thiel

Abstract Many crustacean species are known to provide parental care, with behaviors ranging from ventilating the eggs to providing food for young. This chapter provides an overview of parental care patterns across crustaceans, and then compares crustacean parental care to that of select other taxa (insects, fishes, frogs) that share important traits with crustaceans (exoskeleton, aquatic or amphibious lifestyle, respectively). The aim is to identify gaps in the understanding of the evolution of parental care in crustaceans. We show that nearly all crustaceans provide parental care for early embryos (eggs), while caring for advanced stages is rarer. The most common forms of care are simple behaviors (e.g. fanning and cleaning behaviors), while complex behaviors (e.g. feeding the young) evolved exclusively in groups that also care for longer. Caring is most frequently done by females, while biparental is rare, and exclusive paternal care is nonexistent. When compared across taxa, simple behaviors are also the most common forms of care, and reasons for the evolution of parental care have common themes. First, parental care enhances offspring survival. In crustaceans, early embryo/​egg mortality is apparently high, which might have triggered the evolution of parental care in several crustacean taxa independently. Second, crustaceans that have large eggs and inhabit stable habitats tend to care for longer. Lastly, internal fertilization seems to prevent male crustaceans from caring by not allowing the males to access the eggs and to ensure paternity.

[Parental care] It’s complicated and rare, but I know it when I see it.  —​Royle, Alonzo, and Moore, Current Biology (2016)

Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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INTRODUCTION The preceding quote is a definition expressed by the child of one of the authors of Royle et  al. (2016): she/​he knows what parental is, although she/​he cannot define it. When parents groom, ventilate, feed, or actively defend their offspring it is easy to identify this as parental care, but there are less visible forms of parental behavior, such as juveniles being tolerated to live in the parental dwelling or to snatch food parcels when parents feed on larger prey. Any parental behavior performed toward the offspring, either directly such as provisioning food, or indirectly such as sharing a burrow, can be considered parental care. Ultimately, parental care is any parental trait that enhances the fitness of a parent’s offspring, and that is likely to have originated and/​or to be currently maintained for this function (Smiseth et al. 2012). Parental care usually also carries a cost to parents, for example, by compromising their own survival or reducing the potential for future offspring (Smiseth et al. 2012). Whether to provide parental care and how long to provide it can thus be seen as a trade-​off. On the one hand, the parent increases its current fitness, but on the other hand, the parent may compromise future fitness. Therefore, understanding parental care usually correlates to studying the benefits and costs of such behaviors: benefits should outweigh costs in order to be evolutionarily stable. How these behaviors evolved and why they are maintained are key questions in evolutionary biology that have been posited almost five decades ago (Trivers 1972), but there are still many open questions (Smiseth et al. 2012). Major breakthroughs occurred in the past 10 years through the addition of co-​evolutionary feedbacks, challenging “classical sex roles,” who should care, and other hypotheses (e.g., Kokko and Jennions 2008, Fromhage and Jennions 2016). Discussing these models in detail would go beyond the scope of this chapter (see Royle et al. 2016 and references therein). However, crustaceans represent an ideal model group to explore the conditions for the evolution of parental care, because they inhabit a wide range of habitats with contrasting conditions and parental behaviors are very diverse. Furthermore, parental care has evolved early on in the arthropods, with reports of brood-​carrying females from diverse taxa, starting in the lower Cambrian ~520 mya (e.g., Briggs et al. 2016, Caron and Vannier 2016, Fu et al. 2018, Fig. 5.1). Exclusive maternal care and biparental care are commonly found in recent crustaceans, but in contrast to many other taxa, such as insects, pycnogonids, fishes, and frogs (Kolm and Ahnesjö 2005, Burris 2011, Summers and Tumulty 2014, Gilbert and Manica 2015), exclusive male care has never evolved in crustaceans (Thiel 2007). Furthermore, how much parent(s) care also varies considerably among crustacean

Fig. 5.1. Fossil record evidence of a Cretaceous tanaid providing parental care to eggs within the marsupium and evidence for extended parental care in Fuxianhuia protensa. (A) Female alavatanaids from the Lower Cretaceous amber of Peñacerrada I, Spain, lateral overview of Alavatanais margulisae (holotype MCNA 9583a) showing the oostegites. (B) Camera lucida drawing of the specimen in A, highlighting the oostegites in orange (modified from Sánchez-​García et al. 2018). (C) Detail of right oostegites I–​IV of the same specimen. (D) Detail of the third and fourth right oostegites of A.  carabe (MCNA 13890). (E)  Fossil evidence for extended parental care in Fuxianhuia protensa ELI MU76A-​a, life assemblage including a stage 29—​most likely sexually mature—​adult individual and four stage 8 juveniles. (F) ELI MU76B-​b, counterpart, articulated stage 8 juvenile with preserved eyes. (G) ELI MU76A-​c, articulated stage 8 juvenile with preserved gut; note the presence of reduced tergites underneath head shield. (H) ELI MU76A-​d, two articulated stage 8 juveniles with preserved gut and walking legs. See a color version of this figure in the centerfold. Abbreviations: Abn = abdominal tergite; hs = head shield; tf = tail flukes; Thn = thoracic tergite; wl = walking legs. (A–​D) from Sánchez-​García et al. (2017) under © Creative Commons License; (E–​H) from Fu et al. (2018), under © Creative Commons License.   

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FORMS OF PARENTAL CARE Parental care can be divided into two main phases, pre-​and post-​oviposition care. Pre-​oviposition care can be defined as investments in the egg (e.g., dormancy eggs in fairy shrimp, or ephippium in Cladocera; Egloff et al. 1997), choosing where to oviposit these eggs (Kosobokova et al. 2007), or whether to invest in eggs with high or low yolk content (Kiørboe and Sabatini 1994). Behaviors such as construction of a burrow that is later used to tend to fertilized eggs are also included in “pre-​ oviposition care.” Any behavior performed after the egg is fertilized is called “post-​oviposition care,” which is the central focus of this review. Post-​oviposition care may vary from juvenile tolerance (e.g., burrowing crayfish; Dalosto et al. 2012), to defending offspring against enemies, and providing food for growing juveniles (e.g., Linsenmair 2007). Extreme forms of care involve active management of the offspring environment, such as maintaining environmental conditions within a bromeliad (Metopaulias depressus; Diesel and Schubart 2007). To organize our review, we divide post-​oviposition care into four principal phases of care: (1) developing embryos, (2) advanced embryos, (3) juveniles, and (4) subadults. In the majority of crustaceans, some form of care for developing embryos (phase 1) is provided, usually by females (see Chapter 4 in this volume). The developing embryos are incubated on or in the maternal body until release of larvae. When larvae hatch, parental care ends in most crustacean taxa, but in some species, especially those that have conquered land or freshwater, embryos continue to develop on/​ in the females, which we call care for advanced embryos (phase 2). Growing juveniles receive parental care (phase 3) in many species with direct development, where the extension of parental care is highly variable depending on the species and environmental conditions. Finally, parents of some species even provide care to large offspring that are close to becoming sexually mature themselves (phase 4). Herein, we briefly describe how parents care for their offspring and which phase of post-​ oviposition care is commonly found in the main crustacean groups. We also note who is caring, i.e., female, male, or both parents. Class Branchiopoda Branchiopods inhabit ephemeral ponds that freeze, dry up, or are exposed to other types of environmental stress. Thus, all branchiopods produce resistance eggs and oviposit them. These dormant eggs, or ephippia in Cladocera, withstand these extreme conditions until the environment becomes favorable again, and then they hatch (Lindley 1997). Tadpole shrimps (genus Triops)



“The Caring Crustacean”

produce fertilized dormancy eggs but do not produce other types of eggs as found in anostracans (Seaman et al. 1991). Males grasp the females and position their gonopores on top of the females. After sperm is transferred, males release the female and either seek other females or die (notostracan males are short-​lived; Meintjes 1996). Females then deposit the eggs inside brood pouches, where fertilization occurs (Longhurst 1955). Females carry the fertilized eggs for a brief period (~19 hours in Triops longicaudatus; Grigarick et al. 1961, Scott and Grigarick 1978), after which they are released in the water column and sink to the bottom to adhere to any available surface (Seaman et al. 1991, Meintjes 1996). Hence, tadpole shrimps provide solely pre-​ovipositional parental care; all their investment occurs until the production of the egg. Soon after the eggs are released, the females deposit more eggs in the brood pouch (Longhurst 1955). Male anostracans transfer their sperm to females and swim away, attempting to find more mates (Browne 1980). After copulation, females move their eggs into the ovisacs, where eggs are fertilized. As the eggs begin cleavage, the shell glands positioned beside the ovisac deposit an oil-​like secretion into the ovisac. This oil-​like secretion is responsible for producing cysts. These cysts are constantly turned around by the muscle contractions of the ovisacs. Cysts are then released through the genital opening into the water column (Plodsomboon et al. 2012); this is how dormancy eggs are produced in most anostracans. However, Artemia may also produce uncoated eggs and tend them until release as metanauplii (Browne 1980). Thus, the key difference between cysts and uncoated eggs is parental care: while females care for the uncoated eggs in their ovisac until they are released as metanauplii, cysts do not enjoy post-​ovipositional parental care (Browne 1980). Adult females are also constantly producing eggs, and this carries costs: when food is limited, high reproductive output reduces female lifespan (Browne 1982). Therefore, in anostracans, fertilized eggs are protected in the female’s ovisac, and eggs are constantly being moved around by muscle contractions. The parthenogenetic life cycle of diplostracans differs considerably from the sexual phase. Males are not involved in the parthenogenetic life cycle. Females produce the parthenogenetic eggs in the ovaries, release them in their brood pouch, and care for them until they are released as metanauplii (Spinicaudata and Laevicaudata) or juveniles (Cladoceramorpha; Olesen 2013). While the parthenogenetic eggs are inside the female’s brood pouch, they are constantly aerated by the feeding current of the mother (Patton 2014); in Daphnia, the egg current is separated from the feeding current altogether (Seidl et  al. 2002). Interestingly, Moinidae, Onychopoda, and Penilia provide nutrients to the parthenogenetic embryos via a placenta-​like organ, the “nährboden,” until they are released as juveniles (Egloff et al. 1997). The parthenogenetic eggs in these groups are yolkless, and thus depend on the nährboden to develop. The same pattern does not occur in fertilized eggs: the nährboden does not develop when females are inseminated. To produce the dormancy eggs, male diplostracans typically clasp the female’s carapace, transfer sperm, release the female, and search for a new mate. Female diplostracans do not store sperm, and mate repeatedly before releasing their offspring; thus, males are typically on the prowl for females (Sigvardt and Olesen 2014). When males transfer their sperm, females supposedly close their valves and release their eggs on top of the sperm; fertilization apparently occurs within the female’s branchial cavity (Patton 2014). Fertilized eggs are then moved to the brood chamber, where they develop the external membranes and become resistant. These eggs are then released in clutches (Patton 2014). Overall, female diplostracans provide parental care for their parthenogenetic eggs in the form of water currents, and nutrients in some species. Class Remipedia Remipeds are sequential hermaphrodites that have never been seen copulating (Koenemann and Iliffe 2013). Some records, though, suggest that individuals move toward substrata where other

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Reproductive Biology individuals have previously been (Koenemann et al. 2007). If true, this would hint at an external fertilization of the eggs. However, to date, females (or males) have never been found carrying their brood; not even eggs (fertilized or unfertilized) were found. Therefore, we cannot ascertain whether remipeds provide parental care or not (Koenemann and Iliffe 2013). Class Cephalocarida Cephalocarids are simultaneous hermaphrodites with probable self-​fertilization. There are no records of “true” males or females, and no records of copulation as well (Addis et al. 2013). It is thus hard to distinguish the role of each sex. The terminal zone of the ovaries and the vas deferens form two common genital ducts, which open up in the hermaphroditic genital pore, where mature eggs and spermatozoa may come in contact. From there, the fertilized eggs should go to the paired brooding sacs, where they stay until they hatch as free-​living metanauplii with three or four trunk segments, depending on the species (Hessler et al. 1995). There are no records of any sort of care provided toward the developing egg in the brooding sac. There is, though, one suggestion that adults of Lightiella magdalenina may provide post-​ovipositional care:  three-​segmented metanauplii have been found both inside the egg and attached to the first abdominal segment of its parent (Addis et al. 2013). Therefore, it is possible that L. magdalenina cares for hatched larvae, but this needs to be confirmed. Class Maxillopoda/​Infraclass Ascothoracida Most ascothoracidan males are dwarf and may live near the sessile female or within her brood chamber (Kolbasov et al. 2008a, but see Petrarcidae and Gorgonolaureus; Grygier 1987). There are no records of how and when fertilization occurs, but since males may live within the female, fertilization probably occurs in the dorsal brood chamber, where the fertilized eggs are enclosed in a matrix that completely surrounds the eggs and which disintegrates as eggs develop (Grygier 1981). When the matrix disintegrates, the brood is released as late first instar metanauplii (Itô and Grygier 1990). Thus, this matrix may hold the eggs together and facilitate oxygen transfer, although there are no records of this. Interestingly, the hermaphroditic Petrarcidae do not have a brood chamber: they attach the eggs to the rear of their carapace or lay them inside the gall they form when parasitizing a host. This does not mean that they are not tending to their eggs; laying the eggs within the gall may be an adaptation to the specialized endoparasitic lifestyle (Grygier 1985). Hence, ascothoracidans provide exclusively maternal care until larvae are released. Class Maxillopoda/​Infraclass Cirripedia Male cirripeds may either broadcast their sperm (Barazandeh et al. 2013) or transfer them directly to the female with their long penises (Buhl-​Mortensen and Høeg 2013). Transferring sperm directly is the most common strategy and may correlate with other morphological adaptations: in many species, males are dwarf and attach directly to the females to deliver sperm (Dreyer et al. 2017). Sperm is transferred to the female’s mantle cavity, which is filled with seawater and contains the mature eggs inside (Høeg 1995). The fertilized eggs are then cared for within the mantle cavity, where the flowing seawater aerates the eggs (Høeg 1995). Cirripeds vary in how much they tend for the eggs. Most species tend to their eggs until they are released as free-​swimming nauplii, such as Scalpellum scalpellum and Arcoscalpellum michelottianum. But others, such as Verum brachiumcancri and Weltnerium nymphocola, release their larvae as cyprids (Buhl-​Mortensen and Høeg 2013). The difference between these two forms of care is the distance in which the offspring are able to disperse after being released. All larvae are lecithotrophic, which means that they do not feed; once the



“The Caring Crustacean”

energy reserves are depleted, larvae need to settle and go through metamorphosis (Buhl-​Mortensen and Høeg 2006). Cyprids, thus, are not able to disperse as far as nauplii. In androdioecious species, where larvae settle may have profound impacts on fitness. Larvae develop as hermaphrodites when they settle in areas isolated from other individuals, but develop into males when other individuals are present (Høeg et al. 2016). If sexual selection is strong in the population, this life history developmental “decision” could greatly affect the fitness of the offspring. Therefore, the extent of the exclusive maternal care (or hermaphroditic care) could be crucial for both parent and offspring in this group. Class Maxillopoda/​Subclass Tantulocarida Tantulocarida are small ectoparasitic crustaceans that have a complex life cycle comprising a parthenogenetic and a sexual phase. Unfortunately, we have no information on the sexual phase of the life cycle, which hinders us from inferring about parental care; we can only say what larvae do. Tantulus larvae attach to a host and can either become “parthenogenetic females” or carry a sexual individual. The parthenogenetic females consist of a cephalon, a neck, and a posterior cuticular sac (brooding sac). Inside these brooding sacs, parthenogenetic eggs develop until they are released as other tantulus larvae. Tantulus larvae that carry a sexual individual attach to a host, and the developing sexual individual uses a specialized cord to feed off the host. Once the sexual individual develops, it possibly leaves the tantulus larva to fertilize its eggs, but this has never been observed (Kolbasov et al. 2008b). From the available information, we cannot comment on parental care for this group because we do not know their complete life cycle. Class Maxillopoda/​Subclass Pentastomida Males mature earlier and have a shorter lifespan than females. Males inseminate the immature females by inserting their penis directly into her spermathecae. After insemination, males die, and females store the sperm and continue their life cycle (Riley and Self 1980). Thus, copulation and fertilization are temporally separated in pentastomids: females receive sperm that will be kept until the ovaries are mature, later during her development (Riley 1972). After females mature, eggs are continuously produced, and as the eggs descend the long and convoluted ovarian duct, sperm is added. Development depends on the number of intermediate hosts the species use. Kiricephalus, for instance, parasitizes two intermediate hosts before reaching t he definitive host (Riley and Self 1980). Sebekia, on the other hand, infects only one intermediate host ( Junker et al. 1998). The development of fertilized eggs is also variable, and much of this variation is explained by species-​specific developmental differences. Fertilized eggs might be released as cysts that infect intermediate hosts through direct transmission; they might also be auto-​reinfected by the host (Banaja et al. 1976), or develop directly without a larval stage (Banaja et al. 1975). Despite these several types of infections and modes of development, pentastomids do not show parental care. Class Maxillopoda/​Subclass Mystacocarida Male mystacocarids do not have any specialized morphology that would suggest that sperm is transferred internally; female morphology suggests the same pattern (Hessler and Elofsson 2012). Thus, although fertilization has never been reported, external fertilization is suggested for mystacocarids. Females lay a single (unfertilized) egg onto which males eject their sperm. The egg, then, supposedly hatches as a nauplius larva (Hessler and Elofsson 2012). Overall, there is no evidence that suggests any sort of parental care in mystacocarids.

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Reproductive Biology Class Maxillopoda/​Subclass Copepoda In most planktonic copepod species, males find females by actively searching for female trails to follow (Titelman et al. 2007). This mating system implies that, once males inseminate the female with their spermatophore, they decouple and try to find another mate. Even in species that guard females for a long period (parasitic poecilomastoid), males do not stay with the female after copulation (Boxshall 1990). Fertilization takes place inside the female, and the fertilized eggs may take several routes: they can be broadcast into the water column, maintained within egg sacs (or egg strings; Ohman and Townsend 1998), encysted, or attached to a substratum (Kiørboe and Sabatini 1994, Dahms and Qian 2004). The fertilized eggs that stay within the egg sac enjoy increased survival rate compared to other eggs (Kiørboe and Sabatini 1994). However, there is a trade-​off between female size and carrying egg sacs. By carrying egg sacs, females become more visible to predators and hence have increased mortality rates (Bollens and Frost 1991). If a female already has a large body size, it does not pay off to increase her predation rate by carrying the eggs. Therefore, pelagic females of medium-​sized species (e.g., calanoids) typically broadcast fertilized eggs, while pelagic females of small-​sized species (e.g., cyclopoids) keep them in the egg sac (Kiørboe and Sabatini 1994, Ohman and Townsend 1998). Despite that, egg-​carrying is common among copepods: planktonic Calanoida (e.g., Pseudodiaptomus, Euchaeta; Kosobokova et  al. 2007), freshwater Cyclopoida (e.g., Cyclops, Cyclopina; Nilssen 1980), Harparcticoida, Canuelloida, and even the parasitic copepods of the Siphonostomatoida, Mormilloida, and Mormonilloida carry their eggs until they hatch as nauplii (Huys et al. 2007). Females of some species have other adaptations to carry the eggs. Some Harpacticoida, such as Phyllopodopsyllus and the family Tetragonicipitidae, have a foliaceus leg 5 that covers the egg mass in the ventral region of the genital area. Apparently, the foliaceus leg reduces attrition during swimming (Gamô 1969, Boxshall and Halsey 2004). The cyclopoids Notodelphyidae and Bupropidae form a brood pouch with their thoracic somites, which can be seen as a form of viviparity (Boxshall and Halsey 2004). The parasitic poecilostomoid family Nucellicoilidae is surrounded by a membranous tube that might be originated by the host. Once surrounded by the tube, eggs and developing nauplii fill the tube (Lamb et al. 1996). In Maemonstrilla spp., females deposit the egg mass between the legs on urosome ovigerous spines, which is seen as a unique type of brooding eggs in copepods: a sub-​thoracic brood chamber (Grygier and Ohtsuka 2008). The egg mass is deposited between the legs on the ovigerous spines (Grygier and Ohtsuka 2008). All species cited in the preceding sentences, which show some sort of viviparity, are symbiotic. It seems that carrying the eggs in or on the body is correlated to the small spaces that come with a symbiotic lifestyle (Grygier and Ohtsuka 2008). Despite these adaptations, copepod maternal care seems to last only until eggs hatch as nauplii (or copepodids). Class Ostracoda Male ostracods cling to the female’s carapace and insert their penis (or hemipenis) inside the female’s carapace, reaching the inner side of the vaginal space and releasing the spermatozoa (Horne et al. 1998). The unfertilized eggs meet sperm inside the uterus, where fertilization takes place. Ostracods thus have internal fertilization (Cohen and Morin 1990). The recently fertilized eggs may follow three paths. Fertilized eggs (or dormancy eggs in some instances) may be broadcast into the water column, as in Bairdoidea; eggs may be glued to suitable substrata (e.g., Eucypris, Cypria); or, eggs may be redirected to the posterior side of the carapace (the domicilium), where fertilized eggs are cared for in all Myodocopida and Platycopida (Horne et al. 1998). Ostracods have direct development, which means that both broadcast and brooded eggs hatch as juveniles (Cohen and Morin 1990). During the period of parental care, eggs enjoy higher survival rates and active ventilation



“The Caring Crustacean”

from the mother (Danielopol et al. 1996). Fossil evidence suggests that egg-​caring may have been an adaptive strategy for unstable environments: ventilating the eggs may have given an advantage to egg-​caring species ( Jarvis et al. 1988). Interestingly, the ostracod fossil record (e.g., Beyrichioidea, Kloedenellidae) allows us to infer on parental care due to sexual dimorphism: egg-​caring females have an enlarged domicilium compared to males (Siveter et al. 2007). Overall, ostracods have exclusive maternal care, tending to the eggs until they are released as juveniles. Class Malacostraca/​Subclass Phyllocarida/​Order Leptostraca Information on reproduction is scarce for leptostracans. Most of our knowledge comes from Nebaliidae and Paranebalia belizensis. Copulation has never been seen, but males supposedly swim up from the benthos to locate females (Rainer and Unsworth 1991). Mature females occur in extremely high densities compared to males, so it is likely that after copulation males keep swimming to find more females (Vetter 1996). Fertilized eggs are then carried within a brood chamber, where they are aerated by the female until they hatch at advanced juvenile stages (Modlin 1996). Females apparently pay a large cost for caring, which may be so high as to increase female mortality. The presence of the eggs interferes with the production of feeding currents. Hence, it is possible that females do not feed during parental care (Vetter 1996). By not feeding, females may be weak after releasing the juveniles, which may explain the high female mortality when juveniles appear, and explain the apparent semelparity (Vetter 1996, Modlin 1996). As far as our knowledge allows, leptostracans present exclusive maternal care until the juvenile phase. Class Malacostraca/​Order Stomatopoda In stomatopods, parental care is usually provided by females, which incubate their larvae on their maxillipeds (Caldwell 1986). This is a highly unusual form of brooding, and females have particular cement glands that aid in binding the fertilized eggs together in a mass that is held by the maxillipeds (Wortham-​Neal 2002). The female ventilates and grooms the eggs, and using their mouthparts they clean off infected or dead eggs (Montgomery and Caldwell 1984). During incubation females can drop the egg mass in their cavities, e.g., when defending the burrow against potential invaders, and later pick it up again (Dingle and Caldwell 1972, Herbert 2011). Females of Squilla empusa have been observed to drop the eggs mass one to two days before the larvae hatch (Wortham-​Neal 2002). In Neogonodactylus bredini the hatched larvae remain for a few days in the brood cavity, where they are protected by the female, before leaving and joining the plankton (Dingle and Caldwell 1972). Males of N.  bredini allow receptive females into their burrow, where mating occurs. While cohabiting with the female, males vigorously defend their burrow (Shuster and Caldwell 1989). After the female ovulates and produces the egg mass, the males surrender the highly valuable burrow to the female, thereby offering an essential reproductive resource to the female (Caldwell 1986). Brooding females then aggressively defend the burrow against intruders, but if evicted might take the egg mass with them (Montgomery and Caldwell 1984, Fig. 5.2). In some species, biparental care for offspring has evolved. In Pullosquilla thomassini both females and males care for the egg mass, manipulating and cleaning the eggs, moving them within the burrow and guarding them; in protected laboratory environments, embryos developed successfully even when only one parent was present (Wright and Caldwell 2015, Fig. 5.3). In Lysiosquilla sulcata the sexes divide the labor: females care for the eggs while males hunt and feed the females, which can clearly be considered biparental care, even though the male does not seem to directly manipulate the developing embryos (Caldwell 1991). Both species live in sandy bottoms where costs to

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Fig. 5.2. A female Pullosquilla litoralis (Stomatopoda) carrying the egg mass. See a color version of this figure in the centerfold. Photo courtesy of Roy L. Caldwell.   

build new burrows are assumed to be high due to the need of abundant mucus for stabilizing the burrow (Caldwell 1991). Class Malacostraca/​Superorder Syncarida We do not know what males do after copulations, but we know that males have a copulatory organ, the petasma, that transfers spermatophores to the females (Ahyong 2016). Fertilization probably occurs in the female’s oviduct (Smith 1908), which then deposits the fertilized eggs on the substratum one at a time (Camacho and Valdecasas 2008). All naupliar stages are completed within the egg, and hence, there are no free-​swimming larvae: all individuals hatch as juveniles (direct development; Williams 1965). There is no record of parental care in syncarids. Class Malacostraca/​Superorder Peracarida All peracarids brood their embryos in a ventral brood pouch (marsupium), hatching into fully developed juveniles. Mating in peracarids is diverse, and fertilization in most species occurs in the marsupium. Male amphipods inject sperm into the marsupium, followed shortly thereafter (minutes) by spawning of the eggs into the marsupium (Krishnan and John 1974). In most isopods, a true copula occurs and males inject sperm in the female spermatheca (Wilson 1991). Females can store sperm for long periods (~months) and fertilization is thought to be internal during oviposition (Zimmer 2001). Multiple paternity of clutches has been documented in amphipods and isopods, and is also likely for other peracarids (Birkhead and Pringle 1986, Dennenmoser and Thiel 2015). Mate guarding occurs in some amphipods and isopods ( Jormalainen 1998). Following fertilization, the embryos are incubated in the ventral marsupium. In Thermosbaenacea, females have a dorsal brood pouch where embryos are incubated to advanced stages (Olesen et al. 2015), and in some Tanaidacea females the embryos develop in the inflated oostegites, which form an ovisac (e.g., Johnson and Attramadal 1982). Females ventilate the developing embryos (Dick et al. 1998, Tarutis et al. 2005), they manipulate embryos in



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Fig. 5.3. Eggs lose mass when parental care is not provided in Pullosquilla thomassini. On the other hand, when eggs enjoy biparental, maternal, or paternal care, eggs do not lose mass. From Wright and Caldwell (2015) with permission from © Oxford University Press.   

their brood pouch (e.g., Beermann et al. 2015), manage the marsupial environment (Morritt and Spicer 1996, Surbida and Wright 2001), and they even tolerate juveniles in the brood pouch to share their meals (e.g., Thiel 2007). In terrestrial isopods, females have particular structures (cotyledons) thought to provide nutrition to developing embryos in the marsupium (Hornung 2011). In several species, post-​marsupial care of growing juveniles takes place (Thiel 2007). Carrying of juveniles is found most commonly in epibenthic suspension feeders such as caprellid amphipods or arcturid isopods (Fig. 5.4). Most likely this behavior has evolved to lift small juveniles out of the benthic boundary layer into favorable feeding environments (Thiel et al. 1997). In the offspring-​ caring caprellids Caprella scaura and C. monoceros, juveniles that enjoyed maternal care grew significantly faster than those raised without their mothers (Aoki 1997). Care of growing offspring is also common in species that inhabit dwellings (Thiel 2007, Poore et  al. 2018). Juveniles benefit from better protection against predators and other environmental stressors in the safe dwellings of their parents (Thiel 1999a) and they usually stay until they are able to efficiently construct or secure their own dwellings (Thiel 2001). In most species, parental care is exclusively the task of females, but in some species biparental care has evolved (Thiel 2007). Natural history observations strongly suggest that in those species with biparental care, the dwelling is of high value for family groups and it is difficult for single individuals to construct or conquer new dwellings. For example, in the amphipod Peramphithoe stypotrupetes, the parents excavate a burrow in kelp stipes, where they care for up to three subsequent broods simultaneously (Conlan and Chess 1992). In the desert isopod Hemilepistus reaumuri, the male and female collaborate during the wet season in the construction of a deep burrow in which they then raise their single brood (Linsenmair

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Fig. 5.4. Example of maternal care in peracarids. A female Astacilla longicornis carrying the brood on its antennae lifting the growing juveniles into better current environments favorable for suspension feeding. See a color version of this figure in the centerfold. Photo courtesy of Lill Augen.   

2007). During the dry season, the parents defend the burrow against conspecifics and forage for food in the surroundings, which they then carry back to the burrow to feed their growing offspring; large juveniles initiate their independent life at the beginning of the next wet season (Linsenmair 2007). Also, in the mysid Heteromysis rapax, in which parent-​offspring units inhabit the large shells of hermit crabs, it appears that competition might make it difficult for small juveniles to find and conquer a suitable new host (Vannini et al. 1993). In all these cases of biparental care, some offspring grow to subadult sizes in the parental dwellings, and for the amphipod Leucothoe spinicarpa it has even been suggested (based on the demographic structure of the family groups) that some offspring might inherit their ascidian host from their parents (Thiel 1999b). Even though male participation in parental care tasks clearly has evolved in some peracarid species, no case of exclusive paternal care has been reported. Class Malacostraca/​Order Euphausiacea In euphausids, copulation and fertilization are temporally separated. Males transfer spermatophores to the female’s thelycum, the genital opening, when it opens. Afterward, males move on to find other mates. At that point, however, females are still maturing their eggs (Ross and Quetin 2000). Females still require ~2 weeks for the eggs to reach maturation to be fertilized. By that time, the male that transferred the spermatophore should be long gone (Ross and Quetin 2000). Fertilized eggs, then, are broadcast into the water column in most species. However, Nematoscelis, Nyctiphanes,



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Stylocheiron, and Pseudeuphasia have a pair of membranous sacs attached to their thoracopods (Richter and Scholtz 2001). These sacs hold fertilized eggs until hatching as metanauplii. Eggs are kept attached to each other by a thin mucous membrane secreted by the female, which also oxygenates the eggs and removes any dead eggs (Gómez-​Gutiérrez 2003, Gómez-​Gutiérrez and Robinson 2005). Therefore, the few euphausiid species that carry their eggs provide exclusive maternal care. Class Malacostraca/​Order Decapoda In Decapoda, males transfer their sperm within spermatophores that are attached near the oviduct, or directly injected into the female’s body; hence, internal fertilization is the norm in many decapods. After copulation, male behavior varies considerably, from staying with the females inside a burrow for extensive periods (e.g., burrowing crayfish; Palaoro et al. 2016) to moving away to find more mates right after copula (e.g., shrimps; see Chapter  10 in this volume). The only decapod group that does not care for their eggs are the dendobranchiate shrimps (e.g., peneids). However, not even all of these shrimps follow this pattern:  the Luciferidae shrimps care for their eggs until they hatch as nauplii (Richter and Scholtz 2001). All other decapods care for their fertilized eggs at least until eggs hatch into nauplii. Females do most of the caring, but some instances of biparental care are known (Vogt 2013). The main difference is in the length and the complexity of parental care. Marine species mostly care until the eggs hatch into nauplii, but some species may care for longer, especially those that are commensals on/​in other organisms (e.g., Tunicotheres moseri; Dromiidae, Bolaños, et al. 2004, McLay and Becker 2015). All freshwater species have direct development, and females care for eggs until they hatch as juveniles. In some species, juveniles may even stay for longer, as in freshwater crayfish (Vogt 2013). Decapods that have conquered land (or at least are semi-​aquatic) provide the most extensive and complex kind of parental care, with some records of sociality in the group (Diesel and Schubart 2007, Vogt 2013, Fig. 5.5). Therefore, habitat apparently is a strong selective force of parental care in decapods. For an in-​depth review of this group, see Chapter 4 in this volume.

GENERAL PATTERNS: CRUSTACEANS, INSECTS, FISHES, AMPHIBIANS Maternal care is the norm in crustaceans (Fig. 5.6). Few groups are exclusively non-​carers (e.g., Syncarida), while most groups have species that carry the eggs in particular bags (e.g., Copepoda) or brood pouches (e.g., Peracarida). Biparental care is also rare; male involvement is only found in the stomatopod Pullosquilla, several peracarid species, the bromeliad crab, and some burrowing crayfish. No case of exclusive paternal care has ever been reported in crustaceans. Furthermore, caring for advanced embryos, juveniles, and subadults is rare, only occurring in Peracarida and Decapoda (Fig. 5.6). Outside of the Crustacea, not caring is the norm. If we consider that there are more than 900,000 of described species of insects (Resh and Cardé 2009), and that caring has been reported for roughly 2,000 genera (Machado and Trumbo 2018), not caring for offspring is widespread in insects. Among the insect species that care, maternal care is most common. Biparental care is uncommon, occurring in Coleoptera, Hymenoptera, and Thysanoptera, while paternal care is very rare, occurring only in a few species of Hemiptera and Thysanoptera (Machado and Trumbo 2018; Fig. 5.7). According to our classification, most insects do not care for juveniles; they cease caring during larval stages, and only rarely provide care when offspring achieve nutritional independence (e.g., Cryptocercidae cockroaches; Nalepa and Bell 1997).

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(A)

(B)

(C)

(D)

(E)

(F)

(G)

Fig. 5.5. Extended parental care in freshwater decapods. (A and B) Female of semi-​terrestrial Geosesarma sp. carrying advanced embryonic stages and juveniles. (C) Free-​living hatchling of Geosesarma krathing showing well-​developed eyes and claws (arrows). (D) Terrestrial Geosesarma carrying juveniles on top of the carapace. (E) Mother and young (arrow) of the Jamaican bromeliad crab Metopaulias depressus in a water-​filled leaf axil of a bromeliad. (F) Jamaican snail crab Sesarma jarvisi breeding in a water-​filled snail shell. (G) Marbled crayfish adult with the juveniles (arrow) in the abdomen and walking on the adult. See a color version of this figure in the centerfold. Figures modified after Vogt (2013) with permission from © John Wiley and Sons.   



“The Caring Crustacean”

Taxa

Early embryo

Advanced embryo

Juvenile

Subadult

Anostraca Notostraca

no care

Diplostraca Remipedia

no care1

Cephalocarida Ascothoracida Cirripedia Tantulocarida Pentastomida

no care

Mystacocarida

no care

Copepoda Ostracoda 1

Leptostraca Stomatopoda Syncarida

no care

Isopoda Amphipoda Emphausiacea Decapoda

Fig. 5.6. Overview of crustacean parental care. Columns indicate the duration of care; if a group release the offspring as juveniles (caring until the advanced embryo stage), the bar will appear until advanced embryo. White bars indicates maternal care, while gray bars indicate biparental care. Bar length indicates how common care is in that taxonomic group. ¹ indicates that it is assumed but we do not have rigorous descriptions.   

Not caring is also common in fishes. Care occurs in ~30% of fish families, and of these ~80% correspond to paternal care. Biparental care is the least common form of care (Mank et al. 2005), and in some species, such as Sarotherodon galileaus and Ameiurus nebulosus, patterns of care are labile, and paternal, biparental, and maternal care coexist (Blumer 1979, Balshine-​Earn 1995). Most groups only care for eggs, while caring for juveniles is rare (e.g., Cichlasoma nigrofasciatum), but once juveniles reach nutritional independence parents cease caring (Balshine 2012). A similar pattern is found in amphibians. Parental care has evolved in approximately ~15% of anuran species, with maternal and paternal care being similarly common. Biparental care is also rare. When parental care occurs, caring for juveniles (tadpoles) is common and reaches extremes, such as feeding trophic eggs to tadpoles; feeding of young is rare, though (Balshine 2012). Interestingly, one case of food provisioning to developing offspring with nurse eggs is reported from a small frog (Oophaga pumilio) breeding in the leaf axils of tropical bromeliads (Dugas 2017), the same habitat where the bromeliad crab provides food to its developing larvae (Diesel and Schubart 2007).

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Taxa

Early embryo

Advanced embryo

Juvenile

Subadult

Branchiopoda Remipedia

no care1

Cephalocarida Maxillopoda Ostracoda Stomatopoda Syncarida

no care

Peracarida Eucarida Insecta

Pisces

Amphibia

Fig. 5.7 Overview of parental care in crustaceans, insects, fishes, and frog. Columns indicate the duration of care. White bars indicate maternal care, gray bars indicate biparental care, and black bars indicate paternal care. Bar length indicates how common care is in that taxonomic group. ¹ indicates that it is assumed but we do not have rigorous descriptions.   

If we compare crustaceans to these three groups, we can observe a few differences. First, not caring seems to be the norm, but not for crustaceans, where some form of maternal care is common. And no care is found only in a few groups, such as endoparasites and small syncarids. Second, caring for juveniles is rare, but common in freshwater crabs and isopods, and less so in frogs. Third, paternal care occurs in all three groups (insects, fishes, frogs), although rare in insects; but it does not occur in crustaceans. We tackle each of these issues in the following.

WHY DO MOST CRUSTACEANS CARE FOR DEVELOPING EMBRYOS? Parental care is expected to evolve when care is required to increase offspring survival (Klug et al. 2013). If offspring survival without care is relatively high, then parental care should only evolve in relatively few instances. However, offspring survival encompasses the survival of all developmental stages, as we discussed in our review, but the factors that affect survival of developing embryos differ from those contributing to the survival of advanced embryos, juveniles, or subadults. Thus, to provide a more robust discussion, we separate offspring survival into two phases. First, survival of



“The Caring Crustacean”

developing embryos, hereafter referred to as “egg survival” or “egg mortality,” is affected by all post-​ ovipositional care behaviors that might increase the survival of the developing embryos (i.e., first column of Figs. 5.6 and 5.7). Second, the survival of advanced embryos, juveniles, and subadults, hereafter referred to as “juvenile survival,” depends on all post-​ovipositional care behaviors that might increase the survival of advanced developmental stages (i.e., second, third, and fourth column of Figs. 5.6 and 5.7). Egg mortality is likely to be extremely high if crustaceans would not tend for them:  crustacean eggs do not have any adaptations in their membranes to withstand adverse environmental conditions (see Chapter 4 in this volume). In vitro studies mimicking the marsupial fluid of isopods show that eggs raised outside of the salinity or osmolarity range of the marsupial fluid have higher mortality (e.g., Charmantier and Charmantier-​Daures 1994, Morritt and Spicer 1996, Surbida and Wright 2001). Several in vitro studies in other groups show the same pattern: eggs raised outside of the range of the maternal micro-​environment have higher mortality (e.g., crabs, Bas and Spivak 2000, shrimps, Ituarte et al. 2005). Crustaceans also do not lay their eggs in favorable areas, as they do not have any sort of ovipositor through which they could deposit the eggs in these environments. Therefore, crustacean eggs need to be maintained in particular conditions to survive, and parents cannot choose a favorable environments in which egg survival could be higher without their presence. The pattern of crustacean egg mortality becomes clearer when we compare crustaceans to insects. Insect eggs have two key adaptations that can explain the rarity of parental care of developing embryos. First, the resistant egg shell (i.e., amniotic egg; see Zeh et al. 1989) increases resistance against desiccation and permits oxygen transfer. Second, the ovipositor allows egg-​laying in safe places and/​or favorable environments (Hinton 1981, Zeh et  al. 1989). The amniotic egg and choosing favorable environments to oviposit are considered a form of parental care (Smiseth et al. 2012) since they increase egg survival. Since crustaceans have neither adaptation, egg mortality should be particularly high, which might explain why most crustaceans care for developing embryos (Fig. 5.7, first column). Another important source of egg mortality is brood parasitism. Even though crustaceans are frequently observed grooming and cleaning early embryos (and juveniles), diverse egg parasites manage to invade clumped egg masses, enhancing the risk of catastrophic brood failure, e.g., by preying on the developing eggs (e.g., Kuris and Wickham 1987, Costello and Myers 1989, Baeza et al. 2016). Brood parasites can be found in many crustacean groups and they comprise mostly nemerteans and copepods, but also amphipods and isopods (e.g., Green 1958, Sheader 1977a, 1977b, Kuris et al. 1991). Some of these egg predators have evolved astonishing types of mimicry, resembling eggs in shape, size, and color (Wakabayashi et al. 2013), thereby likely avoiding detection and removal during the regular cleaning activities of the parents. Interestingly, raising the eggs in vitro typically requires adding an anti-​parasitic in the water, which hints at the danger that brood parasitism poses to early embryos (Kuris et al. 1991, see Chapter 4 in this volume). Additional evidence for the potential threats of brood parasitism also comes from morphology. In diverse groups, special appendages (and behaviors) have evolved to manipulate the egg mass and clean out parasitized embryos (e.g., Förster and Baeza 2001, Ferreira and Tavares 2018). Therefore, it seems that crustacean eggs might also incur a high mortality risk from parasites when raised without their parents. Despite the likely high costs of parasites and predators on egg survival, simple behaviors seem to be effective to decrease such costs. In a meta-​analysis, Santos et al. (2017) showed that eggs have a lower mortality whenever insects present cleaning behaviors or oviposit the eggs within burrows or crevices. These behaviors are apparently effective in keeping parasites, fungi, and predators away from the eggs. A similar pattern can be found in fishes and frogs, in which most species that present parental care tend for their eggs with simple behaviors, such as ventilating them, or protecting them with their body (Balshine 2012). Only relatively few species show more advanced behaviors, such

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WHY IS CARING FOR JUVENILES RELATIVELY MORE COMMON IN CRUSTACEANS THAN IN OTHER GROUPS? As mentioned in the introduction, caring too much for the current offspring might suppress parental fitness through decreased future reproduction. A logical outcome is that caring for too long should be rare because of the high costs for the parents. Thus, the fact that comparatively many crustacean parents are caring for juveniles (more and longer than in fishes, frogs, and insects; Fig. 5.7) suggests that either (i) caring for longer might not be as costly for some crustacean groups (decapods and peracarids) as it is for other groups, or (ii) juvenile mortality is high enough to compensate for the potential costs. Investment in egg size may be one of the reasons why crustaceans care for juveniles relatively more than insects, fishes, and frogs. Larger eggs increase early embryo survival and growth, but there is a caveat: larger eggs also take more time to develop and thus spend more time exposed to predators (Fox and Czesak 2000). A common expectation, then, is that larger eggs correlate with more parental care after oviposition (Clutton-​Brock 1991). Although there is no evidence for that correlation in insects (Gilbert and Manica 2010), fishes and frogs have a positive association between the length of post-​ovipositional care and egg size (Kolm and Ahnesjö 2005, Summers et al. 2006). For crustaceans, no formal analysis of this relationship has been attempted, but we discovered some tentative similarities. In decapods, for instance, most species that provide parental care up to the juvenile stage are freshwater decapods. These species are known for tending fewer and larger eggs compared to their marine relatives (Glazier 2018). Peracarids in general also care for few large eggs within their marsupium when compared to other crustaceans with similar body size ( Johnson et al. 2001, Glazier 2018). Therefore, the duration of parental care might correlate with egg size in crustaceans, but future meta-​analyses are needed to test this hypothesis. Other sources of mortality (or increased survival) might include the intensity of egg predation, stable and structured habitats, environmental harshness, and use of rich ephemeral resources. According to Wilson (1975), these are important predictors for the evolution of parental care in insects, but these factors might also influence the duration of parental care in crustaceans. As discussed earlier, egg predation may not be a high cost for crustaceans. Eggs are typically maintained near (or in) the female body, which is already an effective protection against predators (Machado and Trumbo 2018). However, juveniles might be more prone to predation than early embryos. Juveniles perform short excursions away from the mother (Vogt 2013, Fig. 5.5), which leaves juveniles unguarded. These excursions might increase the risk of predation that juveniles face. If the risk of predation on juveniles is indeed higher, then we should find a positive correlation between the intensity of predation and the duration of parental care. We do not know of any studies measuring the correlation between predation and parental care duration, but we do have parent-​removal experiments that test the effectiveness of parental care. And the pattern is similar throughout crustaceans, fishes, and frogs: parental care improves juvenile survival when predators are present (Crump 1996, Jørgensen et  al. 2011, Thiel 2007, Santos et al. 2017). However, there are some differences among these studies that are cause for concern when generalizing across taxa. In insects, fishes, and frogs, researchers might not report the cause of mortality (e.g., fungi or predator) because studies are typically done in the field (see Santos et al.



“The Caring Crustacean”

2017). However, for amphipods and isopods, most studies have been performed in laboratory environments. Thus, researchers controlled the source of mortality: in crustaceans, parental presence only enhances juvenile survival when predators are present; when predators are absent, juveniles with or without parents show a similar rate of survival (Thiel 1999a, Kobayashi et al. 2012, Fig. 5.8). Therefore, intense predation pressure on juveniles likely favors the evolution of parental care, but other factors may correlate with protection from predation (Wilson 1975, Trumbo 2012). For instance, most parent-​removal experiments were performed in species that also provide a stable and structured microhabitat to juveniles (Thiel 1999a, 2001, Linsenmair 2007, Kobayashi et al. 2012). Studies with species that do not provide a stable habitat are less common (e.g., Aoki 1997). Hence, more studies in species in which parents do not provide a stable microhabitat would be useful to disentangle the effects of predation from the effects of a protective dwelling on juvenile survival. Stable microhabitats may promote the evolution of extended parental care, but environmental harshness might also play a role. Marine amphipods that inhabit burrows, tubes, or mud-​whips care for their juveniles for longer than species without dwellings (Thiel 1999c), and terrestrial and marine isopods follow a similar pattern (Thiel 2001). For example, the desert-​living isopods from the genus Hemilepistus provide biparental care for extended periods within a deep and stable burrow (Linsemair 2007). Bromeliad crabs perform complex care for their embryos and juveniles, but they are tended inside water pools that form between leaf axils of bromeliads (Diesel and Schubart 2007). Burrowing crayfish are another good example of how the interaction between stable microhabitats and harsh environments influences parental care. In many species, the mother inhabits a burrow with juveniles (Richardson 2007). Since digging a deep and safe burrow is not an easy task for a small juvenile, the mother tolerates her offspring in her dwelling until conditions improve and the juveniles have grown to sufficient size to establish their own burrows, typically when they reach subadult size (Palaoro et al. 2016). As conditions become harsher, parents cohabit for longer periods with their offspring. In the most extreme case known, crayfish from the genus Engaeus share burrows with up to three subsequent generations (Richardson 2007).

Survival rate of juveniles (%)

100

n.s. P = 0.4506

n.s. P = 0.1161

* P = 0.0113 With mother Without mother

80 60 40 20 0

10 days

30 days Predator-free

15 hours Predator-present

Fig. 5.8. The benefits of parental care. When a predator is present, juveniles of Parallorchestes ochotensis survive ~80% more when they are reared with their mother than when they are reared alone. Figure redrawn from Kobayashi et al. (2002) with permission from © Oxford University Press.   

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Reproductive Biology Similarities abound when we compare to other groups. Beetles that inhabit deserts (Rasa 1999) and frogs that care for offspring in bromeliads (Crump 1996) are groups that also provide extensive and complex parental care to their offspring. As pointed out by Trumbo (2012) in his review, it is hard to disentangle the predictors of parental care in insects (Wilson 1975) as they typically co-​ occur, and are not mutually exclusive (i.e., large eggs, stable microhabitat, and harsh environment). However, based on the examples from marine amphipods, it seems that stable dwellings alone can favor the evolution of extended parental care, while environmental harshness might modulate the duration and complexity of care (at least for crustaceans). Lastly, even though ephemeral and rich resources may favor the evolution of parental care in insects (Wilson 1975), it probably does not influence crustacean parental care. Insects that provide extended parental care typically feed on dung, carrion, or wood, all of which are resources that are either ephemeral or hard to digest (Machado and Trumbo 2018). Crustaceans, on the other hand, do not feed on ephemeral resources, but they do inhabit ephemeral resources, such as sponges, ascidians, echinoderms, and other types of dwellings (Baeza and Thiel 2007, Thiel 2007). Furthermore, crustaceans that care for juveniles typically inhabit (and feed on) rich resources. For instance, the isopod Limnoria chilensis inhabits kelp holdfasts in which they build burrows, tend to their offspring, and also find their primary food source (Thiel 2003). Therefore, feeding on ephemeral and rich resources also correlates to inhabiting stable microhabitats in crustaceans. Perhaps, then, habitat stability is the primary predictor for the evolution of crustacean extended parental care, while other factors modulate the length and complexity of care.

WHY ARE THERE NO CASES OF EXCLUSIVE PATERNAL CARE IN CRUSTACEANS? According to Trivers (1972), males maximize their reproductive success by mating with the highest number of females possible. Under this model scenario, paternal care is unlikely to arise because any male that cares for eggs would not be able to mate with more females, leaving less descendants than a male that does not care. This seems a good explanation for crustaceans, but it does not explain the cases of biparental care that occur mostly in peracarids. Additionally, it does not explain the high frequency of paternal care in fishes and frogs. Queller (1997) and Kokko and Jennions (2008) deconstructed Triver’s model by showing that, in a finite population with an adult sex ratio of 1:1, males maximize their reproductive success by caring for the developing embryos, and not searching for new eggs to fertilize. Since males return to the mating pool much faster than females, they would soon be overrepresented, which would make males care. Although revolutionary, the explanation now does not explain the lack of paternal care in crustaceans. All models, so far, assume that there is a trade-​off between mating and caring, meaning that males cannot care and mate at the same time, which favors males to use a single strategy (i.e., either caring or searching for more mates). However, in several species of insects, fishes, and frogs there is no evidence of a trade-​off between mating and caring (Stiver and Alonzo 2009, Requena et al. 2014). The timing of ovulation and sperm transfer seems to be an important reason for the lack of paternal care in crustaceans. In crustaceans, females first receive male sperm, and only then ovulate to initiate fertilization of the eggs. Since there is a lag between male sperm transfer and fertilization (which occurs on or within the female), males have no opportunity to monopolize fertilizations. Females can reject sperm (e.g., Thiel and Hinojosa 2003)  or mate with multiple males (e.g., Dennenmoser and Thiel 2015), while the best strategy for males would be to leave rapidly and mate elsewhere (without caring for the offspring; Requena et al. 2014). Insects are similar to crustaceans in this regard: females generally maintain control of fertilizations. In contrast, in many fishes and frogs, the females oviposit first, and only then do males eject or transfer sperm to fertilize the eggs.



“The Caring Crustacean”

In these instances, males might have more control over fertilization than insects and crustaceans because males are close to the eggs during fertilization, both in space and time (Williams 1975). In water bugs from the family Belostomatidae, males apparently ensure paternity by soliciting females to deposit their eggs on the male’s dorsal surface immediately after copulation (Smith 1980). Even though paternal care has independently evolved in several insect groups and for various reasons (Tallamy 2001), fishes and frogs have a higher likelihood of presenting exclusive paternal care (Beck 1998, Ah-​King et al. 2005). The distance of the males from the eggs being fertilized thus seems to influence the evolution of paternal care. Williams (1975) was the first to address that external/​internal fertilization aspect through the verbal “territoriality hypothesis.” According to the hypothesis, females would lay the eggs inside the male’s territory, which would decrease the temporal and spatial distance between males and eggs. Hence, if the female lays the eggs within the male’s territory, males would have an increased opportunity to monopolize fertilizations, laying the ground for the evolution of paternal care. For frogs and fishes, external fertilization correlates with the presence of paternal care (Beck 1998), while the presence of territorial males increases the strength of the correlation with paternal care in fishes (Ah-​King et al. 2005). It is interesting to note that there is a positive correlation between territoriality and the presence of paternal care in insects (Gilbert and Manica 2015), even though most insects have internal fertilization, as many crustaceans do. Then, why does territoriality help to explain some cases of paternal care in insects, but not in crustaceans? Pycnogonoids, chelicerates that are neither insects nor crustaceans, might provide us with further insights because paternal care is rampant while maternal care is nearly absent (Bain and Govedich 2004). In pycnogonoids, the female releases unfertilized eggs on her walking legs while the male holds her. After the eggs are released, females start to transfer the eggs to the males. This is a critical period for both because in most reports males only fertilize the eggs after the eggs are on his ovigers (i.e., ovigerous legs; Bain and Govedich 2004). However, there are few species, such as Propallene longiceps, in which males fertilize the female’s eggs before the eggs are transferred (Nakamura and Sekiguchi 1980). Nevertheless, fertilization is external, and, in most species, males are able to ensure paternity due to being close during fertilization (Burris 2011). Male crustaceans, in contrast, do not control any step of the fertilization because fertilization occurs in or on the female. Thus, male crustaceans have no way of ensuring paternity of the offspring despite showing some strategies toward ensuring paternity (e.g., territoriality, mate-​guarding, sperm plugs; Asakura 2009). Unfortunately, it is hard to pinpoint the reason for the lack of a trait in a group, as there are no replicates for hypothesis testing. However, crustaceans and pycnogonoids might be the exceptions that provide evidence to the rule. In pycnogonoids, males have full control of fertilization and thus care for eggs, while in crustaceans these roles are reversed. Thus, it seems that the sex that is controlling fertilization is also the sex that is most likely to provide care.

CONCLUSIONS AND OUTLOOK Here, we have shown that parental care is nearly ubiquituous in crustaceans. But why it is ubiquituous is still unknown. What we do know is that for parental care to evolve, several factors need to interact simultaneously (Royle et al. 2016, Fig. 5.9). The ecology of the species (e.g., resources for offspring, protection from predation, shelter against harsh environment) and parental effects (e.g., egg size) interact with offspring mortality to influence the evolution of parental care. We showed that offspring mortality is an important predictor of the presence of parental care in fishes, frogs, and insects, and it also seems to be important in crustaceans. Early embryos typically face high rates of mortality when raised without their mother, favoring the evolution of maternal care. The main sources of egg mortality in crustaceans apparently are environmental stress and

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Reproductive Biology brood parasitism, both of which can be mitigated by the presence of the mother. Simple behaviors such as egg fanning and cleaning are common among crustaceans, and are behaviors that are able to mitigate both sources of mortality. Therefore, complex forms of care need not evolve to increase egg survival in most crustaceans, which might explain the commonality of simple behaviors. The length and complexity of parental care seem tied to egg size and inhabiting stable microhabitats in which the young can live. Producing large eggs is known to increase egg survival, but it also increases developmental time and the time that the eggs are exposed to external sources of mortality. A common theoretical expectation is that large eggs correlate with the extent of parental care. Fishes and frogs are known to care longer for larger eggs, but we have no such evidence for crustaceans. We show that groups such as amphipods, isopods, and freshwater decapods bear fewer large eggs and care for longer than close relatives, so it seems that crustaceans care longer for larger eggs. But we need quantitative comparative evidence to know the true extent of this pattern. Even though Wilson (1975) pointed out that the evolution of parental care is tied to four predictors, it seems that one of these, habitat stability, seems to be important for caring for juveniles. The first predictor is offspring mortality, and even though juveniles might face higher mortality when unprotected, most groups in which juvenile predation has been tested also inhabit stable habitats. The second predictor is environmental stress: harsh environments would select for longer, more complex care. That also seems to be true in crustaceans, but again, most species also inhabit stable habitats. The third predictor is using rich resources. Once again, those crustaceans that use these resources, such as kelp-​boring isopods (Thiel 2003), also build stable habitats within kelps. Therefore, stable habitats are pervasive in crustaceans that provide longer care. We need further studies to understand whether habitat stability indeed is the primary predictor of crustacean parental care, or if we are missing pieces of the puzzle. Lastly, females are predominantly the caring sex, while biparental care is rare, and paternal care is absent in crustaceans. The predominance of females as caregivers might be related to the position of the sexes when fertilization occurs. In crustaceans and insects, fertilization is internal, which prohibits male access to the fertilized eggs. In fishes and frogs, on the other hand, fertilization is external, which ensures that males are in close connection with the fertilized eggs. Thus, it is not surprising that paternal care is more common in fishes and frogs than in insects and crustaceans.

Behavioral precursors

Ecology

Origin of parental care

Offspring mortality

Parental effects

Transgenerational effects

Fig. 5.9. The origin of parental care is influenced by an interaction of several factors. Ecological (e.g., resource availability, risk of predation) and parental effects (e.g., egg size) interact to influence offspring mortality, which influences the probability of the evolution of parental care. However, behavioral precursors (e.g., presence of active defenses) and transgenerational effects (e.g., genetic correlations between parents and offspring) also influence the probability of parental care evolution. Therefore, there are five factors that influence the origins of care. Figure adapted from Royle et al. (2016) under © Creative Commons License.   



“The Caring Crustacean”

In this overview, our aim was to show the amazing diversity of crustacean parental care and the ecological and evolutionary pressures involved in the evolution of parental care. Sadly, we still lack studies regarding all traits correlated to the evolution of parental care. The sheer diversity of forms of care found in crabs is an example of the diversity we might be missing. Most crabs care only for early embryos, but we can also find complex forms of care, such as those of the bromeliad crabs. Therefore, exploring this diversity through a combined approach of natural history studies, experiments, meta-​analyses, and comparative methodologies might help to answer some of the questions we have raised throughout this chapter.

ACKNOWLEDGMENTS AVP was funded by a post-​doctoral grant provided by FAPESP (process no: 2016/​22679-​3).

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“The Caring Crustacean”

Seaman, M. T., D. J. Kok, B. J. Schlichting, and A. J. Kruger. 1991. Natural growth and reproduction in Triops granarius (Lucas) (Crustacea: Notostraca). Hydrobiologia 212:87–​94. Seidl, M. D., R. Pirow, and R. J. Paul. 2002. Water fleas (Daphnia magna) provide a separate ventilatory mechanism for their brood. Zoology 105:15–​23. Sheader, M. 1977a. Production and population dynamics of Ampelisca tenuicornis (Amphipoda) with notes on the biology of its parasite Sphaeronella longipes (Copepoda). Journal of the Marine Biological Association of the United Kingdom 57:955–​968. Sheader, M. 1977b. The breeding biology of Idotea pelagica (Isopoda: Valvifera) with notes on the occurrence and biology of its parasite Clypeoniscus hanseni (Isopoda: Epicaridea). Journal of the Marine Biological Association of the United Kingdom 57:659–​674. Shuster, S. M., and R. L. Caldwell. 1989. Male defense of the breeding cavity and factors affecting the persistence of breeding pairs in the stomatopod, Gonodactylus bredini (Manning) (Crustacea: Hoplocarida). Ethology 82:192–​207. Sigvardt, Z. M., and J. Olesen. 2014. Mating behaviour in laevicaudatan clam shrimp (Crustacea, Branchiopoda) and functional morphology of male claspers in a phylogenetic context: a video-​based analysis. PLoS ONE 9:e84021. Siveter, D. J., M. D. Sutton, and D. E. Briggs. 2007. Brood care in a Silurian ostracod. Proceedings of the Royal Society of London B: Biological Sciences 274:465–​469. Smith, G. 1909. On the Anaspidacea: living and fossil. Journal of Cell Science 53:489–​578. Smith, R. L. 1980. Evolution of exclusive postcopulatory paternal care in the insects. The Florida Entomologist 63:65–​78. Smiseth, P. T., M. Kölliker, and N. K. Royle. 2012. What is parental care? Pages 1–​20 in N. J. Royle, P. T. Smiseth, and M. Kölliker, editors. The Evolution of Parental Care. Oxford University Press, Oxford. Stiver, K. A., and S. H. Alonzo. 2009. Parental and mating effort: is there necessarily a trade-​off? Ethology 115:1101–​1126. Summers, K., and J. Tumulty. 2014. Parental care, sexual selection, and mating systems in neotropical poison frogs. Pages 289–​320 in R. H. Macedo and G. Machado, editors. Sexual Selection: Perspectives and Models from the Neotropics. Elsevier Academic Press, San Diego, CA. Summers, K., C. S. McKeon, and H. Heying. 2006. The evolution of parental care and egg size: a comparative analysis in frogs. Proceedings of the Royal Society of London B: Biological Sciences 273:687–​692. Surbida, K. L., and J. C. Wright. 2001. Embryo tolerance and maternal control of the marsupial environment in Armadillidium vulgare (Isopoda: Oniscidea). Physiological and Biochemical Zoology 74:894–​906. Tallamy, D. W. 2001. Evolution of exclusive paternal care in arthropods. Annual Review of Entomology 46:139–​165. Tarutis, J., S. Lewis, and M. Dyke. 2005. Active parental care in a freshwater amphipod (Crustacea: Gammarus pseudolimnaeus): effects of environmental factors. The American Midland Naturalist 153:276–​284. Thiel, M. 1999a. Extended parental care in marine amphipods. II: Maternal protection of juveniles from predation. Journal of Experimental Marine Biology and Ecology 234:235–​253. Thiel, M., 1999b. Host-​use and population demographics of the ascidian-​dwelling amphipod Leucothoe spinicarpa -​indication for extended parental care and advanced social behaviour. Journal of Natural History 33: 193–​206. Thiel, M. 1999c. Duration of extended parental care in marine amphipods. Journal of Crustacean Biology 19:60–​71. Thiel, M. 2001. Parental care behaviour in the wood-​boring isopod Sphaeroma terebrans. Crustacean Issues 13:267–​276. Thiel, M. 2003. Reproductive biology of Limnoria chilensis: another boring peracarid species with extended parental care. Journal of Natural History 37:1713–​1726. Thiel, M. 2007. Social behavior of parent–​offspring groups in crustaceans. Pages 294–​318 in J. E. Duffy and M. Thiel, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, New York. Thiel, M., and I. A. Hinojosa. 2003. Mating behavior of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea): indication for convenience polyandry and cryptic female choice. Behavioral Ecology and Sociobiology 55:113–​121.

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Reproductive Biology Thiel, M., S. Sampson, and L. Watling. 1997. Extended parental care in two endobenthic amphipods. Journal of Natural History 31:713–​725. Titelman, J., Ø. Varpe, S. Eliassen, and Ø. Fiksen. 2007. Copepod mating: chance or choice? Journal of Plankton Research 29:1023–​1030. Trivers, R. 1972. Parental investment and sexual selection. Page 179 in M. A. Cambridge, editor. Biological Laboratories, Volume 136. Harvard University Press, Cambridge, MA. Vannini, M., G. Innocenti, and R. K. Ruwa. 1993. Family group structure in mysids, commensals of hermit crabs (Crustacea). Tropical Zoology 6:189–​205. Vetter, E. W. 1996. Life-​history patterns of two Southern California Nebalia species (Crustacea: Leptostraca): the failure of form to predict function. Marine Biology 127:131–​141. Vogt, G. 2013. Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biological Reviews 88:81–​116. Wakabayashi, K., S. Otake, Y. Tanaka, and K. Nagasawa. 2013. Choniomyzon inflatus n. sp. (Crustacea: Copepoda: Nicothoidae) associated with Ibacus novemdentatus (Crustacea: Decapoda: Scyllaridae) from Japanese waters. Systematic Parasitology 84:157–​165. Williams, W. D. 1965. Ecological notes on Tasmanian Syncarida (Crustacea: Malacostraca): with a description of a new species of Anaspides. Internationale Revue der gesamten Hydrobiologie und Hydrographie 50:95–​126. Williams, G. C. 1975. Sex and Evolution. Princeton University Press, Princeton, NJ. Wilson, E. O. 1975. Sociobiology: The New Synthesis. Harvard University Press, Cambridge, MA. Wilson, G. D. 1991. Functional morphology and evolution of isopod genitalia. Pages 228–​245 in R. T. Bauer, and J. W. Martin, editors. Crustacean Sexual Biology. Columbia University Press, New York. Wortham-​Neal, J. L. 2002. Reproductive morphology and biology of male and female mantis shrimp (Stomatopoda: Squillidae). Journal of Crustacean Biology 22:728–​741. Wright, M. L., and R. L. Caldwell. 2015. Are two parents better than one? Examining the effects of biparental care on parental and egg clutch mass in the stomatopod Pullosquilla thomassini. Journal of Crustacean Biology 35:51–​58. Zeh, D. W., J. A. Zeh, and R. L. Smith. 1989. Ovipositors, amnions and eggshell architecture in the diversification of terrestrial arthropods. The Quarterly Review of Biology 64:147–​168. Zimmer, M. 2001. Why do male terrestrial isopods (Isopoda: Oniscidea) not guard females? Animal Behaviour 62:815–​821.

6 AN OVERVIEW OF SEXUAL SYSTEMS

Günter Vogt

Abstract The Crustacea have evolved a broad range of sexual systems, including various types of gonochorism, hermaphroditism, and parthenogenesis. This chapter provides an overview of sexual systems in Crustacea and compares them in the species-​rich Decapoda, Isopoda, Amphipoda, Cirripedia, Cladocera, Copepoda, and Ostracoda, which differ considerably with respect to phylogeny, ecology, and life histories. Gonochorism is considered to be the ancient sexual system of Crustacea. Hermaphroditism and parthenogenesis originated many times independently from gonochorism and occur in an estimated 2.2% and 2.4% of species, respectively. Crustaceans differ from the other arthropod groups mainly by the abundance and diversity of hermaphroditic reproduction. Phylogenetic analysis of extant species, the fossil record, and evolutionary ecological theory enable the reconstruction and explanation of divergent evolutionary trajectories of sexuality in the crustacean groups. The specificities can partly be attributed to differences in lifestyle, life history, and adaptive responses to different environments, but may also be the result of evolutionary constraint and competing adaptive strategies that lower the propensity of sexual system shifts. The genetic underpinning and molecular mediation of sexual system shifts are beginning to be unraveled in entomostracan and malacostracan models. A  better understanding of the sexual systems in Crustacea may help to optimize their culture and conservation and answer key evolutionary questions like the enigma of sex.

INTRODUCTION Sexual system is a key biological factor that affects population structure, genetic diversity, ecology, and evolutionary potential. The Crustacea, which are known for their long evolutionary history

Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology and their diversity in morphology, physiology, life history, and ecology (Schram 1989, Gruner 1993, Martin and Davis 2001), show a particularly broad range of sexual systems when compared to other animal groups (Pandian 2016, Subramoniam 2017). Colonization of new environments and lifestyle changes in crustaceans were sometimes paralleled or followed by alteration of the prevailing sexual system, suggesting that sexual system shift may be an adaptive strategy. However, the patterns of sexual systems are not uniform among higher crustacean taxa living in the same environment, suggesting that other factors like evolutionary constraint and competing adaptive strategies influence the propensity toward sexual system shifts as well. This chapter begins with an overview of the sexual systems in Crustacea. It then describes the patterns of sexual systems in selected higher taxa that differ markedly with respect to phylogeny, ecology, lifestyle, and life history. The following sections discuss the evolutionary reasons for these differences, the genetic underpinning of sexual system shifts, and molecular mechanisms that mediate environmentally triggered conversion of sexual systems. The chapter closes with a comparison of the sexual systems of crustaceans with those of other arthropods and outlines some problems and directions for future research.

OVERVIEW OF SEXUAL SYSTEMS IN THE CRUSTACEA Crustaceans have evolved a broad range of sexual systems, including different types of gonochorism, hermaphroditism, and parthenogenesis (Subramoniam 2013, Pandian 2016). Gonochorism or bisexuality is the most frequent type of reproduction in animals, requiring males and females. Hermaphroditism describes the production of male and female gametes by the same individual. Parthenogenesis is the development of an embryo from an unfertilized egg. Gonochorism is characterized by meiosis and fusion of the female and male gametes to form a zygote. Each individual is either male or female, which is not changed throughout its lifetime. There is a broad spectrum of relative male and female sizes, mating systems, and paternity patterns in bisexually reproducing crustaceans, depending on taxonomic affiliation, social systems, etc. The sexes are either monomorphic or dimorphic, with the larger sex being the male or the female. In some species, males are tiny dwarf males that are lecithotrophic or nourished by the female. In promiscuous species, clutches can be sired by multiple fathers (Dennenmoser and Thiel 2015)  and in eusocial colonies, reproduction can be confined to a single female (Duffy 2007). Hermaphroditism is either sequential or simultaneous (Ghiselin 1969, Munday et al. 2006). In sequential hermaphrodites, the male and female gonads mature and become functional at different times during an individual’s lifetime. The condition is called protogyny when the first sex is female, and protandry when the first sex is male. Simultaneous hermaphrodites are characterized by concurrent functioning of male and female gonads in the same individual. Their ovaries and testes can either be separate or unified in a mixed organ, the ovotestis. In crustaceans, the most frequent type of hermaphroditism is sequential protandry, and the second most frequent type is simultaneous hermaphroditism. Protogyny is generally rare in the animal kingdom and in crustaceans has been documented for some Tanaidacea and Isopoda (Brook et al. 1994). The term intersex is often used for individuals with mixed male and female characteristics but unknown reproductive biology. Intersexes can either represent unidentified hermaphrodites or gonochoristic specimens, in which the hormonal pathway of sex determination has been disturbed by dysfunctioning of the homone glands, parasites, or environmental endocrine disruptors (LeBlanc 2007, Subramoniam 2013, DeFur and Williams 2015).



An Overview of Sexual Systems

Intersexes of gonochoristic species behave and reproduce either as males or females, but their reproductive output is usually lower than that of normal males and females (Ford et al. 2004, Subramoniam 2013). Sometimes intersexes produce sterile offspring, as shown for isopods (Rigaud and Juchault 1998). Parthenogenesis is regarded as unisexual or asexual reproduction, depending on the definition of sexuality (see Chapter 9 in this volume). In the following, I provide descriptions of the types of parthenogensis relevant to understanding crustacean sexual systems. A  more detailed discussion of the different types of parthenogenesis and their definitions are found in Suomalainen et al. (1987) and in Chapter 9 in this volume. For crustaceans, apomictic and automictic thelytoky and facultative, cyclic, obligate, and geographical parthenogenesis are relevant. Apomictic thelytoky is probably the most common type of parthenogenesis in crustaceans. It describes the development of oocytes into females without meiotic reduction. Barring random germline mutations, the offspring is genetically identical to the mother. In automictic thelytoky, the offspring also derives from diploid and unfertilized eggs, but meiosis occurs to some degree. Therefore, the progeny can vary genetically but contain only the maternal genes, in contrast to bisexually produced offspring that contain genes from both parents. Facultative parthenogens can switch between gonochoristic and parthenogenetic reproduction based on environmental cues, obligate parthenogens reproduce exclusively by parthenogenesis, and cyclic parthenogens alternate periodically between bisexual and parthenogenetic reproduction. Cyclic parthenogenesis may be regarded as a subtype of facultative parthenogenesis, but due to the stereotyped sequence of sexual and asexual reproduction it is usually seen as a separate type of parthenogenesis. Geographical parthenogenesis describes the occurrence of obligate parthenogenetic populations at the margins of a species’ distribution range (Hörandl 2009). Geographical parthenogens are typically found at higher latitudes and altitudes. Gonochorism is predominant in 19 of the 24 crustacean groups listed in Table 6.1. Hermaphroditism is the most common sexual system in Cephalocarida, Remipedia, and Cirripedia, while parthenogenesis is most widespread in Ostracoda. Cyclic parthenogenesis, the regular switching between sexual and parthenogenetic phases, is predominant in Cladocera. Of the 24 higher taxa, 11 have evolved only one sexual system, nine have evolved two systems, and four have evolved all three systems. Nine higher taxa are purely gonochoristic, and two are purely hermaphroditic. In four groups, gonochorism occurs together with both hermaphroditism and parthenogenesis. In another four groups, gonochorism occurs together with hermaphroditism; and in five groups, gonochorism occurs together with parthenogenesis. There is no group with a combination of hermaphroditism and parthenogenesis. Only few crustacean families and higher taxa consist exclusively of hermaphrodites or parthenogens. In the other groups with hermaphrodites and parthenogens, these comprise only a small percentage of species. Based on present knowledge, an estimated 2.2% of the approximately 66,900 described crustacean species include hermaphroditic populations, and 2.4% of species include parthenogenetic populations. However, there are great differences between Entomostraca (lower crustaceans) and Malacostraca (higher crustaceans): the former include 4.5% species with hermaphrodites and 6.8% species with parthenogens, while the latter include only ~1% species with hermaphrodites and 0.05% species with parthenogens. In all Metazoa, approximately 5% of species are estimated to have evolved hermaphroditic populations, and about 1% of species have evolved parthenogens (Bell 1982, Bachtrog et al. 2014).

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Reproductive Biology Table 6.1.  Sexual Systems in Crustacea. Group Entomostraca Cephalocarida (SC; 13) Remipedia (SC; 18) Anostraca (SC; 313) Notostraca (O; 15) Conchostraca (SuO; 224) Cladocera (SuO; 632) Copepoda (SC; 15,976) Branchiura (SC; 168) Pentastomida (SC; 130) Ostracoda (SC; 7,549) Tantulocarida (SC; 36) Ascothoracida (SC; 107) Cirripedia (SC; 1,306) Malacostraca Leptostraca (O; 44) Stomatopoda (O; 460) Syncarida (SO; 262) Thermosbaenacea (O; 35) Cumacea (O; 1,523) Mysidacea (O; 1,247) Amphipoda (O; 9,888) Tanaidacea (O; 1,069) Isopoda (O; 10,661) Euphausiacea (O; 87) Decapoda (O; 14,756)

Gonochorism

Hermaphroditism

Parthenogenesis

xxx xxx xxx xxx xxx xx* xxx xxx xxx xxx xxx xxx xx xxx xxx xxx xxx xxx xxx xxx xxx xxx xxx xxx

x x x xxx x

xx x xx xxx

x xx xx

x x x

xx

x

Abbreviations in parentheses are taxonomic units: SC = subclass; SO = superorder; O = order, SuO = suborder. Figures in parentheses are species numbers (after De Grave et al. 2009 and Ahyong et al. 2011). xxx = dominant sexual system; xx = less frequent sexual system; x = rare sexual system; *sexual part of cyclic parthenogenesis. After Gruner (1993), Schminke (2013), and the articles cited in the group-​specific sections of the text.

COMPARISON OF SEXUAL SYSTEMS AMONG HIGHER CRUSTACEAN TAXA In this section, I describe the patterns of sexual systems in some species-​rich entomostracan and malacostracan groups that differ markedly in phylogeny, ecology, lifestyle, and life history. Sexual Systems of the Decapoda The Decapoda are known from the Late Devonian (364–​354 million years ago) but are thought to have already diverged in the Silurian some 440 mya (Porter et al. 2005). They comprise almost 15,000 extant species and are widespread in marine (~80%) and freshwater (~20%) environments (De Grave et al. 2009). Some species are terrestrial. The vast majority of decapods are free-​living



An Overview of Sexual Systems

members of the benthos, and only a few species are pelagic or live as endobionts (Gruner 1993). The decapods include the largest and longest-​lived crustaceans (Martin and Davis 2001, Vogt 2012). For example, lobsters can reach body lengths (inclusive of the chelae) of more than 1 m, body masses of 20 kg, and ages of about 70 years. Most decapods live between one and 20 years (Vogt 2012). The Decapoda are typically gonochoristic. Hermaphroditism is proven for approximately 50 species, and parthenogenesis is known for only two species. The gonochoristic species mostly show a clear dimorphism of males and females. Sometimes the males are the larger sex, like in crayfish, and sometimes the females are larger, like in penaeid shrimps. Males are most easily recognized by their paired gonopods, which are used for the transfer of spermatophores to the female (Becker et al. 2012). Each gonopod is composed of modified pleopods 1 and 2 (A in Fig. 6.1). In species without gonopods, males are distinguished from females by the location of the gonopores and differences in secondary sex characteristics such as chela size, pleon form, and pleopod structure. The females are most easily recognized when they carry developing embryos on the pleopods (B in Fig. 6.1). Carrying of the embryonic stages is typical of all Pleocyemata, which include the vast majority of decapods, whereas most of the basal Dendrobranchiata are broadcast spawners (Anger 2001, Vogt 2013). Intersex individuals with male and female gonopores have been reported in several lineages of the Decapoda and are particularly well known in freshwater crayfish (Sagi et  al. 2002, Martínez

(A)

(C)

(B)

Fig. 6.1. Sexual systems in crayfish. (A) Paired copulatory organs of male of gonochoristic Faxonius cristavarius composed of first (P1) and second (P2) pleopods. Scale bar = 3 mm. Photo courtesy of Tiffany Penland, with permission. (B) Female of obligately parthenogenetic Procambarus virginalis carrying embryos on pleopods. Scale bar = 5 mm. From Vogt et al. (2004), with permission from John Wiley and Sons. (C) Ovotestis of simultaneous hermaphrodite Parastacus brasiliensis consisting of ovarian and testicular portions. O = oocyte; T = testicular acinus. Scale bar = 200 µm. From Almeida and Buckup (2000), with permission from Oxford University Press.   

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Reproductive Biology and Rudolph 2011, Yazicioglu et  al. 2016). They are usually regarded as males of gonochoristic species that have experienced disturbances of the androgenic gland hormone system. However, further study of the gonads and life histories of some intersex individuals revealed them to be real hermaphrodites (Rudolph et  al. 2007). A  special situation has been reported for the South American crayfish Parastacus pugnax and P. pilimanus, which apparently reproduce by gonochorism with permanent external intersex characteristics (Rudolph and Verdi 2010). Hermaphroditism is particularly frequent in the Caridea, occurring in more than 40 species from 15 genera and seven families (Bauer 2007). It is also documented for five crayfish species, two penaeid shrimps, two anomurans, and one thalassinid (Bauer 2000, Martínez and Rudolph 2011). In the sequentially protandric Pandalus species, all individuals mature first as males and then become females as they increase in size and age. The testes and male gonoducts and gonopores disappear or become vestigial after the change from male to female phenotype, which takes place over a number of consecutive molts. In the Caridea, there are several variations on this simple scheme of protandric hermaphroditism as shown in Fig. 6.2 (Bauer 2000, Subramoniam 2013). For example, in the facultatively protandric shrimp Crangon crangon, a certain proportion of individuals seem to be protandric hermaphrodites, whereas the others are primary females that never change sex (Bauer 2000, Schatte and Saborowski 2005). Simultaneous hermaphroditism is typical of the genus Lysmata. Individuals have ovotestes, but first mature as males. Their ovarian portions mature when they become older and larger. In contrast to sequential hermaphrodites, they retain the male gonadal tissues and gonoducts and produce sperm as well as eggs (Bauer 2006). Hermaphroditic shrimps mostly occur in mobile high-​density aggregations (Bauer 2007). However, the protandric hermaphroditic rhynchocinetid shrimp Rhynchocinetes uritai does not fit into this scheme because aside from sex change it showed

Sexual system

Ontogeny

Gonochorism

juvenile

male

juvenile

female

Sequential hermaphroditism

juvenile

male

female

Sequential protandry with primary females

juvenile

male

female

juvenile

primary female

Sequential protandry with primary and early maturing females

juvenile

male

juvenile

primary female

Sequential protandry with primary males

juvenile

male

juvenile

primary male

Simultaneous hermaphroditism

juvenile

male

female early maturing female

female

hermaphrodite

Fig. 6.2. Sexual systems in caridean shrimps. Carideans reproduce either by gonochorism or sequential and simultaneous hermaphroditism. There are various types of sequential hermaphroditism, but all are protandric. Primary males and primary females never change sex. Early maturing females first develop male characteristics but never breed as males. Simultaneous hermaphrodites have ovotestes but function first as males and later primarily as females. Modified after Bauer (2000), with permission from Oxford University Press.   



An Overview of Sexual Systems

no obvious differences in behavior and life-​history traits from those of gonochoric species from similar latitudes and habitats (Osawa et al. 2015). In the South American parastacid crayfish, five species from the genera Parastacus, Samastacus, and Virilastacus show partial protandric hermaphroditism (Almeida and Buckup 2000, Rudolph et al. 2007, Noro et al. 2008). This means that only a proportion of the population changes sex, as indicated by transitional individuals with ovotestes (C in Fig. 6.1), whereas others are primary males or primary females that never change sex. In contrast to the gregarious hermaphroditic carideans, at least two hermaphroditic crayfish species live their whole lives in subterranean burrows at low densities (Noro et al. 2008). Parthenogenesis is convincingly documented for two crayfish species. Obligate parthenogenesis is the only mode of reproduction in the marbled crayfish Procambarus virginalis, a descendant of the bisexually reproducing slough crayfish Procambarus fallax from Florida (Vogt et al. 2004, 2015, Martin et al. 2010). The marbled crayfish was discovered in the German aquarium trade in the mid-​1990s. It is not known whether parthenogenesis originated in nature or in captivity. Primary populations in the wild have not been discovered, but there are thriving secondary populations with high invasive potential in Central Europe and Madagascar, resulting from releases since the year 2003. Facultative parthenogenesis has been reported for the American spiny-​ cheek crayfish Faxonius limosus, which usually reproduces by gonochorism with plastic mating and sperm storage regimens (Buřič et al. 2013). In central Europe, males mostly participate only once per year in reproduction, either in the spring or the autumn reproduction season. However, if they fail to find mates in autumn, they can deposit their spermatophores to females during the next spring, and vice versa. On the other hand, females are able to store spermatophores from several males from both autumn and spring mates, resulting in multiple paternity (Buřič et al. 2013). In captivity, some females reproduced in the absence of males and produced genetically identical offspring, indicating parthenogenesis. Buřič et al. (2013) speculated that the opportunity to occasionally shift to parthenogenesis likely fostered the successful invasion of Europe by this species in the last 125 years. It is presently not known how often and under which conditions these crayfish shift from bisexuality to parthenogenesis. It is apparently a relatively rare event, unlike in cladocerans, which regularly switch to parthenogenesis when the conditions become favorable in spring. Sexual Systems of the Isopoda The Isopoda are known since the Carboniferous (359–​299 mya), comprise approximately 10,600 species, and show particularly broad variability in their ecology (Wägele 1989, Gruner 1993). Most isopods occur in marine and freshwater habitats, including extremes like the deep sea, polar waters, groundwater, and salt lakes. They are mostly free-​living bottom dwellers, but some 2,000 species are parasitic on decapods and fishes. The Oniscidea (~3,500 species) have conquered land and have evolved a completely terrestrial life cycle. Most isopods have sizes of 1–​5 cm and lifespans of 1–​10 years. An extreme is Bathynomus giganteus, which can reach a length of 50 cm. The embryos of isopods are brooded in a ventral brood pouch, the marsupium, to almost fully developed juvenile stages called manca (Warburg 2012). In some species, brood care is extended beyond this stage (Thiel 2003). Isopods are mainly gonochoristic, but hermaphroditism is frequent in parasitic groups and one terrestrial family. Parthenogenesis was demonstrated for a few terrestrial species. In the gonochoristic species, males and females show distinct sexual dimorphism. The females can be easily recognized by the marsupium. Dwarf males residing on females are typical of the five families of the Bopyroidea and seven families of the Cryptoniscoidea, which parasitize other crustaceans (Williams and Boyko 2012). These families have a shared evolutionary history with

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Reproductive Biology their hosts dating back to the Jurassic (201–​145 mya). An example is the bopyrid Robinione overstreeti (A in Fig. 6.3) that infests the branchial chamber of the Mexican ghost shrimp Callichirus islagrande. The greatest total lengths of its females and males were 19.1 mm and 4.9 mm, respectively (Adkison and Heard 1995). Hermaphroditism is probably typical of the 386 species of Cymothoidae (fish parasites), some Bopyridae (crustacean parasites), and the 24 species of Rhyscotidae (terrestrial) (Gruner 1993). The Cymothoidae are apparently sequential protandric hermaphrodites (Smit et al. 2014) and the Rhyscotidae are simultaneous protandric hermaphrodites ( Johnson 1961). Protogyny was found in the intertidal North American Gnorimosphaeroma oregonense and the European brackish water species Cyathura carinata (Brook et al. 1994, Ferreira et al. 2004). Females of the latter transform into males after one or more broods. There are also primary males and primary females in the population that never change sex (Gruner 1993). Geographical parthenogenesis is known for a few North American and European Oniscidea (Fussey 1984, Johnson 1986). These terrestrial woodlice have evolved obligately parthenogenetic populations in the northern parts of their range and bisexual populations in the southern parts. For example, Trichonsicus pusillus that live from the Mediterranean to Scandinavia have bisexual populations in the Mediterranean and triploid parthenogenetic populations in Central Europe and Scandinavia (Gruner 1993). Sexual Systems of the Amphipoda The Amphipoda are a relatively young crustacean group, appearing in the fossil record only in the Eocene (56–​34 mya). They comprise approximately 9,900 species and are common in the sea and freshwater, including polar waters, deep sea trenches, and groundwater (Bellan-​Santini 2015). A few species are terrestrial. Most amphipods are free-​living bottom dwellers, some species are planktonic, and some species are parasites on fishes and whales (Gruner 1993). Amphipods have typical sizes of 1–​15 mm, but Alicella gigantea can reach 29 cm ( Jamieson et al. 2013). Longevity is mostly one to two years, but the extreme is 156 months (Sainte-​Marie 1991). The embryos are brooded

(A)

(B)

(C)

Fig. 6.3. Dwarf males in gonochoristic isopod and copepod parasites. (A) Ovigerous female and male (arrow) of isopod Robinione overstreeti. Arrowhead denotes eggs detached during preparation. Scale bar = 5 mm. Photo courtesy of Brent P. Thoma, with permission. (B) Ventral aspect of posterior part of female copepod Chondracanthus lophii with male (arrow) attached between egg sacs (E). Scale bar = 500 µm. From Østergaard and Boxshall (2004), with permission from Elsevier. (C) Close-​up of male showing antennae with hooks (arrowhead) for adherence and mouthparts. M = maxilla. Scale bar = 100 µm. From Østergaard (2004), with permission from Cambridge University Press.   



An Overview of Sexual Systems

in the marsupium to fully developed juveniles, with the exception of parasitic Hyperiidae that release their offspring as advanced protopleon larvae (Gruner 1993, Bellan-​Santini 2015). Some species extend brood care beyond the juvenile stage (Thiel 2003). The vast majority of species are gonochoristic, but some species include protandric hermaphrodites. The gonochoristic amphipod species often show sexual dimorphism (Conlan 1991). In the epibenthic species the males are usually larger, whereas in the burrowing species the females are larger. The males often perform precopulatory mate guarding of females until the parturial molt of the female, after which sperm transfer is possible. The precopula can last for many days (Jormalainen 1998). Protandric hermaphroditism was shown for several Lysianassoidea by morphological and histological evidence (Lowry and Stoddard 1986). For example, populations of Acontiostoma maronis had small primary males (individuals with penial processes only) and small secondary males (individuals with penial processes and secondary male characters) but large females that retained penial processes. These females were thought to have originated from the small protandric males. An interesting case of hermaphroditism is Echinogammarus marinus. In this species, endocellular bacteria of the genus Wolbachia change chromosomic males into functional females, which produce fertile offspring at low temperature but sterile offspring at high temperature (Ford et al. 2004). Sexual Systems of the Copepoda Copepoda is probably the animal group with the highest number of individuals worldwide. They comprise about 16,000 species and date back to the Ordovician (485–​444 mya) or late Cambrian (497–​485 mya). They have sizes typically below 5 mm and longevities of some weeks to months (Huys and Boxshall 1991, Boxshall and Defaye 2008, Harvey et al. 2012, Eyun 2017). Many copepods produce resting eggs that remain viable for years to centuries, depending on species (Hairston et al. 1995). Copepods are found in almost all aquatic habitats, from deep sea trenches to high mountain lakes, including hypersaline inland waters and hot springs. Most of the free-​living species are members of the marine plankton and interstitial fauna. Approximately half of the described species live in parasitic associations, mostly as ecto-​parasites on crustaceans and fishes. Some of them are severe pests in fisheries and aquaculture. Almost all copepods reproduce by gonochorism, even the parasitic species. Parthenogenesis is rare and hermaphroditism is unknown. Several families of parasitic copepods have evolved dwarf males, which are many times smaller than their corresponding females (Østergaard and Boxshall 2004, Østergaard et al. 2005). In the Chondracanthidae, a family for which all species are parasitic on marine fishes, the males attach to immature females at the second copepodite stage, complete their development on the female, and remain there until they die. A maximum of eight males on a single female has been recorded, but most females have only one male attached. An example is Chondracanthus lophii, in which tiny males (B and C in Fig. 6.3) adhere near the female genital apertures to so-​called nuptial organs, which are special structures for attachment and probably nourishment (Østergaard 2004, Østergaard and Boxshall 2004). The transformation of males into females indicative of protandric hermaphroditism was suspected for some Calanidae on the basis of changes of external morphological characters, but clear proof of hermaphroditism is still lacking (Gruner 1993). Parthenogenesis is documented for populations of the three freshwater harpacticoids, Elaphoidella bidens, Epactophanes richardi, and Canthocamptus staphylinus, and is suspected for some more Elaphoidella species (Sarvala 1979). In Canthocamptus staphylinus, only the northern populations in Finland reproduce by parthenogenesis, whereas the southern populations are gonochoristic, indicating geographical parthenogenesis.

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Reproductive Biology Sexual Systems of the Cladocera The Cladocera evolved in freshwater and only a few species have invaded the sea. They first appeared in the Permian (299–​252 mya) and include some 630 species (Gruner 1993, Forró et al. 2008). Cladocerans are prominent members of the plankton, but there are also many benthic species living on the substrata, on aquatic plants, or even in humid terrestrial environments like mosses and leaf litter. They are mostly in the lower millimeter range in size and have longevities of a few weeks or months. However, resting stages can survive in egg banks of the sediment for decades and even centuries (Radzikowski 2013). All cladocerans are directly developing and brood their young until the juvenile stage. They reproduce mainly by cyclic parthenogenesis and less frequently by obligate parthenogenesis. Purely bisexual and hermaphroditic reproduction are unknown. Cyclic parthenogenesis, the periodic alternation between parthenogenetic and bisexual reproduction (A in Fig. 6.4), arose under freshwater conditions in the ancestors of the Cladocera (Taylor et  al. 1999). It has been retained since the Permian and persisted even in those cladocerans that invaded the sea (Egloff et al. 1997, Decaestecker et al. 2009). Females are generally larger than males and are most easily identified when carrying embryos or juveniles in their dorsal brood chamber (B in Fig. 6.4). The parthenogenetically generated subitaneous eggs (B in Fig. 6.4) develop directly into juveniles, whereas the sexually produced resting eggs are typically enclosed in ephippia (C in Fig. 6.4) and overwinter. The rhythm of alternation between sexual and parthenogenetic reproduction is highly variable and depends on the species and environmental conditions (Dufresne 2011). In ephemeral ponds, sexual reproduction may follow a single round of parthenogenesis, whereas in temperate lakes a sequence of parthenogenetic cycles during spring and summer is followed by a single sexual reproduction in late autumn. Sometimes, a fraction of the parthenogenetic females omits the sexual

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ephippium with sexual eggs

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hatching after diapause

PARTHENOGENETIC CYCLE

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Fig. 6.4. Cyclic parthenogenesis in Cladocera. (A)  Scheme of cyclic parthenogenesis in Daphnia. Modified after a drawing by Dita B. Vizoso, with permission. (B) Daphnia sp. with parthenogenetically produced subitanous eggs in brood chamber (arrow). Scale bar = 2 mm. Photo courtesy of Bruno Erb, with permission. (C) Daphnia sp. with two sexually produced eggs in ephippium (arrow). Scale bar = 1.5 mm. Photo courtesy of Jean-​Pierre Claes; from Vogt (2016), with permission from John Wiley and Sons.   



An Overview of Sexual Systems

phase by overwintering in deeper water, continuing with parthenogenetic reproduction the next spring (Pietrzak et al. 2013). Tropical populations can reproduce parthenogenetically year round. The mode of oogenesis in parthenogenetic females of Daphnia pulex is apparently a special kind of automixis named “abortive meiosis” (Hiruta et al. 2010). The oocytes undergo the first meiotic division up to early anaphase, but then the half-​bivalents move back and assemble to form a diploid equatorial plate. Finally, the sister chromatids are separated and move to opposite poles, and a small polar body is extruded. This abortive meiosis can lead to genetically variable offspring because recombination is possible between homologous chromosomes, but validating genetic analysis is lacking (Hiruta et al. 2010, Hiruta and Tochinai 2012). Some daphnid species have made the transition from cyclic to obligate parthenogenesis. A good example is D.  pulex in North America, where obligately parthenogenetic populations are found along the northern, northeastern, and southern margins of the distribution range, indicating geographical parthenogenesis (Fig. 6.5). The transition from cyclic to obligate parthenogenesis has evolved many times, and thus, thousands of asexual clones were generated in the Great Lakes watershed alone (Hebert and Finston 2001). Daphnia middendorffiana, which inhabits arctic and alpine habitats, seems to reproduce exclusively by obligate parthenogenesis (Dufresne and Hebert 1997). Some of the obligately parthenogenetic daphnids are diploid, suggesting that they were derived from a single parental species, but others are polyploid, indicating a hybrid origin (Adamowicz et al. 2002, Dufresne 2011). However, triploid daphnids may also arise from autopolyploidization, and

tundra boreal forest deciduous forest evergreen forest grassland desert

cyclic parthenogenesis obligate parthenogenesis

Fig. 6.5. Sexual systems of Daphnia pulex in North America. Populations reproducing by cyclic parthenogenesis are restricted to the central and northwestern United States, whereas obligately parthenogenetic populations are found at the northern, northeastern, and southern margins of the distribution range. Mixed populations with both sexual systems occur in the Midwest. Modified after Hebert and Finston (2001), with permission from Nature Publishing Group.   

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Reproductive Biology hybrids can reduce their set of chromosomes to diploidy, complicating interpretation (Dufresne and Hebert 1994, Little et al. 1997). An example of a polyploid obligate parthenogen is D. pulex in Scandinavia, which apparently evolved from several independent hybridizations between D. pulex and a closely related species (Ward et al. 1994). As a rule of thumb, polyploid obligate parthenogens are predominant in low-​temperature regions, whereas diploid obligate parthenogens are found in more temperate zones (Ward et al. 1994, Dufresne and Hebert 1997, Little et al. 1997). Sexual Systems of the Ostracoda The Ostracoda are among the smallest crustaceans, with the majority measuring between 0.5 and 2 mm. An extreme is the deep sea ostracod Gigantocypris agassizi with a length of 3.4 cm (Vermeij 2016). Ostracods probably originated in the Cambrian (541–​485 mya) and comprise some 7,500 marine and freshwater species (Harvey et al. 2012, Oakley et al. 2013). Most species are benthic, living on and in the substrata and on aquatic plants. Some species inhabit mosses and the leaf axils of land plants. Freshwater species usually live for a few months and overwinter as eggs. Marine species have longevities of up to three years. Ostracods can produce desiccation-​resistant and diapausing eggs that foster their distribution. Most ostracods reproduce sexually, but parthenogenetic populations are common (Cohen and Morin 1990, Martens 1998). Chaplin et al. (1994) even assumed that Ostracoda is the animal group with the highest incidence of parthenogenesis. Hermaphroditism is unknown. In gonochoristic species, the sex ratio is often markedly skewed toward females, which may be due to the presence of multiple sex chromosomes (Chaplin et al. 1994, Schön and Martens 1998). In some groups, the embryos are brooded in a posterior brood chamber of the female (A in Fig. 6.6), mostly until the nauplius stage (Horne et al. 1998b). Such females have larger shells than conspecific males. In many species of the freshwater family Cyprididae, the sexually reproducing populations also contain parthenogenetic females, forming a mixed reproduction system (Martens 1998). The superfamily Cypridoidea, which is predominant in freshwater, has evolved giant sperm of up to 11.8 mm in length (B and C in Fig. 6.6) corresponding to several times the shell length of the producing male (Smith et al. 2016). These unusual sperm are ejected one after the other with the help of sperm pumps or Zenker organs. The sperm pumps are located within the paired seminal ducts and are composed of a chitinous skeleton and numerous small muscles (D and E in Fig. 6.6). They are contracted by longitudinal muscles and expanded by the elastic nature of the chitinous part of the pump. The entrance of the pump is controlled by a valve. Details of its function are found in Yamada and Matzke-​Karasz (2012). Sperm is transferred to females with intricate hemipenes (Cohen and Morin 1990, Matzke-​Karasz 2005, Yamada and Matzke-​Karasz 2012). During a single copulation event, several dozen spermatozoa can be transferred to the female’s seminal receptacle. The vast majority of ostracod parthenogens are found in freshwater. More than 40% of the freshwater species and most of the European freshwater populations are purely parthenogenetic, which is in sharp contrast to the British coastal ostracods that include only 5% parthenogens (Butlin et al. 1998, Horne et al. 1998a). Parthenogenesis evolved multiple times in freshwater ostracods, as may be deduced from the presence of parthenogens in seven of 10 families and 24 of 29 North American genera (Chaplin et al. 1994). Parthenogenetic ostracods appear to have arisen by suppression of sexuality in the parental species (diploids) and by hybridization (polyploids) (Chaplin et al. 1994, Martens 1998, Chapter 9 in this volume). Unlike in cladocerans, there is no evidence that functional males could be produced by parthenogenetic females, making the transition to parthenogenesis irreversible (Schön and Martens 1998). Ostracods show no strong tendency toward geographical parthenogenesis like cladocerans. This type of reproduction is almost exclusively found in the Cyprididae (Horne et  al. 1998a). An example is Eucypris virens with southern bisexual populations and northern parthenogenetic



An Overview of Sexual Systems

(A)

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(B)

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(E)

Fig. 6.6. Brood care and giant sperm in Ostracoda. (A) Female of Vargula hilgendorfii with embryos (E) in posterior brood chamber. A  =  first antenna; F  =  furca. Scale bar  =  500 µm. From Siveter et  al. (2014), with permission from Elsevier. (B) Clump of sperm from the seminal receptacle of a female Mytilocypris mytiloides. Scale bar = 100 µm. From Smith et al. (2016), with permission from John Wiley and Sons. (C) Drilled anterior tip of giant spermatozoon of Pseudocandona marchica. Scale bar = 1 µm. From Smith et al. (2016), with permission from John Wiley and Sons. (D) Chitinous skeleton of sperm pump of Fabaeformiscandona subacuta. Scale bar = 40 µm. From Smith et al. (2016), with permission from John Wiley and Sons. (E) Scheme of sperm pump. Asterisk = valve; C = cap; CS = chitinous skeleton; IT = interior tube; L = lumen; M = muscle; S = spermatozoa; SD = sperm duct. Modified after Yamada and Matzke-​Karasz (2012), with permission from Springer.   

populations (Schmit et al. 2013). When parthenogenetic and gonochoristic populations occur in the same geographical region, the parthenogens are predominant in habitats of recent origin such as ponds, whereas the sexuals are predominant in older habitats such as glacial lakes, suggesting that parthenogens are effective colonizers but are sensitive to displacement by sexuals in the long term (Chaplin et al. 1994, Horne et al. 1998a). Accordingly, most parthenogenetic lineages seem to be phylogenetically young. An exception are the freshwater Darwinulidae (31 species), which have persisted without males for more than 100 million years, despite their occupancy of habitats normally associated with sexual reproduction (Martens et al. 2003, Schön et al. 2009). Sexual Systems of the Cirripedia The Cirripedia originated in the Cambrian (541–​485 mya) and comprise approximately 1,300 species. They inhabit marine environments from the littoral (most species) to the deep sea and from the tropics to the polar region. A few species have invaded brackish-​water environments (Collins and Rudkin 1981, Anderson 1993, Gruner 1993). Cirripeds usually have body sizes of some mm to

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Reproductive Biology a few cm and reach ages between one and 10 years. The adults are either sessile filter feeders or highly specialized parasites of crustaceans. All cirripeds brood their embryos at least until release of the nauplius larva. Cirripedia are gonochoristic or hermaphroditic. Parthenogenesis is unknown. Cirriped males are generally dwarf males (Klepal 1987, Lin et al. 2015). The Thoracica are the largest cirriped group and include the sessile acorn and gooseneck barnacles. Some species are protandric hermaphrodites, but most species are simultaneous hermaphrodites. They transfer sperm by an exceptionally long penis (A in Fig. 6.7), which is unique among sessile animals. During the breeding season the simultaneous hermaphrodites can repeatedly alternate between male and female behavioral states (Anderson 1993, Yusa et al. 2013). Only a few hermaphrodites are known to be facultative self-​fertilizers. The female and male gonads are spatially separate, like in cephalocaridan and remipedian hermaphrodites, which is in contrast to the decapod hermaphrodites that have ovotestes. The pedunculate Scalpellidae (268 species) are of special interest because they occur from shallow water to the deep sea and have different types of development (Buhl-​Mortensen and Høeg 2006). They reproduce by hermaphroditism, androdioecy with hermaphrodites and males (B in (A)

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Fig. 6.7. Sexual systems in Cirripedia. (A) Simultaneous hermaphrodite of Balanus glandula showing slightly extended penis (arrow). Scale bar = 2 mm. Photo courtesy of Christopher J. Neufeld; from Vogt (2016), with permission from John Wiley and Sons. (B) Androdioecious gooseneck barnacle Scalpellum scalpellum with penis (arrow) and attached male cyprids (frame, arrowheads) that metamorphose into sac-​like dwarf males of similar size. Scale bar = 0.5 cm. From Spremberg et al. (2012), with permission from Elsevier. (C–​D) Gonochoristic reproduction with large females and tiny dwarf males in parasitic rhizocephalan Sacculina carcini. (C) Scheme of infected crab showing subdivision of Sacculina female in rhizoid interna (arrows) and sac-​like externa. Modified after Gruner (1993), with permission from Springer Nature. (D) Colonization of female receptacle by dwarf male. The male cyprid larva metamorphoses at the entrance of the mantle cavity of the female into a trichogon, which escapes through the antennule of the cypris and migrates to the ovarian receptacle to be implanted as a sperm producing dwarf male. Redrawn after Høeg (1992), with permission from Wiley.   



An Overview of Sexual Systems

Fig. 6.7), and dioecy with females and males. Androdioecy, which is rare in the animal kingdom (Høeg et al. 2016), has been described in ~30 pedunculate species (Kelly and Sanford 2010). It has independently evolved multiple times (Fig. 6.8). Some scalpellids show variants of these three main systems, as detailed in Yusa et al. (2013). Scalpellid dwarf males are lecithotrophic and non-​feeding. They are shorter-​lived than their carrying females or hermaphrodites, and thus, females must repetitively acquire new males during their lifetime (Høeg et al. 2016). It is largely unknown how the tiny dwarf males fertilize the females, but males of Verum brachiumcancri and Gymnoscalpellum indopacificum, which are embedded in a pair of receptacles inside the rim of the mantle cavity of the

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D Ibla cumingi A Ibla quadrivalvis H Lithotrya valentiana H Capitulum mitella D Trianguloscalpellum regium 1.00 H Arcoscalpellum sociabile 0.99 A Arcoscalpellum sp. 0.93 D Scalpellum stearnsii * 1.00 A Scalpellum scalpellum * H Trianguloscalpellum balanoides H Oxynaspis celata A Megalasma striatum H Poecilasma kaempferi 0.82 1.00 A Octolasmis warwickii * H Octolasmis angulata * H Octolasmis cor 1.00 H Temnaspis amygdalum 0.85 H Octolasmis lowei H Conchoderma auritum 1.00 H Conchoderma virgatum 1.00 1.00 H Conchoderma hunteri H Lepas pectinata 1.00 H Lepas anatifera 0.99 H Lepas anserifera 0.99 H Lepas australis 1.00 H Lepas testudinata A Paralepas xenophorae 1.00 D Koleolepas sp. * 1.00 A Koleolepas avis * H Paralepas palinuri H Heteralepas quadrata 0.76 H Paralepas dannevigi 0.65 H Heteralepas japonica D Ornatoscalpellum stroemii 1.00 D Amigdoscalpellum sp. 0.95 D Litoscalpellum discoveryi 1.00 D Arcoscalpellum beuveti H Leucolepas longa 0.97 H Neolepas zevinae 1.00 H Neolepas rapanuii H Ashinkailepas seepiophila 0.95 H Vulcanolepas osheai 0.99 H Pollicipes polymerus H Pollicipes pollicipes 1.00 D Calantica sp. A Smilium peronii 1.00 A Calantica spinosa 1.00 A Calantica villosa

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Fig. 6.8. Reconstruction of the evolution of sexual systems in pedunculate barnacles by phylogenetic analysis. Sexual systems were placed on the Bayesian phylogenetic tree. The graph shows that androdioecy (A) and dioecy (D) evolved repeatedly from simultaneous hermaphroditism (H). The sexual systems can even differ between species of the same genus (asterisks). Redrawn after Yusa et al. (2012).   

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Reproductive Biology females, were shown to possess a relatively long penis that can be stretched deeply into the mantel cavity (Buhl-​Mortensen and Høeg 2013, Chan et al. 2014). The Acrothoracica (56 species), which live in the shells of mollusks and in other chalky substrata, are gonochoristic and have dwarf males that are attached in groups to the females (Gruner 1993, Anderson 1993). Gonochorism with tiny males is also the only known sexual system in the parasitic Rhizocephala (253 species). The body of the rhizocephalan female is composed of a root-​like interna, which penetrates host organs to absorb nutrients, and a sac-​like reproductive externa (C in Fig. 6.7; Høeg 1992). The eggs in the externa are usually fertilized by sperm of extremely reduced dwarf males that originate from invading trichogons (Høeg 1991). Trichogons are the most reduced crustacean larvae originating from male cypris larvae by metamorphosis (D in Fig. 6.7). They migrate to the female’s ovary and settle in special ovarian receptacles to transform into dwarf males. These dwarf males are nourished by the female and produce sperm for months and even years. In some rhizocephalan families, male cyprids inject the spermatogonia directly into the mantle of the females, skipping the dwarf male stage (Høeg 1991).

EVOLUTION OF SEXUAL SYSTEMS IN THE CRUSTACEA The evolution of sexual systems in animals is usually reconstructed by phylogenetic analysis of extant species and explained by evolutionary theory. Direct evidence from the fossil record is relatively rare. Phylogenetic Reconstruction of Sexual Systems In this section, I  discuss three examples of phylogenetic reconstructions of sexual systems in crustaceans:  the evolution of simultaneous hermaphroditism in Decapoda; the shift from hermaphroditism to androdioecy and dioecy in Cirripedia; and the evolution of obligate parthenogenesis in Cladocera. Simultaneous hermaphroditism in caridean shrimps was previously thought to have evolved within the genus Lysmata (discussed in Bauer 2000). However, phylogenetic analysis suggests an origin outside of this genus because simultaneous hermaphroditism also occurs in the genera Exhippolysmata, Lysmatella, and Parhippolyte, which position ancestrally to Lysmata (Fiedler et al. 2010). Since the evolution of simultaneous hermaphroditism clearly predates the radiation of Lysmata, its origin cannot be explained by the special sociobiology and ecology of the extant members of Lysmata (Bauer 2007, Fiedler et al. 2010). In thoracican cirripeds, the predominant sexual system is simultaneous hermaphroditism, but the ancestral system of Cirripedia is probably gonochorism. This can be inferred from the frequency of bisexual reproduction in the acrothoracican and rhizocephalan cirripeds and the Ascothoracida and Tantulocarida, the closest relatives of the Cirripedia (Høeg 1991, Schminke 2013). Phylogenetic analysis indicates that in thoracicans, hermaphroditism has shifted multiple times toward androdioecy and dioecy (Fig. 6.8). In some lineages, sexual systems even differ within genera, suggesting that they can change on relatively short evolutionary timescales (Yusa et  al. 2013). For example, Octolasmis angulata is hermaphroditic but O. warwicki is androdioecious, and Scalpellum scalpellum is androdioecious but S. stearnsi is dioecious (Fig. 6.8). Phylogenetic analysis also contributed significantly to the understanding of the evolution of obligate parthenogenesis from cyclic parthenogenesis in North American cladocerans. Xu et  al. (2013, 2015) revealed that the assemblage of mutated genes underlying obligate parthenogenesis in Daphnia pulex originated from D. pulicaria due to a unique historical hybridization and introgression event. These mutated genes inhibit meiosis in females but not in males. They are spread in a



An Overview of Sexual Systems

contagious manner by rarely occurring males of obligately parthenogenetic lineages that mate with cyclic parthenogenetic females (Paland et al. 2005). About half of the clones that reproduce by obligate parthenogenesis retained the ability to produce males (Dufresne 2011). Tucker et al. (2013) conducted whole genome analysis of cyclic and obligately parthenogenetic genotypes and found that radiation of the latter in North American D. pulex is as recent as 1,250 years, although the origin of the meiosis-​suppressing elements could be substantially older. Evidence for Ancient Sexual Systems in the Fossil Record The best example for the contribution of fossils to reconstructing sexual systems in crustaceans are the Ostracoda, which have one of the most complete fossil record of any animal group (Griffiths and Horne 1998). Gonochorism is usually inferred from the presence of dimorphic valves in a fossil bed (Chaplin et al. 1994). Sometimes, males and females can be distinguished more directly by imprints of the gonads in the insides of the valves, and in rare cases, by preserved male and female reproductive organs. Shell dimorphism turned out to be a valuable tool for investigating the role of sexual system shifts in ecological and geographical adaptation (Griffiths and Horne 1998). For example, the patterns of dimorphic and monomorphic shells in fossil freshwater Cypridoidea indicate frequent transitions from gonochorism to parthenogenesis in the Late Jurassic, which partly explains the rapid geographical expansion of the cypridoids at that time. As well, the absence of a clear correlation between male occurrence and geographical parameter in Quaternary ostracods of Europe refutes the hypothesis of post-​glacial recolonization of Northern Europe by geographical parthenogens. Last but not least, shell patterns demonstrate a more than 100 million-​year-​old history of obligate parthenogenesis in freshwater Darwinulidae and their origin from gonochoristic ancestors in the Late Paleozoic. In the past decade, some exceptional ostracod fossils of soft body parts have been discovered, which allowed for direct identification of sexes and provided decisive conclusions about reproduction in ancient times (Matzke-​Karasz et  al. 2014). Siveter et  al. (2014) found Silurian and Ordovician ostracods with well-​preserved embryos, providing conclusive evidence of a conserved brood care strategy within the marine Myodocopida for at least 450 million years. Matzke-​Karasz et al. (2014) discovered giant sperm in males and females from the early Miocene, closely resembling the spermatozoa of extant relatives. Other well-​preserved reproductive structures were the sperm pumps in males, which are restricted to taxa with giant sperm. Such sperm pumps were also detected in Cretaceous ostracods (Matzke-​Karasz et al. 2009), suggesting that reproduction with giant sperm in the Cypridocopina evolved more than 100 million years ago (Smith et al. 2016). Using Evolutionary Theory to Explain Diversity in Crustacean Sexual Systems The most powerful theories to explain the prevalence and evolution of sexual systems in animals are probably the sex allocation theory and life history theory. The sex allocation theory describes the sexuality of organisms as the result of allocation of resources to male and female functions (Charnov 1982). Life history theory deals with the allocation of resources toward growth, survival, and reproduction, as well as the trade-​offs that bind these traits together (Stearns 1992). Further theoretical tools are the size advantage model, low density model, and gene dispersal model, which are detailed in Ghiselin (1969) and Subramoniam (2013). In the following, I will try to explain three examples of sexual system patterns with evolutionary theory: the diversification of sexual systems in sessile crustaceans; the evolution of dwarf males in parasitic crustaceans; and the adaptive value of parthenogenesis in freshwater crustaceans. Yusa and colleagues have explained the evolution of hermaphroditism, androdioecy, and dioecy in thoracican cirripeds by considering the evolutionary constraints of sessile filter feeding and

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Reproductive Biology sperm transfer with a penis and applying a combination of sex allocation theory and life history theory (Yamaguchi et al. 2012, Yusa et al. 2012, 2013). They identified low population density and resulting limited mating opportunity as the main evolutionary force, and established an evolutionary sequence from gonochorism with normal-​sized males to simultaneous hermaphroditism to androdioecy with dwarf males to dioecy with dwarf males. Their theory explains the abundance of simultaneous hermaphrodites in densely aggregated intertidal barnacles and the restriction of dioecy to solitary deep-​sea pedunculates. Bisexual reproduction by females and dwarf males is predominant in parasitic crustaceans across diverse taxonomic groups such as rhizocephalans, copepods, and isopods. The main advantage of this sexual system is the permanent availability of sperm at comparably low cost while maintaining high genetic diversity (Vollrath 1998). Interestingly, other common reproductive strategies of animal parasites like hermaphroditism or the alternation of bisexual and asexual reproduction (Whitfield and Evans 1983) are not common in crustacean parasites. Hermaphroditism is restricted to two families of isopod ectoparasites, and asexual reproduction is entirely unknown in crustacean parasites. The reasons for these peculiarities may lie in evolutionary constraints. The Ostracoda are often cited as a paradigm for the advantage of parthenogenetic reproduction in freshwater. In the approximately 2,000 species of freshwater ostracods, parthenogenesis is indeed predominant and has originated multiple times, whereas it is relatively rare in marine ostracods (Chaplin et al. 1994, Martens et al. 2008). The ~600 cyclic parthenogenetic freshwater Cladocera seem to support the advantage of parthenogenesis in freshwater (Forró et al. 2008). However, in the 3,000 freshwater Decapoda and 2,800 freshwater Copepoda, parthenogenesis is only known for two and three species, respectively (Sarvala 1979, Vogt et al. 2015), and in the 950 freshwater Isopoda and 1,870 freshwater Amphipoda, parthenogenesis is unknown (Gruner 1993). The differences between these higher taxa may lie in evolutionary constraints, size differences, life history differences, and alternative adapt­ ive strategies that lower the propensity for a shift from gonochorism to parthenogenesis. The exceptionally frequent transition from gonochorism to parthenogenesis in the freshwater Cypridoidea may be explained by the advantages of avoiding the high cost of reproduction with giant sperm, which requires almost one-​third of the body volume of the males (Chaplin et al. 1994, Smith et al. 2016). The Decapoda seem to have adapted to freshwater environments by abbreviation of larval development and extension of brood care, rather than by altering their sexual system. More than 90% of freshwater decapods show abbreviated development, and about 70% have extended brood care until the juvenile stage, which is in sharp contrast to their marine relatives (Vogt 2013). All freshwater isopods and amphipods show brood care until the juvenile stage as well, but they have inherited this presumably advantageous strategy from the marine stem line of the Peracarida (Gruner 1993, Thiel 2003). The idea of extended brood care as an adaptive alternative to parthenogenesis seems to be corroborated by the absence of brood care in the Cypridoidea (Horne et al. 1998b), which comprise the vast majority of ostracod parthenogens in freshwater. However, freshwater cladocerans show both parthenogenesis and extended brood care, making interpretation even more difficult. Hypotheses on the Ancient Sexual System of the Crustacea The discussion of whether the ancient sexual system of the Crustacea is gonochorism, as suggested by Martin and Davis (2001), or simultaneous hermaphroditism, as proposed by Juchault (1999), is highly controversial. A hermaphrodite origin may be inferred from Cephalocarida and Remipedia that reproduce exclusively by simultaneous hermaphroditism (Yager 1991, Hessler and Elofsson 1992). These groups were often regarded as the most primitive crustaceans because of their rather homonomous segmentation. Unfortunately, their evolutionary history is not well documented. The male and female gonads of Cephalocarida and Remipedia are spatially separate, which would be a good anatomical precondition for a later transition to gonochorism.



An Overview of Sexual Systems Table 6.2.  Sexual Systems in Arthropoda. Group Chelicerata Myriapoda Crustacea Insecta

Gonochorism xxx xxx xxx xxx

Hermaphroditism –​ –​ xx x

Parthenogenesis xx xx xx xx

xxx = dominant sexual system; xx = less frequent sexual system; x = rare sexual system.

Support for the gonochorism hypothesis comes from the predominance of gonochorism in the vast majority of extant crustaceans and the lack or extreme rarity of hermaphroditism in the other arthropod groups (Table 6.2). The Anostraca may serve as an illustrative modern example. Similar to the Cephalocarida and Remipedia, they show plesiomorphic homonomous segmentation but are gonochoristic. Their gradual or anamorphic development is even more primitive than that of Cephalocarida and Remipedia, closely resembling the development of ancient Rehbachiella kinnekullensis from the Cambrian (Waloßek 1995).

GENETIC UNDERPINNING OF SEXUAL SYSTEM SHIFTS It is presently unknown whether the propensity toward sexual system shifts depends on the mode of sex determination. In most crustaceans, sex is genetically determined by a XY/​XX or WZ/​ZZ sex chromosome system. XO and XY systems with heterogametic males have been described for ostracods, amphipods, and brachyuran crabs, and WZ systems with heterogametic females are known from branchiopods, isopods, and freshwater crayfish (Ginsburger-​Vogel and Charniaux-​ Cotton 1982, Parnes et  al. 2003, Subramoniam 2013, Chandler et  al. 2016). The sex determination systems are not uniform in higher taxa, as shown in Fig. 6.9 for the Decapoda. For example, the Astacidea and Brachyura both have WZ and XY systems. Some crustaceans, particularly ostracods, have polygenic sex-​determination, in which multiple sex genes are spread over several chromosomes. This unique system can produce broad sex ratio variations in the offspring, ranging from 100% males to 100% females (Schön and Martens 1998). The Cladocera and some Cirripedia, Ostracoda, Isopoda, Amphipoda, and Tanaidacea show environmental sex determination, in which sexes are defined by the interaction of environmental cues and sex genes (Ginsburger-​Vogel and Charniaux-​Cotton 1982, Subramoniam 2013, Høeg et al. 2016). In Malacostraca, each individual possesses the complete genetic information for morphogenesis of both sexes (Charniaux-​Cotton and Payen 1985). The gonad anlagen develop into testes if exposed to the androgenic hormone from the androgenic gland and into ovaries if not exposed. The insulin-​like androgenic hormone (Ventura et al. 2015) also determines the secondary sexual characteristics of males, whereas the female secondary sexual characteristics are determined by an unidentified ovarian factor (Charniaux-​Cotton and Payen 1985). Androgenic gland anlagen are present during embryonic development in both males and females, but their further development depends on the expression of specific alleles in genotypic males. Damage of the androgenic gland system in genetic males explains the occasional occurrence of intersex individuals in otherwise gonochoristic populations. Their proportion in malacostracans is mostly below 1%, but can be considerably higher in populations exposed to environmental endocrine disruptors (LeBlanc 2007, DeFur and Williams 2015).

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(B) Astacidea

WZ/ZZ XY/XX

Thalassinidea

No data

Achelata

XY/XX?

Anomala

No data

Brachyura

WZ/ZZ XY/XX

Long Moderate Good Short Suboptimal day length temperature nutrition day length temperature

Poor nutrition

Sensory receptors

Neurosecretory cells Stimulating neuropeptides

Inhibitory neuropeptides Methyl farnesoate producing tissue

Methyl farnesoate

Ovary Caridea

WZ/ZZ

Stenopodidea No data Dendrobranchiata WZ/ZZ

Female offspring

Male offspring Female sex determination

Male sex determination

Fig. 6.9. Genetic and environmental sex determination in Crustacea. (A)  Genetic sex determination in Decapoda. Sexual development is regulated by a sex-​specific genetic cascade that is initiated through a chromosomal mechanism of sex determination. WZ/​ZZ and XY/​XX systems are present but there is no phylogenetic directionality. Modified after Chandler et al. (2016), with permission from Oxford University Press. (B) Neuro-​ endocrine model for environmental sex determination in daphnids. Poor environmental conditions trigger synthesis and secretion of methyl farnesoate that programs the embryo to develop a male phenotype. In the absence of methyl farnesoate, embryos develop into females. Modified after LeBlanc and Medlock (2015), with permission from John Wiley and Sons.   

Detailed examples of the genetic underpinning of sexual system shifts are rare. A good example is the crayfish Cherax quadricarinatus in which experimental silencing of the androgenic hormone-​ encoding gene Cq-​IAG in intersex individuals induced extensive testicular degeneration, phenotypic feminization, and yolk accumulation in the developing oocytes (Rosen et al. 2010). These data indicate that the Cq-​IAG gene is crucial for sex change from functional male to female, providing a first step toward understanding sequential hermaphroditism. Daphnia pulex is an ideal model to investigate the genetic basis of the gonochorism-​to-​ parthenogenesis transition because as a cyclic parthenogen it must contain the genetic and molecular machinery for both sexual and parthenogenetic reproduction. Moreover, its genome is already fully sequenced and annotated (Colbourne et al. 2011), facilitating investigation of genes involved in sexual system change. Using genome-​wide association analysis, Xu et al. (2015) detected a set of 647 alleles with single nucleotide polymorphisms that were specific to obligate parthenogens. This finding supports the idea that the capacity for meiosis suppression is conferred by the joint action of multiple loci, rather than by a single dominant mutation (Lynch et al. 2008). As explained earlier in the Cladocera section, these “obligatory parthenogenesis genes” were inherited from Daphnia pulicaria via hybridization. Although Xu et al. (2015) were able to classify 206 of these genes into known eukaryotic ortholog groups, the specific factors underlying obligate parthenogenesis remained elusive. Eads et  al. (2012) established that all obligate parthenogens of Daphnia pulex carry a transposable element insertion and a frameshift mutation in the cohesin REC8 encoding gene, suggesting that obligate parthenogens have lost the ability of chromosome segregation at meiosis I.



An Overview of Sexual Systems

The crayfish pair Procambarus fallax and P. virginalis provides another interesting example for research on the genetic underpinning of the transition from gonochorism to obligate parthenogenesis. We have recently shown that parthenogenetic P. virginalis originated instantaneously from bisexually reproducing P. fallax by autotriploidization and a parallel decrease of the DNA-​methylation level (Vogt et al. 2015). The latter finding indicates considerable changes in regulation of the genome besides gene multiplication (Gatzmann et al. 2018). Meanwhile, the genomes of both crayfish are fully sequenced (Gutekunst et al. 2018, Marbled Crayfish Genome Server: http://​marmorkrebs. dkfz.de/​). First comparison of about 13,000 automatically annotated protein-​coding transcripts revealed potential alterations in meiosis-​related genes in the parthenogenetic P. virginalis.

EVOLUTION OF GSD FROM ESD AND THE ROLE OF THE ENVIRONMENT IN SEXUAL SYSTEM SHIFTS Two topics are discussed in this section: the evolution of genetic sex determination (GSD) from environmental sex determination (ESD) in the early history of crustaceans, and the environmental induction of short-​term sexual system shifts in cyclic parthenogenetic crustaceans. GSD is predominant in the Crustacea, but ESD is frequent in Cladocera and some Cirripedia, Ostracoda, Isopoda, Amphipoda, and Tanaidacea. Empirical data collected over the past 40  years in different animal groups demonstrate that gender may have a considerable degree of phenotypic plasticity (environmentally induced phenotypic change; Leonard 2014). Phenotypic plasticity and underlying epigenetic mechanisms are obviously able to induce switches between different developmental trajectories (Levis and Pfennig 2016, Vogt 2017), which may also affect sexual systems. GSD via sex genes or sex chromosomes in animals has probably evolved this way from ESD, which is interpreted as the ancestral state in several major animal groups (Reisser et al. 2017). ESD may have repeatedly evolved into GSD via genetic assimilation of sex-​related traits that were originally environmentally determined (Levis and Pfennig 2016). The reversible shift between sexual systems in cyclic parthenogenetic cladocerans occurs regularly over relatively short time intervals. Therefore, unlike the transition from gonochorism to permanent obligate parthenogenesis, it cannot be explained by genetic mutation. Rather, it must be elicited by changes in the regulation of sex-​determining genes by environmentally induced epigenetic mechanisms. Obviously, cyclic parthenogenetic cladoceran females have the necessary genes for meiosis and the phenotypic expression of males, but can silence and activate them in response to environmental signals, resulting in either parthenogenetic or sexual reproduction. In Daphnia, the initial step of the transition from the parthenogenetic phase to the sexual phase is the production of males by parthenogenetic females (Hiruta and Tochinai 2012, LeBlanc and Medlock 2015, Gómez et al. 2016). The production of males requires appropriate environmental cues, male-​determining genes, and molecular mediators that interpret the environmental signals and activate these genes. The environmental cues that elicit the sexual phase are increased population density, low food availability, low oxygen content, low temperatures, and short day-​length (B in Fig. 6.9). An identified sex-​determining gene is Doublesex, which produces female traits and ovarian maturation when knocked down in embryos and male phenotypes when ectopically expressed (Kato et al. 2011). First candidates for the activation and silencing of genes involved in sexual system shifts are DNA-​methylation and histone modifications. These epigenetic mechanisms respond to environmental signals and can repeatedly be erased and re-​established during a lifetime ( Jaenisch and Bird 2003). The following scenario provides an illustration of the molecular cascade that may underlie environmentally induced generation of males. It is an extension of the hypothesis by LeBlanc and

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COMPARISON OF SEXUAL SYSTEMS BETWEEN CRUSTACEA AND OTHER ARTHROPODA The closest relatives of the Crustacea are the Insecta. They originated from crustacean ancestors, and together with the Crustacea, form the Pancrustacea or Tetraconata (Giribet and Edgecombe 2012). Insects are known since 380 mya ago, but probably already arose in the Silurian (444–​419 mya). They are mainly terrestrial, but some representatives spend some time or their whole life in freshwater. Very few species are marine (Echinophthiriidae = lice on seals). The predominant sexual system is gonochorism. Parthenogenesis is relatively frequent, but hermaphroditism is known only for a single genus of scale insects (Normark 2003). Parthenogenesis includes facultative, cyclic, obligate, and geographical parthenogenesis, as in crustaceans (Normark 2003, Schwander and Crespi 2009). Normark (2003) estimated that obligate parthenogenesis has arisen over 900 times and cyclic parthenogenesis about five times. The latter is widespread in aphids and facilitates the rapid expansion of populations when conditions are favorable, resembling the planktonic cladocerans. Insects have evolved some modes of reproduction that are unknown in crustaceans. An example is haplodiploidy, the development of diploid females from fertilized eggs and haploid males from unfertilized eggs. It is found in ants, bees, and termites. Further examples are sperm-​dependent thelytoky and gonochorism combined with polyembryony (Normark 2003). The Myriapoda, the presumed sister clade of the Pancrustacea within the Mandibulata (Giribet and Edgecombe 2012), are terrestrial and are known since the Silurian. They reproduce mainly by gonochorism. Geographical parthenogenesis has independently evolved in several lineages of the Chilopoda and Diplopoda. Hermaphroditism is unknown (Dunger 1993, Pinheiro et al. 2009). The Chelicerata, the presumed sister taxon of the Mandibulata (Giribet and Edgecombe 2012), have their roots in the Cambrian (541–​485 mya) or Precambrian (before 541 mya), like the Crustacea. The Xiphosura and Pantopoda are marine, but the vast majority of the Arachnida are terrestrial. Chelicerata mostly reproduce by gonochorism. Hermaphroditism is unknown, but parthenogenesis occurs in some groups. It is particularly frequent in the soil-​dwelling Acari, in which approximately 10% of the 10,000 species are estimated to reproduce parthenogenetically, probably by automictic thelytoky (Moritz 1993, Heethoff et al. 2009). Comparison of the sexual systems between crustaceans and the other arthropod groups indicates that gonochorism is by far the most frequent sexual system of Arthropoda, and therefore, it may be interpreted as their ancestral system. Crustaceans differ from the other arthropods mainly by the evolution and diversification of hermaphroditism (Table 6.2). There are also some differences in the modes of parthenogenetic reproduction, but geographical parthenogenesis is shared by all the major arthropod groups.



An Overview of Sexual Systems

PROBLEMS AND FUTURE DIRECTIONS The database on sexual systems in crustaceans is still small, particularly if only firmly established sexual systems are considered, as in this chapter. Future research is expected to considerably modify the patterns shown in Table 6.1. In the past, sexual systems have often been inferred from external sexual characters and the sex ratio of random samples in the wild. Histological investigation of the gonads, genetic parentage analyses, rearing in captivity, and thorough life history analyses would help to determine sexual systems and their specificities more precisely. Good examples are the identification of hermaphroditism in allegedly parthenogenetic clam shrimps (Brantner et al. 2013), the verification of protandry in a rhynchocinetid shrimp (Osawa et al. 2015), and the detection of a link between parthenogenesis and autotriploidy in marbled crayfish (Vogt et al. 2015). The interpretation of sexual system shifts within a species is sometimes hampered by unsettled taxonomy, particularly in cladocerans and ostracods. For example, “Daphnia pulex” and “Eucypris virens” are species complexes rather than distinct species (Bode et al. 2010, Dufresne 2011). Thus, putative geographical parthenogenesis of a “species” may sometimes be an artifact of geographical patterning of multiple, specifically adapted species with different sexual systems. Understanding sexual system shifts in crustaceans requires better knowledge of sex determination and regulation of reproduction. Progress in this field was made in recent years with Cherax quadricarinatus, a crayfish model of inducible sexual plasticity (Rosen et al. 2013). This species is particularly suitable for investigating the transition from intersex males to females. The analysis of entire genomes would be very helpful to identify the genes involved in sexual system shifts. Full genome sequences are currently available for three crustaceans, the water flea Daphnia pulex (Colbourne et  al. 2011), the amphipod Parhyale hawaiensis (Kao et  al. 2016), and the freshwater crayfish Procambarus virginalis (Gutekunst et al. 2018​). Genomics approaches are presently being used to identify the genes underlying obligate parthenogenesis in cladocerans (Xu et al. 2015) and crayfish (Gutekunst et al. 2018). The increased application of modern gene sequencing techniques to crustaceans is expected to reveal genomic information that allows more detailed study of the genetics of sexual system shifts. Parthenogenetic ostracods and cladocerans often show a surprisingly high genetic diversity. This is usually attributed to frequent historical shifts from gonochorism to parthenogenesis, multiple hybridizations between taxonomically related species, and repeated backcrossing of parthenogens with sexual populations. However, genetic diversity could also be generated to a certain degree by abortive meiosis in parthenogenetic females, which is perhaps more frequent in crustaceans than supposed hitherto. Parthenogenetic D. pulex, a classical textbook example of apomixis, was shown to be able to reproduce by this abbreviated form of automixis (Hiruta et al. 2010, Hiruta and Tochinai 2012). More intense cytogenetic investigations and microsatellite analyses of mothers and their offspring are required to establish more precisely the mode of thelytoky in the various crustacean parthenogens. Environmentally induced shifts of sexual systems by the interaction of environmental cues, sex-​determining genes, and molecular mediators can be best investigated in cyclic parthenogenetic cladocerans. The first genes and hormones that are involved in the production of males are already identified (LeBlanc and Medlock 2015). The prime candidate of an environmentally sensitive regulator of “sex change genes” is the DNA-​methylation system, which is presently characterized in Daphnia (Asselman et al. 2016). The investigation of environmental induction of sexual systems shifts in crustaceans on both the evolutionary and annual scale and its mediation by epigenetic mechanisms may significantly contribute to the more general “phenotypic plasticity-​first” (Levis and Pfennig 2016) and related “epigenetics-​first” (Vogt 2017) hypotheses of evolution. Patterns of sexual systems vary markedly among higher crustacean taxa and cannot be explained by a single comprehensive theory. For example, simultaneous hermaphroditism occurs in sessile

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Reproductive Biology cirripeds, mobile high-​density aggregations of shrimps, and burrowing low-​density populations of crayfish. The prevalence of sexual systems obviously depends on multiple factors such as evolutionary constraint, ease of sexual system shifts, and the influence of competing adaptive strategies. In the future, reproductive strategies that may lower the propensity of sexual shifts such as brood care or the production of resting stages should be better integrated into evolutionary ecological theories on sexual systems, as already exemplified by Martens (1998) for ostracods, Buhl-​Mortensen and Høeg (2013) for cirripeds, and Bauer and Thiel (2011) for caridean shrimps.

SUMMARY AND CONCLUSIONS The Crustacea have evolved a particularly broad range of sexual systems when compared to other animal groups, including various types of gonochorism, hermaphroditism, and parthenogenesis. Gonochorism is predominant by far. Hermaphroditism and parthenogenesis originated many times independently from gonochorism and occur in an estimated 2.2% and 2.4% of species, respectively. Gonochorism is considered to be the ancient sexual system of Crustacea, and of Arthropoda in general. Crustaceans differ from the other arthropod groups mainly by the abundance and diversity of hermaphroditic reproduction. The higher taxa of Crustacea show group-​specific patterns of sexual systems that differ markedly from each other. These specificities can, to a certain degree, be attributed to differences in lifestyle, life history, and adaptive responses to different environments. However, other factors like evolutionary constraint and competing adaptive strategies that lower the propensity of sexual system shifts may also have contributed to these patterns. The genetic basis of sexual system shifts is poorly investigated but is beginning to be understood in water fleas and crayfish. There is even less knowledge on the molecular mechanisms that mediate environmentally induced sexual system shifts, but DNA-​methylation and histone modifications are prime candidates of an environmentally sensitive regulator of sex genes.

ACKNOWLEDGMENTS The author is grateful to the following colleagues for providing information and illustrations, as indicated in the figure captions: Alexandre O. de Almeida (Porto Alegre, Brazil), Dieter Ebert (Basel, Switzerland), Bruno Erb (Erlinsbach, Switzerland), Jens T. Høeg (Copenhagen, Denmark), Renate Matzke-​Karasz (Munich, Germany), Pia Østergaard (London, United Kingdom), Tiffany Penland (Raleigh, North Carolina, USA), David J.  Siveter (Leicester, United Kingdom), Dita B.  Vizoso (Basel, Switzerland), and Brent P. Thoma ( Jackson, Mississippi, USA). Many thanks also to Rickey Cothran, Martin Thiel, Mika Tan, Tim Kiessling, and Miguel Penna for valuable comments, linguistic corrections, and editorial work.

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An Overview of Sexual Systems

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An Overview of Sexual Systems

Schwander, T., and B. J. Crespi. 2009. Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution 63:84–​103. Siveter, D. J., G. Tanaka, Ú. C. Farrell, M. J. Martin, D. J. Siveter, and D. E. G. Briggs. 2014. Exceptionally preserved 450-​million-​year-​old Ordovician ostracods with brood care. Current Biology 24:801–​806. Smit, N. J., N. L. Bruce, and K. A. Hadfield. 2014. Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. International Journal for Parasitology: Parasites and Wildlife 3:188–​197. Smith, R. J., R. Matzke-​Karasz, T. Kamiya, and P. De Deckker. 2016. Sperm lengths of non-​marine cypridoidean ostracods (Crustacea). Acta Zoologica 97:1–​17. Spremberg, U., J. T. Høeg, L. Buhl-​Mortensen, and Y. Yusa. 2012. Cypris settlement and dwarf male formation in the barnacle Scalpellum scalpellum: a model for an androdioecious reproductive system. Journal of Experimental Marine Biology and Ecology 422–​423:39–​47. Stearns, S. C. 1992. The Evolution of Life Histories. Oxford University Press, New York. Subramoniam, T. 2013. Origin and occurrence of sexual and mating systems in Crustacea: a progression towards communal living and eusociality. Journal of Biosciences 38:951–​969. Subramoniam, T. 2017. Sexual Biology and Reproduction in Crustaceans. Academic Press, New York. Suomalainen, E., A. Saura, and J. Lokki. 1987. Cytology and evolution in parthenogenesis. CRC Press, Boca Raton, Florida. Taylor, D. J., T. J. Crease, and W. M. Brown. 1999. Phylogenetic evidence for a single long-​lived clade of crustacean cyclic parthenogens and its implications for the evolution of sex. Proceedings of the Royal Society B 266:791–​797. Thiel, M. 2003. Extended parental care in crustaceans: an update. Revista Chilena de Historia Natural 76:205–​218. Toyota, K., H. Miyakawa, C. Hiruta, K. Furuta, Y. Ogino, T. Shinoda, N. Tatarazako, S. Miyagawa, J. R. Shaw, and T. Iguchi. 2015. Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex. Journal of Insect Physiology 80:22–​30. Tucker, A. E., M. S. Ackerman, B. D. Eads, S. Xu, and M. Lynch. 2013. Population-​genomic insights into the evolutionary origin and fate of obligately asexual Daphnia pulex. Proceedings of the National Academy of Sciences USA 110:15740–​15745. Ventura, T., Q. Fitzgibbon, S. Battaglene, A. Sagi, and A. Elizur. 2015. Identification and characterization of androgenic gland specific insulin-​like peptide-​encoding transcripts in two spiny lobster species: Sagmariasus verreauxi and Jasus edwardsii. General and Comparative Endocrinology 214:126–​133. Vermeij, G. J. 2016. Gigantism and its implications for the history of life. PLoS ONE 11:e0146092. Vogt, G. 2012. Ageing and longevity in the Decapoda (Crustacea): a review. Zoologischer Anzeiger 251:1–​25. Vogt, G. 2013. Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biological Reviews 88:81–​116. Vogt, G. 2016. Structural specialties, curiosities, and record-​breaking features of crustacean reproduction. Journal of Morphology 277:1399–​1422. Vogt, G. 2017. Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals. Environmental Epigenetics 3:dvx002. Vogt, G., C. Falckenhayn, A. Schrimpf, K. Schmid, K. Hanna, J. Panteleit, M. Helm, R. Schulz, and F. Lyko. 2015. The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biology Open 4:1583–​1594. Vogt, G., L. Tolley, and G. Scholtz. 2004. Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. Journal of Morphology 261:286–​311. Vollrath, F. 1998. Dwarf males. Trends in Ecology and Evolution 13:159–​163. Wägele, J.-​W. 1989. Evolution und phylogenetisches System der Isopoda. Stand der Forschung und neue Erkenntnisse. Zoologica 140:1–​262. Waloßek, D. 1995. The Upper Cambrian Rehbachiella, its larval development, morphology and significance for the phylogeny of Branchiopoda and Crustacea. Hydrobiologia 298:1–​13. Warburg, M. R. 2012. The oniscid isopod female reproductive system and gestation, with a partial review. Invertebrate Reproduction and Development 56:87–​110.

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7 AN EVOLUTIONARY ECOLOGICAL APPROACH TO SEX ALLOCATION AND SEX DETERMINATION IN CRUSTACEANS

Kota Sawada and Sachi Yamaguchi

Abstract This chapter reviews sex determination and sex allocation strategies among crustaceans with different sexual systems (gonochorism, sequential and simultaneous hermaphroditism, and androdioecy), from the perspective of evolutionary ecology. The discussion includes genetic, environmental, and cytoplasmic sex determination in free-​living and parasitic crustaceans, timing and frequency of sex change especially in partial protandry, the effects of mating group size on resource allocation by simultaneous hermaphrodites, and sex ratio and determination in androdioecious crustaceans. The fascinating diversity of crustacean reproduction stimulated theoretical biologists to construct models to explain them, and empirical biologists attempted to test hypotheses derived from those models. This review clearly shows that the interaction between theoretical and empirical studies has facilitated understanding of the evolutionary conditions of diverse sexual strategies among crustaceans. Since sexual strategies often interact with other aspects of adaptive strategies such as life history, integrating different aspects into both theoretical and empirical studies will provide further understandings into crustacean sexual systems. In addition, the authors point out the potential of phylogenetic comparative analyses using natural history data as a tool to understand the tempo and mode of evolution of sex allocation strategies.

INTRODUCTION Most crustaceans undergo sexual reproduction, and all sexual crustaceans are anisogamous, along with all other sexually reproducing animals; that is, sexual reproduction requires both male function (sperm) and female function (egg). Distribution of male and female functions among individuals within populations is termed “sexual systems” (Leonard 2010). In gonochoristic (dioecious) Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology populations, each individual has one sexual function (either male or female) throughout its lifetime. In contrast, hermaphroditic individuals have both sexual functions. Sequential hermaphrodites (sex changers) first mature as one sex and then change sex, while simultaneous hermaphrodites have both sexual functions at the same time. As discussed in Chapter 6 of this volume, crustaceans exhibit diverse sexual systems, including more complex ones. For example, caridean shrimps in the genus Lysmata first mature as males and then become simultaneous hermaphrodites (protandric simultaneous hermaphroditism; Bauer 2007). As organisms reproduce using a finite amount of available resources, the allocation of resources into male and female functions should be optimized by natural selection. The theory of sex allocation deals with such optimization to study the evolution of diverse allocation strategies (Charnov 1982, West 2009). This theoretical framework covers both the selective pressures favoring the evolution of different sexual systems and the quantitative aspects of resource allocation within each system. The latter describes a different, although theoretically similar and closely related, phenomenon in different systems; that is, offspring sex ratio (production of sons and daughters) in gonochorists, timing and direction of sex change in sequential hermaphrodites, and resource allocation to male and female function at the same time in simultaneous hermaphrodites (Charnov 1982). Sex allocation theory is essentially game-​theoretical, because the fitness returns of male or female allocation depend on the allocation strategy of other individuals in the population. For example, the fitness benefit of producing a male depends on the sex ratio of the whole population, which in turn depends on the sex allocation strategy used by other individuals. Thus we need to identify the “evolutionarily stable strategy,” that is, a strategy that performs better than (or at least as good as) any other strategies when the strategy is prevalent (Maynard Smith 1982). Note that here we focus on the functional sexuality, instead of morphological sexuality. For example, in the planktonic copepod Acrocalanus gracilis, larvae that are genetically and morphologically male differentiate into “intersex” individuals that presumably function as females under limited food availability (Gusmão and McKinnon 2009). Such “intersex” animals are also found in other copepod species, suggesting similar mechanisms of sex determination (Fleminger 1985). While this type of sex determination is described as “sex change” by some authors (Fleminger 1985, Gusmão and McKinnon 2009), it is not functional sex change (sequential hermaphroditism), as each individual reproduces through only one sex. Indeed, functional sex change is impossible since copepods do not molt after maturation (Gusmão and McKinnon 2009). This phenomenon should be classified as functional gonochorism with environmental sex determination (or maybe the combination of environmental and genetic determination, as genetic females presumably cannot become males) in which the proximate mechanism for sex determination is prematurational sex change (Sadovy and Shapiro 1987), a mechanism often found among fishes. In this chapter, we review how the theory of sex allocation is applied and tested for crustaceans with various sexual systems and sex allocation mechanisms (Table 7.1). Diverse ways of reproduction in crustaceans offer an excellent opportunity and challenging puzzles to apply and test theoretical predictions. We focus on the interaction between theoretical and empirical studies, by illustrating how the fascinating diversity of crustacean reproduction stimulated theoretical biologists to construct models to explain them, and also how empirical biologists attempted to test hypotheses derived from those models. While various proximate mechanisms controlling sex allocation (e.g., genes for sex determination, endocrinological triggers of sex change) are interesting and important, we primarily focus on the selective pressures driving the evolution of diverse sex allocation strategies. Since we focus on sexual reproduction, we do not discuss parthenogenesis, a reproductive strategy found among various crustaceans (see Chapter 9 in this volume), though the mixture of parthenogenesis and sexual reproduction provides a unique system to test sex allocation theories (Booksmythe et al. 2018).

Chromosome/​gene

Substrata Substrata + genetic?

Genetic

Environmental Genetic and environmental

Examples Many crustaceans Parasitic barnacle Peltogasterella gracilis Brackish water amphipod Gammarus duebeni Intertidal amphipod Echinogammarus marinus Parasitic barnacle Heterosaccus lunatus Parasitic copepod Cymbasoma danae Parasitic copepod Pachypygus gibber Woodlouse Porcellionides pruinosus Tanaidacean Leptochelia dubia Pandalid shrimp Pandalus spp. ditto Surf barnacle Catomerus polymerus Intertidal barnacle Semibalanus balanoides, Balanus glandula Clam shrimp Eulimnadia texana Tadpole shrimp Triops newberryi Sessile barnacle Conopea galeatus Epizoic barnacle Octolasmis warwickii Pedunculate barnacle Scalpellum scalpellum

Note that this table is not intended to review all known mechanisms, but rather to summarize what is discussed in this chapter. Some mechanisms are hypothetical (i.e., lack strong supportive evidence). See the main text for references.

Protandry Partial protandry

Androdioecy

Intensity of parasitism Food/​mate availability Wolbachia infection Presence of males Age Population size and structure Mating group size

Factor Chromosome/​gene Maternal genotype Photoperiod

Simultaneous hermaphroditism

Environmental

Sex Determination/​Allocation Genetic

Cytoplasmic Female to male sex change Age-​dependent sex change Early maturing female Resource allocation to sexual functions

Sexual System Gonochorism (Dioecy)

Table 7.1.  Summary of Sex Determination/​Allocation Mechanisms Reviewed in This Chapter.

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THEORETICAL AND EMPIRICAL STUDIES ON CRUSTACEAN SEX ALLOCATION Sex Determination and Sex Ratio in Gonochoristic Crustaceans Gonochoristic crustaceans exhibit various mechanisms of sex determination, including both environmental (environmental sex determination, ESD) and genetic (genetic sex determination, GSD) mechanisms (Legrand et al. 1987). The evolution of ESD requires that the effect of environmental conditions on fitness differ between the sexes (Charnov and Bull 1977). This hypothesis is termed “differential fitness model” (West 2009). Imagine that there are two types of habitat patches:  one is better and the other is worse. Those habitat qualities may affect males and females differently. For example, in a species with random mating with respect to male quality, females born in poor patches are highly disadvantaged due to low fecundity, but habitat quality is not as important for males. Under this situation, larvae should differentiate into males and females in worse and better conditions, respectively (Fig. 7.1). This theoretical prediction is clearly demonstrated by studies on crustaceans. An interesting example is a copepod species, Cymbasoma danae, that is parasitic on annelids only in the juvenile stage. Individuals that develop in multiple-​infection hosts (a worse condition in terms of nutrition and space) differentiate into males, while individuals in single-​infection hosts become both sexes (Malaquin 1901, as cited in Christie 1929 and Adams et  al. 1987), supporting the differential fitness model. As multiple infection hosts have lower per capita food and space available, individuals should develop into males instead of less-​fecund females (Charnov and Bull 1977). In the notodelphyid copepod Pachypygus gibber, parasites of sea squirts, larvae experience varying and unpredictable environmental conditions depending on the host individuals they encounter (Hipeau-​Jacquotte 1988, Michaud et al. 2004). Individuals that develop under poor food conditions tend to differentiate into males and under richer conditions into females (Becheikh et al. 1998). In addition, existence of a resident male or female induces the differentiation into a female or a male, respectively, even in food conditions that would induce the opposite sex in the absence of residents (Becheikh et al. 1998). This is because P. gibber mature and mate in the same host individual (except for “atypical males”; see following discussion) and thus the host-​mate is a potential

Reproductive success

180

Habitat quality Age or Size

Fig. 7.1. The differential fitness model for environmental sex determination and size-​advantage model for sex change. Here we assume that female reproductive success more strongly depends on habitat quality and age/​size than males, in differential fitness model and size-​advantage model, respectively. In those cases, natural selection should favor environmental sex determination where poor conditions induce males, or protandric sex change, respectively.   



An Evolutionary Ecological Approach

Female size

Clutch size

Relative pairing success

mating partner or rival, in contrast to C. danae, which finds mates outside the host. Interestingly, plastic sex determination is not the only solution to environmental heterogeneity observed in P. gibber. The worst food conditions, or the combination of intermediate food conditions and the presence of a male, induce the development of “atypical males” (Hipeau-​Jacquotte 1988, Becheikh et al. 1998), which have the ability to swim to better habitats, that is, hosts with females but hopefully without males (Michaud et al. 1999). In contrast to those parasitic species in which better conditions induce development of females, the opposite pattern of sex determination should evolve if environmental quality is more important for male fitness than female fitness, usually due to sexual selection. A  famous example of this type is the brackish-​water amphipod Gammarus duebeni whose sex is affected by photoperiod (Bulnheim et  al. 1967). Instead of spatial variation in patch quality (such as distribution of hosts that vary in quality for parasites), birth seasons form temporal patches that may affect male and female fitness differently (Naylor et  al. 1988). In some populations, this species is annual and generations do not overlap, but the reproductive season spans several months (Naylor et al. 1988). Individuals born early in the reproductive season have more time to grow before the onset of next reproductive season than individuals born later. As a result, the size at reproduction varies according to the birth season. While larger females can produce more eggs, the combination of size-​assortative mating (larger males mate with larger females, producing more eggs) and size-​dependent mating success (larger males are more likely to acquire females) leads to a steeper relationship between size and reproductive success in males than in females (Fig. 7.2; McCabe and Dunn 1997). Therefore, it is adaptive to have a plastic sex determination strategy where individuals born earlier and later differentiate into males and females, respectively. While photoperiod itself does not affect fitness directly, it works as an indicator of birth seasons. Other populations of the same species use another cue, namely temperature, in addition to photoperiod, possibly to assess seasons more accurately (Dunn et al. 2005).

Female size

Male size

Relative fitness

Size

Size

Fig. 7.2. Differential fitness model for the sex determination of an amphipod Gammarus duebeni. The combination of size-​dependent pairing success, size-​fecundity relationship, and size-​assortative mating leads to steeper size-​fitness relationship in males than in females. Drawn from McCabe and Dunn (1997).   

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Reproductive Biology It is well known that 1:1 offspring sex ratio is generally predicted in gonochorists with genetic sex determination (Fisher 1930). As each offspring has one mother and one father, the sum of the reproductive success as mothers in a population must be equal to fathers. If most mothers produce more male offspring than female offspring, the expected fitness return of producing a male (the population-​level sum of reproduction divided by the number of male offspring) must be higher than that of producing a female (the population-​level sum of reproduction divided by the number of female offspring). Fitness returns of a male offspring and a female offspring are the same when equal numbers of males and females are produced, and this condition is evolutionarily stable. To be exact, if males and females cost differently for mothers, the total investment, rather than number, of male and female offspring should be equal. This can be important in crustaceans with sexually dimorphic egg size, such as kentrogonid rhizocephalans (Yanagimachi 1961a, 1961b, Høeg 1995a, Yamaguchi et al. 2014; see later discussion in this chapter). Although the Fisherian theory of sex ratio successfully explains the prevalence of 1:1 sex ratio in many animals, it requires several assumptions not necessarily met in all organisms, and hence a biased sex ratio is predicted under various conditions (Bull and Charnov 1988). In the following we discuss a few examples of such conditions. Cytoplasmic factors such as symbiotic bacteria inherit only through female functions, i.e., they can infect from mothers to their offspring but not from fathers. As a result, there should be a strong selective pressure favoring offspring sex manipulation toward females (Bull and Charnov 1988). Wolbachia is a proteobacteria famous for feminizing insects (Kageyama et al. 2012), but it is also found in various crustaceans, especially in terrestrial isopods (Bouchon et al. 1998, Cordaux et al. 2012; see also Chapter 14 in this volume). As in insects, Wolbachia infecting crustaceans often manipulate the offspring sex ratio of hosts (Rigaud et  al. 1997b). It causes apparent environmental sex determination in a woodlouse Porcellionides pruinosus, that is, thermal inhibition of manipulation ability causes temperature-​dependence of sex ratio (Rigaud et al. 1997a). Though this phenomenon is similar to the environmental sex determination discussed earlier, there is an important difference: it is not an adaptive strategy of hosts. As a result, selection on the host genome favors resistance to feminization (Rigaud et al. 1997b). This selection can lead to the origin of novel sex chromosomes and may explain frequent transitions of sex determining systems among isopods (Becking et al. 2017). Interestingly, Wolbachia infection is also detected in the hermaphroditic goose barnacle Lepas anatifera (Cordaux et al. 2012), though its effect on hermaphroditic sex allocation has never been studied, as far as we know. Group structure may also affect optimal sex allocation. If closely related individuals (such as siblings) often compete over mates or resources, and the intensity of competition differs between the sexes, then mothers should bias sex ratio toward the sex with weaker kin competition (Hamilton 1967, Clark 1978). This hypothesis, known as “local mate/​resource competition,” is supported by the studies of animals such as insects, mammals, and birds, but presumably is not important for most marine crustaceans in which kin interaction is uncommon due to larval dispersal through planktonic stages. However, local mate competition may be important in terrestrial or freshwater crustaceans or species with direct development because limited dispersal ability may lead to sibling competition. In addition, sibling competition may occur in marine species when, for example, siblings disperse together (Kamel et al. 2010). If the extent of sibling conflict differs between the sexes, it may cause biased sex ratios. Offspring sex ratio is not predicted to follow Fisherian theory under environmental sex determination (Charnov and Bull 1989). Under the differential fitness model, offspring sex ratio should bias toward the sex that is induced under poorer conditions (Charnov and Bull 1989). This might explain the female-​biased sex ratio commonly observed among calanoid copepods (Burris and Dam 2015). Better food conditions induce the differentiation into males in planktonic copepods Calanus spp., probably because males require more energy to find mates (Irigoien et al. 2000).



An Evolutionary Ecological Approach

Sex Determination in Parasitic Barnacles Here we discuss a theoretical study of sex determination in parasitic (rhizocephalan) barnacles to illustrate how a theoretical approach is applied to a specific system. In contrast to thoracican barnacles in which most species are hermaphroditic, rhizocephalan barnacles, parasites of other crustaceans, are exclusively gonochoristic (Høeg 1995a, 1995b). While females directly attach and parasitize a host, males are very small (“dwarf males”) and live in the bodies of their mates (see Chapter 15 in Volume 5 of this series). The system of sexual differentiation and mating differs between the two orders of this group: Kentrogonida and Akentrogonida (Høeg 1995a, Yamaguchi et al. 2014; Fig. 7.3). In Kentrogonida, eggs and larvae are sexually dimorphic (males are larger than females, the opposite pattern of sexual dimorphism found in adults). It indicates that sex is genetically determined, or at least determined before infecting the host. Those larvae must find hosts that are suitable, that is, female larvae must find an uninfected host, and male larvae must find a host already infected by a female whose “receptacles” (specialized organs to accept males) are unoccupied (Fig. 7.4). In Akentrogonida, eggs and larvae are monomorphic, suggesting the possibility of environmental sex determination dependent on the status of the host they encountered (Høeg 1995a), although this has not been empirically confirmed. Because females do not have specialized receptacles, the number of males per female does not have a strict upper limit. Yamaguchi et al. (2014) theoretically analyzed how those two systems evolved. The advantage of ESD is obviously that larvae can utilize both uninfected hosts and hosts infected by females, while GSD larvae can utilize only one of those two types of hosts, depending on the predetermined sex. However, larval sexual dimorphism in GSD species implies that the optimal size and morphology differ between the sexes. GSD larvae can specialize to their sex and settle more efficiently than ESD larvae, as long as they find suitable hosts. As a result of this trade-​off between sexual specialization and plasticity, GSD should evolve when the sexual difference of optimal size is sufficiently large. Yamaguchi et al. (2014) argued that intense competition over female receptacles (see Fig. 7.4) favored large larval size in Kentrogonida, leading to GSD. Interestingly, the mixture of ESD and GSD is also evolutionarily stable under intermediate sexual difference of larval size, while such a mixture is not found among rhizocephalans.

Fig. 7.3. A kentrogonid rhizocephalan Sacculina carcini (left, arrow indicates an externa, a part of parasite body emerged from host body) and an akentrogonid rhizocephalan Diplothylacus sinensis (right, numerous small sacs on the surface of crab body are externae). Although both are parasites of brachyuran crabs, their reproductive systems differ greatly (see the main text).   

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R

R

Fig. 7.4. A  schematic drawing of the reproductive system in kentrogonid rhizocephalans. Male larvae invade in the receptacles (denoted by R) of females. Drawn from Yamaguchi et al. (2014).   

Sex determination and allocation in rhizocephalans have other interesting aspects. Unfertilized eggs show dimorphism in Kentrogonida, suggesting that sex is determined before fertilization (Yanagimachi 1961a, 1961b, 1990). In Peltogasterella gracilis, a parasite of hermit crabs, some females produce only large (i.e., male) eggs, but others with an extra chromosome called “F chromosome” produce only small (female) eggs, while there were some exceptional observations where one female produces both types of eggs (Yanagimachi 1961b). Yanagimachi (1961b, 1990)  hypothesized that sex is determined by the genotype of mothers rather than the offspring. However, studies on other rhizocephalan species demonstrated different patterns: each brood often contains both sexes in Sacculina carcini, a parasite of shore crabs (Høeg 1984), and each female produces both male-​only and female-​only broods in Lernaeodiscus porcellanae, a parasite of porcelain crabs (Ritchie and Høeg 1981). Females in Heterosaccus lunatus, a parasite of swimming crabs, produce broods with both sexes, and the sex ratio depends on the photoperiod (Walker 2005), probably an adaptation to the seasonal fluctuation of available hosts. While these studies suggest diversity of sex determination mechanisms and sex allocation strategies among rhizocephalans, evolutionary patterns and adaptive significance of such diversity have not been fully explored. Timing and Frequency of Sex Change Sex change, or sequential hermaphroditism, is observed among a wide variety of plants and animals (Policansky 1982, Vega-​Frutis et al. 2014), including crustaceans (see Chapter 8 in this volume). Both protandrous (male to female) and protogynous (female to male) sex changes have been reported among crustaceans (Brook et al. 1994, Chiba 2007). The evolution of sex change is widely explained by the “size-​advantage hypothesis” (Ghiselin 1969, Warner 1975, Charnov 1982, Munday et al. 2006), that is, when size-​dependency of reproductive success differs between the sexes, individuals should change from the sex with weaker dependence to the sex with stronger dependence. For example, males in the sand-​dwelling tanaidacean Leptochelia dubia fight against each other to compete over females, and large males are likely to win the fight (Highsmith 1983). As predicted



An Evolutionary Ecological Approach

by the size-​advantage hypothesis, this species is protogynous, and sex change is induced by the absence of rival males (Highsmith 1983). In contrast, protandry should evolve when sexual selection is weak or absent, and the size-​fecundity relationship causes stronger size-dependence of reproductive success in females than in males. Note that this theory is highly similar to the differential fitness model for environmental sex determination in gonochorists (see Fig. 7.1). Partial protandry (digyny, mixture of pure females and protandrous hermaphrodites) in pandalid shrimps has been studied extensively (e.g., Charnov 1979, 1982, 2004, Charnov et al. 1978, Charnov and Anderson 1989, Bergström 1997, Charnov and Skuladottir 2000, Chiba et al. 2003, 2013). In many species of pandalid shrimps such as Pandalus jordani, sex changers reproduce as males in the first breeding season after maturation and as females in the later seasons. However, some individuals, termed “primary females” or “early maturing females,” mature directly as females before the first breeding season without experiencing reproduction as males (Charnov 1982, Bergström 1997). While the sexual systems of this family are diverse (Bergström 2000, Chiba and Goshima 2003), many studies have been done about this partial protandry. Charnov (1979, 1982) theoretically examined how the ratio of two reproductive phenotypes evolves. If all individuals are sex changers and the average reproductive success as a female is, say, F, then the average reproductive success as a male must also be F, due to the Fisher condition (the total reproductive success via male and female function must be equal). Thus a primary female must achieve more reproductive success than 2*F to be adaptive. However, if this condition is met and thus primary females exist in a population, then sex changers enjoy higher reproductive success as males, leading to an equilibrium in which a sex changer and a primary female are equally successful. As a result, the ratio of primary females should be non-​zero if they achieve more than 2*F and positively correlated with the ratio of their success to F. Charnov (1979, 1982) supported this prediction using the estimated patterns of female reproductive success among populations of pandalid shrimp, based on growth rate, size-​fecundity relationship, and mortality. The age structure of pandalid shrimp fluctuates due to the inter-​annual variations in recruitment and post-​recruitment mortality. According to Charnov et  al. (1978), the ratio of primary females should correlate positively with the ratio of young (first breeding) to older adults. This prediction is also supported by the analyses of time-​series data on P. borealis, P. jordani, and P. latirostris (Charnov et al. 1978, Charnov and Anderson 1989), though temporal autocorrelation (Bence 1995) was not taken into consideration. Temporal change of sex ratio suggests environmental sex determination in terms of sex at the first reproduction, while Bergström (1997, 2000) argued against ESD based on the data from P. borealis and proposed an alternative explanation that the variation of sex ratio is rather determined by natural selection acting on the genetic polymorphism of sexuality. Later, Chiba et al. (2013) experimentally demonstrated that sex determination in P. latirostris depends on the size structure, as predicted by Charnov et al. (1978). Because sex determination occurs before the onset of the breeding season, individuals must “predict” the social condition during the breeding season to be the optimal sex (Bergström 1997, 2000). This is not so challenging because a population can evolve by natural selection to adopt a reaction norm based on the correlation between conditions at differentiation and at reproduction. This correlation is supposed to be disrupted by the intense female-​biased selective fishery in P. latirostris, leading to maladaptive sex ratios (Chiba et al. 2013). In addition, Chiba et al. (2013) suggested that only individuals that grew faster than others can be females earlier, implying the importance of individual-​level studies of sex change, in addition to population-​level studies. Partial protandry is also exhibited by the mole crab Emerita asiatica (Subramoniam 1981, Subramoniam and Gunamalai 2003). However, the maturation size of primary females is almost the same as the size at sex change of protandric individuals (Subramoniam 1981), unlike Pandalus shrimp, in which primary females start to reproduce at a smaller size than the size at sex change of protandric individuals. The advantage of being non-​reproductive, instead of being male, for small-​ sized primary females in E. asiatica is unclear. It is possible that reproduction as males incurs costs in terms of growth or survival and thus immature primary females enjoy faster growth or better

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Reproductive Biology survival until maturation as females (see Charnov 1987, Iwasa 1991, Yamaguchi et al. 2013c, for similar arguments on fishes). Sex Allocation in Simultaneous Hermaphrodites Simultaneous hermaphroditism evolved in several lineages of crustaceans (Jarne and Auld 2006). A classical “low density” hypothesis argues that hermaphrodites are favored when finding mates is difficult, because they can reproduce via selfing (self-fertilization) alone or outcrossing with all mature individuals they encounter, in contrast to gonochorists who need to find an opposite-​sex individual to reproduce (Tomlinson 1966, Ghiselin 1969). This hypothesis fits for the evolution of hermaphroditism among clam shrimps, in which reproductive assurance by selfing is important in ephemeral habitats (Weeks et al. 2009). Charnov (1982) theoretically demonstrated that simultaneous hermaphroditism is favored by diminishing returns for allocation to one sex. For example, if the number of potential mates is strongly limited, fitness returns for male allocation diminishes fast because total fecundity of all potential mates determines the upper limit, and a smaller amount of sperm is required to outcompete rivals in sperm competition. While both of the two hypotheses predict hermaphroditism under low mate availability, they assume different aspects of “mate availability.” In contrast to the Tomlinson-​Ghiselin hypothesis, Charnov predicts hermaphroditism when individuals easily find a limited, but non-​zero, number of mates. A phylogenetic study suggested that simultaneous hermaphroditism in lysmatid shrimps evolved in a free-​living and grouping ancestor, rather than a symbiotic and monogamous one as predicted by the Tomlinson-​Ghiselin hypothesis (Baeza 2013). Baeza (2013) speculated that diminishing returns for male allocation due to weak sperm competition and for female allocation due to brood space limitation (Heath 1979, Charnov 1982) favored hermaphroditism in this group. A clear example to contrast the predictions by the two hypotheses is the prevalence of simultaneous hermaphroditism among shallow-​water thoracican barnacles (Lin et al. 2015), most of which are rarely solitary but the number of potential mates is limited due to sessility and the length of copulatory organs (Kelly et al. 2012). This pattern can be easily explained by Charnov’s hypoth­ esis, but not by the Tomlinson-​Ghiselin hypothesis. Incidentally, both theoretical (Charnov 1987, Yamaguchi et al. 2008, 2012, 2013d) and empirical (Yusa et al. 2012, Lin et al. 2015) studies indicate the prevalence of gonochorism among barnacles under low density, apparently contradictory to gen­eral predictions (Leonard 2010). This is because adults cannot move to find mates and thus mate search solely depends on the settlement of dwarf males on the female body surface. In the next section, we discuss the evolution and differentiation of such dwarf males in androdioecious barnacles, from which gonochoristic barnacles are estimated to be derived (Yusa et al. 2012, Lin et al. 2015). Not only the evolution of hermaphroditism itself, but also the quantitative sex allocation by hermaphrodites is predicted to depend on mating opportunities. When simultaneous hermaphrodites use their male function for self-​fertilization only (e.g., Brantner et al. 2013), only a limited allocation to male function is expected, since they only need to produce just enough sperm to fertilize their own eggs. In contrast, evolutionarily stable sex allocation in outcrossing hermaphrodites depends on the intensity of mating competition experienced as males. One of the important factors is the mating group size (MGS), i.e., the number of hermaphrodites that can mate with each other (Charnov 1982, Yamaguchi et al. 2008, 2012). For example, when only two outcrossing hermaphrodites live in an isolated patch, the optimal allocation to male function (sperm production) should be small, because only a small amount of sperm is enough to fertilize the partner’s eggs. In contrast, as the mating group size becomes larger, hermaphrodites should allocate more to male function, because they need to produce more sperm, not only to provide enough sperm for fertilization, but also to win the competition with sperm from rivals (Charnov 1982). When MGS is sufficiently large, optimal allocation to male function asymptotically approaches to 0.5 (Fig. 7.5), corresponding to random mating in



An Evolutionary Ecological Approach 0.5 Male allocation

0.4 0.3 0.2 0.1 0.0 1

2

4 6 8 Mating group size

∞

Fig. 7.5. Relationship between mating group size and predicted male allocation in simultaneous hermaphrodites.   

the whole population. This “local sperm competition” hypothesis (Schärer 2009) is mathematically equivalent to the “local mate competition” hypothesis among gonochoristic animals (see earlier discussion) in which the number of mothers that spawn in a patch corresponds to MGS. The local sperm competition hypothesis is supported by many, though not all, studies using various hermaphroditic animals (Schärer 2009), including crustaceans. Because thoracican barnacles are sessile and generally copulate using penes (but see Barazandeh et al. 2013, 2014, Barazandeh and Palmer 2015), their number of potential mates is simply determined by the number of neighboring individuals. This makes them ideal to test the local sperm competition hypothesis. Raimondi and Martin (1991) tested the correlation between MGS and sex allocation using the surf barnacle Catomerus polymerus and demonstrated that hermaphrodites collected at high density allocate relatively less resources to female function than ones collected in low density. This result is consistent with the local sperm competition hypothesis. However, Kelly and Sanford (2010) found no relationship between density and sex allocation in the volcano barnacle Tetraclita rubescens. To conduct such tests, it is important to know how MGS, which is not necessarily equal to social group size, varies. In case of T. rubescens, a genetic survey indicated few cases of multiple paternity and male allocation was not correlated with siring success, suggesting that scramble sperm competition is weak in this species (Kelly et al. 2012). If one clutch of eggs is almost always fertilized by only one sperm donor via sperm displacement or cryptic female choice, then the MGS as a measure of sperm competition should be consistently small, even when the social group size is large. The same explanation may also be applied to the lack of correlation between group size and sex allocation in the peppermint shrimp Lysmata wurdemanni (Baeza 2007), in which individuals first mature as males and then become simultaneous hermaphrodites, because pre-​spawning hermaphrodites receive sperm from only one other individual (male or hermaphrodite) per spawning cycle. Another factor that may complicate the effect of MGS is the way animals assess MGS. Hoch and Levinton (2012) experimentally manipulated the pattern of crowding in two species of intertidal barnacles, Semibalanus balanoides and Balanus glandula. As a result, allocation to male function increased in densely aggregated conditions (presence of physical contact among individuals), but not in large group sizes (the number of neighboring individuals), suggesting that physical contact is a cue to assess group size in those species. Sex Determination in Androdioecious Crustaceans Androdioecy, the coexistence of males and hermaphrodites, is observed among several crustacean taxa (Weeks et al. 2006, Weeks 2012). A variety of sex determination systems can be found among androdioecious crustaceans. In the following we focus on two taxa: thoracican barnacles and branchiopods.

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Reproductive Biology Males in androdioecious thoracican barnacles are much smaller (“dwarf ”) than conspecific hermaphrodites, and attach on the body surface of their sexual partner throughout their lives (Fig. 7.6). The mechanism of sex determination between hermaphrodites and dwarf males is not well understood (Crisp 1983, Yusa et al. 2013). Callan (1941) suggested environmental sex determination depending on substrata (conspecific body or not) in the pedunculate barnacle Scalpellum scalpellum, based on karyotype analysis, rudimentary oogonia in males, and the occurrence of a wrongly differentiated individual. Wijayanti and Yusa (2016) showed that individuals increase the allocation to male function when artificially attached on conspecifics like dwarf males in a crab-​ epizoic barnacle Octolasmis warwickii, supporting environmental determination. However, Gomez (1975) argued for genetic sex determination in another androdioecious barnacle, Conopea galeatus, based on the fact that both males and hermaphrodites developed from larvae when metamorphosis was induced by a juvenile hormone mimic without any substrata. In androdioecious taxa, sex determination can also be affected by both environmental and genetic factors (Svane 1986, Høeg et al. 2016). In S. scalpellum, virtually all individuals on receptacles (specialized areas to carry males) of conspecific hermaphrodites are dwarf males, and others are hermaphrodites (Callan 1941, Svane 1986, Buhl-​Mortensen and Høeg 2006, Spremberg et al. 2012, Høeg et al. 2016, Dreyer et al. 2018b). Svane (1986) reported that more larvae settled on receptacles and differentiated into males when more adult hermaphrodites were present. In addition, some of the larvae that settled on conspecific receptacles (i.e., larvae that differentiate into males if not manipulated) differentiated into hermaphrodites when they were artificially removed from conspecific bodies just after settlement (Høeg et  al. 2016). Although these results indicate environmental sex determination, the proportion of larvae settled on receptacles and differentiated into males never exceeded 50 percent (Svane 1986). Thus, it was suggested that half of the larvae are genetically determined hermaphrodites and never settle on conspecific receptacles, and the other half are plastic in terms of attachment site and sex differentiation (Svane 1986, Spremberg et  al. 2012, Høeg et  al. 2016). Absence of predetermined males is adaptive because some larvae may

Fig. 7.6. An androdioecious pedunculate barnacle Octolasmis unguisiformis. Five dwarf males (small individuals) attached on a much larger hermaphrodite. Scale bar = 1 mm. From Sawada et al. (2015).   



An Evolutionary Ecological Approach

not find hermaphrodites to attach themselves on and thus have no opportunity to be dwarf males (Yamaguchi et al. 2013b, Høeg et al. 2016). In addition, Høeg et al. (2016) argued that presence of predetermined hermaphrodites prevents the overproduction of males under the presence of aggregated hermaphrodites, because dwarf males are less adaptive in large mating groups, as discussed in the following. Sex allocation theories predict that the presence and proportion of males should depend on MGS (mating group size; see earlier discussion) among androdioecious barnacles (Charnov 1987, Yamaguchi et  al. 2008, 2013d, reviewed by Yamaguchi et  al. 2012). As discussed earlier, hermaphrodites should allocate less to male function when MGS is small, due to local sperm competition. This leads to weak sperm competition and allows dwarf males to achieve sufficient fertilization success, even though they produce much less sperm than hermaphrodites and also lack reproductive success through female function. This prediction is supported by the evolutionary patterns of androdioecy among barnacles, i.e., dwarf males are likely to evolve in lineages with small MGS (Yusa et al. 2012) or in lineages dwelling in the deep sea where group size is generally low (Lin et al. 2015). However, there are few studies that have analyzed the variation of sex ratio among androdioecious barnacles, despite their importance to understand evolutionary transitions and patterns (Yamaguchi et al. 2012). Spremberg et al. (2012) reported that the presence of males on a hermaphrodite does not correlate with solitariness in Scalpellum scalpellum. Ewers-​Saucedo et al. (2015) found that mating group size differs among different host species in the turtle barnacle Chelonibia testudinaria, but the frequency of males does not. Both of these studies do not support the prediction, although they did not directly test the prediction. Note that originally theoretical studies were designed to evaluate between-​population (species) variation of evolutionarily stable sex allocation rather than within-​population variation, which should be affected by various proximate factors, including sex determination and larval settlement mechanisms. Both empirical and theoretical studies are required to elucidate this issue. Androdioecy also evolved in branchiopods such as clam shrimps and tadpole shrimps. Unlike androdioecious barnacles in which hermaphrodites receive sperm from both males and other hermaphrodites (Ewers-​Saucedo et al. 2016, Dreyer et al. 2018a), hermaphrodites in those taxa do not outcross with other hermaphrodites and reproduce via selfing in the absence of males (Weeks et al. 2006). Outcrossing only occurs between males and hermaphrodites. Such a system is common among androdioecious animals other than barnacles, such as nematodes and killifishes (Weeks et al. 2006). The clam shrimp Eulimnadia texana is well studied in terms of sex determination and sexual systems, and has a unique system of genetic sex determination (Sassaman and Weeks 1993, Weeks et al. 2010). There are three types of individuals: monogenic hermaphrodites that produce hermaphroditic offspring only; amphigenic hermaphrodites that produce both hermaphroditic and male offspring; and males. These three types can be explained by chromosomal sex determination in which the genotypes of monogenics, amphigenics, and males are ZZ, ZW, and WW, respectively. Interestingly, an androdioecious tadpole shrimp, Triops newberryi, has a similar system of sex determination (Sassaman 1991, Mathers et al. 2015), despite the independent origins of androdioecy in clam shrimps and tadpole shrimps (Mathers et al. 2013). Otto et al. (1993) constructed a population genetic model to predict an evolutionarily stable sexual system and sex allocation incorporating factors such as male reproductive success, inbreeding depression, relative viability of males, and the fertilization rate by selfing. In addition, Pannell (2008) incorporated the lower viability of amphigenic hermaphrodites compared to monogenic individuals. However, both models predicted a higher ratio of males than those observed in an empirical study based on a long-​term field survey (Weeks et al. 2014). Weeks et al. (2014) speculated that this discrepancy may be caused by temporal variability of parameters included in those models, calling for the need of non-​equilibrium modeling.

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FUTURE DIRECTIONS In this chapter we have illustrated how sex allocation theories can be applied to various crustaceans (see Table 7.1). Here we discuss two areas that warrant attention:  interactions among existing theoretical frameworks, and the potential utility of a comparative approach using phylogenetic information. Sex allocation is an aspect of adaptive strategy to cope with various environmental conditions and thus is expected to interact with other fitness-​relevant traits, including dispersal strategies and life history traits. For example, as discussed earlier, “atypical males” in a parasitic copepod Pachypygus gibber adopt a combination of dispersal tactic and sex differentiation to make the best of bad situations under the heterogeneity of host quality and mating status (Michaud et al. 1999). One aspect that often interacts with sex allocation is life history, the resource allocation between reproductive and non-​reproductive functions such as growth and mortality, while sex allocation and life history theories have been developed separately (Zhang and Wang 1994). We have already mentioned differences in viability among different sexual types in an androdioecious clam shrimp (Pannell 2008) and the effects of growth on the sex change of pandalid shrimp (Chiba et al. 2013). Dwarf males in barnacles are another striking example of the interaction between sex allocation and life history, because males and females/​hermaphrodites show vastly different life history trajectories (Yamaguchi et al. 2012, Yusa et al. 2013, Sawada et al. 2015). Difficulties for growing due to poor food availability or spatiotemporal limitation is theoretically predicted to favor dwarf males in androdioecious barnacles (Yamaguchi et al. 2008, 2013a, 2013b, 2013d) because they are small and require less food, time, or space to mature. This may be important for species living in short-​lived habitats, such as a crab carapace (Sawada et  al. 2015). When individuals with different sex allocation strategies also differ in life history, as in the case of sexual size dimorphism, evolutionary conditions of sexual systems may not be understood without modeling and measuring both aspects simultaneously. We emphasize the importance of comparative studies using natural history data from a wide range of taxa, while detailed studies of specific model species are undoubtedly important. The statistical method for comparative analysis is rapidly growing and expanding (Garamszegi 2014). While there are several comparative studies on qualitative aspects of sexual systems and sex determination (e.g., Yusa et al. 2012, Lin et al. 2015, Mathers et al. 2015), ones on quantitative aspects such as sex ratio are unexplored (but see Allsop and West 2004). Fortunately, necessary data such as sex ratio are often available from natural history collections at museums specimens or the literature (e.g., Spremberg et al. 2012). Phylogenetic comparative approaches can also be used to answer how and why evolutionary rates and patterns of sex allocation strategies differ among different crustacean lineages. It is widely known that sexual systems are evolutionarily conservative in many metazoan lineages (Leonard 2013). Among crustaceans, while evolutionary transitions of sexual systems are quite common in some lineages such as thoracican barnacles and tadpole shrimps (e.g., Yusa et al. 2012, Mathers et al. 2013, Lin et al. 2015), such a transition does not exist or is rare in other groups, such as brachyuran crabs that are invariably gonochoristic (McLay and Becker 2015). There are some examples of crustacean sex allocation strategies that are attributed to the lack of evolution even when the selective regime changed. Guler et al. (2012) argued that environmental (photoperiod) sex determination in an intertidal amphipod Echinogammarus marinus may no longer be adaptive but remains as an ancestral trait, because it does not meet the supposed evolutionary conditions (restricted breeding season and lack of generation overlap) for a similar form of environmental sex determination found in other gammaridean amphipods (e.g., Gammarus spp.). Bauer (2006) proposed the “historical contingency” hypothesis that simultaneous hermaphroditism in caridean shrimps of the genus Lysmata evolved in the ancestral pair-​forming (limited



An Evolutionary Ecological Approach

mating opportunity) species and remains even when the selective pressure favoring hermaphroditism weakened in the group-​forming species. Does this implicate that some crustacean reproductive strategies cannot be explained adaptively? We should be cautious about applying non-​adaptive hypotheses as a “last resort” just because adaptive explanations are unclear (Blomberg and Garland 2002). Phylogenetic comparative analysis can help to critically test both adaptive and non-​adaptive hypotheses, though it is difficult to directly test causal hypotheses (Blomberg and Garland 2002). For example, Baeza (2013) refuted the historical contingency hypothesis by phylogenetically reconstructing the social system at the origin of hermaphroditism in Lysmata (and its relative) shrimps. To test whether sex determination in Echinogammarus is non-​adaptive, one could reconstruct the evolutionary history of sex determination mechanisms in this group. By adopting quantitative and statistical comparative approaches, we can avoid both “just-​so” adaptive hypotheses and “last resort” non-​adaptive hypotheses.

CONCLUSIONS As demonstrated throughout this chapter, combining theoretical and empirical studies will further our understanding of the evolutionary ecology of crustacean sex allocation and sex determination. Theoretical biologists are inspired by fascinating natural history observed by field and lab biologists, and empiricists know, from theoretical models, what kinds of data are key to answer biologically important questions. We believe that facilitating this interaction will help us to tackle unanswered questions concerning the extreme diversity of crustacean reproductive strategies.

ACKNOWLEDGMENTS We appreciate the editors for inviting us to write this chapter and also for helpful comments on the manuscript, and Drs. U. Spremberg and J. T. Høeg for supporting photography of specimens. This work was supported by a grant for Basic Scientific Research (B) (15H04416) to S.Y. from the Japan Society for the Promotion of Science.

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8 HERMAPHRODITISM AND GONOCHORISM

Chiara Benvenuto and Stephen C. Weeks

Abstract This chapter compares two sexual systems:  hermaphroditism (each individual can produce gametes of either sex) and gonochorism (each individual produces gametes of only one of the two distinct sexes) in crustaceans. These two main sexual systems contain a variety of alternative modes of reproduction, which are of great interest from applied and theoretical perspectives. The chapter focuses on the description, prevalence, analysis, and interpretation of these sexual systems, centering on their evolutionary transitions. The ecological correlates of each reproductive system are also explored. In particular, the prevalence of “unusual” (non-​gonochoristic) reproductive strategies has been identified under low population densities and in unpredictable/​ unstable environments, often linked to specific habitats or lifestyles (such as parasitism) and in colonizing species. Finally, population-​level consequences of some sexual systems are considered, especially in terms of sex ratios. The chapter aims to provide a broad and extensive overview of the evolution, adaptation, ecological constraints, and implications of the various reproductive modes in this extraordinarily successful group of organisms.

INTRODUCTION Historical Overview of the Study of Crustacean Reproduction Crustaceans are a very large and extraordinarily diverse group of mainly aquatic organisms, which play important roles in many ecosystems and are economically important. Thus, it is not surprising that numerous studies focus on their reproductive biology. However, these reviews mainly target specific groups such as decapods (Sagi et al. 1997, Chiba 2007, Mente 2008, Asakura 2009), caridean

Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology shrimp (Correa and Thiel 2003) and crayfish (Yazicioglu et al. 2016), or are more general reviews of mating strategies and behaviors (Subramoniam 2013, Dennenmoser and Thiel 2015), hormonal regulations (Ventura et  al. 2011a), sex determination (Rigaud et  al. 1997)  and/​or sexual systems (Bauer and Martin 1991, Subramoniam 2016), focusing more on proximate mechanisms than ultimate causes. Comprehensive reviews of crustacean reproduction, especially from an evolutionary perspective, are largely missing from the literature. This gap in our knowledge is even more obvious when we consider the paucity of modern reviews of the evolution of hermaphroditism in the Crustacea (Charniaux-​Cotton 1975, Juchault 1999), with the exception of a few taxa (e.g., branchiopods: Weeks et al. 2014, barnacles: Yamaguchi et al. 2012, Yusa et al. 2012, 2013) or specific systems (e.g., androdioecy: Weeks et al. 2006a, Weeks 2012). This is not unique to the Crustacea: the evolution of hermaphroditism has not been widely discussed in animals more generally (but see Ghiselin 1969, Jarne and Charlesworth 1993, Jarne 1995, Jarne and Auld 2006, Eppley and Jesson 2008, Schärer and Janicke 2009, Vega-​Frutis et al. 2014, Meconcelli et  al. 2015), even though more than 65,000 animal species are hermaphroditic ( Jarne and Auld 2006). Here, we review reproductive systems in crustaceans (see also Chapter 6 in this volume), with an emphasis on the various forms of hermaphroditism, including sequential and simultaneous hermaphroditism (male and female reproductive organs are present and function sequentially or at the same time), mixed sexual systems (such as androdioecy), and plastic strategies (population geographic variation in sexual systems in the same species; presence of non-​sex-​changing individuals in sequentially hermaphroditic populations, etc.). In particular, we list the known species that exhibit these hermaphroditic forms and consider the evolution of the numerous reproductive systems in crustaceans, documenting their taxonomic ranges and discussing their likely evolutionary transitions. We conclude by briefly discussing the environmental correlates of the various reproductive forms found among crustaceans.

OVERVIEW OF REPRODUCTION IN THE CRUSTACEA Types of Reproductive Systems in the Crustacea Few animal groups have as many reproductive systems as crustaceans (see Table 8.1 for definitions): asexual (parthenogenetic) lineages are common in freshwater ostracods (Butlin et al. 1998, SchÖn et al. 2000), in the brine shrimp Artemia (A in Fig. 8.1; Asem et al. 2016), in some terrestrial isopods (Bell 1982, no males have been found in Armadillidium virgo [Caruso and Bouchon 2011, D in Fig. 8.1]), and have been described in crayfish (Scholtz et al. 2003); cyclic parthenogenesis is often found in cladocerans (Hebert 1987, Decaestecker et al. 2009); separate sexes (functional males and functional females) are present in gonochoristic (dioecious) species as well as in sequential hermaphrodites (sex changers), where the same individual acts as one sex and successively as the alternate sex at different times of its life cycle; combined sexes (hermaphroditism) are found in systems where all individuals mature both male and female gonads at the same time (synchronous or simultaneous hermaphroditism), or in mixed sexual systems, where only some individuals are hermaphrodites but others are pure males (androdioecy; see Table 8.2). Coexistence of hermaphrodites and males can also occur following the development of female tissue in males (protandric simultaneous hermaphroditism), a mixed sexual system mainly found in the Infraorder Caridea (Bauer and Holt 1998, Bauer 2000). This amazing variety of modes of reproduction can thus be seen as a continuum (Ah-​King and Nylin 2010, Kelly and Sanford 2010, Yusa et al. 2013).



Hermaphroditism and Gonochorism Table 8.1.  Definition of Sexual Systems Based on the Presence of Sexual Types Sexual System Androdioecy Gynodioecy Gonochorism (Dioecy) Asexual (Parthenogenetic) Cyclic Parthenogenesis

Simultaneous hermaphroditism Sequential hermaphroditism i. Protandry

ii. Protogyny

Protandric simultaneous hermaphrodites

Population Composed of Males + hermaphrodites* Females + hermaphrodites* Males + females Females only Asexual females most of the year followed by a single bout of sexual (male + female) reproduction at the end of the growing season Hermaphrodites* Male-​first sex changers. Individuals reproduce as males initially and then switch to females, the second sex, also called secondary females in digynic populations (populations with two types of females) where some individuals are born directly as females (primary females). In some cases, some males might not change to females (and remain males through all their lives) Female-​first sex changers. Individuals reproduce as females initially and then switch to males, the second sex, also called secondary males in diandric populations (populations with two types of males) where some individuals are born directly as males (primary males). In some cases, some females might not change to males (and remain females through all their lives) Males → Simultaneous hermaphrodites

* Simultaneous production of both male and female gametes

Sex-​determining mechanisms also vary greatly in crustaceans (see Chapter 14 in this volume). Some isopod and amphipod females can produce offspring of exclusively one sex, a process known as monogeny (Bulnheim 1978, Juchault and Legrand 1986). Additionally, crustaceans can use both internal and external fertilization. When internal fertilization occurs, females can often be fertilized only during a brief period after molting, before their exoskeleton hardens again (Hartnoll 1969, Raviv et al. 2008). In this situation, males guard females until they are receptive (mate guarding; Jormalainen 1998). In some species, characterized by a terminal molt (after which the individual no longer grows), females can be fertilized even with a hard exoskeleton (Raviv et al. 2008). Given this variety and complexity of reproductive modes and systems, crustaceans are great model organisms to test theoretical predictions and perform applied studies on the ecology, reproductive behavior, sexual selection, and evolution of social and sexual systems of animals (Duffy and Thiel 2007, Dennenmoser and Thiel 2015, Chak et al. 2015).

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Reproductive Biology Below, we describe the diversity of hermaphroditic reproductive systems in crustaceans. The vast bulk of crustaceans are gonochoristic (dioecious), and we do not specifically delineate those species in this chapter. We also refer readers to Chapter 9 of this volume for a complete discussion of asexual re­production. Here instead, we first describe the various reproductive systems, and then present a brief discussion of their evolutionary transitions. Sexual Reproduction Gonochorism Gonochorism or dieocy (separate sexes) is the most common sexual system in crustaceans ( Juchault 1999, Correa and Thiel 2003, Subramoniam 2013). When genetically determined, separate sexes are fixed throughout the life cycle of individuals. Sexual development is regulated in malacostracan crustaceans by a hormone produced by the androgenic gland: the default sex is female (Ford 2008), and primary and secondary male characters are induced by the insulin-​like androgenic gland hormone (Sagi et al. 1997, Chang and Sagi 2008, Ventura et al. 2011a, 2011b). In the presence of the hormone, testicular differentiation is initiated and the animal matures as a male; in its absence (i.e., in females), ovaries develop instead (Chang and Sagi 2008). In many crustacean groups, sexual dimorphism allows the easy recognition of males from females, each sex characterized by a sex-​specific phenotype. Males are usually larger than females and have larger chelipeds, or other weapons, in species where male-​male competition is the rule, either in the form of direct aggressive interactions, mate guarding or territorial/​burrow defense (see Chapter 10 in this volume). Larger females than males are found in penaeoidean shrimp, in many caridean shimp (Bauer et al. 2014), and in other groups where high abundances allow for frequent contact between the sexes. In instances when one sex grows faster than the other, there has been interest in creating single-​sex populations for aquaculture purposes (Ventura and Sagi 2012, see the successful manipulations of the giant freshwater prawn Macrobrachium rosenbergii; Ventura et al. 2012). Extreme sexual dimorphism is found in some dioecious barnacles (in particular in the order Pedunculata), where males are much smaller than females. Darwin (1851) called them “dwarf ” males: they are attached directly to the “fertilization site” (on a female) and do not require the long (“groping”) penises that their hermaphroditic counterparts require for successful fertilization; multiple dwarf males can be attached to the same female (Yusa et al. 2012, Lin et al. 2015). Even though there are two sexes, more than one male morphotype can be present, as found, for example, in the marine isopod Paracerceis sculpta where α-​, β-​and γ-​males coexist in populations (Shuster and Wade 1991), the rock shrimp Rhynchocinetes typus where “typus,” “intermedius,” and “robustus” males are found (Correa et al. 2000), and M. rosenbergii where small, medium orange-​ clawed and large blue-​clawed males (Ventura et  al. 2011b) use different strategies to mate with females. When different male morphotypes are present, one type often phenotypically resembles a female (β-​males, typus, and small, respectively, from the preceding examples), to allow them to enter unnoticed in the harem of the dominant males. When secondary sexual characters are not evident, the localization of gonopores (or their absence in parthenogenetic crayfish; Vogt et al. 2004) can be used to differentiate males from females (and hermaphrodites, when both set of sexual gonopores are present), as well as the presence of an appendix masculina in males of many decapods, which regresses during sex change in protandrous species (Carpenter 1978, Bauer 1986a, Schatte and Saborowski 2006, Zupo et  al. 2008). In some species (such as the brown shrimp Crangon crangon; G in Fig. 8.1) evidence of sex change can be inferred by comparing consecutive molts (Schatte and Saborowski 2006).



Hermaphroditism and Gonochorism (C) (A) (D) (B) (E)

(G)

(F)

(H)

(I)

(J)

Fig. 8.1. Selected examples of non-​gonochoristic species, to show the variety of reproductive modes in crustaceans. (A)  The anostracan Artemia parthenogenetica, characterized by mixed sexual and asexual (parthenogenetic) populations. (B)  The notostracan Triops cancriformis exemplifies “geographical hermaphroditism,” where populations can be gonochoristic, androdioecious, and hermaphroditic. (C)  The free-​living isopod Cyathura carinata, one of the few examples of protogynous (female-​first sex changer) crustaceans. (D) The parthenogenetic cave-​dwelling isopod Armadillidium virgo. (E) The protandric simultaneous hermaphrodite Exhippolysmata oplophoroides. (F) The protandrous (male-​first sex changer) Emerita analoga. (G) The facultative protandrous Crangon crangon. (H) The protandrous Pandalus danae. (I) The simultaneous hermaphrodite Allaxius cf picteti, belonging to the family Axiidea, the only known example of simultaneously hermaphroditic decapods. ( J) The simultaneous hermaphrodite Amphibalanus improvisus. See color version of this figure in the centerfold. Photos: (A and B) Jean-​François Cart; (C) Hans Hillewaert; (D) Domenico Caruso; (E) J. Antonio Baeza; (F and I) Arthur Anker; (G) Asma Althomali; (H) Ann Dornfeld; ( J) Ian Frank Smith.   

Sequential Hermaphroditism There are several forms of sequential hermaphroditism, which is defined as changing from one sex into another during some portion of the life cycle. Starting life as male and then changing to female is termed protandry, whereas starting life as female and changing to male is termed protogyny (Table 8.1; Warner 1975, Policansky 1982, Munday et al. 2006). It is hypothesized that sequential hermaphroditism is a response to size-​specific difference in maximized fitness of each sex (size advantage model; Ghiselin 1969). In scenarios where the fitness of small males is not too different from the fitness of large males but small females are less fecund than large females, a male-​first strategy (protandry) can allow successful production of sperm early in life with a later switch to females when the individuals are larger and can better afford higher egg production. Protandry is very common among malacostracans (Table 8.3), especially in decapods, amphipods, and isopods. Outside these taxa, it has been described only in two parasitic species of barnacles: Waginella (formerly Synagoga) sandersi and Gorgonolaureus muzikae (Brook et al. 1994, Policansky 1982). Among decapods, the majority of described occurrences of protandrous sex change is found in the family Pandalidae (31 species; the genus Pandalus seems to be completely protandrous; Chiba 2007, H in Fig. 8.1), but also in the families Atyidae (six species), Crangonoidea

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Reproductive Biology (five species), Campylonotidae (four species), Alpheidae, Hippidae (see Emerita analoga, F in Fig. 8.1), Hippolytidae and Merguiidae (two species each) with individual occurrences in four more families (Table 8.3). In some cases (e.g., C. crangon; G in Fig. 8.1), protandry is facultative (Schatte and Saborowski 2006). Among amphipods, seven protandrous species have been recorded in the family Lysianassidae and one species, Stegocephalus inflatus, among stegocephalids ( Johnson et al. 2001). Among parasitic isopods, 17 protandrous species have been described in the Cymothoidae (this family, comprising 386 species, is possibly all completely protandric; Brusca 1981) and two in the Bopyridae. Their parasitic lifestyle makes it particularly difficult to study their reproductive cycle (Smit et al. 2014). Among the ectoparasitic cymothoids, different sites are parasitized in fish hosts: gill chambers, buccal cavity and body surface (Fig. 8.2). While parasitic isopods are mainly protandrous, both protandry and protogyny are found among free-​living aquatic isopods. Among terrestrial isopods (superfamily Oniscoidea), one species is recorded as protandrous and one as protandric simultaneous hermaphroditic ( Johnson et al. 2001). In systems where males compete for females, large males have higher reproductive success, and small individuals maximize their fitness as females (protogyny). Interestingly, protogyny is very common in fish but not in crustaceans: out of the 114 known sequentially hermaphroditic crustacean species, 93 are protandrous and only 21 are protogynous (Table 8.3). Protogynous species are distributed among free-​living (non-​parasitic) isopod species (Tsai et al. 1999), with four species in the family Anthuridae (C in Fig. 8.1) and four in the family Sphaeromatidae. Among the Tanaidacea there are seven protogynous species in the family Leptochelidae, two in the family Nototanaidae, and one each in the families Paratanaidae, Kalliapseudidae, Tanaididae, and Apseudidae (e.g., Highsmith 1983, Brook et  al. 1994). Protogyny is probably more common among the Tanaidacea than what is reported here (Dojiri and Sieg 1997, Larsen 2001). Protogynic tanaids often have p­ olymorphic males: males that used to be females (“secondary males”; Table 8.2) are m ­ orphologically different from males developed directly from juveniles (“primary males”). Also, “tertiary males” (who developed from females who had two broods, and not just one) are different from the other males (Larsen

(A)

(D)

(B)

(C)

(E)

Fig. 8.2. Ectoparasitic isopods in the family Cymothoidae (obligate parasites of fishes). (A) The gill chamber parasite Anphira branchialis on Metynnis lipincottianus. (B) Ceratothoa italica in the mouth of Lithognathus mormyrus and (C)  escaping after realizing its host is dead. (D)  Braga patagonica in the gills of Pygocentrus naterreri. (E) Anilocra physodes on L. mormyrus. See color version of this figure in the centerfold. Photos: (A and D) Charles Baillie; (B) Maria Sala-​Bozano; (C and E) Stefano Mariani.   



Hermaphroditism and Gonochorism

2001). Not all females change into males: this strategy seems to respond to a skewed sex ratio, due to higher mortality and a lack of feeding in males (Larsen 2001). In the tanaid Leptochelia africana, once females molt into their male phase, they lose their functional mouth parts, do not feed anymore, and invest only in reproduction (Larsen and Froufe 2013). In Leptochelia dubia males not only do not feed, but also are aggressive and fight for females (Highsmith 1983). Often protogyny is socially mediated (the dominant male prevents the other females from changing sex), which has been confirmed in tanaids (Highsmith 1983) and some isopods, even though this does not seem to be the case in Gnorimosphaeroma oregonensis (Brook et al. 1994). A high level of plasticity is present in both protandric and protogynic sexual systems:  not all individuals in all populations are sex changers. Some individuals can be born directly as the second sex (“primary males” in diandric protogynous species and “primary females” in digynic protandrous species; Tables 8.1 and 8.2) and thus do not change sex. Moreover, some species are facultatively sequentially hermaphroditic; i.e., not all individuals born as the first sex will change into the second sex, as is also seen in the tanaids, mentioned earlier, where the protogynous strategy depends on the population sex ratio (Larsen 2001). Both protandrous and protogynous hermaphrodites can be considered functionally dioecious, given that populations comprise males and females at any given time (Weeks 2012). However, the ability of individuals to be either sex at different times of their lives clearly differentiates these systems from strict dioecy. Interestingly, while protogyny is the most common system among fish, the majority of sex-​changing crustaceans are protandric, as noted earlier. This difference is possibly related to the differing mating strategies employed by fish and crustaceans: while many fish have haremic systems, where protogyny is advantageous (a female can greatly increase her fitness becoming the large dominant male; e.g., Munday et al. 2006), harems are not common in crustaceans. In haremic crustacean species, like P. sculpta mentioned previously, alternative mating strategies are employed by males (Shuster and Wade 1991, Johnson et al 2001). Instead, in crustacean groups where protogyny is the norm, a change from female to male seems to be favored because of low abundance of males (see earlier discussion of tanaids), or large males might be favored during mate guarding, as hypothesized by Brook et al. (1994) in the isopod G. oregonensis. Bi-​directional sex change (the ability of an individual to change sex multiple times, in either direction) is not confirmed in crustaceans, but is postulated in alpheid shrimps, Arete kominatoensis and A. dorsalis (Nakashima 1987, Gherardi and Calloni 1993, Chiba 2007). An unusual form of sequential hermaphroditism is termed “protandric simultaneous hermaphroditism” (Bauer 2000, 2006, Bauer and Newman 2004, Baeza et al. 2007). In this system, individuals develop first as males and then change into simultaneous hermaphrodites (Bauer 2000, Baeza 2009). This reproductive mode is typical of Lysmatidae (31 out of the 40 known species; Table 8.3; Lin and Zhang 2001, Bauer and Newman 2004, Bauer 2006, Baeza et al. 2007, E in Fig. 8.1) and possibly is found in Barbouriidae (four species) and Parastacidae (four species) and, unique among isopods, is reported in Rhyscotus ortonedae (formerly Oniscoidea). This sequential sexual change is also a response to differing reproductive values at different sizes: smaller males actually accrue more mates than larger males (Baeza 2007). When the shrimp attain a certain size, they then develop a female gonad but retain male functionality (Bauer 2000). Hermaphrodites do expend more effort in female gamete production, but still perform limited outcrossing as males (Baeza 2007). These shrimp have evolved from protandric sequential hermaphrodites (Baeza 2009, Baeza et al. 2009), so the retention of male function is a derived character in these species. Interestingly, protandric simultaneous hermaphroditism is similar to androdioecy, in that at any one time the populations are mixtures of males and hermaphrodites. However, unlike other androdioecious crustaceans, wherein males are genetically distinct from hermaphrodites (Weeks et al. 2006a, Weeks 2012), in protandric simultaneous hermaphrodites, each individual

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Reproductive Biology Table 8.2  Definition of Sexual Types

will be both male and simultaneous hermaphrodite, depending on its age and size (Bauer 2000). In this way, the two reproductive modes are developmentally and ecologically different (Weeks 2012). Simultaneous or Synchronous Hermaphroditism Pure simultaneous hermaphroditism (all mature individuals in a population able to produce male and female gametes at the same time) is considered to be rare in crustaceans (Michiels 1998), as it is almost completely absent in the Malacostraca, where it is present in just two families: Apseudidae in the Tanaidacea ( Johnson et  al. 2001, Kakui and Hiruta 2013, Table 8.3) and putatively in the Axiidae ( Johnson et al. 2001, Chiba 2007, Poore and Collins 2009, Komai et al. 2010, I in Fig. 8.1) within the Decapoda (see later discussion). In other non-​malacostracan orders, populations comprising entirely hermaphrodites have been reported in the Cephalocarida (Addis et  al. 2012), in the cave-​dwelling Remipedia (Neiber et al. 2011, Kubrakiewicz et al. 2012), in some spinicaudatan branchiopods (Scanabissi and Mondini 2002, Weeks et  al. 2005, Weeks et  al. 2014, Brantner



Hermaphroditism and Gonochorism

et  al. 2013a), in notostracans (Macdonald et  al. 2011, Mathers et  al. 2013), and in the Cirripedia (Thoracica; Charnov 1987, Kelly and Sanford 2010, Yusa et al. 2012, J in Fig. 8.1). However, simultaneous hermaphrodites do often co-​occur with males in androdioecious (in Branchiopoda and Cirripedia, see later discussion) and in protandric simultaneous hermaphroditic systems (e.g., caridean shrimp). Simultaneous hermaphroditism has apparently evolved four separate times in the Spinicaudata (Weeks et al. 2014) and five times in the Notostraca (Mathers et al. 2013). In some branchiopods, gonochoristic, androdioecious, and hermaphroditic populations occur in the same species (“geographical hermaphroditism,” as in the case of the tadpole shrimp Triops cancriformis; Zierold et al. 2007; B in Fig. 8.1). In the Cephalocarida self-​fertilization is probable: the male and female functional gonads are separated, but the gonoducts join together and open in a single pair of hermaphroditic geni­ tal pores (Addis et al. 2012); the immotile, aflagellate sperm is also a sign of very low mating competition (Morrow 2004), which could be found in selfing hermaphrodites. Among the previously mentioned groups, aflagellate sperm is found in Branchiopoda and Cephalocarida, but not in Remipedia and Cirripedia (Morrow 2004), and internal fertilization or pseudo-​ copulation (sperm is released in the mantle cavity of the other hermaphrodite; Barazandeh et al. 2013) or fertilization in a brood pouch/​chamber (Weeks et al. 2002) is probable or confirmed in all of them (Morrow 2004). Hermaphroditic barnacles, on the other hand, seem to perform cross-​fertilization among sessile mates, using groping penises, given their sessile condition (Charnov 1987). Only a few species are considered capable of self-​fertilization, at least facultatively (Furman and Yule 1990), but for many of them this ability is not fully confirmed (Wrange et al. 2016). The assumption was partially due to the fact that isolated barnacles could produce fertilized eggs, but a recent paper has reported spermcast mating (the possibility for barnacles to capture sperm from the water; Barazandeh et al. 2013), and thus this assumption may not be valid. Among Malacostraca, simultaneous hermaphroditism has been recorded only in two tanaid species: Apseudes spectabilis (Kakui and Hiruta 2013) and A. sculptus (former A. hermaphroditicus; Johnson et al. 2001). The first described instance of self-​fertilization in malacostracans is for Apseudes sp. (Kakui and Hiruta 2013). The infraorder Axiidea is suggested to be hermaphroditic (see family Axiidae, formerly Calocarididae, in Table 8.3; I in Fig. 8.1), due to the presence of both gonopores in each individual ( Johnson et al. 2001, Chiba 2007, Poore and Collins 2009, Komai et al. 2010), even though the internal reproductive system (i.e., the presence of an ovotestis; Davison 2006) has not been described. In other families, individual “intersexes” have been described (Dworschak 2002), but there are just a few specimens and the functionality of both gonopores has not been investigated. Simultaneous hermaphroditism maximizes the number of females in a population and the chances of finding a mate under low densities (Clark 1978). These two benefits do not apply completely, though, if the eggs can be fertilized only after molting (Raviv et al. 2008). In this case, during the reproductive season simultaneous hermaphroditic individuals can act as females only for a limited period after their molt, while they can act as males most of the time (Baeza 2007). This would reduce the possibility of reciprocity of gamete transfer. Self-​fertilizing hermaphrodites do not have this problem, but inbreeding depression instead may limit the fitness benefits of using this reproductive strategy (Weeks et al. 2006a). Molting as a physiological constraint to receptivity might explain why pure simultaneous hermaphroditism is so rare among crustaceans, and possibly instead promoted the evolution of protandric simultaneous hermaphroditism and androdioecy in this taxon.

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Reproductive Biology Androdioecy Branchiopod Crustaceans Androdioecy has been described from two orders of branchiopod crustaceans (Table 8.3), which occupy ephemeral, aquatic habitats that experience a broad range of abiotic environmental conditions and population densities (Hamer and Martens 1998, Weeks et  al. 2006b, Benvenuto et  al. 2009, Calabrese et al. 2016). The ephemeral nature of populations combined with low population densities has been argued as the reason that androdioecy evolves from dioecy in animals (Pannell 2002), and it likely explains why androdioecy is so widespread in these two orders (Weeks 2012). The best studied of these branchiopods are spinicaudatan clam shrimp in the genus Eulimnadia (see later discussion) that have hermaphrodites and males (Fig. 8.3); the hermaphrodites can either self-​fertilize or can mate with males, but they cannot outcross with other hermaphrodites. Eulimnadia is the most speciose androdioecious lineage of any known plant or animal, having upwards of 53 species (Reed et al. 2015). Although some Eulimnadia appear to be all-​hermaphroditic (Weeks et al. 2005), androdioecy is thought to be the ancestral breeding system in this genus (Weeks et al. 2006c, Weeks et al. 2009b). Thus, these crustaceans are both the most speciose and the longest-​lived (minimally 25 million years) clade of androdioecious animals (Weeks et al. 2006c, Weeks 2012). Androdioecy has also been described in the notostracan tadpole shrimp:  in four species of Triops, namely T. newberryi (Sassaman 1989), T. cancriformis (Zierold et al. 2007), T. longicaudatus (Sassaman et al. 1997), and T. australiensis sp. B (Mathers et al. 2013 supplementary material), and in two species of Lepidurus (L. arcticus and L. apus; Mathers et al. 2013 supplementary material). However, the details of the reproductive system and its ecological significance in these species have not been thoroughly investigated. Androdioecious branchiopods produce a small amount of sperm in an otherwise female gonad (Zucker et al. 1997, Scanabissi and Mondini 2002, Weeks et al. 2005) and in most other respects resemble the females of closely related gonochoristic species (Weeks et al. 2008). Several clam shrimp species have been studied histologically (Zucker et al. 1997, Scanabissi and Mondini 2002, Weeks et al. 2005, Weeks et al. 2006d, Weeks et al. 2009a, Weeks et al. 2014, Brantner et al. 2013a, 2013b), and in the four separate derivations of hermaphroditism from dioecy, all clam shrimp were found to produce a small amount of sperm in different locations throughout the ovotestes (Weeks et al. 2014). In the Notostraca, fewer histological studies of hermaphrodites have been undertaken, but in the one species examined, ovotestes produce small amounts of sperm intermingled with egg production (Longhurst 1955). In all other respects, the hermaphrodites of both orders are indistinguishable from females (Sassaman 1995), which is consistent among animals that have derived hermaphroditism from dioecy (Weeks 2012). Cirriped Crustraceans Androdioecy has been established in 35 barnacle species, across nine families (Table 8.3). The males of the androdioecious barnacles (termed “complemental” males by Darwin, 1851, Table 8.2) settle on or in depressions in the shell plates of the hermaphrodites, or in some cases even crawl inside the mantle (Foster 1983). The mode of sex determination in these species is uncertain. Two hypotheses have been proposed: (1) all larvae are potentially hermaphroditic, but those that settle in niches on large hermaphrodites do not grow to a size where female tissues may develop (i.e., the substratum determines sex expression); or (2)  the sexes are actually genetically fixed and will develop into each sexual type regardless of environmental conditions. Each of these ideas may be valid in different species, given that complemental males have arisen separately in at least seven instances in the Cirripedia (Foster 1983, Yusa et al. 2012). Crisp (1983) and Charnov (1987) hypothesized that cirripedes stemmed from a hermaphroditic ancestor. However, this assessment was based purely on a historical perspective without a phylogenetic analysis, which has been later conducted by Høeg (1995), tracing mating system transitions on

Family Artemiidae Triopsidae

Limnadiidae

Order Anostraca Notostraca

Spinicaudata

CLASS BRANCHIOPODA

Limnadia

Calalimnadia Cyzicus Eulimnadia

Lepidurus

Genus Artemia Triops

Species parthenogenetica cancriformis longicaudatus australiensis sp.B newberryi Apus articus mahei gynecia africana agassizii antlei Azisi brasiliensis braueriana colombiensis cylindrova dahli diversa feriensis follisimilis gibba graniticola gunturensis michaeli texana thompsoni lenticularis

Table 8.3.  List of Non-Gonochoristic Species, Identified from Literature, with Description of Reproductive Mode

RepMode M D, A, H A A A A A H H A H A H A A A A A A A A A A H A A, H A H 14

9

13

7

7

12

7

11

8

8

11

8

8

8

8

7

10

9

8

7

6

4

4

5

4

3

2

1

Ref

(Continued)

Genus Hutchinsoniella Lightiella

Conchoderma

Koleolepadidae

Lepadidae

Lepadiformes

Oxynaspididae

Koleolepas

Heteralepadidae

Lepadiformes

Oxynaspis

Lepas

Paralepas

Synagogidae

Laurida

Gorgonolaureus Waginella Heteralepas

CLASS MAXILLOPODA (THECOSTRACA) CIRRIPEDIA Order Family Genus Ibliformes Iblidae Ibla

CLASS CEPHALOCARIDA Order Family Brachypoda Hutchinsoniellidae

Table 8.3. (Continued.)

Species pygmaea quadrivalvis muzikae sandersi japonica quadrata vetula dannevigi klepalae palinuri xenophorae avis willeyi (tinkeri) auritum hunteri virgatum anatifera anserifera australis pectinata testudinata celata

Species macracantha magdalenina

RepMode A A PA PA SH SH A SH A SH A A A SH SH SH SH SH SH SH SH SH

RepMode SH SH

19

19

19

19

19

19

19

19

19

23;24

22

19

19

21

19

20

19

19

18

18

17

16

Ref

15

15

Ref

208

Scalpelliformes

Scalpellidae

Trianguloscalpellum

Smilium

Scillaelepas

Aurivillialepas Euscalpellum Scalpellum

Arcoscalpellum

Lithotryidae Pollicipedidae

Ashinkailepas Leucolepas Neolepas

Poecilasma Temnaspis Calantica

Octolasmis

Vulcanolepas Lithotrya Capitulum Pollicipes

Eolepadidae

Calanticidae

Poecilasmatidae

angulata cor lowei kaempferi amygdalum siemensi spinosa studeri villosa seepiophila longa rapanuii zevinae osheai valentiana mitella pollicipes polymerus sociabile sp. calycula squamuliferum peronii scalpellum vulgare arnaudii bocquetae falcate fosteri hastatum peronii balanoides

SH SH SH SH SH A A A A SH SH SH SH SH SH SH SH SH SH A A A A A A A A A A A A SH 19

19

25

30

30

30

29

17

27;28

27

25

26

19

19

19

19

19

19

19

19

19

19

19

19

25

19

25

19

19

19

19

19

(Continued)

Pachylasmatidae

Catophragmidae Chelonibiidae

Bathylasmatidae

Tetrapachylasma

Megalasma Octolasmis

Megabalanus Bathylasma Bathylasma Catomerus Chelonibia

CLASS MAXILLOPODA (THECOSTRACA) CIRRIPEDIA cont. Order Family Genus Sessilia Archaeobalanidae Semibalanus Balanidae Amphibalanus Balanus

Table 8.3. (Continued.)

Species balanoides improvisus calceolus galeatus glandula masignotus merrilli azoricus alearum corolliforme polymerus patula testudinaria striatum warwickii unguisiformis trigonum

RepMode SH SH A A SH A A SH A A SH A A A A A A 42

41

19

19

26;40

26

39

38

37

36

34

34

31

35

34

32;33

31

Ref

210

Decapoda

Acontiostoma

Crangonyctidae

Lysianassidae

Atyoida

Stegocephalidae Alpheidae

Atyidae

Austratya Caridina Paratya

Scolopostoma Stegocephalus Arete

Amphorites (Stomacontion) Conicostoma Ocosingo

Genus Paraprotella Crassicorophium (Corophium) Stygobromus

CLASS MALACOSTRACA Order Family Amphipoda Caprellidae Corophiidae RepMode P P P P P PA PA PA PA PA PA PA PA PA*** PA*** PA PA PA PA PA PA

Species teluksuang bonelli albapinus pseudospinosus spinatus marionis tuberculata pungapunga karta borlus fenwicki prionoplax inflatus dorsalis indicus bisulcata serrata pilipes striolata richtersi curvirostris

45;49;53;54

49;52

49

49

49;52

49;52

49;51

49;50

46

46;48

18

48

47

45,48

46

45;48

43

43

44

43

43

Ref

(Continued)

CLASS MALACOSTRACA cont. Order Family Decapoda cont. Axiidae (Calocarididae)

Table 8.3. (Continued.)

colpos crosnieri formosus laevis laurentae mexicanus myalup stilirostris felix manningi mclaughlinae serrata

Calastacus

Calaxiopsis

Bouvieraxius

Species altimanus aberrans flanklinae foveolatus japonicus propinquus surugaensis springeri

Genus Ambiaxiopsis Ambiaxius

RepMode SH? SH? SH? SH? SH? SH? SH? SH?PA? PG? SH? SH? SH? SH? SH? SH? SH? SH? SH? SH? SH? SH? 49

49

49

49

49

60

49

59

49

56

49

49

58

49;57

56

49

49

49

49

55

Ref

21

Campylonotidae

Cambaridae

Barbouriidae

Orconectes Procambarus Campylonotus

Parhippolyte

Barbouria

Paracalocaris Paraxiopsis

Eucalastacus Lophaxius

Calocaris

barnardi caribbaeus macandreae templemani torbeni granulosa investigatoris rathbunae sagamiensis sagamiensis dianae majuro plumosimanus yanezi cubensis cf. uveae misticia limosus fallax f. virginalis capensis rathbunae semistriatus vagans

SH? SH? PSH?SH? SH? SH? SH? SH? SH? SH? SH? SH? SH? SH? PSH? PSH? PSH PSH M P PA PA PA PA 49

49

49

49

66

65

62-64

63;64

62

39

58

58

61

55

49

49

49

49

49

49

49;52;57

49

49

(Continued)

Lysmatidae

Hippolytidae

Hippidae

CLASS MALACOSTRACA cont. Order Family Decapoda cont. Crangonidae

Table 8.3. (Continued.)

Lysmata

Chorismus Hippolyte Calliasmata Exhippolysmata

Notocrangon Emerita

Genus Argis Crangon

Species dentata crangon franciscorum vulgaris antarcticus analoga asiatica antarcticus inermis nohoci ensirostris ophloporoides amboinensis ankeri argentopunctata bahia boggessi californica cf. acicula cf. anchisteus cf. trisetacea Debelius galapaguensis

RepMode PA PA PA PA PA PA PA PA PA? PSH? PSH PSH PSH PSH PSH PSH** PSH PSH PSH PSH PSH PSH PSH 70

49;70

70

62

62

49;72

49;70

49;71

68

49;70

49;69

62

68

68

49;62

49

52

45;52;67

49

49

49

52;49

49;52;66

Ref

214

Lysmatella Merguia Pandalopsis

Merguiidae

Pandalidae

grabhami gracilirostris Hochi holthuisi Lipkei intermedia Moorei nayaritensis Nilita pederseni Rafa rmhbunae seticaudata ternatensis Vittata wurdemanni prima oligodon rhizophorae coccinata dispar gibba glabra japonica

PSH PSH PSH PSH PSH PSH** PSH PSH PSH PSH PSH PSH PSH PSH PSH PSH** PSH PA PA PA? PA PA PA? PA 49

49

49

45;49;77

49

62; 64

62; 64

62;64;76

49; 75

64

62

49;66;71

75

70

49;64;70

49,62;71

74

62

64;71

62

73

64;71

64

49;71

(Continued)

CLASS MALACOSTRACA cont. Order Family Decapoda cont. Pandalidae cont.

Table 8.3. (Continued.)

Pandalus

Genus Pandalopsis cont.

Species lamelligera cf. longirostris montagui tridens pacifica rubra stenolepis borealis chani curvatus danae eous formosanus goniurus gracilis gurneyi hypsinotus jordani kessleri latirostris (kessleri) montagui nipponensis platyceros prensor stenolepis teraoi tridens

RepMode PA PA PA PA? PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA 49

49

45;49;77

49

45;49;77

49

45;49;52;77

49;52;78

52

45;49;77

45;49;52;77

49

49

45;49;52;77

49

49

45;49;52;77

49

49

45;49;52;77

52

49

49

52

49

49

Ref

216

Isopoda

Penaeidae Processidae Rhynchocinetidae Solenoceridae Thoridae

Cryptoniscidae

Armadillidiidae Bopyridae

Ptilanthura Armadillidium Munidion Orthione Liriopsis

Cyathura

Samastacus Virilastacus Penaeus Processa Rhynchocinetes Solenocera Thor

Anthuridae

Parastacus

Parastacidae

brasiliensis nicoleti spinifrons rucapihuelensis kerathurus edulis uritai membranacea amboinensis manningi carinata polita profunda tenuis virgo pleurocondis griffenis pygmaea

PSH? PSH PSH PSH PA PA PA PA? PA PA PG PG PG PG P PA PA PA 85

84

18

83

82

45

52

45; 52; 82

45;49;6266

81

52

79;80

49

52

49,65

49,65

49

49

(Continued)

Gnorimosphaeroma

Paraleptosphaeroma Nagurus Trichoniscus

Hemioniscidae Philosciidae Platyarthridae Rhyscotidae

Sphaeromatidae

Trachelipodidae

Trichoniscidae

Anphira Braga Ceratothoa Cymothoa

Genus Anilocra

Elthusa (Lironeca) Emetha Glossobius Ichthyoxenus Ichthyoxenus (Lironeca) Kuna Mothocya Nerocila Philoscia Hemioniscus Atlantoscia (Ocelloscia) Platyarthrus Rhyscotus

CLASS MALACOSTRACA cont. Order Family Isopoda cont. Cymothoidae

Table 8.3. (Continued.)

Species frontalis pomacentri physodes branchialis patagonica oestroides excisa italica frontalis vulgaris audouinii hemiramphi fushanensis puhi insularis epimerica acuminata (californica) elongata balani floridiana aiasensis ortonedae parallelus insulare (luteum) naktongense oregonensis glynni cristatus modestus pusillus (elisabethae)

RepMode PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA PA P M, P PSH PA PG PG PG PG P P M 99;100

83

83

45

19;45

45;98

97

94

52

83

83

96

52

93;95

91

94

93

45;94

90

52

93

89

88

92

87

CB

CB

52

86

52

Ref

218

Limnocytheridae

Darwinulidae .

CLASS OSTRACODA Order Family Podocopida Cyprididae

Paratanaidae Tanaididae

Nototanaidae

Limnocythere

Vestalenula

Genus Candellacypris Eucypris Prionocypris Alicenula Darwinula Microdarwinula Penthesilenula

Leptochelia Leptochelia (Hargeria) Nototanais Nototanoides Paratanais Sinelobus (Tanais)

Leptochelidae cont.

Leptochelidae

Monokalliapseudes (Kalliapseudes) Heterotanais Leptochelia

Apseudes

Kalliapseudidae

CLASS MALACOSTRACA cont. Tanaidacea Apseudidae

RepMode P M P P M P P P P P P

PG PG PG PG PG PG PG PG PG PG PG

oerstedi acrolophus africana dubia forresti neapolitana rapax dimorphus trifurcatus maleficus standfordi Species aragonica virens zenkeri inversa stevensoni zimmeri brasiliensis kohanga cornelia molopoensis inopinata

SH SH PG PG

sculptus (hermaphroditicus) spectabilis holthuisi (sarsi) schubartii

100

109

100

109

109

109

109

109

109

109;110

109

Ref

102

108

107

106

45

18

45

17;45

105

104

45;52

103

102

101

82

(Continued)

Godzillius Pleomothra Cryptocorynetes

Pleomothridae

Speleonectidae

Lasionectes Lasionectes (Kumonga) Speleonectes

Genus Godzilliognomus

Family Godzilliidae

Species frondosus schrami robustus apletocheles fragilis elmorei haptodiscus longulus entrichoma exleyi atlantida emersoni epilimnius gironensis kakuki lucayensis minnsi ondinae parabenjamini tulumensis benjamini tanumekes

RepMode SH* SH* SH* SH* SH* SH* SH* SH* SH SH* SH* SH* SH* SH* SH* SH* SH* SH* SH* SH* SH* SH* 111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

111

Ref

A: Androdioecious; D: Dioecious; SH: Simultaneous hermaphrodite; H: Hermaphroditic; PSH: Protandric simultaneous hermaphrodite; M: Mixed (asexual and sexual); PA: Protandry; PG: Protogyny; P: Parthenogenetic; * assumed; ** it is possible that some males “never switch to hermaphrodites”; *** (partial)—bidirectional; ? not confirmed. 1 Muñoz et al. 2010, 2Zierold et al. 2007, 3Sassaman et al. 1997, 4Mathers et al. 2013, 5Sassaman 1991, 6Weeks et al. 2014,7Brantner et al. 2013,8Weeks et al. 2006a, 9Weeks et al. 2005, 10Sassaman 1988, 11Weeks et al. 2008, 12Rogers et al. 2010, 13Sassaman and Weeks 1993, 14Scanabissi and Mondini 2002, 15Addis et al. 2012, 16Foster 1978,17Darwin 1851, 18Brook et al. 1994, 19Yusa et al. 2012, 20Newman 1996 as noted in Yusa et al. 2001, 21Kolbasov and Zevina 1999, 22Yusa et al. 2001, 23Newman et al. 1969 as noted in Yusa et al. 2001, 24Hosie 2014, 25Young 2003, 26Crisp 1983, 27Callan 1941,28Høeg et al. 2016, 29Jones and Lander 1995, 30Newman 1980, 31Hoch and Levinton 2012, 32Furman and Yule 1990, 33 Wrange et al. 2016, 34McLaughlin and Henry 1972, 35Gomez 1975, 36Dionisio et al. 2007, 37Foster 1983, 38Dayton et al. 1982, 39Raimondi and Martin 1991, 40Ewers-Saucedo et al. 2016, 41Sawada et al. 2015, 42Foster 1988, 43Lim et al. 2015, 44Taylor and Holsinger 2011, 45Allsop and West 2004, 46Lowry and Stoddart 1986, 47Lowry and Stoddart 2012, 48Lowry and Stoddart 1983, 49Chiba 2007, 50Nakashima 1987, 51Gherardi and Calloni 1993, 52Policansky 1982, 53 Carpenter 1978, 54Carpenter 1983, 55Komai 2011, 56Komai et al. 2010, 57Dworschak et al. 2012, 58Kensley 2003, 59Ngoc-Ho 2011, 60Poore and Collins 2009, 61Poore 2008, 62Fiedler et al. 2010, 63Onaga et al. 2012, 64Baeza et al. 2013, 65 Yazicioglu et al. 2016, 66Bauer 1986b, 67Barnes and Wenner 1968, 68Baeza 2013, 69Fiedler 1998, 70Baeza et al. 2009, 71Baeza 2008, 72Bauer and Newman 2004, 73Anker et al. 2009, 74Baeza et al. 2007, 75Lin and Zhang 2001, 76Murray et al. 2012, 77Butler 1964, 78Chiba et al. 2000, 79Osawa et al. 2015, 80Bauer and Thiel 2011, 81Baeza and Piantoni 2010, 82Johnson et al. 2001, 83Caruso and Bouchon 2011, 84Williams and Boyko 2012, 85Adema and Huwae 1982, 86Adlard and Lester 1995, 87Mladineo 2003, 88Pawluk et al. 2015, 89Aneesh et al. 2015, 90Bakenhaster et al. 2006, 91Bello et al. 1997, 92Cook and Munguia 2015, 93Brusca 1981, 94Tsai et al. 1999, 95Brusca 1978, 96Arnott 2001, 97Hiebert 2015, 98Abe and Fukuhara 1996, 99Bell 1982, 100van der Kooi and Schwander 2014, 101Kakui and Hiruta 2013, 102Highsmith 1983, 103Pennafirme and Soares-Gomes 2009, 104Bird 2015, 105Larsen and Froufe 2013, 106Marinovic 1987, 107Sieg and Heard 1985, 108Larsen 2001, 109SchÖn et al. 2003, 110Schmit et al. 2013a,b; 111Neiber et al. 2011, CB: Charles Baillie personal communication

CLASS REMIPEDIA Order Nectiopoda

Table 8.3. (Continued.)

20



Hermaphroditism and Gonochorism

the resulting tree. The analysis revealed that the two outgroup lineages were dioecious. Additionally, within the Cirripedia, the Acrothoracica and the Rhizocephala exhibit dioecy. The Thoracica is the most derived lineage and exhibits the first transition to hermaphroditism (Høeg 1995). The families within the Thoracica exhibit dioecy, hermaphroditism, and androdioecy, but the evolution of these sexual systems remains unclear. The Iblidae is the most basal family, diverging at the node where hermaphroditism is thought to have evolved. From this, it may be argued that complemental males in this family could have evolved from a dioecious ancestor. In the remaining families, it is more parsimonious that the complemental males evolved secondarily from hermaphrodites (Høeg 1995). Yusa et al. (2012) argue that androdioecy evolves from hermaphroditism and then dioecy is derived from androdioecy. To address the evolution of mating systems adequately in this group, a more robust phylogeny is required. The barnacles described as androdioecious occur in various regions of the world, exhibit a variety of life histories, and are phylogenetically diverse (Yusa et  al. 2012). Darwin (1851) first noted this mating system in Scalpellum vulgare and Ibla quadrivalvis. In the genus Scalpellum, two more species are known to have complemental males:  S.  scalpellum and S.  peronii. Additionally, in the Scalpellidae, five species in the genus Scillaelepas are androdioecious (one now recorded as Aurivillialepas; Table 8.3). Within the genus Ibla, there is some confusion as to the number of androdioecious species (Table 8.3). Some of this confusion may stem from authors often using the terms “hermaphrodite” and “female” interchangeably, as well as “dwarf males” and “complemental males.” Within the order Sessilia, the families Balanidae and the Pachylasmatidae each contain four species with complemental males (Table 8.3). Two species of Chelonibia are androdioecious, C. patula and C. testudinaria, and both are commensal barnacles (Crisp 1983). Koleolepas avis and K.  tinkeri (junior synonym of K.  willeyi) are the only two species in the family Koleolepadidae that have been described as androdioecious (Hosie 2014). Other less-​studied androdioecious barnacles include two species of Bathylasma (B. alearum and B. corolliforme) and two species of Paralepas (P.  xenophorae and P.  klepalae). Additionally, androdioecy has been described in four species of Calantica, two species of Smilium and Octolasmis, and one species each of Heteralepas, Arcoscalpellum, Euscalpellum, Megalasma, and Tetrapachylasma (Table 8.3).

EVOLUTION OF CRUSTACEAN REPRODUCTIVE SYSTEMS Ancestral Crustacean Reproduction There is growing consensus on the phylogenetic relationships among crustacean lineages ( Jenner 2010; see Chapters 4 and 5 in Volume 8), but the reproductive mode of the first crustacean lineage (sometimes termed the “urcrustacean”; Hessler and Newman 1975) is unclear. Cisne (1982, p. 67) suggested that the first crustacean was free-​living, marine, benthic and “probably” dioecious. However, others (Hessler and Newman 1975, Juchault 1999)  suggested that the hermaphroditic Cephalocarida are representative of the ancestral crustacean. In this group, according to Cisne (1982, p. 69), hermaphroditism is likely derived as “an accommodation for reproduction at the low population densities at which cephalocarids seem to occur.” This again suggests a dioecious ancestry in Crustacea. Phylogenies based on morphological characters often place the Remipedia (especially the Nectiopoda) as the basal lineage (Wills 1997). Nectiopodans are hermaphroditic (Ito and Schram 1988). Molecular phylogenetic analyses have suggested that ostracods may be basal for crustaceans (Spears and Abele 1997, von Reumont et al. 2012). Ostracods are primarily dioecious, except for the derived cases of parthenogenesis (Cohen and Morin 1990). Thus, further research needs to be done to determine whether the ancestral crustacean reproduced via dioecy or hermaphroditism.

221

2

222

Reproductive Biology Although we do not know the reproductive mode of the “urcrustacean,” we do know that evolutionary transitions between various reproductive modes have occurred repeatedly within the Crustacea (e.g., Høeg 1995, Perez-​Losada et al. 2012, Yusa et al. 2012, Mathers et al., 2013, Weeks et al. 2014). Below, we will discuss these transitions. Reproductive Transitions Transitions from Dioecy to Hermaphroditism The evolution of hermaphroditism from separate sexes has not been widely debated, but it has been commonly assumed that an “intermediate” of androdioecy or gynodioecy (Table 8.1) may facilitate such a transition. Gynodioecy appears to be exceptionally rare in animals (Weeks 2012), but Pannell (1997, 2002) suggested that androdioecy might be a transitional strategy when evolving hermaphroditism from dioecy in a structured metapopulation in which “reproductive assurance” (i.e., the ability to self-​fertilize when mates are rare) is strongly advantageous (e.g., in early colonizing species) but in which outcrossing is still advantageous when population size allows locating a suitable mate. Weeks and colleagues (Weeks et al. 2006a, Weeks et al. 2009b, Weeks 2012) proposed the “constraint” hypothesis for why androdioecy should be commonly derived from dioecy:  if hermaphroditism is selectively favored in a previously dioecious species (e.g., for reproductive assurance), the constraint hypothesis suggests that the most likely hermaphrodite to evolve from a dioecious progenitor would be a female-​biased hermaphrodite that allocates limited resources to sperm production but lacks the ability to mate with other hermaphrodites because of a lack of male secondary sexual characters (e.g., copulatory or mating structures; C in Fig. 8.3). Consequently, (B)

(A)

(C)

Fig. 8.3. Hermaphrodite (left) and male (right) clam shrimp, Eulimnadia texana. In addition to the basic differences between male and female gametes, clam shrimp also have several secondary sexual differences. Clam shrimp females and hermaphrodites require extensions of the phyllopods (A) and a modified carapace to produce a brood chamber (B) to brood their eggs. Additionally, they need to dig holes in the sediment to bury their eggs. Males require specific mating behaviors (i.e., faster swimming) as well as clasping appendages (C) to pair for outcrossing. In clam shrimp, hermaphrodites have only the male characteristic of sperm production and none of the other secondary male characters, and thus cannot outcross with other hermaphrodites. See color version of this figure in the centerfold. Photos courtesy of Jean-​François Cart.   



Hermaphroditism and Gonochorism

these female-​biased hermaphrodites can only self-​fertilize. This hypothesis assumes that in dioecious species with many sex-​specific traits, an evolutionary transition to effective expression of both sexes would be highly improbable (Weeks 2012), requiring the simultaneous acquisition of both primary (e.g., gamete production) and secondary sexual characters (Fig. 8.3). Therefore in sexually dimorphic, dioecious ancestors, androdioecy is more likely to evolve than gynodioecy because the number of evolutionary changes needed to produce a functional hermaphrodite from a male would be much higher. Weeks (2012) tested these ideas and found that in 40 crustacean species, androdioecy had evolved from a dioecious ancestor in four genera: Eulimnadia, Ibla, Lysmata, and Triops (Fig. 8.4). Two of these are branchiopod crustaceans (Eulimnadia and Triops), one is a barnacle (Ibla), and one is a decapod (Lysmata). The latter two groups deserve special comment. As noted earlier, barnacles have complemental males that in some species are environmentally induced, becoming males when settling on larger hermaphrodites, but in other cases are genetically determined. The decapod Lysmata is a “simultaneous protandric hermaphrodite,” which means that the various Lysmata species are mixes of younger males that eventually develop into simultaneous hermaphrodites (Baeza 2007, 2009, Baeza et al. 2009). In both cases, the populations are mixes of males and hermaphrodites and thus could be considered androdioecious (Weeks 2012). As predicted earlier, there are no examples of crustaceans that have evolved gynodioecy from dioecy (Fig. 8.4).

Arcoscalpellum Balanus Bathylasma Calantica Chelonibia Heteralepas Koleolepas

Megalasma Octolasmis Paralepas Scalpellum Scillaelepas Smilium

Androdioecy 66 spp.

13 genera

Eulimnadia Ibla Lysmata Triops

4 genera

Hermaphroditism

Dioecy

Gynodioecy 0 spp. Fig. 8.4. Evolutionary transitions in reproductive systems from dioecy to hermaphroditism (or vice versa) through androdioecy (males and hermaphrodites) and gynodioecy (females and hermaphrodites). The thickness of the arrows represents the known occurrence of genera (listed in the figure). Dotted arrows represent a lack of known occurrences. The number of species for each intermediate reproductive type are noted below each type, and the identification of the various genera are shown above the respective arrows.   

223

24

224

Reproductive Biology A good example of the constraint hypothesis (Weeks 2012)  can be found in branchiopod crustaceans, especially the well-​studied clam shrimp (Weeks et al. 2009b). Males produce amoeboid sperm that fertilize the females’ eggs externally in a “brood chamber” (B in Fig. 8.3) on the dorsal surface of the female (Weeks et al. 2004). A hermaphrodite developed from a female would only need to produce sperm within the tubular gonad typifying clam shrimp (Scanabissi and Mondini 2000) to be capable of self-​fertilization in the absence of males. On the other hand, a hermaphroditic clam shrimp developed from a male would need to gain the ability to produce yolk, shell the eggs, develop a brood chamber, gain the ability to store eggs in the brood chamber (i.e., by attaching them to extensions of the phyllopod appendages; A in Fig. 8.3), and develop the digging behavior needed to bury the eggs in the pond bottom (Zucker et al. 2002). Unless all of these phenotypes are controlled by the same regulatory pathway, it is highly unlikely that all of these evolutionary changes could occur simultaneously within an otherwise male genetic background. Thus one should expect the simplest pathway to produce a hermaphrodite would be the evolution of hermaphrodites from a female progenitor, which is what is observed in these clam shrimp (Zucker et al. 1997, Weeks et al. 2005, Weeks et al. 2006a, Weeks et al. 2009b). These patterns are mirrored in the branchiopod Triops as well (Zierold et al. 2007, Mathers et al. 2013). Indeed, in all the androdioecious crustacean species derived from dioecious ancestors in which relative allocation patterns between male and female gametes have been reported, the hermaphrodites closely resemble females, with only minor amounts of reproductive effort devoted to sperm production (Weeks et al. 2006a, Chasnov 2010). As noted earlier, androdioecious branchiopod hermaphrodites resemble the females of closely related dioecious species (Weeks et al. 2008), and decapod shrimp in the genus Lysmata (Bauer 2006) also show female-​biased allocation. As suggested earlier, these overall patterns can be explained by assuming a constraint on the development of a hermaphrodite that can competently perform as a male while simultaneously being competent as a female when there are numerous traits required to be competent in both male and female roles (Weeks 2012). Transitions from Hermaphroditism to Dioecy If the ancestral crustacean was hermaphroditic, then dioecy is a derived condition in all gonochoristic species. Juchault (1999) has an intriguing hypothesis for how such a transition occurred, suggesting that a cytoplasmic parasite (e.g., Wolbachia) infected hermaphrodites and inhibited male expression to increase the parasite’s inheritance. This would create all-​female invaders to otherwise hermaphroditic species. If this parasitic infection spread through the population, it would select for increased allocation to male function in the non-​infected hermaphrodites. Over time, as the parasite spread, uninfected hermaphrodites would be selected to eventually lose female function to become strictly male. This would complete the transition from ancestral hermaphroditism to dioecy ( Juchault 1999). We are unaware of any evidence that this has happened in any crustacean, but it is an intriguing idea. More definitive results have been developed in the botanical literature where transitions from hermaphroditism to dioecy have been considered in detail. Such transitions have occurred dozens of times in flowering plants (Bawa 1980, Ashman 2002, Barrett 2010). Theoretical work suggests that dioecy does not evolve directly from hermaphroditism, but rather that either gynodioecy or androdioecy acts as an intermediate stage in the transition (Charlesworth and Charlesworth 1978). It is predicted that the intermediate breeding system of gynodioecy will be more common than androdioecy in plants (Lloyd 1975, Charlesworth and Charlesworth 1978), which is indeed observed (Pannell 2002). In crustaceans, we find no transitions from hermaphroditism to gynodioecy and 13 generic transitions from hermaphroditism to androdioecy (33 total species; Fig. 8.4). Interestingly, each one of these transitions is a barnacle species evolving dwarf (or complemental) males from



Hermaphroditism and Gonochorism

hermaphroditic progenitors (Weeks 2012). In these androdioecious species, males are specifically serving a different purpose than the hermaphrodites, being a ready source of sperm to nearby, larger hermaphrodites (Yusa et al. 2012). Some have argued that these smaller males are following the same sequential reproductive maturity as the Lysmata noted earlier (i.e., maturing as males when small and then growing to simultaneous hermaphrodites; Callan 1941, Crisp 1983). If so, then this switch may indicate that barnacles are more fit as males when they are small because sperm are cheaper to produce than eggs, but then do better by switching to hermaphrodites when they are larger and can afford the higher cost of producing eggs, as argued by Charnov (1982). Others argue that the smaller males are a distinct morph to the larger hermaphrodites (Gomez 1975). In either case, the expression of the sexes is based on the different roles of hermaphrodites and males that correspond to different body sizes and population densities (Ghiselin 1969, Charnov 1982, Blanckenhorn 2000). It appears that the evolution of dioecy from hermaphroditism in crustaceans is quite different from that proposed for flowering plants. The transition from hermaphroditism to dioecy in flowering plants has been discussed in terms of avoidance of inbreeding (Lloyd 1975, Charlesworth and Charlesworth 1978)  and is much more likely via the gynodioecious intermediate stage (Charlesworth 2006). However in crustaceans, the only known transitions from hermaphroditism are to androdioecy and not gynodioecy (Fig. 8.4), and these transitions are almost certainly not to avoid inbreeding depression, since barnacles are not inbreeding (Weeks 2012, Yusa et al. 2012). The groping penises of hermaphroditic barnacles are not likely to allow self-​fertilization, as noted earlier. Instead, it appears that differential selective pressures on differently sized individuals drive sexual expression (i.e., differential sex allocation strategies with size; see Ghiselin 1969, Charnov 1982).

ECOLOGICAL CORRELATES OF REPRODUCTIVE SYSTEMS Crustaceans have successfully colonized a wide variety of environments, including the most ­extreme, such as deserts, hydrothermal vents, and Antarctic lakes (Benvenuto et al. 2015), where population densities can be very low. Their success is due to their extraordinary adaptability, ­reflected by the tremendous diversity in morphology, physiology, ecology, behavior, and ­reproductive strategies that they display. We have identified from the literature 334 species belonging to 67 families in 13 orders of five classes of crustaceans (Table 8.4), which are not gonochoristic (also, the list is not comprehensive for parthenogenetic species). Two classes, the Remipedia and Cephalocarida, seem to be completely characterized by simultaneous hermaphroditism (but data are scarce). These two classes have been commonly considered basal in the phylogenetic tree of crustaceans, although recent analyses group them together with Hexapoda as Allotriocarida (von Reumont et al. 2012; see Chapter 5 in Volume 8). They inhabit anchialine cave systems and marine benthic substrata, respectively, and their population densities are very low (Neiber et al. 2011). Thus, being able to simultaneously act as both sexes increases the chances to find a mating partner in these groups. Another challenging habitat, where densities can fluctuate broadly, are ephemeral freshwater pools. In these environments, some spinicaudatan branchiopods are simultaneous hermaphrodites (six species), although the majority of non-​gonochoristic species (which are also present) are androdioecious (15 species). Among the notostracan branchiopods, one species (T. cancriformis) presents androdioecious, hermaphroditic, and dioecious populations. In ephemeral environments, the ability to self-​fertilize (in absence of males; see discussion of androdioecious populations) allows these species to colonize new pools with only a single individual (the self-​fertile E. texana can produce offspring of different sexes: males and hermaphrodites; Weeks et al. 2006a).

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Table 8.4.  Number of Non-​Gonochoristic Species, by Order and Family, with Description of Reproductive Mode Order

Family

Total Number A SH PA PG PSH of Genera and Species Notostraca Triopsidae 2, 15 6 Spinicaudata Limnadiidae 5, ~61 15 6 Brachypoda Hutchinsoniellidae 5, 13 2 Ibliformes Iblidae 2, 6 2 Laurida Synagogidae 8, 27 2 Lepadiformes Heteralepadidae 3, 39 3 4 Lepadiformes Koleolepadidae 1, 1 2 Lepadiformes Lepadidae 3, 12 8 Lepadiformes Oxynaspididae 1, 20 1 Lepadiformes Poecilasmatidae 8, 40 5 Scalpelliformes Calanticidae 10, 44 4 Scalpelliformes Eolepadidae 4, 7 5 Scalpelliformes Lithotryidae 1, 3 1 Scalpelliformes Pollicipedidae 2, 7 3 Scalpelliformes Scalpellidae 28, 268 12 2 Sessilia Archaeobalanidae 12, 121 1 Sessilia Balanidae 16, 94 4 3 Sessilia Bathylasmatidae 4, 20 2 Sessilia Catophragmidae 2, 2 1 Sessilia Chelonibiidae 1, 6 2 Sessilia Pachylasmatidae 7, 26 4 Amphipoda Caprellidae 88, 401 Amphipoda Corophiidae 25, 149 Amphipoda Crangonyctidae 9, 225 Amphipoda Lysianassidae 78, 491 7 Amphipoda Stegocephalidae 25, 108 1 Decapoda Alpheidae 47, 659 2 Decapoda Atyidae 42, 468 6 Decapoda Axiidae 44, 112 33 (Calocarididae) Decapoda Barbouriidae 3, 8 4 Decapoda Cambaridae 12, 428 Decapoda Campylonotidae 1, 5 4 Decapoda Crangonoidea 5 Decapoda Hippidae 3, 27 2 Decapoda Hippolytidae 37, 336 2 Decapoda Lysmatidae 31 Decapoda Merguiidae 1, 2 2 Decapoda Pandalidae 23, 188 31

P

M

1 1 3

1

1

Order

Decapoda Decapoda Decapoda Decapoda Decapoda Decapoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Isopoda Tanaidacea Tanaidacea Tanaidacea Tanaidacea Tanaidacea Tanaidacea Podocopida Podocopida Podocopida Nectiopoda Nectiopoda Nectiopoda

Family

Total Number of Genera and Species Parastacidae 15, 165 Penaeidae 32, 222 Processidae 4, 68 Rhynchocinetidae 2, 25 Solenoceridae 9, 83 Thoridae Anthuridae 25, 291 Armadillidiidae 15, 315 Bopyridae 158, 614 Cryptoniscidae 8, 24 Cymothoidae 43, 386 Hemioniscidae 3, 10 Philosciidae 114, 569 Platyarthridae 9, 122 Rhyscotidae 1, 23 Sphaeromatidae 96, 706 Trachelipodidae 21, 245 Trichoniscidae 89, 519 Apseudidae 22, 167 Kalliapseudidae 11, 41 Leptochelidae 11, 61 Nototanaidae 6, 10 Paratanaidae 7, 34 Tanaididae Cyprididae Darwinulidae Limnocytheridae Godzilliidae 3, 4 Pleomothridae Speleonectidae 4, 16

A SH PA PG PSH

P

M

4 1 1 1 1 2 4 1 2 1 18 1 1 1 1

1 4 2 1

2

56

3 2 17 99

1 1 7 2 1 1

93

21

40

2 6 1

1 1

20

4

A: Androdioecious; SH: Simultaneous hermaphrodite; PA: Protandry; PG: Protogyny; PSH: Protandric simultaneous hermaphrodite; P: Parthenogenetic; M: mixed. Total number of genera and species per family retrieved from Zhang (2011). Taxa in bold are possibly completely characterized by the same sexual system. For the order Anostraca, family Artemiidae please refer to Chapter 9, this volume.

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Reproductive Biology A combination of simultaneous hermaphroditism and androdioecy is also found in the Cirripedia (34 hermaphroditic species belonging to 11 families; 37 androdioecious species belonging to nine families). Indeed, barnacles show a great variety of sexual systems, which might have evolved in response to their sessile lifestyle, densities (mating group sizes), and spatial limitations (Yusa et al. 2013, Sawada et al. 2015). Morphological constraints (small internal mantle cavity space to brood eggs) and energy allocation have also been considered to be linked to the evolution of a hermaphroditic lifestyle in this group (Hoch and Levinton 2012), favoring an almost completely female individual that can produce small amounts of sperm (with the male function that can be adjusted based on crowding and sperm competition). Locating mates is also problematic in deep-​sea habitats. Here, hermaphroditism is commonly reported for fishes (Warner 1984) and analogously we have found information for 33 simultaneous hermaphroditic species of deep-​water axiid burrowing shrimps (class Decapoda; Table 8.4; I in Fig. 8.1). These species, and only two species in the family Apseudidae (class Tanaidacea, otherwise characterized by protogynous sequential hermaphroditism), are the only ones expressing simultaneous hermaphroditism, among the Malacostraca. Simultaneous hermaphroditism increases the chances of successful fertilization, enhancing encounter rates with potential mates (any individual of the same species can be a potential mate, while gonochoristic species need to find a mate of the opposite sex). An even more extreme mechanism for reproductive assurance is self-​fertilization, which can be advantageous when the density of conspecifics is extremely low and in early colonizing species (Baker 1955). This advantage might exceed the cost of inbreeding depression. Self-​fertilization has been described in branchiopods and in one malacostracan species (Apseudes sp.; Kakui and Hiruta 2013); it is not excluded in the Cephalocarida (Addis et  al. 2012), and might occur in some barnacles (still debated; Kelly and Sanford 2010, Barazandeh et al. 2013, Wrange et al. 2016). If simultaneous hermaphroditism augments fertilization success, sequential hermaphroditism (sex change) increases individual lifetime reproductive success (Warner 1975), as is the case in decapods (Charnov 1979, Charnov and Anderson 1989). Sequential hermaphroditism is often found among obligate parasites (Ghiselin 1969). The isopods belonging to the family Cymothoidae (obligate parasites of fishes; Fig. 8.2), Bopyridae, and Cryptoniscoidea (obligate parasites of crustaceans; Dreyer and Wägele 2001) are protandric sequential hermaphrodites. In the genus Cymothoa (which parasitizes the buccal cavity of fishes; B, C in Fig. 8.2), the first free-​swimming male manca (post-​ larval juvenile) reaching a host will attach to the tongue of the fish, becoming a female, while the subsequent ones will remain males (Cook and Munguia 2013, Pawluk et  al. 2015). Parasites face challenges similar to colonizing species and sessile organisms living at low densities; thus, sequential hermaphroditism will ensure the presence of the two sexes in the same host, as well as increasing individual lifetime reproductive success (larger females are highly fecund; Tsai et al. 1999). Among barnacles, in the infraorder Ascothoracida (parasites of coelenterates and echinoderms), two species, W. sandersi and G. muzikae, are protandrous (Policansky 1982, Brook et al. 1994), while the Rhizocephala (parasites of decapods) are dioecious (Høeg et al. 2016). Overall, protandry is favored to increase offspring production when there is little male competition and thus the second sex (female) is older, larger, and more fecund than the first sex, as well as being favored in parasitic species. When male competition is high, larger males are more successful than smaller ones (but see Blanckenhorn 2000 for exceptions), thus individuals reproduce initially as females and then switch to males. As mentioned earlier, protogynous sex change is commonly found in haremic fish (e.g., Munday et al. 2006), where it is often socially regulated (a condition-​dependent strategy: females will not change to males in the presence of other males). Protogynous sex change does not appear to be socially regulated in the intertidal isopod Gnorimosphaeroma oregonensis (Brook et al. 1994),



Hermaphroditism and Gonochorism

but in this case, females can produce only one brood and males mate-​guard females, so it is advantageous to produce a single clutch as a female and then keep reproducing as a male (with the additional advantage of larger size, to compete with other males). Socially mediated sex change also occurs in some parasitic protandric isopods (where females might release a pheromone to prevent other males from changing into female; Ravichandran et al. 2009) and in some protandric simultaneous crustaceans (Baeza and Bauer 2004). Protandric simultaneous hermaphroditism (40 species described in 4 families) is less common than protandrous hermaphroditism (93 species belonging to 21 families), which may seem ­counterintuitive, given the possible advantage of maintaining male abilities (as a non-​ selfing ­hermaphrodite) when switching to the female phase. Initially, this unusual mating system was linked to a symbiotic lifestyle (expressed by socially monogamous species specialized as fish cleaners; Bauer 2000) characterized by limited mobility (for site fidelity to the cleaning station) and low population densities. In this condition, protandrous simultaneous hermaphroditism would have initially evolved and then been maintained in species occurring in denser aggregations (­historical contingency hypothesis; Bauer 2000). However, recent phylogenetic analyses (Baeza 2013) do not support this hypothesis, leaving some questions about the evolution of this “puzzling” sexual system (Bauer 2000). In general, most of the “unusual” reproductive strategies in crustaceans seem indeed beneficial when encounter rates with conspecifics are low and/​or environments are unpredictable/​unstable, which is commonly found in “colonizing,” parasitic, and symbiotic species (Baeza and Thiel 2007). The flexibility of crustacean reproductive systems allows them to be a very successful group in these challenging circumstances. Population Consequences of Reproductive Systems The type of reproductive mode influences sex ratios, mating success, and colonization events and thus has important ecological consequences at the population level. Sequentially hermaphroditic species experience skewed sex-​ratios toward the first sex (male in protandry and female in protogyny), but sex ratios are even more variable due to the possibility that some individuals develop directly as the second sex (primary females in protandrous species and primary males in protogynous species; Table 8.2; Allsop and West 2004, Chiba 2007). Many species of the genus Pandalus are dyginic (with primary and secondary females), as is Processa edulis. More complex is the situation of Thor manningi, where not all males change sex; so secondary females coexist with sex-​changing males, but also with primary females (shrimp born directly as the second sex) and males that will never change sex (Bauer 1986b). Primary and secondary males are also found in the protogynous tanaid Leptochelia africana (Larsen and Froufe 2013), the two alpheid species Athanas indicus and A. kominatoensis, and in the pandalid Pandalus hipsinotus (Correa and Thiel 2003). In all these cases, the reproductive value of an individual and its mating success depend on its sexual type and the frequency of other sexual types in the population. Apart from primary and secondary males and different male morphotypes, “miniature males” are also present:  complemental males in some androdieocius species and dwarf males in dioecious ones (Table 8.2), including barnacles (as mentioned earlier), epicaridean parasitic isopods, in the superfamilies Bopyroidea and Cryptoniscoidea (Dreyer and Wägele 2001, Asakura 2009), copepods (Vogt 2016), and anomurans (genus Emerita, where neotenous males maintain physical contact with females in turbulent surf waters; Asakura 2009). These tiny males, attached to females, can have a similar role as hermaphrodites, and they can be seen as an adaptation to low densities in challenging environments and during parasitism (Ghiselin 1969).

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FUTURE DIRECTIONS AND CONCLUSIONS Future Directions The diversity of crustacean reproductive types offers excellent opportunities for carcinologists to explore the evolution and ecology of various sexual systems. A most productive start to these future studies would be to map reproductive modes onto a robust phylogeny of Crustacea to infer ancestral reproduction in these interesting animals. From such a mapping, we could determine which sexual systems evolved from which progenitors, and how frequently transitions occurred between various reproductive modes. Such a mapping could also reveal which systems are unlikely to lead to future changes (i.e., “evolutionary dead ends”). Adding comparisons to habitat types could also inform larger questions of reproductive evolution and evolutionary transitions between reproductive types. Herein, we have concentrated primarily on various forms of hermaphroditic and mixed sexual systems (Table 8.4). Specific questions for these systems include the following: Are androdioecious species “transitional” stages between hermaphroditism and dioecy, or are they stable endpoints? More detailed phylogenetic analyses of androdioecy in the Notostraca that better resolve reproductive transitions as well as likely lineage ages for androdioecious taxa would be particularly revealing (Mathers et al. 2013). If androdioecy is determined to be long-​lived in both the Notostraca and Spinicaudata, what ecological conditions select for androdioecy in these crustaceans? Correlations of reproductive system with habitat or other life-​history traits in Eulimnadia, Triops, and Lepidurus could shed light on the conditions that select for androdioecy in these freshwater crustaceans. A correlate of the preceding is whether there are any gynodioecious crustaceans, and if not, why not? Although gynodioecy is exceptionally rare in animals, it is likely that this mating system is simply under-​reported (Weeks 2012). Hermaphroditic crustaceans are excellent systems to explore further for cases of gynodioecy, especially among the reproductively labile barnacles. In particular, self-​compatible hermaphroditic barnacle lineages that experience inbreeding depression would be the most likely to evolve gynodioecy (Charlesworth and Charlesworth 1978), so that would be a fruitful area to explore. Simultaneous and protogynous hermaphroditism are rare in crustaceans. Empirical tests, phylogenetic analyses, and theoretical models should be employed to gain a better understanding of the hypothesized physiological (e.g., molt) constraints for the former and possibly low presence of haremic species in the latter. More research is needed in this field. Protandric simultaneous hermaphroditism appears to be limited to the family Lysmatidae and a minority of other crustacean species (Table 8.4). We have listed 334 non-​gonochoristic species, strictly limiting our list only to species where actual data are known about life-​history traits and reproductive strategies. Some taxa seem to be completely characterized by the same sexual system, but we have preferred to be overly cautious in our analysis. Indeed, the paucity of detailed data on the mating and sexual system of many groups is a limiting factor to gather a better overview and a more detailed resolution on evolutionary processes. More studies should confirm what mating and sexual systems are found in crustacean groups to develop a more complete picture of the evolutionary transitions between dioecy, simultaneous hermaphroditism, and sequential (protandric and protogynous) hermaphroditism in crustaceans. Focused attention on reproductively labile taxa (e.g., the Branchiopoda, Ostracoda, and the barnacles) would allow a more complete picture of reproductively diverse crustaceans. The Isopoda are another large and heterogeneous group that should be explored (phylogenetically and ecologically), as they show a breadth of ecological niches (marine, freshwater, and terrestrial) and life-​history strategies (free-​living, commensal, and parasitic), as well as reproductive modes (Table 8.4), providing interesting comparative possibilities. Pairing such a broad phylogenetic comparison



Hermaphroditism and Gonochorism

among taxa with their corresponding ecological correlates would provide invaluable insights into the likely environmental pressures that selected for reproductive switches. Finally, what are the applied implications of mating systems for conservation and management of commercially important stocks or endangered species? Conclusions Clearly, crustaceans exhibit a broad range of reproductive types (Tables 8.3 and 8.4), which reflects both the wide array of habitats in which they are found and their various ecological roles. The majority of crustaceans are gonochoric (dioecious), but as we have outlined in this chapter, there are numerous variations from the “standard” male + female reproductive mode. We have concentrated on delineating the variety of hermaphroditic reproductive modes, leaving the delineation of asexual reproduction to another chapter in this volume (see Chapter 9 in this volume). We have noted a lack of gynodioecy in Crustacea, which is mirrored throughout the Animalia (Weeks 2012). We have also noted the likely evolutionary transitions between these various reproductive systems and remarked on the known ecological correlates of many of these systems. Overall, comparative studies of crustacean reproductive modes in an ecological and evolutionary context are only in their infancy, with investigations of individual taxa (e.g., branchiopods, Lysmata decapods, barnacles) allowing glimpses into larger scale evolutionary patterns. However, much more research needs to be done to allow us to fit together the interesting information from these various taxa into a larger-​ scale view of crustacean reproductive evolution and what drives such evolution. There are plenty of unanswered questions in reproductive evolution. Crustaceans are wonderful systems in which to delve into these questions.

ACKNOWLEDGMENTS We would like to thank Jean-​François Cart, Hans Hillewaert, Domenico Caruso, Antonio Baeza, Arthur Anker, Asma Althomali, Ann Dornfeld, Ian Frank Smith, Charles Baillie, Maria Sala-​ Bozano, and Stefano Mariani for allowing us to use their beautiful photographs. Charles Baillie also provided us with information and interesting discussion on parasitic isopods. This chapter was improved by insightful comments by Martin Thiel and Rickey Cothran. Thanks are due also to Tim Kiessling and Miles Abadilla for their great editorial work.

REFERENCES Abe, M., and H. Fukuhara. 1996. Protogynous hermaphroditism in the brackish and freshwater isopod, Gnorimosphaeroma naktongense (Crustacea: Isopoda, Sphaeromatidae). Zoological Science 13:325–​329. Addis, A., F. Fabiano, V. Delogu, and M. Carcupino. 2012. Reproductive system morphology of Lightiella magdalenina (Crustacea, Cephalocarida): functional and adaptive implications. Invertebrate Reproduction and Development 57:142–​155. Adema, J. P. H. M., and P. H. M. Huwae. 1982. New and supplementary records of marine isopoda for the Netherlands and the southern North Sea since 1956, with a note on Peltogaster paguri (Crustacea, Cirripedia). Zoologische Bijdragen 28:33–​57. Adlard, R. D., and R. J. G. Lester. 1995. The life-​cycle and biology of Anilocra pomacentri (Isopoda, Cymothoidae), an ectoparasitic isopod of the coral-​reef fish, Chromis nitida (Perciformes, Pomacentridae). Australian Journal of Zoology 43:271–​281. Ah-​King, M., and S. Nylin. 2010. Sex in an evolutionary perspective: just another reaction norm. Evolutionary Biology 37:234–​246.

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9  PARTHENOGENESIS

David J. Innes and France Dufresne

Abstract The dominant mode of reproduction in eucaryotes is sexual. This has been described as a paradox given that sex is much more costly than reproducing asexually, such as by parthenogenesis. In the Crustacea, parthenogenesis is commonly found in the Ostracoda and Branchiopoda (Artemia and Cladocera), and studies of these species have made important contributions to understanding the ecological and evolutionary relationship between sexual and asexual reproduction. With respect to parthenogenesis, researchers have explored its taxonomic distribution and phylogeny, origin and mode, ecological genetics, and genomic signatures. Parthenogenetic Crustacea include both diploid and polyploid clones that have originated multiple times from related sexual species but appear to have a relatively limited evolutionary lifespan. Darwinulid ostracods may be one exception, with no known sexual forms and possibly an example of ancient asexuality, although this is controversial. Most parthenogenetic crustacean groups appear to have a wider geographic distribution than related sexual species and are often found in marginal habitats associated with higher latitudes and altitudes. Such patterns of geographic parthenogenesis have yet to be fully explained, but could possibly be due to colonization and adaptation advantages of asexuality; further studies are required to eliminate polyploidy alone as an explanation. There are many examples of parthenogenetic ostracods, cladocerans, and Artemia showing high levels of genetic diversity likely due to recent multiple origins from related sexual species. Phylogenetic analyses support this explanation and for Artemia and Daphnia, cases have been documented for rare functional males produced by parthenogenetic females that can mate with sexual females as a mechanism for generating new clonal lineages. The diversity of asexual species, combined with prior ecological and genetic information, suggests that crustaceans will continue as important models for understanding parthenogenesis, particularly with the application of new genomic tools.

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INTRODUCTION Two influential books (Williams 1975, Maynard Smith 1978) explored the question of why most organisms engage in some form of sexual reproduction compared to avoiding many of the costs of sex and simply reproducing asexually. Understanding the evolutionary advantages of sexual compared to asexual reproduction continues to be an active area of research (Stelzer 2015). Parthenogenesis is a common form of asexual reproduction where females produce offspring from unfertilized eggs by a variety of mechanisms. Simon et al. (2003) reviewed the modes and origins of parthenogenetic lineages from sexual species. The main modes of parthenogenesis include apomixis (essentially producing genetically identical eggs by mitosis) and “meiotic parthenogenesis” (eggs produced by meiosis but various mechanisms for restoring diploidy exist) (Fig. 9.1). Under automixis, meiotic products are fused at meiosis 1 or at meiosis 2, restoring ploidy levels. Terminal fusion involves fusion of products from meiosis 2 (comprising sister chromatids), thus leading to a loss of heterozygosity, whereas under central fusion, meiotic products from meiosis 1 are fused (do not comprise sister chromatids), thus maintaining heterozygosity. Research areas for different groups of parthenogenetic organisms include determining the following: (1) the taxonomic distribution and phylogeny of parthenogenesis, (2) the origin and mode of parthenogenesis, (3) the ecological and evolutionary relationship to related sexual species, (4) the ecological genetics of the parthenogens (number of clones, geographic and habitat distribution), and (5) the genomics of parthenogenesis. Automixis Central fusion

Automixis Terminal fusion

Egg

Meiosis I

Meiosis II 1 2 3 4

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Apomixis Unreduced egg cell

Fig. 9.1. Under automixis, two of the four meiotic products fuse restoring diploidy with different genetic consequences depending on which products are fused. When products of the 1st meiosis are fused (central fusion), heterozygosity is preserved. By contrast, when products of the 2nd meiosis are fused (terminal fusion), homozygosity at the loci close to the centromere is maintained. Apomictic reproduction involves the production of unreduced eggs with mitosis-​like divisions resulting in genetically identical offspring (clones). Modified from Mirzaghaderi and Hörandl (2016).   

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Reproductive Biology Parthenogenesis is widely distributed among many animal phyla (Bell 1982), but the evidence suggests that parthenogenetic lineages have limited long-​term evolutionary success, with perhaps only a few exceptions that could be considered ancient asexual lineages ( Judson and Normark 1996). Nevertheless, studying the evolutionary relationship between parthenogenetic and related sexual species can lead to a better understanding of the ecological and genetic factors that explain the short-​term success of asexual reproduction and the longer-​term success of sexual reproduction. For example, differences in the geographical distribution of sexual and related parthenogenetic lineages (known as geographic parthenogenesis) can provide evidence for the environmental factors that favor one mode of reproduction over the other. Geographic parthenogenesis was originally defined based on observations that asexual forms often occur in marginal habitats (such as higher altitudes and latitudes) characterized by abiotic factors rather than biotic interactions, and several non-​mutually exclusive hypotheses have been proposed to explain such patterns (Vandel 1940, Haag and Ebert 2004). In addition, any observed differences in geographic distributions have to be assessed in light of other complicating factors such as the common association of parthenogenesis with polyploidy (Adolfsson et al. 2010). Furthermore, it can be difficult to discriminate among various hypotheses. In some cases, the observation of a wider distribution of parthenogenetic forms may be a consequence of: (1) the ease of dispersing and establishing new populations (only a single individual required), (2) avoidance of inbreeding, (3) broadly adaptive general-​purpose genotypes, (4) a large number of narrowly adapted clones, or (5) a combination of these factors (Haag and Ebert 2004, Maniatsi et al. 2011). In the Crustacea, parthenogenetic forms are commonly found within Ostracoda and Branchiopoda (Artemia and Cladocera) (Fig. 9.2). Cyclical parthenogenesis is only found in the Cladocera, in which a sexual phase alternates with an apomictic clonal phase producing genetically identical daughters. Although most Cladocera reproduce by cyclical parthenogenesis, a few species have eliminated the sexual phase and only reproduce by apomictic parthenogenesis, described as obligate parthenogenesis. In Ostracoda, asexual diploid species appear to reproduce by apomictic parthenogenesis, whereas in Artemia, only the polyploid clones reproduce by apomixis with the diploid clones reproducing by automixis. While apomixis generates genetically identical offspring and preserves heterozygosity, automixis can generate some genetically variable offspring by segregation in heterozygous parents, similar to self-​fertilization (Fig. 9.1). The development of genetic and genomic markers has played a major role for identifying parthenogens and determining phylogenetic relationships, biogeography, and origin of these crustacean parthenogenetic lineages from sexual species. The goal of this short review is to summarize the occurrence of parthenogenesis within the Crustacea and provide an overview of studies addressing the evolutionary relationship between sexual and related parthenogenetic forms. Our approach is to first summarize research on parthenogenetic Artemia, ostracod, and cladoceran species and any other crustacean species where parthenogenesis has been reported. Finally, we integrate this information to provide a general overview of the contributions that crustacean species have made in understanding short-​term advantages of parthenogenesis and the longer-​term advantages of sex.

PARTHENOGENETIC ARTEMIA The genus Artemia consists of four Old World sexual species:  A.  salina (Mediterranean basin), A. urmiana (Lake Urmia, Iran, and Crimean salt lakes, Russia), A. sinica (China and Mongolia), A.  tibetiana (Qinghai–​Tibetan Plateau, China) and three New World sexual species:  A.  monica (Mono Lake, United States), A. franciscana (North America, Central America, and South America), A.  persimilis (Argentina and Chile) (Asem et  al. 2016). Parthenogenetic forms are confined to

Euphausia superba Petrolisthes cinctipes Eriocheir sinensis

Branchiopoda

Copepoda

Cirripedia

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) are found primarily within Ostracoda and Branchiopoda (Artemia, Cladocera). From von

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Caligus rogercresseyi

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Tigriopus californicus

Balanus amphitrite

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Litopenaeus vannamei Penaeus monodon

Macrobrachium nipponense

Carcinus maenas Homarus americanus

Artemia franciscana Triops cancriformis Lynceus brachyurus

Fig. 9.2. A  portion of the pancrustacean phylogeny. Parthenogenetic crustacean taxa ( Reumont et al. (2012), Fig. 1.

  

Sarsinebalia urgorii Nebalia bipes

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Reproductive Biology Europe and Western and Eastern Asia, and are often referred to as A. parthenogenetica even though this is not a formal taxonomic group (Browne and MacDonald 1982). Types of Parthenogenesis in Artemia Parthenogenetic Artemia consists of diploid (2n) and polyploid (3n, 4n, 5n) females. Polyploid parthenogenetic females produce eggs by apomixis (clonally), resulting in genetically identical female offspring, barring any mutations. In contrast, diploid parthenogenetic females produce offspring from unfertilized eggs via automixis (MacDonald and Browne 1987, Maccari et  al. 2013a, Maccari et al. 2014). There are several different types of automixis that can have different consequences on the genetic identity of the offspring relative to their female parent (Fig. 9.1). Automixis in Artemia involves central fusion during anaphase I of meiosis I that preserves heterozygosity in the region of the centromere, but a low level of recombination results in increased homozygosity in chromosome regions distal to the centromere (Nougue et al. 2015). In Artemia, females are the heterogametic sex (ZW) and meiosis with central fusing and low recombination can explain the observed occurrence of rare males from diploid parthenogens, assuming the sex-​determining genes are close to the centromere with low levels of recombination (Nougue et al. 2015). Origin of Parthenogenetic Artemia Parthenogenetic Artemia populations are restricted to Europe and Asia, occasionally coexisting with sexual species (Browne and MacDonald 1982, Triantaphyllidis et  al. 1998). Initial mtDNA analyses showed large differences between sexual and parthenogenetic Artemia (Perez et al. 1994, Nascetti et al. 2003, Mura 2005) and revealed that parthenogenetic lineages (ploidy not reported) were likely of polyphyletic origin and most closely associated with the sexual species A. urmiana, A. tibetiana, and A. sinica (Baxevanis et al. 2006) (Fig. 9.3). A later survey from a wider geographic range revealed that diploid parthenogens were more closely related to an undescribed sexual species from Kazakhstan and to sexual A.  urmiana than to A. tibetiana (Fig. 9.4) (Muñoz et al. 2010). Parthenogenetic populations had low levels of CO1 haplotype diversity with one common haplotype (accounting for 79% of the eight haplotypes detected) found in almost all populations, suggesting a recent and polyphyletic origin of diploid parthenogenetic Artemia. Maniatsi et al. (2011) examined the relationships of polyploid parthenogens with diploid parthenogens and sexual species, and revealed that both diploid and triploid parthenogens were closely related to A.  urmiana at the CO1 gene, whereas tetraploid parthenogens were more closely related to A. sinica(Fig. 9.5). Similar results were reported by Maccari et al. (2013a). Maccari et al. (2013b) added diploid parthenogens from more eastern locations than Muñoz et al. (2010) and showed that A. urmiana, Artemia sp. Kazakhstan, and A. tibetiana were closely related to diploid parthenogens, as was found by Muñoz et al. (2010), and excluded A. sinica as a possible source for the diploid parthenogens, as was also concluded by Eimanifar et al. (2015). Although the results suggested a multiple origin for diploid parthenogens, the pattern of genetic variation between the sexual species and the parthenogens did not provide any clear explanation for the origin of parthenogenesis, despite the observation of rare males produced by some parthenogens as a potential mechanism for gene flow with sexual species and a source of new parthenogenetic lineages. Parthenogens coexisting with A.  urmiana in three populations did not share haplotypes, also suggesting a lack of gene flow between the asexual and sexual forms. Further genomic information is required to distinguish hybridization between sexual species from mating by rare males as possible mechanisms for explaining diploid parthenogen genetic diversity Maccari et al. (2013a, 2013b).

Parthenogenesis

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OUTGROUP PIC7 BAI8 BAI7 A. BAI9 TDP3 TDP2 SAN4 SFA9 SFA4 SAN6 A. WNA4 WNA5 LAR8 LAR9 MAD4 TCL2 TCL1 URM2 A. URM3 URM1 MAD6 POL14 NAM1 NAM5 MEM9 MEM4 TIB3 A. TIB7 EIL2 EIL1 JIA7 SIN2 SIN1 A. SIN3 ING3 SFB8 MAS1 SFB5 SFB9 IQU1 A. SFB2 SFB1 MAS7 MAS6 GSL1 GSL3

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Fig. 9.3. Bayesian phylogeny for Artemia based on nuclear ITS1 sequences (thick lines parthenogenetic lineages). From Baxevanis et al. (2006), Fig. 4.   

The phylogeny by Asem et  al. (2016) confirmed the closest relationship among diploid and triploid parthenogens with sexual A.  urmiana (Artemia sp. Kazakhstan was not included in the study) and somewhat more distantly related A. tibetiana (Fig. 9.6). This phylogenetic group was distantly related to a group consisting of a close relationship between sexual A.  sinica and the polyploids (tetraploids and pentaploids) from China. The mtDNA variation suggests that triploid parthenogens have arisen from diploid parthenogens, perhaps involving production of rare males by diploid parthenogens and unreduced gametes from either A. urmiana or the parthenogens, but the exact mechanism of origin remains to be determined. Similarly, the low genetic distance between

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Reproductive Biology A. parthenogenetica APD02 A. parthenogenetica APD03 A. parthenogenetica APD04 A. parthenogenetica APD05 96 97

A. parthenogenetica APD01 A. sp. Kazakhstan DQ119653 A. parthenogenetica AY953368, Australia A. parthenogenetica AY953369, Australia

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A. tibetiana ARC1524 Jingyu, Tibet A. tibetiana ARC1348 Lagkor Co, Tibet

A. tibetiana ARC1611 Qixiang, Tibet 88 99

A. tibetiana ARC1609 Nîma, Tibet A. tibetiana ARC1610 Yangnapeng, Tibet A. sp. DQ119652, Qi Xiang Cuo, Tibet A. sinica DQ119650, Mongolia A. franciscana DQ119645, USA

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Fig. 9.4. Artemia phylogeny based on mtDNA CO1 sequences for A.  parthenogenetica and sexual species (A. sp. Kazakhstan, A. urmiana, A. tibetiana, A. sinica). From Muñoz et al. (2010), Fig. 4.   

tetra-​and pentaploids suggests an origin of tetraploids from A. sinica and the origin of pentaploids from the tetraploids, but again, the exact mechanism is unknown. Elucidating the mechanisms for the origin of polyploid parthenogens will require an increased number of nuclear markers that are becoming more accessible with new genomic techniques. The phylogenetic studies, to date, all suggest a polyphyletic pattern for the origin of parthenogenetic Artemia, and in some cases have identified the most likely sexual species involved. A polyphyletic pattern is evident when different parthenogenetic lineages share different most recent common ancestors with distantly related sexual species. Although the dating of the origin of parthenogenetic lineages based on sequence divergence is imprecise, Eimanifar et al. (2015) estimated that the Eurasian parthenogenetic complex diverged from a common ancestor with A. urmiana approximately 2 mya and diversified within the last 0.84 mya. Accurate dating of the origin of different parthenogenetic lineages will no doubt improve as more molecular genetic information accumulates. Although phylogenetic relationships based primarily on mtDNA sequences support multiple origins from related sexual species, discriminating among various hypotheses for mechanisms

Parthenogenesis A. persimilis

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Fig. 9.5. Artemia phylogeny based on (A) 21 COI haplotypes and (B) 60 COI sequences. Parthenogenetic (H1–​H21, diploid (2n) and polyploid (3n, 4n)) and sexual species (A.  persimilis, A.  sinica, A.  urmiana, A.  tibetiana, A. franciscana, A. salina). From Maniatsi et al. (2011), Fig. 5.   

involved in the transition to parthenogenesis has been hampered by the lack of reliable information from nuclear genes (Maniatsi et al. 2011, Asem et al. 2016). The occurrence of rare males produced by some diploid parthenogens probably provides the best opportunity for determining the mechanism for the origin of diploid and triploid parthenogens. Rare males have often been reported for diploid parthenogens and have been shown to successfully mate with A. urmiana, A. sinica, A. tibetiana, and Artemia sp. Kazakhstan sexual females and to produce viable F1 hybrid offspring (Maccari et  al. 2013a). Maccari et  al. (2014) took these matings one step further and demonstrated that the F1 hybrids all reproduced sexually. However, parthenogenetic females were observed for some of the F2 crosses involving Artemia sp. Kazakhstan and A. urmiana, but only sexual females were observed for crosses involving A. sinica. These experimental crosses provide strong support for potential gene flow between sexual and parthenogenetic populations and a mechanism for generating new parthenogenetic genotypes. The absence of parthenogenetic F1 hybrids, but the appearance of parthenogenetic F2 offspring, also suggests that the genes for parthenogenesis are likely recessive. However, the origin of new parthenogenetic clones in nature may be extremely rare (Maccari et al. 2014). Limitations include the following: (1) parthenogenetic and sexual species rarely occur in the same habitat; (2) where parthenogenetic and sexual species are found at the same location, seasonal differences in occurrence can reduce encounter probability; (3) male production by diploid parthenogenetic females is very rare; (4) rare F1 x F1 mating is required to produce new parthenogenetic clones in the F2 generation since genes for parthenogenesis are recessive; and (5) survival of the F2 generation is very low, at least under laboratory conditions. Laboratory mating experiments and additional information from nuclear genes

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Fig. 9.6. Artemia phylogeny based on mtDNA 16s gene. Diploid (2n) polyploidy (3n, 4n, 5n) Artemia parthenogens and sexual species (A. urmiana, A. tibetiana, A. sinica). From Asem et al. (2016), Fig. 9.   

Parthenogenesis (A)

(B)

Fig. 9.7. Distribution of samples of (A) parthenogenetic and (B) sexual Artemia. From Nascetti et al. (2003), Baxevanis et al. (2006), Lin et al. (2006), Munoz et al. 2010, Maniatsi et al. (2011), Maccari et al. (2013), Eimanifar et al. (2014, 2015), and Asem et al. (2016).   

can be used to test the role of unreduced gametes for the origin of triploid and higher polyploid parthenogens and to identify the parent contributing unreduced gametes (Maniatsi et  al. 2011, Asem et al. 2016). These results, combined with other published studies, confirm a pattern of geographical parthenogenesis with the restricted geographic range of the Old World sexual species that contrasts with the much wider geographic range of both the diploid and polyploidy parthenogens (Fig. 9.7; Browne 1992). Furthermore, diploid parthenogen clones appear to consist of a large number of possible specialist clones, each with limited distribution compared to a small number of more broadly distributed, thus possibly more generalist, triploid and tetraploid clones (Maniatsi et al. 2011). Genetic Variation within and among Populations of Parthenogenetic Artemia A better understanding of the ecological genetics of parthenogenetic Artemia can benefit from estimating clonal diversity within populations and the geographic distribution of individual clones. Earlier studies documented extensive clonal variation (Abreu-​Grobois and Beardmore 1980), and some of this variation is likely a consequence of different clonal genotypes adapted to different environments (Browne and Hoopes 1990). A broad geographic survey (Maniatsi et al. 2011) used a microsatellite analysis (5 loci) to identify a total of 31 distinct multilocus genotypes (MLGs often referred to as clones) among diploid and polyploid individuals sampled from 23 populations in

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Reproductive Biology Europe and Asia. The survey uncovered 20 diploid, nine tetraploid, and only two triploid clones. The greater genetic diversity for the diploids could be a consequence of automixis segregating variation for heterozygous genes compared to apomictic replication of single genotypes for the polyploids. The number of clones per population ranged from one to seven with 10 (43%) uniclonal populations. The most widespread clones were polyploid, occurring in six to seven populations. In contrast, only one of the 20 diploid clones were found in more than one population. This suggests that the diploid clones are specialists, adapted to local environmental conditions, and the polyploid clones generalists, but further research is required to test this hypothesis. Life-​History Differences and Competition between Parthenogenetic and Sexual Artemia Laboratory experiments have tested the hypothesis that competition should favor parthenogenetic over sexual Artemia because parthenogenesis avoids many of the costs associated with sex. Initial studies (Browne 1980a) involved experimental competition between Old World asexuals (Madras and Kutch, India) and New World sexuals (San Francisco, Puerto Rico). Although the specific outcome of each experiment was a function of food level and density, sexuals tended to outcompete asexuals in most (11/​13) of the trials. However, none of the previously measured life-​history trait differences (length of reproductive span, reproductive output) measured at high and low food density at a single high temperature condition (26oC) could explain the outcome of competition (Browne 1980b). Browne and Halanych (1989) conducted experiments involving Old World parthenogenetic strains from diverse sources (France, Turkey, Spain, India) in competition with Old (A. tunisiana) and New World (A. franciscana) sexual populations at two different food levels. New World sexual A. franciscana almost always outcompeted the parthenogens, and this may explain the invasion success of this species across large areas of Asia (Eimanifar et al. 2014). In contrast, the Old World sexuals were almost always outcompeted by the parthenogens. These outcomes could differ under different environmental conditions, making it difficult to extrapolate results from laboratory experiments to natural populations. Nevertheless, the competitive superiority of the parthenogens in the laboratory may also explain their wider geographical distribution than the sexuals across the Old World sample sites (Fig. 9.7). Parthenogenetic and sexual Artemia rarely coexist (Shadrin et  al. 2012, Zheng and Sun 2013), but were found together in nine salterns within a small area of southern Spain (Amat 1983) and showed seasonal variation in relative frequency associated with variation in temperature and salinity. Other observations showed that parthenogens dominate during the warmer summer months and sexuals during the cooler winter months (Barata et  al. 1996a, 1996b). Laboratory competition experiments and measurements of life-​history traits at different temperatures suggested that differences in thermal optima may partially explain coexistence (Barata et al. 1996a, 1996b). Seasonal samples of hypersaline Lake Urmia (Iran) showed that sexual A. urmiana dominated when salinity was high, and parthenogenetic females occurred seasonally in adjacent lagoons with much lower salinity (Agh et  al. 2007). Such niche differentiation avoids direct competition, explaining the co-​occurrence of sexual species and parthenogens at a particular site. Areas for Future Artemia Research Research to date provides a very comprehensive overview of the extent and distribution of parthenogenetic and sexual Artemia throughout much of Eurasia. In addition, phylogenetic analysis has identified the most likely sexual species giving rise to the parthenogens and hypotheses for the origin of polyploid parthenogens. Increased confidence in these relationships would benefit

Parthenogenesis from additional nuclear genetic markers as well as additional samples from central Asia, with a larger sample size from each locality. Most studies have utilized small sample sizes over a large number of localities, suitable for phylogeny reconstruction. Larger sample sizes utilizing a larger number of nuclear markers would allow for better estimates of genetic diversity and also would increase the chances of detecting sites where sexual and parthenogenetic population co-​occur. Such co-​occurrence is required to support the hypothesis for the origin of new clones through mating between rare males from diploid parthenogens and sexual females. The frequency of rare males produced by parthenogenetic females has been measured in the laboratory (Maccari et al. 2013a, Chang et al. 2017). However, current evidence for co-​occurrence in natural populations is limited, lacking quantitative estimates of the frequency of sexual females, parthenogenetic females, and males from parthenogenetic females. An increased number of nuclear markers would also assist in detecting gene flow between any coexisting parthenogens and the sexual population. Finally, a large number of nuclear genetic markers would provide a closer examination of the spatial and temporal genetic variation in habitats where parthenogenetic and sexual Artemia co-​occur, and such studies would contribute to a better understanding of the ecological and evolutionary relationship between these drastically different modes of reproduction.

PARTHENOGENETIC OSTRACODS Ostracods are small benthic-​dwelling crustaceans that are widely distributed in marine and freshwater habitats (Martens 1998). There are many documented parthenogenetic species, suggesting a high transition to asexual reproduction (Chaplin et al. 1994). Marine species are predominantly sexual, and most parthenogenetic species are found in freshwater habitats (Butlin et  al. 1998a), although the reasons for the association of parthenogenesis with freshwater are not completely understood. The identification of asexual taxa is often based on the lack of males. However, this approach can be unreliable for species that exhibit little sexual dimorphism (Chaplin et al. 1994). Genetic markers have been invaluable for detecting asexual reproduction based on patterns of genetic variation that deviate from those expected for sexual reproduction. Parthenogenetic freshwater ostracod species have originated independently many times and are distributed among several families within the superfamily Cypridoidea (including Candonidae, Cyprididae, and Ilyocyprididae) and the superfamily Darwinuloidea (Family Darwinulidae) (Chaplin et  al. 1994)  with only some parthenogenetic species in the mostly sexual Candonidae (superfamily Cypridoidea) and superfamily Cytheroidea (Butlin et al. 1998a). Among the ostracod families, parthenogenesis is most common in Cyprididae and the ancient asexual Darwinulidae, and hence species within these families have been the focus of most studies (Butlin et al. 1998a). Earlier studies on the evolutionary genetics of ostracod parthenogenesis have been reviewed by Chaplin et al. (1994), Butlin et al. (1998a, 1998b), Martens (1998), and Rossi (1998). Asexual forms are much more geographically widespread than sexual populations, but high genetic divergence among some asexual and sexual lineages suggests the possibility of species complexes (Chaplin et al. 1994, Adolfsson et al. 2010, Symonoá et al. 2018). Low levels of heterozygosity appear to rule out an interspecific hybrid origin for some parthenogens. High levels of clonal diversity point to congeneric sexuals as a potential source for genetic variation, either through multiple origins or ongoing gene flow. Hybridization between asexuals and related sexuals could also generate the polyploid parthenogenetic clones observed for some species (Turgeon and Hebert 1994, 1995). Many of the parthenogenetic clones coexist with related sexuals, suggesting a recent origin for some lineages. However, the family Darwinulidae, with no extant sexual relatives (although see Smith et al. 2006 and Schön et al. 2009), are thought to be an example of an ancient asexual lineage (Schön et al. 2003, Schön

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Reproductive Biology et al. 2009), although this is controversial (Little and Hebert 1996). Sex determination in sexual species is chromosomal and appears to involve multiple sex chromosomes that may be related to the observed but unexplained female-​biased sex ratios (Schön and Martens 1998). Chaplin et al. (1994) suggest a possible link between female-​biased sex ratios and sperm limitation that could favor the evolution of asexual lineages, particularly in small, isolated freshwater populations. Butlin et al. (1998a, 1998b) and Rossi (1998) provided detailed summaries of studies showing the extent of clonal diversity in various parthenogenetic species. Variation in observed clonal diversity was partially explained by the numbers of populations, individuals, and polymorphic loci involved in each study. They noted several exceptions with much higher clonal diversity than expected among some parthenogenetic species. The high clonal diversity appears to be due to a combination of multiple origins and accumulation of mutations within parthenogenetic lineages. Mitochondrial and nuclear DNA variation provides further support for the multiple origins of clones within some species (Schön et  al. 2000, Adolfsson et  al. 2010, Bode et  al. 2010). In some cases, colonization bottlenecks can result in reduced clonal diversity (Little and Hebert 1994). In other studies, there was little association between clonal diversity and habitat permanence or latitude (Rossi et al. 1998, Rossi et al. 2008, Adolfsson et al. 2010). Life-​history variation among clones related to environmental characteristics associated with different habitats may explain the coexistence of different clones (Rossi and Menozzi 1993, Martins et al. 2010, Schmit et al. 2013a). Some of the patterns of variation in clonal diversity could also be due to differences in colonization ability (Cywinska and Hebert 2002). Thus, several ecological and genetic factors can potentially explain clonal diversity, and these explanations can differ among different parthenogenetic species. Types of Parthenogenesis in Ostracods Based on the intact inheritance of multilocus genotypes, Chaplin (1992) concluded that reproduction in Candonocypris novaezelandiae was apomictic confirming previous cytological observations (Bauer 1940, cited in Chaplin 1992). Havel and Hebert (1989) found a similar result for subitaneous eggs (eggs developing without a delay); however, diapausing eggs were not tested. Rossi et  al. (2008) confirmed that parthenogenesis for Eucypris virens is apomictic by genotyping clonal lineages from diapausing eggs. However, these results do not preclude the possibility of automixis occurring in parthenogenetic species yet to be studied in detail (Butlin et al. 1998b). The conclusion of apomictic reproduction preserving heterozygosity has been extended to other asexual ostracods, although apomixis has not been directly determined for these species (Schön et al. 1998). Origin of Parthenogenetic Ostracods Heterozygosities similar to related sexual species support a spontaneous origin for parthenogenetic clones for some ostracods rather than involving interspecific hybridization (Chaplin et  al. 1994, Turgeon and Hebert 1994)  and high clonal diversity could be due to (1)  recent multiple origin of asexual clones from related sexuals, some of which may have gone extinct, or (2) more ancient asexual clonal lineages that have diversified due to accumulated mutations (Cywinska and Hebert 2002). Evidence for gene flow involving males from related sexuals mating with asexual females may explain observed high clonal genotypic diversity (Rossi 1998). Turgeon and Hebert (1994, 1995) provided evidence for genotypically diverse polyploid asexual clones that could have been generated by gene flow between parthenogens and related sexual species. They note that if some of the newly generated asexual clones are competitively superior and outcompete the sexuals, then the asexual lineages will have lost an important source of genetic variation. Eucypris virens in areas around the Mediterranean showed strong mating encounters between males and sexual females, but with some rare mating encounters between males and asexual females (Schmit et al. 2013b) that

Parthenogenesis at least support the potential for gene flow between sexual and asexual lineage (Rossi et al. 2008). However, there are currently no examples of laboratory experiments using genetic markers to provide evidence for successful mating resulting in viable progeny. Three parthenogenetic species with no related sexual species had lower levels of clonal diversity compared to several parthenogens with congeneric sexual species (Havel et al. 1990), providing further evidence that the source of clonal diversity could be gene flow with sexual species. The origin of parthenogenetic clonal diversity for E. virens (Rossi et al. 2008, Schön et al. 2000, Adolfsson et al. 2010, Bode et al. 2010) and Heterocypris barbara (Rossi et al. 2007) may also be connected to coexisting sexual populations. The absence of sexual species in the Darwinulidae may explain low levels of genotypic diversity observed for species such as Darwinula stevensoni (Rossi et al. 2004). However, current limits of the power to accurately assess genetic variation suggest that further genetic studies are clearly required to link the origin of parthenogenetic genotypic variation to related sexual species. Genetic Variation within and among Populations of Parthenogenetic Ostracods Initial surveys of parthenogenetic ostracods revealed high levels of genotypic diversity (Table 15.2 in Rossi et al. 1998 provides a list of 39 summaries of clonal diversity for 28 different parthenogenetic species and all but four consisted of multiple clones). An update (Table 9.1) of studies published since that review also shows high levels of clonal diversity even using as few as three polymorphic loci. Many of the sampled populations were multiclonal, some with very high clonal diversity. Three important questions are often addressed: (1) Does the geographic genetic structure of parthenogen populations provide information on dispersal and population connectivity? (2) How widely distributed are individual clones and is there evidence for general-​purpose-​genotypes (GPGs)? (3) What factors maintain within-​population clonal diversity? Parthenogenetic ostracods often consist of clonal genotypes that are rare and restricted to one or a few sites with only a small number of more broadly distributed clones (Havel and Hebert 1989, Rossi et al. 1998, Rossi et al. 2006, Rossi et al. 2008). In contrast, Chaplin and Ayre (1997) concluded a high degree of clonal dispersal for C. novaezelandiae. They found that 13 of the 26 (50%) multilocus genotypes (clones) were limited to one or two populations, suggesting limited dispersal, but six of the genotypes (23%), representing 88% of the sampled individuals, were geographically widespread. Further support for a high dispersal was the absence or weak negative relationship between the proportion of shared clonal genotypes and increasing geographic distance separating pairs of populations over several hundred kilometers. A  similar weak negative relationship has been reported for Heterocypris incongruens (Rossi et al. 2006). A strong negative relationship would be expected if successful dispersal were more likely between adjacent rather than more widely separated sites. However, indirect estimates of dispersal based on population genetic structure can be misleading due to the following: (1) different clones can vary in their ability to disperse and successfully establish in a new habitat; and (2) the same multilocus genotype from different populations may not actually represent the same clone since a small number of polymorphic markers may not accurately reflect clone membership. Conclusions about the underlying causes of observed population structure for parthenogenetic ostracods should be viewed with caution. The observation of widely distributed MLGs might be considered as evidence for GPGs that are adapted to a range of environmental conditions (van Doninck et al. 2002). This interpretation is likely too simple, partially because the same MLG from different populations may not actually represent the same genetic clone. Furthermore, a widely distributed clone may occupy habitats with similar environmental conditions that may also be widely distributed, such as the rice fields occupied by common clones of H. incongruens (Rossi et al. 2006). Most parthenogenetic ostracods show high levels of clonal diversity, and this probably contributes more to their wide distribution than single, broadly adapted clones. One exception is the ancient asexual Darwinula stevensoni that exhibits low

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Total N 270 100 140 141 1,964 403 3,235 816 488 369

Pops 6

5

2

7

34

10

47

28

12

12

Source: An update of Table 15.2 from Rossi et al. (1998).

Species Callistocythere badia Cypridopsis vidua Heterocypris incongruens Darwinula stevensoni Darwinula stevensoni Cypris pubera Heterocypris incongruens Eucypris virens Limnocythere inopinata Eucypris virens 5

2

3

3

3

1

47

3

3

Loci 3

Table 9.1.  Clonal Diversity of Parthenogenetic Ostracod Species.

66

33

214

125

23

7

33

4

42

Clones 8

N/​A

1 -​14

1 -​40

1 -​36

1 -​9

1 -​7

1 -​14

1 -​4

3 -​15

per Pop 2 -​6

Clones

Spain

Italy

Britain, Italy, Spain

Italy

Germany

Belgium, France, Ireland, Spain Europe, Israel, S. Africa

Belgium

Ontario

Location England

Schmit et al. (2013b)

Rossi et al. (2010)

Rossi et al. (2008)

Rossi et al. (2006)

Little (2005)

Rossi et al. (2004)

Van Doninck (2004)

Cywinska and Hebert (2002) Van Doninck (2002)

Reference Hull and Rollinson (2000)

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Parthenogenesis levels of genotypic diversity but has a broad distribution. Van Doninck et al. (2002) compared the tolerances (as measured by survival and mobility) of D. stevensoni from different habitats to a range of salinity and temperature conditions. The genetically monomorphic D. stevensoni showed evidence for broader environmental tolerance than the genetically polymorphic H.  incongruens, providing evidence for GPGs that may also explain their long-​term persistence (van Doninck et  al. 2003). However, additional DNA markers have uncovered variation doubting the existence of broadly distributed clonal lineages of D. stevensoni (van Doninck et al. 2004). More surveys with higher resolution genetic markers, along with additional laboratory experiments, are clearly required to explain the spatial and temporal success of these parthenogenetic species and the role played by GPGs. A variety of processes may explain the coexistence of ostracod clones, including ongoing origin from related sexuals and recurrent colonization from different populations (Cywinska and Hebert 2002). Coexistence could also involve ecological differences among clones; otherwise the clone with the greatest fitness could eventually outcompete all other clones. Differences in life-​history traits could explain clonal coexistence (Rossi and Menozzi 1993, Geiger et al. 1998), and coexistence could also be maintained under conditions of intermediate levels of environmental stress (Martins et al. 2010). Diapausing eggs accumulating in the sediment may act as a reservoir that can restore any loss in genotypic diversity following hatching. Despite short-​term clonal coexistence, parthenogenetic lineages likely have a limited evolutionary life and depend on the continual origin of new clones from related sexual species. In some cases, estimates of clone age can be obtained from extensive genome sequencing, as was recently reported for Daphnia pulex where some individual asexual lineages may be less than 30 years old (Tucker et al. 2013). The ancient asexual Darwinulidae species appear to be an exception to this generalization, requiring further studies to explain their long-​term persistence with no known related sexual species as a source of clonal diversity. Geographical Parthenogenesis in Ostracods Parthenogenetic clones often occupy marginal habitats (higher latitudes and altitudes) where they escape competition from sexuals. Although geographical parthenogenesis has been documented for ostracods (Horne and Martens 1999), the exact reasons are not fully understood. For both E. virens and H. incongruens, sexual populations are confined to areas surrounding the Mediterranean, and parthenogenetic populations are much more widespread at higher latitudes, perhaps a consequence of superior colonizing ability (Horne and Martens 1999). Sexual and parthenogenetic populations are not completely segregated geographically, as both forms coexist around the Mediterranean. Geographical parthenogenesis in ostracods has focused almost exclusively on E. virens that may actually be a species complex (Bode et  al. 2010, Symonoá et  al. 2018). Schön et  al. (2000) confirmed the polyphyletic origin of asexual clones (Fig. 9.8), but Schön (2007) found no evidence for postglacial range expansion, suggesting that more recent dispersal has erased the historical genetic evidence. Sexual populations of E. virens coexist with polyploid clones (Rossi et al. 2008), with triploid clones also found at higher latitudes than diploid asexuals and sexuals, suggesting that higher ploidy is responsible for the observed wider distribution of parthenogens, rather than asexuality (Adolfsson et al. 2010). A variety of features of each pond habitat (pond area, depth, and water chemistry) can be used to separate environmental from geographical associations to explain geographical parthenogenesis. Local environmental conditions played an important role in explaining the distributions of sexuals and asexual E. virens (Schmit et al. 2013a), decreasing the emphasis on historical factors and differences in dispersal potential. Sexual populations were more likely to occupy habitats with shorter, more unpredictable hydroperiods, and different ecological requirements may explain their coexistence in some areas (Schmit et  al. 2013c). Eucypris virens provides an excellent example of the range of ecological, experimental, and genetic approaches required to fully understand geographical parthenogenesis.

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Reproductive Biology Prion Prions1

Extr6 99 100

79 100

69 70

65 89

100 100

80 100

Extr5 Extr2M Extr8M 60 Extr10 64 Extr9M 65 Extr7M Extr11 53 Bram2 98 Leed Bram1 Haan2 Kett Sici2 Sici7 65 Sici5 98 Sici6 Sici4 SiciM Sici1 Haan1 82 Sang1 100 Sang2 Sang Vent3 72 Vent2 100 Vent1 Bram3 Berz1 91 100 Morc Pico Pico2 75 100

Berz2 Pico3 Pico1 Berz3

Asin

Big1

group I

group II

70 61 100 100

Fig. 9.8. Phylogenetic relationship between sexual and asexual Eucypris virens based on ITS1 sequences. Sexuals: all Sici and all Extr except asexual Extr5 and Extr6. All remaining individuals are asexual. From Schön et al. (2000), Fig. 1.   

Parthenogenesis appears to be a successful life-​history strategy for many ostracods, judging by their wide geographical distribution and perhaps even in the very long term with the persistence of Darwinulidae species. Their success can be attributed to high levels of genetic variation derived from related sexual species and likely contributes to adaptation to a variety of environments over wide geographical areas. However, there is little evidence for broadly distributed clones (GPGs) since most surveys found that the majority of individual clones were restricted to single sites. For some species, phylogenetic analyses confirmed multiple origins of clones from sexual populations, including the origins of polyploid clones (Adolfsson et  al. 2010). Furthermore, polyploidy may be a more important factor in explaining the wide distribution of parthenogens than asexuality (Adolfsson et  al. 2010). Earlier studies examined the evolutionary genetics of a wide variety of

Parthenogenesis parthenogenetic ostracods, but more recent studies (since about 2007) have focused almost exclusively on E. virens, which has the advantage of having both sexual and asexual populations. Areas for Future Ostracod Research Ostracods have proven to be an excellent group to study the ecology and evolution of parthenogenesis in the Crustacea because of the many examples of transitions to asexual from sexual reproduction (Chaplin et al. 1994). The diversity of asexual Ostracoda taxa poses more challenges for understanding the origin of parthenogenesis relative to the more taxonomically restricted occurrence of parthenogenesis in the Branchiopoda. Future research should continue to explore ecological and genetic factors to explain the high rate of transition to parthenogenesis, including the more frequent occurrence of parthenogenesis in freshwater compared to marine environments. Both of these avenues of research would benefit from the development and application of genomic tools with wider field sampling to reconstruct the evolutionary history of sexual and asexual modes of reproduction. Parthenogenesis has evolved numerous times, but evidence from phylogenetic studies involving both asexual and closely related sexual ostracod taxa is limited. Ostracod species that include both sexual and asexual forms would be suitable for a phylogenetic analysis, particularly since some may actually be species complexes. Phylogenetic methods have been useful for resolving species relationships within the ancient asexual darwinulids (Martens et al. 2005, Schön et al. 2012). A similar approach for E. virens (Bode et al. 2010, Adolfsson et al. 2010, Symonoá et al. 2018) revealed extensive cryptic diversity among sexual and asexual populations, suggesting a species complex, and confirmed the multiple origins of parthenogenetic lineages. However, the phylogenetic analysis was unable to determine the probable mechanism and timing for transitions to parthenogenesis, and interpretable results may be obscured by undetected sexual and asexual lineages, some of which may have gone extinct. These studies with E. virens can serve as a model for future research on other ostracod groups consisting of both parthenogenetic and sexual species, and would benefit from the additional information from nuclear genes.

PARTHENOGENETIC CLADOCERA Since cyclical parthenogens (see the next section) possess the machinery to alternate between sexual and asexual reproduction, one might expect to find fewer constraints for switching to obligate parthenogenesis in cladocerans than in any other crustacean groups reproducing sexually. Despite this, transitions to obligate parthenogenesis have only been reported in a few of the 620 known species (Taylor et al. 1999): Bosminidae (Bosmina longirostris, Little et al. 1997), Daphniopsis (D. truncata x D. pusilla, Hebert and Wilson 1994), Ctenodaphnia (D. thomsoni, Hebert and Wilson 1994) and in Daphnia (Daphnia pulex complex, Dufresne et al. 2011). The D. pulex complex has been the most widely studied group in Cladocera to understand the origins of transitions to asexuality, the costs of reproduction, and the geographical distributions of parthenogens. Types of Parthenogenesis in Cladocera Cyclical parthenogenesis (CP), the reproductive mode practiced by most cladoceran species, involves alternations between a clonal phase, during which females develop from unfertilized eggs, and a mixing phase where males and females produce haploid gametes, with sperm fertilizing eggs to produce diapausing embryos enclosed in a protective structure modified from the carapace (the ephippium) (Taylor et al. 1999) (Fig. 9.9). Male production is triggered in response to changes in the environment (environmental sex determination), such as increased population density, and both males and females are produced clonally by an abortive meiosis rather than by

259

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Reproductive Biology true mitosis (Hiruta et al. 2010). This reproductive mode allows for the benefits of both sexual and asexual reproductive strategies. The clonal phase allows a rapid exploitation of the water column in summer, and the mixing phase in the fall generates new genotypic arrays against the vagaries of unpredictable future environmental conditions. Despite the ubiquity of this reproductive mode, only a small number of Daphnia lineages have eliminated sexual episodes from their life cycle and produce the diapausing eggs by apomixis, thus leading to the production of all-​female clones with identical genotypes (Innes and Hebert 1988). This reproductive mode has been termed obligate parthenogenesis (OP). Ephippial eggs can also be produced by automixis, as recently shown in Daphnia magna (Svendsen et al. 2015). In this species, some clones readily produce males under fall conditions, whereas other clones specialize in the female function and only produce females (non-​ male producers). Occasionally, these clones produce viable dormant eggs in the absence of males. Genetic comparisons of ephippial offspring with their mothers using both microsatellites and SNPs markers helped determine that these offspring were the result of automixis involving mostly terminal fusion of meiotic products (Svendsen et al. 2015). Additional studies are needed to determine if additional Daphnia species use this form of reproduction and its frequency. Polar populations of the freshwater cladoceran Holopedium gibberum are also thought to reproduce by automixis, as no males were observed in natural populations and extremely low levels of genetic diversity were reported using allozyme analyses (Hebert et al. 2007). Origins of Parthenogenetic Cladocera Obligate parthenogenesis evolved at least four times independently in the D. pulex complex: (1) D. pulex, (2) D. middendorffiana, (3) D. tenebrosa, (4) European D. pulicaria. This species complex has been the focus of a large body of work on the evolution of obligate parthenogenesis. Transitions to obligate parthenogenesis have been attributed to mutations that suppress meiosis during dormant egg formation in females but fail to suppress meiosis during spermatogenesis in males (Innes and Hebert 1988, Hebert et al. 1988). Initial experimental crosses have shown that males carrying these mutations can mate with females and the resulting progeny is about half asexual, as expected under a single dominant gene model (Innes and Hebert 1988). About half of the clones that reproduce by obligate parthenogenesis retain the ability to produce males and thus will transmit these asexual elements to sexual females (Innes and Hebert 1988, Lynch et al. 2008). Meiosis suppressor alleles are known to have spread in natural populations in a contagious fashion and to have generated numerous apomictic clones (Hebert et al. 1993). Initial conversions to asexuality likely took place in northeastern North America between 1,250 to 100,000 years ago and are still ongoing (Paland et  al. 2005, Lynch et  al. 2008, Tucker et  al. 2013). As a result, northeastern populations of D. pulex are obligate parthenogens, central populations are mixed, and northwestern and midwestern populations are cyclical parthenogens (Hebert and Finston 2001). Genome-​wide association studies contrasting obligate parthenogens and cyclical parthenogens of D. pulex revealed that four unlinked regions of the genome residing on chromosomes V, VIII, X, and the entire copy of chromosome IX are almost perfectly associated with asexuality (Lynch et al. 2008, Tucker et al. 2013, Xu et al. 2015). Intriguingly, these “asexuality alleles” are generally present as unique, single alleles within asexual isolates and appear to have been transmitted as a suite to obligate parthenogenetic D. pulex through hybridization with its sister taxon, D. pulicaria. (Fig. 9.10). The exact role of hybridization in the origin of obligate parthenogenesis in Daphnia remains to be determined. The D. pulex complex is notorious for its reticulate history; eight of its 11 taxa include lineages that reproduce by obligate parthenogenesis, and all of these show signs of hybridization (Dufresne and Hebert 1995, Dufresne et  al. 2011). European populations of D.  pulicaria are genetically distinct from their North American counterparts and belong to the other major clade of the D. pulex complex: the tenebrosa clade. In Europe, D. pulicaria inhabits various habitats such as manmade

Diploid resting eggs

Ameiotic reproduction

Diploid eggs

Males

Obligate Parthenogenesis

Diploid resting eggs

Potential to mate with sexual females

  

Fig. 9.9. Reproductive modes in Daphnia. In cyclical parthenogenesis, there is an alternation of asexual reproduction in the summer where females produce subitaneous eggs without fertilization, and a sexual phase in the fall where males and females produce haploid gametes that unite to form the diploid resting eggs. By contrast, in obligate parthenogenesis, females produce unreduced resting eggs. Male production is retained in some of the clones reproducing by obligate parthenogenesis.

Ameiotic reproduction

Sexual females

Males

Cyclical Parthenogenesis

26

15 op 1 op2 4 op2 0 op3 op18 op25 op31 op8 op23 op17 op4 op9 op27 op7 op5 op1 op3 2 op1 0 op1 op 3 6 op op 12 op 3 op 2 29

Reproductive Biology

px

px 3 px1 px1 px2 px2 px10 px10 px5 px6 px6 px5 px7 px7 px4 px4 px8 px8

19 op 26 op 11 op 6 pa 8 op2 pa7 0 op2 pa8 pa13 pa10 pa11

3

CP D. pulex OP sexual background haplotype OP asexual-specific haplotype D. pulicaria

100

0.1

D. pulicaria

100

pa1 pa5 pa2 pa4 pa12 pa9 pa14 pa3 pa6 pa12 pa9 pa1 pa3 4 pa 1 pa pa 2 5 pa 4 pa 7

13 pa 11 pa 8 pa 10 pa

ta

rena

100

100

8 op1p19 0 o p2 o

D. pulex

D. a

px11 px11 px9 px9 7 op1 p7 o 10 op 11 op p1 o 2 op

op13 op15 op21 op5 op6

o op p3 1 op 2 op 4 op 28 2 op3 6 op2 0 5 op3 1 op23 op29 op24 op32 op27 op9 op8

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Fig. 9.10. Neighbor-​joining tree of the phased concatenated haplotypes for 647 SNP sites containing asexual-​specific alleles. CP = cyclical parthenogenesis, OP = obligate parthenogenesis, pa = D. pulicaria, px = D. pulex. From Xu et al. (2015).   

reservoirs, lowland lakes, and alpine lakes. Deeply divergent mtDNA lineages are known to occupy the Pyrenees, the High Tatra Mountains, and lowland areas (Bellati et al. 2014). Populations from the Pyrenees reproduce by cyclical parthenogenesis, whereas those from the High Tatra Mountains and from the Swiss Alps are obligate parthenogens (Dufresne et al. 2011, Dufresne et al. unpublished data). Loss of sex in Daphnia from the High Tatra Mountains has been ascribed to meiotic incompatibilities caused by hybridization between divergent lineages of the D. pulex complex (Dufresne et al. 2011), but the recent finding of the “asexuality alleles” in D. pulicaria from the Alps suggests that hybridization with North American populations of D.  pulicaria could also explain how sex was lost in these lineages (Dufresne et al. unpublished data). Daphnia seem to travel long-​ distances quite easily, as a clone of Daphnia pulex from North America has recently invaded Kenya, likely through accidental human introductions (Mergeay et al. 2006). It is possible that a single initial hybridization event brought the asexuality alleles into a new genetic background and subsequent hybridization events then spread these alleles to various lineages in the complex. In addition to these cases where asexuality is caused by meiosis suppressor alleles, there are known examples

Parthenogenesis of hybrids locked in the parthenogenetic phase, likely due to meiotic incompatibilities. Members of the Daphnia longispina complex include species whose ancestors diverged more than 8 million years ago and that still hybridize readily (Schwenk and Spaak 1995). Hybrids between D. galeata, D. cucullata, and D. longispina have lost the ability to produce resting eggs but can still reproduce parthenogenetically. Obligate Parthenogenesis Associated with Polyploidy In Daphnia, as in many other groups, asexual reproduction is often associated with polyploidy (Dufresne and Hebert 1994, Otto and Whitton 2000). Hybridization events between North American populations of D. pulex and D. pulicaria have occurred repeatedly and have generated triploid clones that are restricted to arctic areas and that reproduce exclusively by obligate parthenogenesis (Beaton and Hebert 1988, Dufresne and Hebert 1994, 1997). The recent finding that males from obligate parthenogenetic clones sometimes produce diploid sperm suggests that triploid clones could have arisen through the union of a haploid egg from a CP clone with unreduced sperm from these rare males carrying the asexuality elements (Xu et al. 2013). A very small number of triploid clones have been found in the Great Lake region, an area that has been extensively sampled (Innes and Ginn 2014). Experimental crosses have confirmed that unions between rare males from OP clones and CP females do generate a high number of clones showing signs of triploidy at some loci (Lynch et al. 2008). Furthermore, whole genome sequencing of three triploid clones from subarctic areas revealed that these clones also harbor the suite of asexuality alleles (Xu et al. 2015). This suggests that asexuality might be an important prerequisite for the evolution of polyploidy in Daphnia. Polyploids are also found in the D. tenebrosa clade and include a majority of triploid clones with some less frequent tetraploid clones (Vergilino et al. 2009). The mode of origin of these polyploid clones has not been determined, but genetic analyses did show divergent mtDNA lineages and high heterozygosity levels in these clones, as expected under a hybridization scenario (Vergilino et al. 2009). Geographical Parthenogenesis in Cladocera Members of the Daphnia pulex complex appear to comply with the geographical parthenogenesis pattern, as lineages that reproduce by OP are prevalent at high latitudes (Dufresne et al. 2011). No cyclical parthenogens from the D. pulex complex have been found north of 55°N (Vergilino et  al. 2009). Daphnia pulicaria from the Alps and the Tatra Mountains are all diploid obligate pathenogens (Dufresne et al. 2011, Dufresne et al. unpublished data). Asexual polyploid clones genetically similar to the D. pulex-​pulicaria hybrids found in the Canadian Arctic are known to occur in the Bolivian Andes and in Patagonia in the absence of diploid counterparts, likely as a result of dispersal by migratory birds (Adamowicz et al. 2002, Aguilera et al. 2007). OP is thought to be advantageous in arctic and alpine environments since the time allowed to reproduction is short and hence females that hatch from dormant eggs can readily invest their resources to produce dormant propagules, rather than sparing a generation of parthenogenesis to produce males that then mate with females to produce the resting eggs meiotically. Interestingly, another cladoceran, H. gibberum, reproduces by automixis in the arctic but by CP in temperate zones, another beneficial way to escape short growing seasons as no males are required (Hebert et al. 2007). The fact that OP is frequently associated with polyploidy raises the question of whether it is asexuality or polyploidy that might be advantageous in extreme environments. Polyploidy may be advantageous to buffer the effects of environmental stressors (cold, UV stress) through increased gene copy (Chao et al. 2013). Alternatively, it could be that polyploid clones are at a selective disadvantage in temperate areas since they typically have lower intrinsic rates of increase than diploid

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Reproductive Biology clones (Weider and Hebert 1987, Dufresne and Hebert 1998) and, as a result, are forced to occupy habitats where diploid clones are rare. Interactions of Parthenogens with Sexuals in Daphnia Despite a wealth of studies identifying the genetic factors involved in the loss of sex in Daphnia (Lynch et al. 2008, Eads et al. 2012, Xu et al. 2013), we still lack information on the ecological factors that lead to the displacement of the sexual D. pulex populations by the asexual clones. These clones are known to co-​occur regionally and locally with the sexual lineages (Hebert and Finston 2001). Theory on the evolution of sex stipulates that, with equal survival and fecundity, sexuals should be replaced by asexuals given the twofold costs of sex (Williams 1975). It is not clear how much Daphnia pay for producing males. Sexual clones likely incur a small cost to produce males since males are only produced at the end of the clonal phase and are very short-​lived (Decaestecker et al. 2009). The cost could also be reduced if sexually reproducing females outnumber males, but sex ratio and sexual selection is an under-​studied area within Daphnia. Furthermore, a survey indicated that roughly 60% of the clones reproducing by CP were male producers, the other clones specializing in the female function (Lynch et al. 2008). By contrast, nearly half of the obligate clones retained the ability to produce males, hence their advantage over sexuals is somewhat reduced (Lynch et al. 2008). Another study reported higher rates of male production in cyclical than in obligate parthenogens (Innes et al. 2000). The higher male production of these clones appeared to have been compensated by an increased fecundity and/​or survivorship relative to the obligate parthenogens, as no replacement of sexuals by asexuals occurred during a 40-​day mesocosm study (Innes et al. 2000). Recent evidence suggests that all males derived from obligate parthenogens may not be equally proficient at faithfully transmitting the genetic determinants of meiosis suppressors since many of them produce aneuploid sperm (sperm with missing chromosomes), and a third of laboratory crosses between males from OP and CP females did not produce offspring (Lynch et al. 2008, Xu et al. 2013). Theoretically, provided there are no immediate costs to the obligate parthenogens, they should replace cyclical parthenogens within 100 generations (Lynch et al. 2008). Long-​term studies of ponds in areas where both facultative and obligate parthenogens co-​occur are ideal for understanding the dynamics of the expected displacement of sexuals by asexuals. Such studies have been carried out by Innes and Ginn (2014) in the Great Lake area over an 18-​year period. The focus of their study was a pond dominated by cyclical parthenogens in an area where 97% of the ponds contained exclusively asexual populations. Frequent flooding of a nearby river facilitated dispersal of the asexual clones, and genetic analyses indicated that different asexual genotypes did invade the pond over the years but have remained at very low frequencies (Innes and Ginn 2014). The failure of the invasion to progress could be caused by the inability of a small number of invading asexual clones to directly compete with the genotypically diverse resident sexual population. In addition, the monopolization hypothesis predicts that a much larger resident population monopolizes resources and may be better adapted to local conditions, and this hypothesis has been proposed as a mechanism to explain the low establishment success of invaders despite high rates of dispersal (De Meester et al. 2002). Another possible impediment to the conversion of a sexual population to asexual is if the invading asexual clones fail to produce males and/​or if these males produce aneuploid sperm. However, successful invasions may also be facilitated by periodic bottlenecks of the sexual populations, resulting in reduced fitness through inbreeding depression, which would favor more outbred asexual clones (Haag and Ebert 2004). Genetic Variation within and among Populations of Parthenogenetic Daphnia The polyphyletic origins of meiosis suppressors in North American populations of D. pulex have resulted in the creation of hundreds of clones spanning largely disjunct distributions in the eastern

Parthenogenesis and mid-​continental portions of North America (Hebert and Finston 2001). Hence these obligate parthenogens have captured and frozen high levels of genetic diversity from their sexual ancestors. While clonal diversity is typically regionally high, it is locally low as compared to cyclical parthenogens (an average of 1.8 asexual clones per pond in subarctic areas; Weider and Hebert 1987). Surveys of asexual Daphnia have shown that a few common asexual genotypes have very wide geographic distributions, spanning over a thousand kilometers, whereas many other clones have more restricted distributions (Dufresne and Hebert 1995, Weider et  al. 1999, Pantel et  al. 2011). These common clones may be broadly adapted to a wide array of environmental conditions, i.e., may have a GPG or their preferred habitat may be widespread (Lynch 1984). A recent study has shown that clonal dominance is not explained by high intrinsic rates of increase in the laboratory (Holmes et al. 2016). Few experiments have assessed whether clones have broad or narrow tolerance to a suite of environmental factors and if this can explain their distributions (but see Jose and Dufresne 2010). Ecological surveys have shown that clones are strongly associated with environmental variables such as salinity, temperature, food, and predators (Loaring and Hebert 1981, Weider and Hebert 1987, Wilson and Hebert 1992, Aguilera et al. 2007, Jose and Dufresne 2010). This pattern is expected if strong interclonal selection acts to retain the best clones under specific environmental conditions, as exemplified with the frozen niche variation hypothesis (Vrijenhoek 1979). Genomics of Parthenogenesis in Daphnia Whole genome sequencing has revealed that the genes residing in the four genomic regions associated with asexuality in Daphnia have characteristic roles in meiosis (Lynch et al. 2008). One of these candidate genes, REC8, was found to differ greatly between sexuals and asexuals. This gene is essential for meiotic sister-​centromere cohesion, as it helps keep the sister chromatids associated during meiosis (Nasmyth 2001). All obligate asexual clones carried an allele containing an identical upstream insertion of a transposable element as well as a frameshift mutation, both of which were completely absent from sexual lineages. It is tempting to speculate that the mutations that have disrupted the function of this gene have caused the transitions to OP in Daphnia. Interestingly, clones of D.  pulicaria do not possess the REC8 insertion (Eads et  al. 2012). The 200kb region associated with OP has been probed to identify other genes that may be involved in the transitions to asexuality (Xu et al. 2015). Many genes involved in DNA replication, repair, recombination, cell cycle, spindle formation, and chromatin assembly were found (Xu et al. 2015). Other genes involved in male production and in the activation of unfertilized diploid resting eggs should also be present in these regions but have yet to be identified. Transcriptome studies comparing obligate and cyclical parthenogens may reveal dosage-​sensitive genes that play a role in the transition. Areas of Future Research in Cladocera While chromosomal regions associated with asexuality have been identified, we still do not know much about the functional roles of the genes residing in these regions, i.e., if they are the cause or the consequences of apomixis. Transcriptional studies on sexual and asexual females would help shed some light on gene function. Results from genomic studies have suggested that the asexual clones could be much younger than previously thought (less than 1,250  years, as opposed to 150,000 years). Asexual Daphnia lineages are expected to have a limited lifespan, doomed due to high rates of gene conversions resulting in loss of heterozygosity and exposure of preexisting deleterious alleles. Luckily the continuous injection of new clones from sexual species would ensure the persistence of asexual clones in nature. Considerable insights on the temporal dynamics of this process could be gained from sediment dating of asexual resting eggs.

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OTHER PARTHENOGENETIC CRUSTACEA Although parthenogenetic crustaceans are primarily found in the Branchiopoda and Ostracoda, sporadic occurrences have been documented in the Malacostraca. These include the common woodlouse Trichoniscus pusillus (Isopoda). Based on sex ratio data, a survey in the British Isles discovered that most sites consisted of a mixture of sexual individuals (diploid T.  pusillis provisorius) and asexual (triploid T. pusillis pusillis) females (Fussey 1984). No geographic pattern in the occurrence of the parthenogenetic form was evident, but there was an association of the sexual form with calcareous soils. Further studies provided evidence for the multiple origins of four triploid clones and that different clones were associated with different microhabitats characterized by different soil types and moisture (Christensen et al. 1988). The only other documented cases of parthenogenetic Malacostraca are crayfish (order Decapoda). The spiny-​cheek crayfish Orconectes limosus, which reproduces by facultative parthenogenesis, was introduced to Europe from North America and is considered a serious invader (Buric et al. 2011). Parthenogenesis was confirmed in laboratory experiments where females were isolated from males. It is not known how often parthenogenesis occurs in nature, but it is likely rare since populations appear to conform to Hardy-​Weinberg equilibrium as expected for sexually reproducing populations (Buric et al. 2011). The marbled crayfish (Procambarus fallax forma virginalis) is triploid and reproduces by obligate apomictic parthenogenesis (Martin et al. 2015). MtDNA genes confirmed the phylogenetic relationship to sexual P. fallax (Scholtz et al. 2003). Martin et al. (2015) suggested that the origin of the triploid asexual involved the initial formation of diploid parthenogens (but not involving hybridization), followed by the fertilization of diploid parthenogenetic eggs by haploid sperm from related sexual males. The asexual marble crayfish is only known from the aquarium trade but has been released in Europe, into other areas (Madagascar), and is an invader with the potential for negative consequences for native crayfish species. A genomic analysis (Gutekunst et al. 2018) confirmed a very recent origin of a single clone. The triploid genome consists of two almost identical P. fallax genomes and a third more distantly related P. fallax genome consistent with fertilization of an autopolyploid egg. The marbled crayfish can therefore serve as a valuable model for studying the evolution of a clonal genome. Another native North American crayfish (Procambarus clarkii) has invaded China, where it consists of both sexual and parthenogenetic individuals (Yue et al. 2008). Based on five microsatellite loci, the four clones clustered with sexual individuals, suggesting a recent origin. Some genetic or environmental aspect of the invasion may have triggered parthenogenesis since asexual reproduction has not been observed for this species in other areas. Other reports, such as species in the parasitic Tantulocarida subclass within the class Maxillopoda (Boxshall and Vader 1993, Huys et al. 1993) and the amphipod Corophium bonnelli (Moore 1981), suggest that parthenogenesis may be more widespread within other crustacean taxonomic groups and deserves closer examination.

FUTURE DIRECTIONS There has been much progress in understanding parthenogenesis in the Crustacea, and this information has formed a major component of the efforts to explain the evolutionary advantages of sex given less costly asexual alternatives. The basic geographic distribution of sexual and parthenogenetic Artemia has been determined across wide areas of Europe and Asia, providing a resource for detailed sampling on a local scale where sexual and parthenogenetic forms coexist. However, the remote, isolated areas in central Asia can be difficult to sample, and many areas have been invaded by the American sexual species, A. franciscana, that may be in the process of eliminating

Parthenogenesis resident populations before they can be studied in detail (Eimanifar et al. 2014, Pinto et al. 2014). Therefore, more easily accessible areas that can shed light on the origin of parthenogenetic lineages should be sampled before similar invasions and disturbances remove this opportunity. Samples of diapausing cysts represent an important resource that can be deposited in the Artemia Reference Collection (Ghent University, Belgium). An increasing number of studies have resolved phylogenetic relationships among sexual and parthenogenetic Artemia, suggesting hypotheses for the origin of diploid and polyploid parthenogens. These studies should be complemented with a better understanding of the environmental and genetic factors explaining the geographical distributions of sexual and parthenogenetic populations, including the role of polyploidy. Understanding the origin of parthenogenetic ostracods has also benefited from phylogenetic reconstructions with related sexual species. However, the exact mechanism for the evolution of parthenogenetic ostracod lineages has yet to be determined. In both Artemia and Daphnia, matings between rare males produced by parthenogenetic females and sexual females provide a potential mechanism for producing new asexual clones, but no such males have been reported in parthenogenetic ostracods. There is only some suggestion that sexual ostracod males can mate with parthenogenetic females to generate new clonal genotypes. More detailed genomic sequencing may shed further light on exactly how parthenogenetic lineages have originated. Genomic sequencing may also resolve the question of whether or not Darwinulidea are ancient asexuals. Further surveys of marine ostracods would also be useful to confirm the lower frequency of parthenogenetic forms in marine environments. Additional sampling over wide geographic areas with an increased number of genetic markers would assist in determining if observed geographical parthenogenesis is due to asexuality or polyploidy. Such studies would also help resolve any species complexes that may be obscure and may contribute to misinterpretations of geographical patterns. Our knowledge of factors involved in the transitions to parthenogenesis is far more complete in Daphnia than in other crustacean groups, owing to its small genome and to the large community of limnologists and evolutionary biologists interested in this group. Past allozyme surveys have provided initial screens of reproductive mode in a large number of Daphnia species and have flagged potential cases of apomixis. As previous studies have been limited to the D. pulex complex, studies examining other parthenogenetic species such as Daphnia thomsoni from Australia would help ascertain if different paths to asexuality exist. Additional genomic data from other crustacean “non-​model” species will help determine how general the contagious spread of meiosis suppressor genes is, as well as the importance of hybridization for the success of parthenogenetic Crustacea.

CONCLUSION Most crustaceans reproduce sexually; however, parthenogenesis avoids many of the costs associated with sex, and studies on parthenogenetic crustacean species have contributed to a better understanding of the evolutionary relationship between sexual and asexual reproduction. Parthenogenetic Artemia are only found in Europe and Asia, with a much wider distribution than related sexual species. Polyploid (3n, 4n, 5n) parthenogenetic females reproduce by apomixis, but diploid parthenogens by automixis, occasionally producing males. These rare males likely play a role in the origin of new clonal lineages involving mating with sexuals, consistent with phylogenetic evidence for a polyphyletic origin of the parthenogens. Competition experiments found that parthenogens almost always outcompeted sexuals, but coexistence in natural habitats was linked to differences in adaptation to temporal and spatial variation in temperature and salinity. Parthenogenetic ostracods also consist of diploids and polyploids, but all appear to reproduce by apomixis. In some cases, parthenogens show very high levels of clonal diversity, possibly resulting from gene flow with related sexual species, consistent with a polyphyletic origin. A  common

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Reproductive Biology observation is the restricted distribution of most clones to one or a few sites and a minority of more broadly distributed clones. However, accurate assignment of individuals from widely separated areas to particular clones may be limited by the number and variability of the genetic loci used. Parthenogenetic E. virens shows a much wider geographic distribution compared to the sexuals, a pattern referred to as geographical parthenogenesis. However, triploid clones showed a wider distribution than diploid clones, suggesting that differences in distribution may be more of a function of polyploidy than asexuality. Sexual and parthenogenetic E. virens differ in life histories that probably explain their coexistence in some areas and the observed differences in their distribution. Most cladoceran species reproduce by cyclical parthenogenesis (CP) involving an alternation between asexual and sexual phases. Only a few species have dispensed with sex and independently made the transition to obligate parthenogenesis (OP). Much of the research has focused on the Daphnia pulex complex with at least four independent transitions to obligate parthenogenesis. Within D. pulex, the origin of OP involves hybridization with the sister species D. pulicaria. Rare males produced by some OP clones have mated with sexual D. pulex females, transmitted the genes for suppressing meiosis, and repeatedly generated new OP clones. Hybridization events have also generated polyploid clones restricted to arctic and subarctic areas, with sexual populations restricted to more temperate habitats where they coexist with diploid OP clones. Some sexual populations of D. pulex coexist with a low frequency of asexual clones. The greater genetic diversity of the sexual populations may be preventing or retarding a successful invasion and replacement by asexual clones. Crustacean species represent a diversity of model systems to explore the ecology and evolutionary genetics of parthenogenesis utilizing natural populations and laboratory experiments. These three major groups differ on a number of characteristics associated with parthenogenesis. The incidence of transitions appears much higher in Ostracoda than in Cladocera and Artemia. One might have expected to observe a higher incidence of obligate parthenogenesis in species that reproduce by cyclical parthenogenesis, as is the case in the vast majority of cladocerans (but not in ostracods and Artemia), but representatives of only two of 13 cladoceran families reproduce by OP. In Artemia, transitions to parthenogenesis have been limited to a species collectively known as A. parthenogenetica. Contagious modes of asexuality involving rare male production by parthenogens appears to be the case in both Daphnia and Artemia but has yet to be documented in ostracods. Hybridization associated with the origin of parthenogenesis has only been confirmed in Daphnia. In Artemia, diploid clones have recently been found to reproduce by automixis, whereas polyploid clones reproduce by apomixis. As this was only detected using a combination of high-​ resolution markers, it is possible that it is also the case in ostracods since these types of analyses have not yet been carried out. Major differences between these three crustacean groups also lie in their sex-​determining mechanisms. Ostracods display an XY system with males being the heterogametic sex, Artemia with a ZW system (females, the heterogametic sex), and Daphnia with no sex chromosomes. A common pattern in all three groups is the wider geographical distribution of asexuals, though it is not yet clear if this is due to the association between polyploidy and apomixis. Additional work comparing niche characteristics of sexuals, diploid asexuals, and polyploid asexuals is needed to better comprehend ecological factors associated with the distributional success of apomicts.

ACKNOWLEDGMENTS We would like to thank our many students and colleagues who have contributed to our research on parthenogenesis over the years. We also thank the Natural Sciences and Engineering Research Council Canada for grant funding in support of this research. Continuing support from Memorial University of Newfoundland and Université du Québec à Rimouski is also gratefully acknowledged.

Parthenogenesis

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10 OVERVIEW OF THE MATING SYSTEMS OF CRUSTACEA

Alexandre V. Palaoro and Jan Beermann

Abstract Due to an exceptional variety of habitats, body plans, and lifestyles, crustaceans exhibit a wide array of mating systems. Some groups engage in simple, pure-​search polygamous systems in which males usually search for receptive females. In other groups, males defend valuable resources to attract and/​or guard females to ensure paternity. Some species have developed highly complex systems of harem defense polygyny and monogamy, even cases of sub-​and eusociality are reported. The expression of mating systems does not seem to be uniformly correlated to taxonomic affiliation, but is rather diverse within certain groups, suggesting that the evolution of mating systems is largely facilitated by the lifestyle of the species. Despite the broad range of mating systems in crustaceans, and although some groups have been studied comparably well, there remains a lack of knowledge about the behavioral and sexual biology of many species. In the light of the high diversity of lifestyles, mating systems, and habitats of certain groups, crustacean species would be ideal models to unravel the evolution of reproductive strategies and social behaviors.

INTRODUCTION Mating systems can be defined as the circumstances under which mating and fertilization occur within a species. This includes the direct processes of both mating and fertilization and also comprises the role and number of individuals involved. The categorization of sex roles allows for linking mating systems to sexual selection theory: if we know who mates with whom, we can examine how individuals differ in the number of mates acquired (i.e., variance in mating success) due to the mating system, allowing for conclusions about selective pressures on the sexes (Shuster 2007). In the current literature, mating systems are usually perceived in two different ways:  one addresses genetic relationships between the mates and employs terms such as random mating, Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology positive assortative mating (inbreeding), and negative assortative mating (outbreeding). The second use of mating system derives from the field of behavioral ecology and is mainly focused on, but not restricted to, the number of mates for each sex within a defined period (e.g., a single mating season or over a lifetime; Shuster and Wade 2003). Two well-​known terms from the latter application of mating systems would be “monogamy” and “polygamy” (single mate for both sexes vs. several mates for at least one of the sexes). Polygamy can be further differentiated into polygyny (females mating once and males mating multiply), polyandry (females mating multiply and males mating once), polygynandry (both sexes mating multiply, with emphasis on males), and polyandrogyny (both sexes mating multiply, with emphasis on females; Kokko et al. 2014). Although useful, the latter terms only cover the number of individuals involved in mating interactions. They do not, however, describe the acquisition of mates, or how the mating system may be affected by the spatial and temporal distribution of potential mating partners (Kokko et al. 2014). The parental investment theory (PIT) provides a theoretical perspective on the categorization of mating systems (Fisher 1930, Bateman 1948, Trivers 1972). According to PIT, female reproduction is limited by the availability of resources needed for developing oocytes and rearing juveniles, i.e., gonadal investment and parental care. Since females produce fewer and more expensive gametes than males, male reproduction should be directly limited by the spatiotemporal distribution of sexually receptive females. By extension, male reproduction should be indirectly limited by the availability of the essential resources necessary for female reproduction. In a broader context, the sex that provides parental care limits the reproduction of the other sex that does not provide parental care. Hence, this determines the “typical” sex roles that are found in nature, where usually the females care for the eggs and limit the reproduction of males, which, in turn, often do not care for the offspring and would compete for access to females or resources vital to females (Trivers 1972). Emlen and Oring (1977) further developed this concept with two ideas: operational sex ratio (OSR) and environmental potential for polygamy. The OSR is the ratio of potentially receptive males to receptive females at any given time. If OSR > 1, there are few females available for mating and competition between males should be strong, whereas if OSR < 1, competition between males should be reduced and sex roles may even be reversed. The environmental potential for polygamy, on the other hand, measures the economic defensibility of a mate, or of resources vital to the mate: e.g., as females become receptive more asynchronously and (or) occur in patches, they become easier to monopolize (i.e., higher economic defensibility), which leads to a higher environmental potential for polygamy. By merging OSR and environmental potential for polygamy, Emlen and Oring (1977) were able to categorize mating systems based on the ecological and behavioral potential to monopolize mates and on how monopolization occurs. Due to their enormous diversity of species, body plans, lifestyles, and behaviors, crustaceans represent an excellent and exciting group to study mating systems (Martin and Davis 2001). For example, the range of body sizes in crustaceans spans from tiny planktonic copepods to the largest known terrestrial invertebrate species, the anomuran Birgus latro. Crustaceans also inhabit a variety of ecosystems (freshwater, marine, and terrestrial systems) and extreme environments including abyssal water depths and hydrothermal vents (Schram 2013). In this chapter, we provide an overview of crustacean mating systems and the respective sex roles from an evolutionary perspective. We follow this with a discussion of the primary ecological drivers that tend to be associated with various types of mating systems. In general, we followed the classifications of Emlen and Oring (1977) with a few modifications (e.g., monogamy) that are explained as they appear in the text.



Overview of the Mating Systems of Crustacea

OVERVIEW OF MATING SYSTEMS Pure-​Search Polygamy Pure-​search polygamy encompasses mating systems that are settled by scramble competition. This competition for females (seldom for males) is based on finding a mate quickly, copulating, and then moving on to the next mate. It is usually illustrated as a race where the fastest, most efficient competitor has the highest mating success. However, the temporal and spatial positioning of the sexes (i.e., population densities) can affect the strategy that males use to find females. When population densities are high, individuals may not need to invest in behavioral adaptations (i.e., searching) or morphological structures (e.g., sensory appendages); as potential mates occur in direct vicinity, there is no need to search. Additionally, female receptivity can be synchronized, which may cue individuals to form mating aggregations, sometimes referred to as “explosive breeding.” As individuals do not have to search great distances, sexual dimorphism is particularly low. However, females tend to be larger than males because their reproductive success is linked to the number of eggs they produce, which typically correlates positively with body size (see Chapter 11 in this volume). Furthermore, males tend to be slightly smaller in size due to their higher motility (Blanckenhorn 2000). Smaller bodies are able to move faster through the water, allowing for a faster encounter of potential mates and thus higher reproductive success, such as in free-​living copepods (e.g., Dioithonia oculata; Ambler et al. 1991) and in some free-​living amphipods (e.g., epimeriids and iphimediids; A in Fig. 10.1). One way to increase population densities is to form mating aggregations, such as those reported for anostracans (Artemia) and diplostracans (Cladocera). In Artemia, males constantly swim in the water column, while adult females join males only when they become receptive (Pearse 1913, Wiman 1979). Receptive females thus rarely swim in dense male aggregations (Wiman 1981, Belk 1991), which skews the OSR toward males. Interestingly, when researchers manipulated the OSR in the laboratory to an even ratio, a large number of females were found unmated, whereas when the OSR was skewed toward males, all females were mated (Belk 1984, Sugumar 2010). This pattern may be due to limited amounts of sperm, or to a longer time needed for males to detect suitable mates when there is an even sex ratio. After successful copulation, anostracan males then continue to swim in the water column searching for new mates, whereas mated females decrease their swimming speed and rest near the bottom until the eggs are released (Pearse 1913, Wiman 1979). In cladocerans, females usually reproduce through parthenogenesis (see Chapter 9 in this volume), but sexual reproduction occurs under specific environmental conditions (Larsson 1991, Innes 1997). Under harsh environmental conditions, females produce males, allowing for sexual reproduction (Larsson 1991, Innes 1997), such as in Moina affinis and Daphnia magna (Ratzlaff 1974, Young 1978). In most species, the sexually dimorphic, smaller, and more active males attach to the carapace margins of the female, engaging in a copulatory amplexus (Damme and Dummont 2006, La et al. 2014). When population densities are lower, finding a mate becomes more difficult. Therefore, the reproductive success of those males that search more efficiently for mates is increased. Besides smaller body sizes in the (highly motile) males, this also selects for two further strategies: well-​developed sensory organs to detect receptive females and mate guarding. Male shrimps often exhibit a larger number of sensory structures on the antennae, which may allow them to find females more quickly (Bauer and Martin 1991, Bauer and Caskey 2006, but see Sardà and Demestre 1989). Free-​living planktonic copepod males also have more aesthetascs on their antennae, facilitating the detection of pheromones and/​or hydrodynamic cues (Boxshall 1998, Kiørboe 2007, Hirst and Kiørboe 2014). Males of many free-​living amphipods have well-​developed sensory organs, such as in the bathyporeids and lysianassoids (i.e., long antennae with aestethascs and/​or calceoli, enlarged eyes; B in Fig. 10.1) which improves their ability to detect receptive females (e.g., Moore 1981, Borowsky

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(B)

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Fig. 10.1. Differences in sexual dimorphism and mating systems in peracarids and decapods. Male amphipods that do not engage in mate-​guarding but in pure-​search polygamy usually feature smaller body sizes and enlarged sensory organs—​such as (A) in the Iphimedia cf. obesa; males are markedly smaller than females (in situ photograph of the copulation; Oslofjord, Norway). (B) In the lysianassoid Tryphosella sarsi adult males can clearly be distinguished from conspecific females by the longer second antenna that bears calceoli and aestethascs to detect receptive females (specimens caught with a baited trap at the island of Helgoland, North Sea, on July 25, 2011). (C) In decapods with female-​defense polygamy mating systems, males are usually larger and possess larger claws than females. Males guard females that are close to molting by positioning themselves on top of the female, such as the males of Cervimunida johni (Anomura) that stay on top of the females in a “cradle-​like” position, aggressively displacing intruders to secure mating with one claw while holding the female with the other claw. See color version of this figure in the centerfold. (A) Photo courtesy of Lill Haugen; (C) photo courtesy of Ivan L. Hinojosa.   

1986, 1991, Conlan 1991). Hence, this sort of adaptation seems widespread in individuals that engage in prolonged search behaviors. In pure-​search systems where mating opportunities are scarce, the costs of finding a mate may favor a short mate-​guarding strategy. For example, the gonochoristic branchiopod Lynceus brachyurus inhabits ephemeral ponds in which the sex ratio is more balanced than in other congeners.



Overview of the Mating Systems of Crustacea

Males may occasionally take over paired females by clinging either to the other side—​i.e., the side not occupied by its opponent—​of the female’s carapace or the carapace of the opponent, similar to a tandem formation (Sigvardt and Olesen 2014). Androdioecious clam shrimps (Eulimnadia) also display an interesting mate-​guarding behavior because males guard hermaphrodites (usually) for short periods. Males can detect the hermaphrodite’s receptivity only through clasping; when the hermaphrodite is receptive, the male stays until the eggs are fertilized. Since hermaphrodites are more abundant than males, and they can wait for a male to appear, the chance of finding a new mate may be higher than waiting long periods for the hermaphrodite to mature (Weeks and Benvenuto 2008). Dendrobranchiate shrimps can also display a short mate-guarding, depending on the female molt status. Females exhibit a specialized sexual appendage, the thelycum, where sperm is stored after mating (Bauer 1991). Females can have an open thelycum (such as Litopenaus or the families Aristeidae and Solenoceridae), which allows for mating without molting, or they can have a closed thelycum (e.g., Penaeus, Farfantepenaeus), which is found in females that mate shortly after the molt (Bauer 1991). In closed-​thelycum females, males might need to guard the female for a brief period before the molt to ensure paternity. Therefore, short mate-​guarding periods are expected when females synchronize their receptivity with their molt status. In general, intrasexual aggression in species with pure-​search polygamy is rare (Bauer 1996, Asakura 2009), but sperm competition is common. Both sexes mate with more than one partner, and strategies to ensure male paternity can be found. Several dendrobranchiate shrimps use sperm plugs to prevent other males from copulating with the female (e.g., Marsupenaeus, Rimapenaeus; Bauer 1991, Bauer and Min 1993, Fuseya 2006). This kind of strategy should occur whenever sperm competition is strong. However, females of other species can also store the sperm (e.g., copepods Calanus spp., Eurytemora affinis; Marshall and Orr 1955, Katona 1975, respectively) or mate every reproductive cycle (e.g., copepods Acartia tonsa, Temora stylifera; Wilson and Parrish 1971, Ianora et al. 1989, respectively) and do not seem to have any sort of postcopulatory mate guarding. For example, oniscid isopods have lost the precopulatory amplexus, probably in the course of their evolutionary shift from an aquatic to a terrestrial lifestyle (reviewed in Zimmer 2001). A  possible explanation could be that oniscid females can store sperm, such as in Porcellio, Venezillo, and Armadillidium. They mate with several males, resulting in sperm competition and multi-​paternal broods with no postcopulatory guarding (Lueken 1968, Sassaman 1978, Johnson 1982, 1985, Longo et al. 2011). Either the guarding of females became too costly on land, and/​or males cannot ensure paternity and thus increase their fitness by finding and mating with a higher number of females. Although commonly occurring in free-​living species, some parasites also exhibit a prolonged search mating system. In the obligate fish ectoparasites, the Branchiura, the mating system is driven by characteristic shifts in sex ratio during development. In the early stages, males are more abundant and have larger body sizes than females. When females mature, however, males of the same age are smaller in size and less abundant than females and sex ratios become female-​biased (Pasternak et al. 2004). This pattern is probably caused by an increased mortality of males during mate search, as mature males are more motile and actively change hosts to find receptive females (Mikheev et al. 2015). After copulation, females detach from the host and search for a good substratum (e.g., rocky bottoms) to deposit their eggs, where these develop into metanauplii. During this search, females face a higher mortality than males and the sex ratio thus turns to 1:1 again. Overall, reproductive costs are assumed to be similar between the sexes: males face a higher mortality before and during the copulation, whereas females have higher mortality after copulation (Mikheev et al. 2015). In barnacles, the choice of a settling location may be regarded as a form of “mate-​searching behavior” because that choice may depend on the characteristics of the assemblage. In most simultaneous hermaphrodite barnacles, mating success largely depends on the distance to neighboring individuals and penis length (Yuen and Hoch 2010, Ewers-​Saucedo et al. 2015). Some thoracican barnacles, however, exhibit hermaphroditism, dioecy, and androdioecy in which pure male forms

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Reproductive Biology coexist with hermaphrodites (see review of Kelly and Sanford 2010 and Chapter 8 in this volume). Androdioecy is apparently confined to species with only limited mating opportunities (i.e., small assemblages), such as in symbionts/​epizoic species (e.g., Yusa et al. 2010, 2012, 2015). Here, sex determination (i.e., hermaphrodite or pure male) seems to depend not only on genetic factors (not all cyprids can become pure males), but also on environmental factors: cyprids that settle on a conspecific hermaphrodite become pure (dwarf) males, whereas cyprids that settle in isolation always become hermaphrodites (Svane 1986, Yusa et al. 2010, 2015, Høeg et al. 2016, Ewers-​Saucedo et al. 2016). The decision on where to settle thus has major fitness implications and may be considered a mate-​searching strategy. Resource-​ and Female-​Defense Polygamy Defense-​based polygamy systems are usually based on a male defending a resource, or the female itself, to reproduce. We consider them as sub-​parts of the same category because these mating systems usually present the same pattern:  a large variance in male fitness (i.e., one male mates with several females, while the other males mate with one or none) with OSRs highly skewed toward males. Since the resource is usually important for female reproduction (e.g., defense from predators, Christy 2007) and males need to ensure their paternity, fighting is common. Hence, selection for traits such as weapons that increase male fitness by monopolizing access to females is widespread (Emlen 2008). For instance, most decapods present highly sexually dimorphic body sizes and claws (e.g., lobsters, crayfish, fiddler crabs; Christy 2007, Asakura 2009). Consequently, defense-​based polygyny is by far the most common mating system found in decapods (Asakura 2009). Similar patterns can be found across crustacean taxa. Benthic and parasitic copepod males (e.g., Harpacticoidea, Pennellidae, respectively) bear larger appendages for grasping the females (e.g., maxillipeds, antennae, antennules; Parastenocaris phyllura, Tachidius discipes; Glatzel and Schminke 1996, Dürbaum 1997, respectively). Males of many amphipod species have enlarged second gnathopods to fend off competitors while guarding receptive mates (see Borowsky 1984, Conlan 1991, Johnson et al. 2001). Crustaceans usually guard the females using one of two approaches: direct guarding of the female, or controlling the access to the female in some sort of dwelling. Both types can select for similar morphologies (e.g., the claw dimorphism in lobsters and in portunid crabs), but they can predispose groups to different evolutionary pathways (see section “Drivers of Mating Systems”). However, directly guarding the female is more variable than guarding access to the female. For instance, male hermit crabs monopolize the female by grasping its shell and dragging it around (Asakura 2009), brachyurans (and some anomurans) stay on top of the female in cradle-​like position until it molts and they copulate (C in Fig. 10.1; Christy 1987), and many free-​living amphipods carry the female with the first pair of gnathopods (and sometimes the fifth pereopods in caprellids; A  in Fig. 10.2). Some cumaceans also perform a precopulatory embrace (Gnewuch and Croker 1973), and males of the isopods Jaera hopeana and Iais pubescens are even reported to carry around and mate with early manca stages and juveniles (Veuille 1980, Franke 1993, Thiel 2002). Parasitic poecilomastoid copepods also cling to the female to mate, but since males are smaller than females, males cannot carry females around. Instead, males stay attached to the female until the female molts (B in Fig. 10.2). Guarding the female in a dwelling or a territory is more straightforward than guarding the female directly. Males block access to the females and fend off competitors. Most crayfish and lobsters stay at the entrance of the burrow (or near it) (Atema et al. 1979, Berrill and Arsenault 1984, Ra’anan and Sagi 1985). In tube-​or burrow-​dwelling amphipods, “cruising males” usually guard the mate by attending and/​or sharing the tube with the female (C in Fig. 10.2; reviewed in Borowsky 1984, 1991, see Caine 1991, Conlan 1991, Takeshita and Henmi 2010, Takeshita et al. 2011,

Moore and Eastman 2015 and references therein). Cruising males that use tube sharing to guard (A)

(C)

(B)

(D)

Fig. 10.2. Female-​defense polygamy in various crustacean groups. (A) In freshwater amphipods of Parahyalella penais, males display a precopulatory mate-​guarding behavior in which males grab and carry the female until it is ready to molt and copulate. A similar behavior can be found in (B): a parasitic poecilomastoid copepod male clings to an egg-​sac bearing female until she molts—​males cannot carry females due to their smaller size. Males also defend access to the female. (C) An unidentified stenothoid male amphipod attending a female and fending off potential competitors (in situ photo near Ørsta, northwestern coast of Norway). Note, the female has greenish, dorsal translucent eggs. (D) Male fiddler crabs (shown as Leptuca terpsichores) build burrows and defend them against intruders while signaling (“claw-​waving”) to attract females. See color version of this figure in the centerfold. (A) Photo courtesy of Ivan L. Hinojosa; (B) photo courtesy of Arthur Anker; (C) photo courtesy of Lill Haugen; (D) photo courtesy of John H. Christy.   

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Reproductive Biology receptive females can also be found in tanaids (Ramírez 1965, Borowsky 1983). Some amphipods may defend spongocoels or empty barnacle shells (Shuster 1991). As these cannot be built or dug, they are probably a more limited resource than tubes or burrows. If they are indeed more limited, males might defend these resources more aggressively, and only the most competitive males would be able to secure one of these microhabitats. This scenario may facilitate harem defense, which can be considered as an extension of the resource-​defense system and may also coevolve with alternative mating strategies. Observations suggest that some isopods and amphipods engage in polygynous harem mating systems. In Paracerceis sculpta, α-​males defend attractive spongocoels, which are approached and inhabited by several females. Additionally, there is a strong male polymorphism where harems also attract β-​and γ-​males that follow different reproductive strategies (“sneaker males”) (Shuster 1991, Shuster and Wade 1991). The amphipod Corophium volutator is characterized by synchronous reproduction and a marked female-​biased sex ratio. These patterns have been interpreted as an indication for harem defense polygyny but need to be confirmed by further evidence (Forbes et al. 1996, McCurdy et al. 2010). Good evidence for harem defense is documented for other amphipod groups: females of Megalorchestia californiana assemble around the burrows of the largest males, which bear enlarged antennae with conspicuous red colorations (Bowers 1964, Iyengar and Starks 2008); and males of Siphonoecetes dellavallei and related species monopolize access to females by simply gluing them to the sides of their own mobile housings (Richter 1978, Just 1988). There are few examples of harem defense polygyny in isopods. Males of Dynamene bidentata are usually accompanied by a small harem of sexually mature females (Holdich 1968), and males of Paragnathia formica are reported to guard harems of up to 25 females in their simple burrows (Upton 1987a, 1987b). An interesting and well-​studied example of resource-​defense polygamy occurs in fiddler crabs. Individuals live at high densities and dwell in a self-​dug burrow with a small adjacent territory around its entrance. The burrow serves several purposes depending on the species (e.g., escape from predators, refuge from the tide), but in all cases, it is used as a place for mating (see Christy 2007), oviposition, and incubation (Asakura 2009). As the burrow is important for mating success, males fiercely defend their burrows against other males in most species (e.g., American species, Leptuca beebei, Leptuca pugilator, Minuca pugnax). Males may use claw-​waving displays with their single enlarged claws to visually attract females at the entrance of the burrow (e.g., Leptuca terpsichores; D in Fig. 10.2); alternatively, males of other species can roam around to court females on the surface (e.g., Uca stylifera, Austruca annulipes) or mate at the entrance of the female’s burrow (Tubuca paradussumieri; Christy 1987, 2007). In some species, males use acoustic signals or build sand structures near the entrance of the burrow (e.g., pillars, mudballs, hoods, and mudball trails) to complement claw waving in order to attract the attention of the females (Christy and Rittschof 2011). In these cases, males fight for dominance, which includes the most attractive locations for burrows (Christy 1983). Females usually prefer stable burrows that are not flooded by incoming tides or by groundwater, which is usually high in the supratidal zone, but that varies among species (Christy 1983). Due to the intense intrasexual competition, males bear a strongly enlarged claw on one side that is used during the claw-​waving displays and for fights. This sexual dimorphism is so striking that the fiddler crab’s claw is commonly used as a typical example of an enlarged, conspicuous, dual-​utility trait (i.e., armament and ornament; Dennenmoser and Christy 2013). Females, in turn, wander around to choose a male and after visiting (or being approached by) several males, a female enters the chosen male’s burrow or mates with the male at the entrance of the burrow, depending on the species. Mating ensues and the male leaves the burrow and plugs the entrance, while the female remains inside and incubates the eggs until they are released with the ebbing tide.



Overview of the Mating Systems of Crustacea

Lek Mating Leks are surprisingly rare in crustaceans, or at least are rarely described. Lek mating is a specific case of polygynandry in which males aggregate in a given location to attract females. The lek is a place where males compete both for females and preferential locations to display their sexually selected traits (Emlen and Oring 1977). In this scenario, the variance in male fitness is relatively high compared to other polygynandrous mating systems (e.g., mating swarms, scramble competition). Therefore, sexual dimorphism is expected, with males being conspicuous and/​or having large weapons to defend their rank within the mating lek (Rowe and Houle 1996). The best-​studied example of a lek mating system within crustaceans are bioluminescent myodocopid ostracods. The small males aggregate to perform bioluminescent displays to attract the larger females during dusk and dawn, and are therefore categorized as having a lek mating system (Morin and Cohen 1991, Gerrish and Morin 2016). Males and females are benthic, but swim up in the water column to mate. Males swim first and aggregate to begin their visual displays. In these luminescent clouds, males may have different roles. Some males may be considered as “leaders” that initiate the display alone and attract other males to aggregate and display together. Others are considered “followers” that follow the leaders and start displaying with them. Finally, there are also “silent sneaker” males that enter the luminescent cloud without displaying (Rivers and Morin 2009). These alternative mating strategies with some sort of hierarchy are typical of a lek mating system (Shuster and Wade 2003). Although individuals may change their roles during the displays (i.e., leaders become followers and vice versa), it can still be classified as lek mating. Within the luminescent clouds, females are rare (Morin and Cohen 1991), and it was suggested that they mate only once during their lifetime (Cohen and Morin 1990). The sex ratio is therefore clearly skewed toward males. Females are benthic and only swim up to the luminescent cloud when they are receptive. After copulation, the male spermatophore hardens and seals the genital entrance of the female, which designates the females as monogamic (Cohen and Morin 1990). Females then return to the benthos to brood their eggs while males mate again with other females. It is still unknown, however, if some males can monopolize matings or if leaders have higher mating success than followers. A trait that may influence male mating success is the brightness of the display (Rivers and Morin 2009), but this needs to be further studied. The hierarchical system “neighborhoods of dominance” described for caridean shrimps (e.g., Rhynchocinetes, Macrobrachium; Correa and Thiel 2003a) may be another case of lek mating. In Rhynchocinetes typus, for example, females are drawn to large males (“robustus”) by chemical cues, while small males (“typus”) roam around and try to rapidly mate with females (Díaz and Thiel 2004). These hierarchical systems resemble lek mating because large robustus males often occupy cavities in groups, probably aggregating to attract females (Díaz and Thiel 2004). Thus, as females search for robustus males, the small typus can intercept and sneak for copulations. Once the female finds a robustus male, the male holds it in a “cradle-​like” position (See C in Fig. 10.1 for an anomuran example.). Thus, robustus males monopolize most copulations, while typus males use an alternative sneaking tactic to copulate. Additionally, it is hypothesized that females may solicit copulations from small typus males to encourage robustus males to fight among themselves. This way, the female ensures that only the strongest male fathers its offspring (Correa et al. 2003, Díaz and Thiel 2004, Thiel and Correa 2004, Bailie et al. 2014). Mating Swarms Mating swarms are a specific case of polygynandry in which males and females aggregate to mate. Swarms typically have even sex ratios, which contrasts to the skewed sex ratios of the explosive breeding systems (e.g., reaching up to around 10 females for each male in Cladocera; Ratzlaff

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Reproductive Biology 1974, Young 1978). In mating swarms, individuals do not hold any territories or any apparent resources that are defended. Insects usually start mating aggregations around “pheromone markers” (Sullivan 1981) or landscape markers such as treetops (Downes 1969), but there is nothing known about these mechanisms in crustaceans. The only recorded case for a possible trigger is found in amphipods: Bathyporeia species seem to follow a semi-​lunar cycle with falling spring tides to form mating swarms (see Conlan 1991 and references therein; Borowsky 1991). The mating aggregations are typically short-​lived, and individuals mate promiscuously and repeatedly. As males and females are typically found in similar ratios, variance in fitness should be low. Consequently, sexual dimorphism is low in swarming species and no aggressive behavior has been reported (Pearce 1966). These dense aggregations occur in the water column in all swarming Crustacea. For instance, mysids and most cumaceans seem to engage in planktonic mating swarms (see Johnson et al. 2001 and references therein). Some amphipods were also reported to form mating swarms, for instance in Ampelisca, individuals leave their tubes annually, mate in the water column, and return to the substratum (Mills 1967). Leaving the dwelling, swimming to the swarm, and returning may be costly, and other mating strategies could be less costly in terms of predation pressure. However, the formation of mating swarms may increase the mating rate (Downes 1969) due to the visual mark that draws conspecifics (Downes 1969). Similar observations from insects (e.g., Downes 1969, Sullivan 1981) suggest that these strategies largely depend on the biology of the species. To date, there is no clear evolutionary explanation for such swarms in crustaceans. The best-​described swarm, and the only two decapod species that have been reported to swarm, are the pinnotherid crabs Tumidotheres maculatus and Fabia subquadrata (Pearce 1966, Kruczynski 1973). Pinnotherids are known for their parasitic/​commensal lifestyle (e.g., cohabiting with annelids, sea slugs, shrimp burrows; Cheng 1967), but they are usually considered pure-​ searchers, with males roaming around in search of stationary females (e.g., Calyptraeotheres garthi; Ocampo et  al. 2012). Mating swarms are thus unexpected in this group. Tumidotheres maculatus and F. subquadrata are commensals of mussels. Males dwell in mussels until they reach sexual maturity, and females until their first “true-​crab” molt stage. They then leave their mussel hosts and form mating swarms in the open water. Females mate in the hard-​shelled condition and both sexes show promiscuity, copulating repeatedly in the mating swarm (Pearce 1966). After mating, females re-​enter a host, continue to grow, molt, and start egg production; males, in turn, die after mating (Kruczynski 1973). It remains unclear why only these two species display this sort of mating system within pinnotherid crabs. Since there are only two recorded cases of mating swarms across two pinnotherid genera, future studies should reconfirm and re-​examine existing accounts and explore other species in these two genera. Monogamy Two forms of monogamy are found in crustaceans:  pair bonds that last over a single breeding season and monogamous pair bonds that last over several breeding seasons in a row (and maybe the entire lifespan). There is no consensus on whether monogamic taxa should display sexual dimorphism or not, and this may depend on the biology of the species. Some species are characterized by strong sexual dimorphism, such as the shrimps Alpheus angulatus and A. armatus (Correa and Thiel 2003a), but most species show little dimorphism, such as the stomatopod Neogonodactylus bredinii, in which males are slightly larger than females and have larger striking appendages (Vetter and Caldwell 2015). Interestingly, all monogamous species tend to occupy some sort of dwelling, such as tubes and burrows, and the duration of the monogamous association seems to be correlated to the overall effort to defend the burrow (i.e., burrow economic defensibility theory; Brown 1964). For instance, Conlan and Chess (1992) documented that monogamous pairs of the amphipod Peramphitoe



Overview of the Mating Systems of Crustacea

stypotrupetes cohabit with several generations of their offspring within kelp stipes. An observation by Myers (1971) also suggests that the tube-​dwelling amphipod Microdeutopus gryllotalpa may form monogamous pairs: two individuals (male and female) each shared a tube over several breeding cycles. However, the observations of Myers (1971) must be regarded with caution, as males of M. gryllotalpa showed only temporary attending behaviors in other laboratory setups (i.e., “cruising males”; Borowsky 1980, 1983). Stomatopods (A in Fig. 10.3) assign different values to their burrows according to species. As a consequence, different degrees of monogamy can be distinguished within the group. Males and females of N. bredinii, for example, inhabit coral crevices and defend them fiercely against any intruder (Vetter and Caldwell 2015). A few days prior to the full moon, pairs are formed: females leave their cavities to find a male while males stay in their cavities, waiting for a female to arrive and defending the cavity against conspecific males. The female, however, is tolerated in the male’s cavity, and after several matings, the female is guarded by the male until spawning takes place. The male then leaves the cavity and starts searching for a new cavity to occupy while the female stays behind in the cavity (Shuster and Caldwell 1989). Female receptivity in N. bredinii is synchronized with the lunar cycles. Due to this synchronicity, males cannot easily monopolize access to several females, and the system is considered monogamic for at least one breeding event (Knowlton 1979). In contrast, species of the “spearer” Lysiosquilla exhibit an even more pronounced form of monogamy. Heterosexual pairs inhabit rather large excavated burrows (up to 10 m in length) in sandy substrata. Burrows are comparably expensive to build, and in at least one species, Lysiosquilla sulcata, individuals are unable to construct new burrows once evicted from their old homes (Caldwell 1991). These pairs are thought to form prior to or at the onset of sexual maturation, probably cohabiting in the same burrows for years. Long-​term monogamy is thought to be favored in this group because both sexes have lost most of their body armor and thoracic appendages, thus being better adapted for a fossorial lifestyle rather than roaming. Decapods that are symbiotic (e.g., with reef-​building corals, sea urchins, sponges, sea anemones) or that live confined to spatially limited habitats form a “territorial cooperation” or “resource-​ defense” monogamous mating system (Baeza and Thiel 2007; B in Fig. 10.3). For example, some species of the hippolitid shrimp (genus Lysmata) inhabit sponges and sea anemones in socially monogamous pairs. Congeneric free-​living species, however, form aggregations and feature a pure-​ search polygamy mating system (Bauer 2006, Baeza et al. 2009). Other examples of this mating system can be found in Stenopodidea, in caridean shrimps, porcelaniid (Anomura), and trapeziid crabs (Brachyura) (Huber 1987, Asakura 2009). Males and females (or hermaphrodites; see Lysmata in Bauer 2006) can live in pairs that defend territories (or their mate) for at least an entire breeding season (Bauer 2011). In some species, males cohabit with the female until the next mating event, but the bonding duration is still unknown for most species. Nevertheless, some species were found to form stable pairings and to recognize their mate (e.g., the stenopodid Stenopus hispidus or the caridean shrimps Lysmata debelius and Hymenocera picta; Chak et al. 2015). Pairs that share limited and valuable refuges are less likely to be evicted by intruders (Wickler and Seibt 1981). This mating system is therefore referred to as “resource-​defense” or “territorial cooperation” monogamy by some researchers (Subramoniam 2013), as pairs fiercely defend their territory (Huber 1987). An interesting type of monogamy is reported in parasitic bopyroid isopods. When undifferentiated juveniles encounter a female, they attach to it and develop to sexually dimorphic dwarf males that form lifelong pair bonds with the female (Reinhard 1949, Cericola and Williams 2015, C in Fig. 10.3). When several juveniles attach to the same female, strong intrasexual competition seems to result in the depletion of competitors until a single individual is left, which then grows to maturity (Reinhard 1949). This form of monogamy thereby clearly differs from other types, as the male is coalesced with the female. After the transformation has been realized, the individuals cannot be separated anymore.

285

286

286

Reproductive Biology (A)

(B)

(C)

Fig. 10.3. Monogamy in different crustacean groups. (A) Stomatopod “smashers” are typically monogamous (although some of them are polygamous, such as the Odontodactyluss scyllarus), while “spearers” tend to be polygamous. (B) Snapping shrimps show a diversity of mating systems and their monogamic-​eusociality continuum may be tied to both sexes cohabiting in sponges, such as seen in Alpheus and Synalpheus genera. (C) Parasitic bopyroid isopods form monogamous lifelong pair bonds with a large and strongly modified female and an attached dwarf male such as in Athelges paguri (shown is a dwarf male (m) of A. paguri attached to the pleotelson of a female on the host Pagurus bernhardus caught at Helgoland, North Sea in July 2011; note the numerous eggs (e) in the partly shown marsupium). See color version of this figure in the centerfold. (A) Photo courtesy of Roy L. Caldwell; (B) photo courtesy of Arthur Anker; (C) photo courtesy of Jan Beermann.   

The desert isopod Hemilepistus reaumuri forms a unique, well-​studied type of monogamy that includes both sexual and social monogamous bonds. This species forms stable family groups to endure the extreme environmental conditions of the desert. At the beginning of the spring, females dig burrows while males search for empty burrows or burrows with single females inside. Typically, the female stays within the burrow until a male is able to defend the burrow against competitors for many hours. After pair formation, male and female cooperate to guard and maintain the burrow throughout the whole breeding season. Accordingly, copulation is followed by extended biparental



Overview of the Mating Systems of Crustacea

care, resulting in fortress defense of an isopod family (a parental couple and their offspring; Baker 2004, Linsenmair 2007).

DRIVERS OF MATING SYSTEMS The current overview illustrates that most mating systems can be found in the Decapoda (Table 10.1). Other crustacean groups either lack some (e.g., Peracarida) or most mating system types (e.g., Stomatopoda). Despite possible research biases, the main drivers of variation in mating systems can be placed in two categories: (a) the biology of the species/​group, and (b) the biotic/​abiotic environment. Here, we discuss a topic within each category and a broader topic on how to quantify mating systems. First, we discuss the role of the female molt on mating systems. Second, we propose that mating and social systems are linked in some crustaceans because of their reliance on dwellings to mate and rear the young. Lastly, current research is mainly focused on a single metric for mating systems, the OSR, whereas other useful metrics are not commonly used. In the following, we provide a brief explanation of these metrics and argue that they might aid in revealing different patterns about the mating systems. Female Molt and Mating Systems An obligatory molt prior to copulation has a profound effect on the mating systems of most crustaceans, as it defines the duration of female receptivity in the mating pool (i.e., when females are receptive and ready to mate; Kokko et al. 2014). Females that only mate in soft-​shelled conditions are receptive for only a short period after the molt, restricting the time for finding the female and copulating. As females are receptive only for a very brief period, the mating pool is skewed toward males, which consequently affects the OSR and the strategies used to maximize reproductive success. The three main ways males maximize their reproductive success is either via the monopolization of matings, efficiently locating mates, and/​or caring for the young. Exclusive male parental care has never been reported in crustaceans (see Chapter 5 in this volume), but males frequently guard resources and/​or females that are nearing their molt until copulation. As competition increases, males will guard the females for a longer time (Wellborn and Cothran 2007). Furthermore, males may detect the byproducts of the female molting process to assess their receptivity (e.g., Carcinus maenas, Hardege and Terschak 2011, peracarids, Thiel 2011 and references therein). Therefore, female molt circumstances can predispose the species for pre-​and postcopulatory mate guarding, favoring female/​resource defense mating systems due to their effect on female time in the mating pool. In contrast, brief associations should be favored when females do not molt prior to copulation because of the unpredictability of how long females stay in the mating pool (Christy and Wada 2015, but see Espinoza-​Fuenzalida et al. 2012). Overall, the female molt is an important predictor of crustacean mating systems in several theoretical models (e.g., Wickler and Seibt 1981) and is probably an important contributor to sexual conflict in crustaceans ( Jormalainen 1998; see Chapter 11 in this volume). Nevertheless, other factors such as population density, sex ratio, and spatio-​temporal distribution of vital resources also play important roles (Kokko et al. 2014), probably interacting with the female molt in individual mating systems.

287

Ostracoda

Anostraca and Diplostraca and Branchiura and Cirripedia + -​ -​ -​

+ -​ -​ -​

+ + -​ +

++ -​ -​ -​

+

++ -​ -​ +

-​

++ + -​ +

+

+ -​ + +

++

+ -​ -​ ++

-​

Note: Minus-​symbols indicate taxa for which we did not find any information on that mating system. Plus-​symbols indicate the mating systems found for that taxa and double plus-​symbols indicate the most common mating system in that taxa.

-​ + -​ -​

Copepoda

-​ -​ -​ -​

Peneoidea

Resource/​female defense polygamy Leks Mating swarms Monogamy

Caridea ++

Palinura and Astacidea

++

Stenopodidea

++

Brachyura and Anomura

++

Peracarida

++

Stomatopoda

Pure-​search polygamy

Mating System

Table 10.1.  Mating Systems of Crustacea and Occurrence for Each Group According to the Current Scientific Knowledge.

28



Overview of the Mating Systems of Crustacea

Mating, Social Systems, and Life in Dwellings Dwellings represent vital resources for the survival and reproduction of individuals, and crustaceans are known to fight for their ownership; this means that the economic defensibility theory is applicable (Brown 1964). A dwelling’s value as a resource increases when dwellings are rare and/​or require much effort to build and maintain, and/​or are difficult to defend, and as the value increases, species are expected to become territorial (Brown 1964). However, economic defensibility theory also predicts that when a resource is extremely rare, defense is no longer viable and individuals should return to scramble competition (e.g., Grant et al. 2000). Pairing up with an opposite-​sex partner might be an alternative solution to this problem: two individuals may share the labor of building, maintaining, and defending the dwelling, and in turn are less likely to be evicted, increasing the survival and fitness of both individuals. Monogamy would thus decrease the costs of defending dwellings and would facilitate the evolution of “resource-​defense” or “territorial cooperation” monogamy (Mathews 2002, Linsenmair 2007). A built-​in assumption of this hypothesis states that the dwellings are used as both mating grounds and dwelling place. If individuals mate outside of the dwelling, they would eventually need to leave and risk losing their territory, potentially altering the mating system. Therefore, economic defensibility theory and some assumptions regarding mating biology can thus explain at least one driver of monogamy in crustaceans. The influence of the defensibility of a dwelling on mating systems has already been proposed for symbiotic crustaceans (e.g., on sea anemones, sponges, ascidians; Baeza and Thiel 2007). In that model, the authors suggest that host abundance, host complexity/​size, and predation risk can predict the mating system of the crustacean symbiont. Here, we argue that these abiotic variables may not only predict the mating system but that the mating system itself may facilitate the evolution of social systems in crustaceans. In contrast, in most social taxa (e.g., hymenopteran insects), the mating system seems uncorrelated to the social system: in eusocial bees, mating systems vary from monogamy (e.g., Bombus terrestris) to polygamy (e.g., Bombus hypnorum; Paxton 2005). Consequently, although life history may be restricted by social mechanisms, it may not affect the mating system. However, in crustaceans, most species that display some sort of social system inhabit dwellings (e.g., Synalpheus snapping shrimps, burrowing crayfish, desert isopods, Jamaican bromeliad crabs; Duffy 2007, Richardson 2007, Linsenmair 2007, Diesel and Schubart 2007, respectively). One behavioral key difference between Hymenoptera and Crustacea is how species mate in relation to the dwelling (or nest). Bees can mate away from and within the nest (Paxton 2005), whereas crustaceans that display some sort of social system mate within their dwelling (or near its entrance). Hence, using dwellings as mating grounds may facilitate the expression of some mating systems, which in turn may favor the evolution of social systems in crustaceans (Fig. 10.4). In this case, we would expect that (1) crustaceans that inhabit dwellings that are rare, difficult to build, and hard to defend will display territorial cooperation; and (2)  crustaceans that display parent-​ offspring associations (i.e., a tendency toward more complex social behaviors) will also inhabit rare and difficult-​to-​build dwellings that are hard to defend. To test this idea, we used Thiel’s (2007) review on parent-​offspring groups as a basis and added randomly selected species from the literature that appeared in this chapter. We underline that this is not a complete list, but a simple assemblage of examples. Our purpose was not to provide an exhaustive list, but rather to encourage further research to test this idea. Overall, the current overview used examples from six amphipod species, five isopod species, three tanaidacean species, six astacidean species, three brachyuran crab species, three caridean shrimp species, and two stomatopod species, summing up to a total of 28 species (Table 10.2). Of these species, 11 (39%) exhibited cohabiting parent-​offspring groups without the description of a social system by reasearchers. Only three species (11%) were considered subsocial, and a single species (4%) lives in eusocial associations. Regarding our first prediction, that crustacean taxa that display territorial cooperation will be found

289

920

290

Reproductive Biology Dwelling traits How hard to find? (spatiotemporal distribution)

common

rare

How hard to build/maintain?

easy

hard

How hard do defend?

easy

hard

Brief association

Territorial cooperation

None

Parent-offspring groups

(1) facilitation Mating system (2) facilitation Social system

Fig. 10.4. Schematic depiction of how dwelling traits can facilitate the evolution of mating systems and social systems in crustaceans. We highlight that they only facilitate the evolution; they do not select specific mating or social systems.   

to inhabit rare, difficult-​to-​build and hard-​to-​defend dwellings, we found that 12 (86%) of the 14 territorially cooperative species (“monogamy” in Table 10.2) inhabit dwellings that are hard to build and/​or defend. Furthermore, regarding our second prediction that parent-​offspring associations would inhabit the same type of dwelling, eight (89%) of the nine monogamic species that presented parent-​offspring associations inhabit dwellings that are hard to build and/​or defend. It must be noted that we excluded almost all Synalpheus shrimps from our survey, a group that is known to inhabit rare sponges and represents subsocial/​eusocial species (Chak et al. 2017). The group was excluded because eusociality originated from pair-​living groups in these shrimps (Chak et al. 2017), which also provides further support to our hypothesis. We highlight that more empirical or literature research on this topic would be essential for a robust test of this hypothesis. Overall, it seems plausible that the evolution of sociality is facilitated by the mating system and the life in dwellings in crustaceans. The Mismeasures of Mating Systems Over the course of the chapter, we have commented on the role of the OSR on mating systems. We made that decision to facilitate the classification of mating systems while using the framework by Emlen and Oring (1977). The OSR describes the magnitude of intrasexual competition among individuals of the most abundant sex. This is usually achieved by calculating the number of mature males in relation to mature females that are available at any given time. It is by far the most common metric used in crustacean studies. However, several metrics of mating systems are available in the current literature (reviewed in Henshaw et al. 2016), and they provide different kinds of information about mating systems, such as the opportunity for sexual selection within a mating system (Krakauer et al. 2011). To provide a perspective of how common OSR is in relation to other metrics, we performed three Google Scholar searches using three terms. First, we used “operational sex ratio” + “crustacean,” which yielded 484 results. Second, we used “Imates” + “crustacean,” yielding 87 results, of which only

Amphipoda Casco bigelowi (Blake, 1829) Dulichia rhabdoplastis (McCloskey, 1970) Dyopedos monacanthus (Metzger, 1875) Dyopedos porrectus (Spence Bate, 1857) Lembos websteri (Bate, 1856) Phronima sedentaria (Forskål, 1775) Isopoda Hemilepistus elongatus (Brandt, 1880) Hemilepistus reaumuri (Adóuin, 1826) Porcellio albinus (Budde-​ Lund, 1885) Porcellio Fuert-​P.spec.1 Porcellio Fuert-​P.spec.2 Tanaidacea Heterotanais oerstedi (Krøyer, 1842) None

None Parent-​offspring

None Subsocial Parent-​offspring Parent-​offspring Parent-​offspring Parent-​offspring

Resource-​defense polygamy Resource-​defense polygamy Resource-​defense polygamy Pure-​search

Monogamy

Polygamy

Monogamy

Polygamy

Polygamy Polygamy

Pure-​search

None

None

None

Social System

Monogamy

Mating System

Female, juveniles

Female, juveniles Female, juveniles

Female, juveniles

Male, female, juveniles

Female, juveniles

Male, female, juveniles

Male (partially), female, juveniles, subadults Male and female(s) until juveniles are born Male and female(s) until juveniles are born Male and female(s) until juveniles are born Female, juveniles

Low

Low Low

Low

High

Low

High

Low

Low

Low

Low

Low

Inhabitants of Dwelling Difficulty of Building/​ Defending

(Continued)

Ramírez 1965

Linsenmair 2007 Linsenmair 2007

Linsenmair 2007

Röder and Linsenmair 1999 Linsenmair 2007

Davenport 1994

Mattson and Cedhagen 1989 Mattson and Cedhagen 1989 Mattson and Cedhagen 1989 Moore 1981

Thiel 1998

Reference

Table 10.2.  Exemplary Overview on Mating Systems, Social Systems, Inhabitants of the Dwelling, and the Difficulty of Building/​Defending the Dwelling.

Tanais cavolinii (Milne-​ Edwards, 1840) Tanais dulongii (Adóuin, 1826) Astacidea Parastacus pilimanus (von Martens, 1869) Parastacus pugnax (Poeppig, 1835) Engaeus leptorhynchus (Clark, 1936) Cambarus harti (Hobbs, 1981) Ombrastacoides huonensis (Hansen and Richardson, 2006) Procambarus clarkii (Girard, 1852) Brachyura Metopaulias depressus (Rathbun, 1896)

Table 10.2. Continued.

Subsocial Parent-​offspring Subsocial

Monogamy

Monogamy

Monogamy

Male, female, juveniles

Female, juveniles

Males, females, juveniles

Male or female, juveniles

Subsocial

Females, juveniles

Parent-​offspring

Monogamy

Female, juveniles

Monogamy

Parent-​offpsring

Monogamy

Female, juveniles

Female, juveniles

Parent-​offspring

Pure-​search

High

Low

High

High

High

High

Low

Low

Inhabitants of Dwelling Difficulty of Building/​ Defending Female, juveniles Low

Female-​defense polygamy Parent-​offspring

Parent-​offpsring

Social System

Pure-​search

Mating System

Diesel and Schubart 2007

Gherardi 2006

Richardson 2007

Helms et al. 2013

Richardson 2007

Palaoro et al. 2016

Dalosto et al. 2012

Johnson and Attramadal 1982 Rumbold et al. 2012

Reference

29

Male Male

Males, females, juveniles Male, female Male, female

Female Male, female

None None

Eusocial None None

None None

High

High

High

High

High

High

High

Shuster and Caldwell 1989 Caldwell 1991

Omori et al. 1994

Knowlton 1980

Duffy 2007

Sal Moyano et al. 2012

Christy 1983

Note: Information on the difficulty of building/​defending the dwelling was inferred from the literature using the following criteria: if individuals fought for the dwelling, had specialized appendages to create it, or had a decrease in their fitness due to loss of the dwelling, the difficulty was considered as “high.” All other instances were considered as “low.” Note that this is not a complete list, but only a representative compilation of examples.

Uca pugilator (Bosc, 1802) Resource-​defense polygamy Neohelice granulata (Dana, Resource-​defense 1851) polygamy Caridea Synalpheus regalis (Duffy, Monogamy 1996) Alpheus armatus Monogamy (Rathbun, 1901) Periclimenes ornatus Monogamy (Bruce, 1969) Stomatopoda Neogonodactylus bredinii Monogamy (Manning, 1969) Lysiosquilla sulcata Monogamy (Manning, 1978)

924

294

Reproductive Biology three were real hits; the rest were typos such as “approx-​imates.” Lastly, we used “bateman gradient” + “crustacean,” with 11 hits with only one conference poster being a true hit. Additionally, we found a meta-​analysis that tested the correlation between OSR and another metric opportunity for sexual section (Is, explained in the following) including only two species of crustaceans (Gammarus minus and Paracerceis sculpta), because there were no more data for crustaceans in the literature (Moura and Peixoto 2013). Although OSR is a good metric to measure the intensity of competition, there are still several drawbacks (see Klug et al. 2010, and the following discussion). Other complementary measures and indexes are needed to provide a better understanding of mating systems. In the following, we provide a brief description of other quantitative measures of sexual selection that are relevant to mating systems and why OSR provides incomplete information about the whole picture. The OSR calculates the potential intrasexual competition within the more abundant sex, coming along with a number of restrictions. First, the OSR does not include the spatial clustering of individuals, and usually does not consider temporal clustering as well (but see Correa and Thiel 2003b). The OSR is a snapshot of current conditions and thus usually does not account for the temporal variability within a mating season (e.g., more receptive females at the beginning of the season than at the end; Clutton-​Brock 2017). As shown in the examples of this overview, the number of available individuals (particularly females) in the mating pool varies over the course of a mating season. Thus, the level of competition also varies across time. A measure that encapsulates the idea of fluctuating levels of competition from the OSR is the time spent by each sex outside of the reproductive pool (e.g., parental care, foraging, molting; Kokko et al. 2012). The mean time each sex spends out of the reproductive pool can provide an estimate for which sex should compete the most for mates: the sex that spends more time within the reproductive pool will become more frequent and should compete more for the opposite sex. This is an important metric for the assessment of competition between individuals and has been employed in a few studies (e.g., valuable and complementary information Correa and Thiel 2003b). However, this metric also does not indicate the potential fitness gains of each mating event, while not indicating to which degree single individuals affect mating opportunities in a population (i.e., mating variance). Thus, OSR and time-​out provide insights on how individuals compete, but they do not provide information on who is successful in the mating pool, and who is not. This information, however, is crucial for understanding selective pressures (Shuster and Wade 2003). Second, the OSR does not allow for conclusions on the variation of individual mating success. The monopolization of mates by a single individual, on the other hand, allows for a first assessment on how to operationalize the potential for sexual selection within a population, allowing for a general prediction of the mating system of that species. The Is framework, developed by Wade and Arnold (1980), provides an explanation of how much variance in mating success can be found in a population: the larger the variance, the stronger the sexual selection could be in that population (note that this is a potential for sexual selection). The Is is calculated by dividing the variance in mating success by the squared mean mating success (Wade 1979, Wade and Arnold 1980). It is a useful descriptor of the potential for sexual selection to act on a given population or species and can be partitioned in several components to examine the relative opportunity for selection from male-​male competition and female mate choice (DuVal and Kempenaers 2008, see Krakauer et al. 2011 for more examples). Without the calculation of the Is, a lot of information on mating systems is thus lost. Third, the OSR does not encompass any measure of how much the reproductive success is tied to the ability to acquire mates. This can be achieved by measuring the covariance between reproductive success (e.g., number of offspring) and mating success (e.g., number of copulations or mates) given a morphological trait; in other words, calculating the Bateman gradient (Bateman 1948). Calculating the gradient yields a slope that can suggest the strength of selection acting on that trait: steeper gradient slopes correlates with stronger links between fitness and the trait used to acquire mates (Kokko et al. 2012). The Bateman gradient can therefore be used to study the potential magnitude of selection on specific traits (Clutton-​Brock 2017).



Overview of the Mating Systems of Crustacea

Each of these metrics described in the preceding paragraph provides valuable and complementary information to understand mating systems and how to approach sexual selection (see Henshaw et al. 2016 for further metrics). Currently, information available on crustacean mating systems is largely descriptive and underexplored. This may partly be due to the clear dominance of the use of OSR in the vast majority of studies. We are aware that using any of these metrics requires a considerable amount of effort. For a reliable estimate of OSR, researchers need to know who is in the mating pool at that time and the time each sex spends outside of the mating pool, which is rarely done (but see Correa and Thiel 2003b, Espinoza-​Fuenzalida et al. 2012). In species where females do not molt prior to copulation, it is hard to estimate the timing of female receptivity; and sometimes their receptiveness is short lived. The Is requires measuring the number of individuals within a population and the number of copulations of each individual; this may allow for inferring on mating variance. For the Bateman gradient, researchers need to identify the number of copulations of each individual and how many offspring it sired, and measure the traits that are supposedly used for reproduction. Therefore, data on the strength of sexual selection are not easily acquired. However, these alternative metrics nonetheless provide much needed information on sexual selection, which might, for instance, improve understanding of how traits are being selected and how individuals enhance their ability to find mates.

FUTURE DIRECTIONS There is a clear research bias in mating system research among animal groups. Insects, mammals, and birds have been the focus of mating system studies for decades (Greenwood 1980, Clutton-​Brock 1989, Shuker and Simmons 2014), whereas data on most crustacean groups are still insufficient. This issue may partly result from the lack of alternative metrics on mating systems. However, we think that more species-​level studies on crustaceans will provide information about mating systems that is urgently needed. For example, the large aggregations (“podding”) of some commercially important crabs (e.g., Libinia emarginata, Paralithodes camtschaticus) are still largely unexplained (i.e., if for mating or for other reasons such as predator protection or cooperation; Asakura 2009). Furthermore, reports on the mating swarms of pinnotherid crabs also need further clarification to understand if these swarms are really part of the mating system or if they may have another underlying cause. Despite this clear lack of studies, the diversity of crustacean mating systems can be considered as equally high to those of comparably well-​studied model groups, as highlighted in Table 10.1. This underlines the potential of crustaceans to serve as model organisms for studies on mating systems and sexual selection (e.g., Shuster 2007). As a first step, published evidence for OSR and any other metrics could be carefully reviewed and groups that could be used to calculate alternative metrics should be identified. For example, the number of copulations of an individual within a population (or a subset of the population) can be used to calculate the Is, which can be calculated separately for males and females if warranted by the research question (Krakauer et al. 2011). Research bias on mating systems is also evident within crustaceans. Although peracarids are characterized by a high diversity of mating systems, probably due to the wide range of body plans and lifestyles (e.g., they are found in aquatic and terrestrial habitats), our current knowledge depicts fewer types of mating systems in peracarids than in decapods. This may be due to a large research gap in the field of peracarid behavior, where detailed studies are only available for very few groups or select species (e.g., Linsenmair 2007)  and behavioral patterns of most terrestrial and marine peracarid groups are clearly understudied. Small body sizes and difficult species identification, such as in amphipods, probably makes most peracarids “less attractive” model organisms to study behavior and mating systems compared to decapods (Beermann et al. 2015). However, we argue that peracarids have a great potential for exciting discoveries. For example, a previously unpublished observation in the marine isopod Astacilla longicornis could even imply the existence of a so-​far

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Fig. 10.5. Undescribed mating system for crustaceans in arcturid isopods? Adult individuals of the isopod Astacilla longicornis exhibit an undescribed mating behavior: when a female is close to its molt, two males are always found clinging to the much larger female, with one male on each lateral body side. No physical interference between the two males seems to occur (see text for further information). See color version of this figure in the centerfold. Photo courtesy of Heinz-​Dieter Franke, digitally remastered here.   

unknown mating system:  in a laboratory culture that was maintained over several generations, amplexi (i.e., a precopulatory embrace of males with females) always consisted of two males and a receptive female, with one male each clinging to a lateral side of the female’s pereon. No physical interference seems to occur between the males. This surprising pattern was consistent throughout all adult individuals of the population (personal communication, H.  D. Franke and L.  Gutow; Fig. 10.5). It remains unclear, however, if both males contribute equally to the parentage of the offspring by separately inseminating each of the paired female ovaria (e.g., as for Sphaeroma in Heath et al. 1990), or if the males are related to each other, as even the copula itself in Astacilla has not been observed to date (personal communication, Wolfgang Wägele).

CONCLUSIONS Although we recognize that crustacean mating systems are clearly understudied when compared to other groups (e.g., insects, mammals, and birds; Greenwood 1980, Clutton-​Brock 1989, Shuker and Simmons 2014), the diversity of crustacean mating systems can be considered as equally high. This reflects the high diversity of lifestyles and body plans found in crustaceans. Several environmental factors drive the diversity of mating systems. For instance, burrow dwelling or a commensalism may predispose some species to “territorial cooperation” monogamy. Furthermore, crustacean social systems seem to be closely connected to the respective mating system (at least in evolutionary history), which may be less common in non-​crustaceans. Further research is required to elucidate this connection. In addition, elaborate behavioral studies on the mating systems of Crustacea and more studies on alternative metrics to measure the opportunity of sexual selection would help to unravel the evolution of this fascinating group. All things considered, we believe that crustaceans represent excellent models that still have much to teach us about mating systems and sexual selection.



Overview of the Mating Systems of Crustacea

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Kokko, H., H. Klug, and M. D. Jennions. 2014. Mating systems. Pages 42–​58 in D. M. Shuker and L. W. Simmons, editors. The Evolution of Insect Mating Systems. Oxford University Press, Oxford. Krakauer, A. H., M. S. Webster, E. H. Duval, A. G. Jones, and S. M. Shuster. 2011. The opportunity for sexual selection: not mismeasured, just misunderstood. Journal of Evolutionary Biology 24:2064–​2071. Kruczynski, W. L. 1973. Distribution and abundance of Pinnotheres maculatus Say in Bogue Sound, North Carolina. Biological Bulletin 145:482–​491. La, G. H., J. Y. Choi, K. H. Chang, M. H. Jang, G. J. Joo, and H. W. Kim. 2014. Mating behavior of Daphnia: impacts of predation risk, food quantity, and reproductive phase of females. PloS ONE 9:e104545. Larsson, P. 1991. Intraspecific variability in response to stimuli for male and ephippia formation in Daphnia pulex. Hydrobiologia 225:281–​290. Linsenmair, K. E. 2007. Sociobiology of terrestrial isopods. Pages 339–​364 in J. E. Duffy and M. Thiel, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, New York. Longo, G., M. Trovato, and V. Mazzei. 2011. Variability of the female genital system morphology and of sperm storage in terrestrial isopods (Isopoda, Oniscidea). Italian Journal of Zoology 78:287–​297. Lueken, W. 1968. Mehrmaliges Kopulieren von Armadillidium Weibchen (Isopoda) während einer Parturialhäutung. Crustaceana 14:113–​118. Marshall, S. M., and A. P. Orr. 1955. The Biology of a Marine Copepod Calanus finmarchicus. Oliver and Boyd, London. Martin, J. W., and G. E. Davis. 2001. An Updated Classification of the Recent Crustacea. Natural History Museum of Los Angeles County, Los Angeles, CA. Mathews, L. M. 2002. Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-​living snapping shrimp. Animal Behaviour 63:767–​777. Mattson, S., and T. Cedhagen. 1989. Aspects of the behaviour and ecology of Dyopedos monacanthus (Metzger) and D. porrectus Bate, with comparative notes on Dulichia tuberculata Boeck (Crustacea: Amphipoda: Podoceridae). Journal of Experimental Marine Biology and Ecology 127:253–​272. McCurdy, D. G., J. Sherman Boates, and M. R. Forbes. 2010. Reproductive synchrony in the intertidal amphipod Corophium volutator. Oikos 88:301–​308. Mikheev, V. N., A. F. Pasternak, and E. T. Valtonen. 2015. Behavioural adaptations of argulid parasites (Crustacea: Branchiura) to major challenges in their life cycle. Parasites and Vectors 8:394. Mills, E. L. 1967. The biology of an ampeliscid amphipod crustacean sibling species pair. Journal of the Fisheries Board of Canada 24:305–​355. Moore, P. G. 1981. The life histories of the amphipods Lembos websteri Bate and Corophium bonnellii Milne Edwards in kelp holdfasts. Journal of Experimental Marine Biology and Ecology 49:1–​50. Moore, P. G., and L. B. Eastman. 2015. The tube-​dwelling lifestyly in crustaceans and its relation to feeding. Pages 35–​77 in M. Thiel and L. Watling, editors. The Natural History of the Crustacea, Volume 2: Lifestyles and Feeding Biology. Oxford University Press, New York. Morin, J. G., and A. C. Cohen. 1991. Bioluminescent displays, courtship, and reproduction in ostracodes. Pages 1–​16 in R. T. Bauer, and J. W. Martin, editors. Crustacean Sexual Biology. Columbia University Press, New York. Moura, R. R., and P. E. C. Peixoto. 2013. The effect of operational sex ratio on the opportunity for sexual selection: a meta-​analysis. Animal Behaviour 86:675–​683. Myers, A. A. 1971. Breeding and growth in laboratory-​reared Microdeutopus gryllotalpa Costa (Amphipoda: Gammaridea). Journal of Natural History 5: 271–​277. Ocampo, E. H., J. D. Nuñez, M. Cledón, and J. A. Baeza. 2012. Host-​specific reproductive benefits, host selection behavior and host use pattern of the pinnotherid crab Calyptraeotheres garthi. Journal of Experimental Marine Biology and Ecology 429:36–​46. Omori, K., Y. Yanagisawa, and N. Hori. 1994. Life history of the caridean shrimp Periclimenes ornatus Bruce associated with a sea anemone in southwest Japan. Journal of Crustacean Biology 14:132–​145. Palaoro, A. V., E. Del Valle, and M. Thiel. 2016. Life history patterns are correlated with predictable fluctuations in highly seasonal environments of semi-​terrestrial burrowing crayfish. Hydrobiologia 767:51–​63.

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Sigvardt, Z. M., and J. Olesen. 2014. Mating behaviour in laevicaudatan clam shrimp (Crustacea, Branchiopoda) and functional morphology of male claspers in a phylogenetic context: a video-​based analysis. PloS ONE 9:e84021. Subramoniam, T. 2013. Origin and occurrence of sexual and mating systems in Crustacea: a progression towards communal living and eusociality. Journal of Biosciences 38:951–​969. Sugumar, V. 2010. Reproduction in the brine shrimp Artemia Leach, 1819 (Branchiopoda, Anostraca) from South India: laboratory cross fertility tests and mating behaviour. North-​Western Journal of Zoology 6:162–​171. Sullivan, R. T. 1981. Insect swarming and mating. The Florida Entomologist 64:44–​65. Svane, I. 1986. Sex determination in Scalpellum scalpellum (Cirripedia: Thoracica: Lepadomorpha), a hermaphroditic goose barnacle with dwarf males. Marine Biology 90:249–​253. Takeshita, F., and Y. Henmi. 2010. The effects of body size, ownership and sex-​ratio on the precopulatory mate guarding of Caprella penantis (Crustacea: Amphipoda). Journal of the Marine Biological Association of the UK 90:275–​279. Takeshita, F., R. C. Lombardo, S. Wada, and Y. Henmi. 2011. Increased guarding duration reduces growth and offspring number in females of the skeleton shrimp Caprella penantis. Animal Behaviour 81:661–​666. Thiel, M. 1998. Reproductive biology of a deposit-​feeding amphipod, Casco bigelowi, with extended parental care. Marine Biology 132:107–​116. Thiel, M. 2002. Reproductive biology of a small isopod symbiont living on a large isopod host: from the maternal marsupium to the protective grip of guarding males. Marine Biology 141:175–​183. Thiel, M. 2007. Social behaviour of parent–​offspring groups in crustaceans. Pages 294–​318 in J. E. Duffy and M. Thiel, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, New York. Thiel, M. 2011. Chemical communication in peracarid crustaceans. Pages 199–​218 in T. Breithaupt and M. Thiel, editors. Chemical Communication in Crustaceans. Springer, New York. Thiel, M., and C. Correa. 2004. Female rock shrimp Rhynchocinetes typus mate in rapid succession up a male dominance hierarchy. Behavioral Ecology and Sociobiology 57:62–​68. Trivers, R. 1972. Parental investment and sexual selection. Pages 136–​179 in B. G. Campbell, editor. Sexual Selection and the Descent of Man. Transaction, New York. Upton, N. P. D. 1987a. Gregarious larval settlement within a restricted intertidal zone and sex differences in subsequent mortality in the polygynous saltmarsh isopod Paragnathia formica (Crustacea: Isopoda). Journal of the Marine Biological Association of the UK 67:663–​678. Upton, N. P. D. 1987b. Asynchronous male and female life cycles in the sexually dimorphic, harem-​forming isopod Paragnathia formica (Crustacea: Isopoda). Journal of Zoology 212:677–​690. Vetter, K. M., and R. L. Caldwell. 2015. Individual recognition in stomatopods. Pages 17–​36 in L. Aquiloni and E. Tricarico, editors. Social Recognition in Invertebrates: The Knowns and the Unknowns. Springer International, New York. Veuille, M. 1980. Sexual behaviour and evolution of sexual dimorphism in body size in Jaera (Isopoda Asellota). Biological Journal of the Linnean Society 13:89–​100. Wade, M. J. 1979. Sexual selection and variance in reproductive success. American Naturalist 114:742–​747. Wade, M. J., and S. J. Arnold. 1980. The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence. Animal Behaviour 28:446–​461. Weeks, S. C., and C. Benvenuto. 2008. Mate guarding in the androdioecious clam shrimp Eulimnadia texana: male assessment of hermaphrodite receptivity. Ethology 114:64–​74. Wellborn, G. A., and R. D. Cothran. 2007. Ecology and evolution of mating behavior in freshwater amphipods. Pages 147–​167 in J. E. Duffy and M. Thiel, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, Oxford. Wickler, W., and U. Seibt. 1981. Monogamy in Crustacea and man. Zeitschrift für Tierpsychologie 57:215–​234. Wilson, D. F., and K. K. Parrish. 1971. Remating in a planktonic marine calanoid copepod. Marine Biology 9:202–​204. Wiman, F. H. 1979. Mating patterns and speciation in the fairy shrimp genus Streptocephalus. Evolution 33:172–​181.

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11 SEXUAL SELECTION AND SEXUAL CONFLICT IN CRUSTACEANS

Rickey D. Cothran

Abstract Research using crustaceans has improved the understanding of sexual selection and sexual conflict. This is particularly true for understanding the biology of male weaponry and sexual conflict over mate guarding. Male crustaceans often are equipped with exaggerated claws that they use to monopolize access to females or resources that females use for reproduction. However, these weapons are often used in other contexts, e.g. mate choice and coercion of females, and understanding their evolution requires a broader perspective of how these traits are built and the fitness consequences of their use for both the bearer and interacting individuals. Although less well studied than male weaponry, crustaceans also provide excellent examples of elaborate sensory structures that are used in scramble competition among males for females. In addition to studies on male-​male competition, crustaceans have been well represented in research on intrasexual selection (for the most part, female mate choice). Crustacean females use a variety of sensory channels to assess mates, and a challenge is to better understand what is being conveyed by signaling males and the fitness consequences of mate choice for females. In some cases the female’s sensory system appears to be exploited by males, and this could lead to sexual conflict over mating. Research on crustaceans has also informed the understanding of sexual conflict over mate guarding, including the evolution of traits used to resolve conflict and how the ecological context shapes the costs and benefits of guarding for both sexes.

INTRODUCTION Sexual selection and sexual conflict, in the form of sexually antagonistic selection, are both important causes of mating trait evolution. Although often presented as alternative mechanisms of Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology evolutionary change (I myself have painted this overly simplistic picture; Cothran 2008a, Cothran et  al. 2010), both are often at work in populations. Kokko and Jennions (2014) have eloquently explained the relationship between sexual selection and sexual conflict in mating trait evolution. Sexual selection, differential mating success among individuals of the same sex due to phenotypic differences among them, inevitably leads to sexual conflict. One clear conflict between the sexes is the conflict between the choosy sex and individuals of the opposite sex that are not chosen as mates. If these unlucky individuals can trick or coerce individuals into mating, then they would increase their fitness at the expense of their mate. A less apparent conflict arises because sexual selection results in a situation where one sex can benefit by pursuing matings with other individuals of the opposite sex at the expense of its current mate. These two examples illustrate the importance of considering sexual selection and sexual conflict not as alternative mechanisms, but rather as co-​ conspirators in driving the evolution of mating traits. Sexual selection and the resulting sexual conflict will ultimately be mediated by the environment in which these interactions take place (Andersson 1994, Wellborn and Cothran 2007). The environment can affect mating interactions in a number of ways. First, the development of sexual traits will be sensitive to the environment in which an individual develops. Traits that are expensive to produce, such as large weapons and brilliant ornaments, may be particularly sensitive to differences in environmental quality (Rowe and Houle 1996, David et al. 2000, Bonduriansky and Rowe 2005, Cothran et al. 2012a). Even if an individual has a trait that will increase mating success or a preference that will reap indirect benefits (i.e., genetic) or direct benefits (i.e., those that increase the female’s survival or reproduction), expression of these traits may be costly in some environments (Pomiankowski 1987, Andersson 1994). Consequently, the variation that selection has to filter (i.e., phenotypic differences that manifest due to underlying genetics and the environment) and the filter itself (i.e., selection) will ultimately depend on the environment (i.e., ecology) in which mating interactions take place. In the following sections, I  discuss some examples of sexual selection and sexual conflict in crustaceans. I attempt to draw connections between different mechanisms of sexual selection and between sexual selection and sexual conflict. I then discuss some areas of research that may advance our understanding of sexual selection and sexual conflict in crustaceans. Mechanisms of Sexual Selection Sexual selection is a powerful evolutionary force that has produced some of the most eye-​catching traits that we see in the natural world. This is certainly true for crustaceans that exhibit impressive weaponry (e.g., claws of many decapods), brilliant colors and visual displays (e.g., brilliant carapaces of stomatopods and luminescent displays of ostracods), built structures (chimneys of fiddler crabs), and produce a cocktail of chemicals (shrimp, crayfish, lobsters, copepods) that individuals, usually males, use to improve their mating success. Sexual selection occurs via two mechanisms that can operate together in populations to shape the evolution of mating traits (Darwin 1871). Intrasexual selection results in elaborate sensory structures and impressive weaponry that individuals use to compete against other members of the same sex for access to the opposite sex. Intersexual selection occurs through interactions between the sexes where one sex uses their sensory system or physical power to filter available phenotypic variation in the other sex. In return, the “choosy” sex is expected to receive some sort of benefit that maintains the selective behavior in the population (Kokko 2001). However, the choosy sex may not always receive benefits from intersexual interactions. In these circumstances, their sensory system may be exploited to benefit the signaler, or they may be coerced into mating. Such circumstances result in sexual conflict over mating (Arnqvist and Rowe 2005).



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Intrasexual Selection Two broad categories of traits often result from intrasexual selection: weapons and elaborate sensory structures. I  will discuss crustacean examples of each of these categories, but first I  would like to start with body size and its ubiquitous role in resolving competition over mates. Sexual size dimorphism is common in crustaceans, and in many species, males are larger than females (e.g., Adams et al. 1985, Harvey 1990, Wellborn and Cothran 2007, Bauer et al. 2014). This pattern is consistent with sexual selection for large male body size, although sexual size dimorphism can also stem from other ecological causes (Shine 1989). In addition to this indirect evidence for sexual selection on male body size, measurements of sexual selection have been performed in some natural crustacean populations, and the general pattern is a positive relationship between male body size and mating success (e.g., Ward 1988, Wellborn 2000, Bertin and Cézilly 2003). While such studies provide the first steps toward understanding how body size affects mating success, they do not provide information about the mechanism of sexual selection responsible for the pattern. A mechanistic understanding of the relationship between body size and mating success requires careful observations and experiments. This can be especially difficult with body size because many traits, including weapons, scale with body size, and body size itself is always under many sources of selection, including correlated selection acting indirectly through other traits, e.g., selection on weapon size or body size in females (Fairbairn 1997, Bonduriansky and Day 2003). Clever experiments are necessary to overcome these obstacles. For example, Sneddon et al. (1997) used natural variation in relative chelae size in the shore crab, Carcinus maenas, to determine the relative importance of body size and chelae size in predicting winners of fights. They found that males with larger chelae were more successful than individuals with smaller chelae, but body size itself had little effect on the outcome of fights. Using natural variation in relative weapon size or expanding variation using phenotypic manipulation (given the ability of crustaceans to regenerate lost appendages) may provide clearer insights into the role that body size plays in intrasexual selection (Cothran et al. 2015). Weaponry Crustaceans exhibit some of the most impressive weaponry in the animal kingdom (Emlen 2008). These weapons are used to physically compete for access to females, a form of interference competition. In decapods and amphipods, males often use claw-​like traits to settle contests over females or resources that females use in reproduction. In decapods the claws consist of exaggerated chelae that males use to display to opponents, fight off competitors, or both. Perhaps the most impressive of these weapons, a record breaker (see Chapter 19 in this volume), is the single, greatly enlarged claw of fiddler crabs in the genus Uca, which has been broken up into Afruca, Australuca, Austruca, Cranuca, Deltuca, Gelasimus, Leptuca, Minuca, Paraleptuca, Thalassuca, Tubuca, and Uca (Shih et al. 2016; A in Fig. 11.1). In the context of intrasexual selection, the claw is used to signal to competitors (Pratt et  al. 2003, but see Jennions and Backwell 1996)  and to engage in contests over breeding burrows, and males with larger claws generally win contests over such burrows (Christy and Salmon 1984, Jennions and Backwell 1996). Importantly, this trait has also been found to be energetically expensive to bear and affects endurance, suggesting that it may be an accurate signal of male quality (Allen and Levinton 2007). In the hermit crab Pagurus nigrofascia, males use their chelae to fight for access to females. Males typically guard sexually mature females using their minor chelae to hold the female’s occupied gastropod shell (Hazlett 1968, 1972). The major chela is important in determining the outcome of takeover attempts. Males with larger chelae are more likely to win contests for females, even when they are smaller than their competitor, and loss of the major chela greatly reduces male competitive ability across a range of male competitor size asymmetries (Yasuda et al. 2011).

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Fig. 11.1. Examples of exaggerated chelae found in male decapods. (A)  Male and female of the fiddler crab, Uca deichmanni, demonstrating the enlarged chela of the male. (B) The three male morphs (robustus, intermedio, and typus) found in the rock shrimp Rynchocinetes typus. See color version of this figure in the centerfold. (A) Male from creative commons (https://​commons.wikimedia.org/​wiki/​File:Uca_​deichmanni.jpg); female courtesy of Arthur Anker with permission. (B) Courtesy of Martin Thiel with permission.   

In caridean shrimps (Decapoda: Caridea), several species have up to three morphotypes that vary in chelae size and consequently the strategy they employ to achieve mating success (B in Fig. 11.1). In each case, males make ontogenetic shifts from small males with relatively small claws that employ a sneaking mating strategy to large males with very large chelae that employ a strategy where they restrict access by other males to resources including females (Correa and Thiel 2003). Chelae are used to signal to competitors, and both size (Lee and Fielder 1982, Correa et al. 2003) and color (Rojas et al. 2012) of the claw may contain information that competitors use to modulate behavior. Large differences in weapon size result in subordinate males positioning themselves to avoid direct confrontations with dominant males (Lee and Fielder 1982). Escalation of contests to physical interactions tends to be more common in males with larger weapons, as evidenced by the increased number of wounds found in dominant male morphotypes (Thiel et al. 2010, Rojas et al. 2012, Bauer et al. 2014). In most species, large body size accompanies large weapon size, and males are larger than females (Correa et al. 2003, Bauer et al. 2014). However, in the dancing shrimp Rhynchocinetes brucei, dominant males are similar in size to females, suggesting that natural selection may oppose sexual selection for larger size in this species (Thiel et al. 2010). Despite the frequent pattern of sexual dimorphism in claw size in decapods, relatively few studies have demonstrated that males with larger claws have higher mating success due to their superior function in male-​male competition for mates (e.g., Sneddon et al. 1997). One obvious hurdle in studying the relationship between chela size and mating success is allometry. Large males typically have larger claws so that the relative importance of these two traits in settling contests is important. Moreover, few studies have addressed the possibility that claws are used in intersexual selection or have a dual purpose. For example, the major chelae of the crayfish Orconectes rusticus have chemosensory structures that are used to detect female odors (Belanger and Moore 2006), and the claws of fiddler crabs and other decapods are used to display to females (Christy and Salmon 1991, Mariappan et al. 2000), to forage, and to handle mates (Lee 1995). Addressing claw function in a variety of different contexts will improve our understanding of the evolution of weaponry and its maintenance in decapod lineages.



Sexual Selection and Sexual Conflict in Crustaceans

Males in several species of amphipods possess exaggerated claw-​like appendages. In most amphipods the first two pereopods are modified into claws called gnathopods (Fig. 11.2). In some species these claws are sexually dimorphic, with males possessing larger claws than females. Sexual dimorphism of gnathopods is associated with how males obtain mates: sexually dimorphic species tend to guard mates, whereas species with no sexual dimorphism employ a searching strategy (Conlan 1991). When sexual dimorphism exists, it is usually the second pair of pereopods that are modified (i.e., the posterior gnathopods; Conlan 1991). Two broad categories of mate guarding are common in amphipods mate attenders and contact mate guarders (Conlan 1991). The most impressive gnathopods are found in species that attend their mates (Borowsky 1984, Conlan 1991). Despite the menacing appearance of these claws, evidence for their use in male-​male combat over access to females is sparse in the literature, and much of the evidence that exists is from observational studies. Borowsky (1985) used detailed behavioral observations to reveal the role of posterior gnathopods in mating interactions in the tube-​dwelling amphipod Jassa falcata. Males attend the tubes of females and aggressively guard access to their mate. Males come in two types, thumbed and thumbless males, with the former using their gnathopods in agonistic interactions with other males. When two thumbed males battle for access to females, the males lock posterior gnathopods and then push each other with their antennae and attack their opponent’s head with the smaller anterior gnathopods. Males with fully developed, thumbed gnathopods were more successful at gaining access to females regardless of their relative size. In the congener J. marmorata, however, these weapons were less effective when thumbed males had to deal with a majority of thumbless males (Clark 1997). Thumbless males are smaller and quicker than thumbed males and

Aquatic carriers

Semi-terrestrial carriers

Attenders

Fig. 11.2. Examples of exaggerated posterior gnathopods of amphipods. From top to bottom, aquatic carriers:  Eulimnogammarus obtusatus(from Lincoln, 1979), Echinogammarus marinus (from Lincoln, 1979), Hyale nilssoni (from Lincoln, 1979), Allorchestes angusta (unpublished), and Melita nitida (unpublished); semi-​ terrestrial carriers: Pseudorchestoidea brito (from Lincoln, 1979); Megalorchestia californiana (from Bousfield, 1982b), Traskorchestia traskiana (from Bousfield, 1982b), Orchestia mediterranea (from Lincoln, 1979), and Talorchestia deshayesii (from Lincoln, 1979); attenders:  Lembos websteri (from Lincoln, 1979), Dyopedos porrectus (from Lincoln, 1979), Jassa falcata (from Conlan, 1990), Ericthonius brasiliensis (from Lincoln, 1979), and Caprella gorgonia (from Laubitz and Lewbel, 1974). Figure redrawn from Conlan (1990), with permission from Kluwer Academic Publishers.   

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Reproductive Biology employ a sneaking strategy to obtain matings. These two male morphs fluctuate seasonally with the large, aggressive, thumbed males occurring in the late spring and early summer when females are large, fecund, and rare (Clark 1997). It is possible that these weapons may be used in male-​female interactions to overcome the resistance of larger females, which can mate with multiple males during their receptive period. Based on similarity in mating systems, with cruising males searching for receptive females and attending the females during their receptive period, other tube-​dwelling peracarids that have similar extreme patterns of sexual dimorphism in posterior gnathopods likely employ these structures in battles with males over access to females (Borowsky 1983). In many amphipod species with sexually dimorphic posterior gnathopods, males use contact mate guarding in which they physically attach to and sometimes carry the female in an effort to monopolize access. Contrary to intuition, males do not employ their exaggerated posterior gnathopods to carry the female, but rather use the anterior, more sexually monomorphic gnathopods for attachment (Borowsky 1984). Evidence for the use of posterior gnathopods in intrasexual selection is equivocal in this group. One obvious way the gnathopods could be used in the context of contact mate guarding is in takeovers. Takeovers have been documented in some amphipods, but the use of gnathopods in this context is unknown. There is some evidence that larger males are more successful at resisting takeover attempts and taking over females from smaller males, but takeovers are rare (Strong 1973, Ward 1983, Elwood et al. 1987, Wen 1993). This could be because larger males tend to pair more often with females, or because the behavior itself is rare in amphipods. The manipulative experiments that have been performed on the use of gnathopods demonstrated that these traits were used in male-​female interactions that lead to pairing or fertilization rather than in male-​male combat over access to females (Hume et al. 2005, Cothran et al. 2010, Cothran et al. 2015). In mate-​attending caprellid amphipods, males engage in sometimes lethal combats over access to females. Caprellids often possess extreme sexual dimorphism in the posterior gnathopods, with males possessing much larger claws equipped with a poison spine (Takeshita and Wada 2012). Males use these claws in agonistic interactions over access to females, and these fights are often lethal, contributing to female-​biased sex ratios in populations (Lewbel 1978, Lim and Alexander 1986, Takeshita and Henmi 2010). Stomatopods have a pair of enlarged second maxillipeds that they use to capture prey, defend against predation, and resolve contests with other stomatopods (Reaka and Manning 1981, A  in Fig. 11.3). However, the use of these raptorial appendages in mating interactions is poorly understood. Most of the research concerning aggressive interactions centers on contests over defendable burrows. These burrows are important for predator avoidance and brooding of offspring. In some species, both morphological (meral spot) and behavioral components (meral spread) of claws contain information that is used in signaling during agonistic interactions (Hazlett 1979). In Neogonodactylus bredini (both size-​matched and randomly staged contests, dyadic contests) had consistent patterns: (1) visual tracking and approaching opponent, (2) visual meral spread or antennal flicking, (3) ritualized striking of telson using second maxillipeds, and (4) contest resolution based on mutual assessment of resource-​holding potential (Green and Patek 2018). Winners of contests did not have greater strike force than losers but did strike more often. Winners were also more massive than losers, and 94% of strikes were received on the recipient’s telson while in the telson coil posture. Rarely, winners of contests would stab retreating losers, causing significant injury. The authors suggest that these behaviors may accurately signal body size, which could be hard to discern in these burrow-​dwelling animals. The meral spread was effective in limiting physical altercations in Gonodactylus zacae, with smaller individuals exhibiting a greater number of spreads (Caldwell and Dingle 1975). These studies show that stomatopods do use both morphological and behavioral information in agonistic interactions, but future studies need to address whether males use this information in resolving competition for access to females.



Sexual Selection and Sexual Conflict in Crustaceans (A)

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Fig. 11.3. Possible weapons that are not considered “claw-​like.” (A) Second maxillipeds of stomatopods. (B) Alternative male morphs of the isopod Paracereis sculpta showing enlarged uropods and pleotelsons of alpha males. (C)  Exaggerated antennae of the California beach flea Megalorchestia californiana. The enlarged posterior gnathopods, claw-​like appendages, are also highlighted in the photo. (D) Dorsal horns of Deto echinata. See color version of this figure in the centerfold. (A) From Green and Patek (2015), with permission from Royal Society Publishing; (B)  figure redrawn from Shuster (1992), with permission from Brill; (C)  picture courtesy of Vikram Iyengar with permission; (D) From Glazier et al. (2016), with permission from John Wiley & Sons, Inc.   

There are other cases in crustaceans where males use claw-​like traits in mating interactions. For example, males of the tanaid Leptochelia dubia use their enlarged chelae to fight rival males (Highsmith 1983). All aggressive interactions observed were between males. Clam shrimp and cladoceran males have claspers that they use to hold on to the female’s carapace in precopula (Weeks and Benvenuto 2008, Sigvardt and Olesen 2014). These claspers are modified thoracic appendages, and there are no records of them being deployed directly in male-​male combat (Elmoor-​Loureiro  2006). Other examples of weapons outside of “claws” can be found in the Crustacea. In the marine isopod Paracerceis sculpta three alternative male morphs compete for access to females: alpha, beta, and gamma males (Shuster 1987; B in Fig. 11.3). Alpha males have enlarged uropods and pleotelsons. Alpha males use these traits to defend females located in spongocoels from intruding males when in the “resident” position and to evict resident males when in the “intruder” position (Shuster 1992). The other two types of males lack this weaponry and employ a female mimic and sneaker strategy, respectively (Shuster 1992). Antennae have also been considered weapons in some crustaceans. In terrestrial isopods (Oniscidae), sexual dimorphism of the antennae (males have larger antennae than females) has been interpreted as evidence that males use these structures in combat over females (reviewed in Kight 2008). However, the most complete study to date on the use of antennae in terrestrial isopods discovered a negative correlation between the magnitude of sexual dimorphism in antennae and

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Reproductive Biology male-​male combat in this group (Lefebvre et al. 2000). The authors concluded that these structures are more likely used to find females in scramble competition for mates. In the California beach flea Megalorchestia californiana, extreme sexual dimorphism is observed in body size, posterior gnathopod size and color, and antenna size and color (Iyengar and Starks 2008; C in Fig. 11.3). These amphipods are found on beaches, where they occupy burrows during the day, and males compete for burrows that may house several females (Bowers 1964). Larger males with larger gnathopods and antennae are more successful at competing for mates (Iyengar and Starks 2008). Males use their exaggerated antennae to evict smaller males from burrows and hold on to them while attacking them with their gnathopods. Grasping antennae are also found in copepods (particularly harpacticoids, but also in cyclopoids and calanoids) and in anostracans. Despite the menacing appearance of these structures, I found no evidence that these traits are used as weapons in male-​male competition. Rather, evidence suggests that these structures are used in intersexual interactions (Boxshall 1990, Ohtsuka and Huys 2001, Rogers 2002). Another unusual, sexually dimorphic trait is the dorsal horns found in the South African horned isopod Deto echinata (D in Fig. 11.3). Males of this species have six or seven exaggerated dorsally projecting spines that are paired and occur laterally on the surface of the pereon segments (Glazier et al. 2016). These spines vary in size among males, have a steeper scaling relationship with body size in males than juveniles and females, and are condition dependent. However, they are not particularly sharp, and it is unclear how males would use these spines as weapons against rivals. Exaggerated Sensory Structures Males need not engage in physical contests to compete for mates. Scramble competition, a form of exploitative competition, is common in crustaceans. In these cases, sexual selection favors traits in males that make them more efficient at finding females. In crustaceans, the most obvious traits used to locate mates are the two pairs of antennae (the first pair referred to as antennules); however, chemosensory structures have also been observed on gnathopods and other appendages (Kaufmann 1994). In the following paragraphs, I highlight some studies that have advanced our knowledge of scramble competition for mates and the traits involved in this form of mating competition. Although sometimes employed to battle same-​sex rivals or grasp females, the antennae of crustaceans most often serve a sensory role. These structures are covered with chemosensory and mechanosensory structures that allow individuals to receive information about their environment. The antennae of many crustaceans contain microstructures (e.g., aesthetascs and calceoli) with known chemosensory functions that are often more abundant in males than females (Thiel 2011, A in Fig. 11.4). The common sexual dimorphism that occurs in these appendages is often assumed to be due to selection for efficient location of females. Surprisingly, there are few studies that have confirmed that these traits are indeed under sexual selection, or that have experimentally identified their function in mate location. Perhaps the best-​studied group in terms of the role of antennae in mate competition are the isopods. In the freshwater isopod Asellus aquaticus, antennae were under sexual selection in five populations collected from Burgundy, France (Bertin and Cézilly 2003). The same authors confirmed the function of antennae in mate location using a manipulative experiment in which they reduced the size of the second antennae, producing two groups of males: short antennae (flagella cut to 1 mm in length) and long antennae (flagella cut to 4 mm). They included both an anesthesia control and an intact control in the study and controlled for body size differences between males. They discovered that males from all treatments could successfully form precopulatory pairs with females (trials lasted 7 hours), but males with shorter antennae were both less effective at finding females and less likely to pair with females during a relatively short observation period (15 minutes). This study confirmed both pattern of sexual selection on antenna size and mechanism of how this



Sexual Selection and Sexual Conflict in Crustaceans (A)

(B)

Fig. 11.4. Exaggerated sensory structures found in male crustaceans. (A) Scanning electron micrograph showing sexual dimorphism in the chemosensory structures (callynophore aesthetascs) found on antennae of the scavenging Lysianassoid amphipod Orchomene abyssorum. (B) Sexual dimorphism in eyes found in myodocopa ostracods. See color version of this figure in the centerfold. Lateral view of animals with half of carapace removed. Lateral eyes are indicated by arrows. Scale bar is 500 um. (A) From Kaugmann (1994), with permission from Brill; (B) from Rivera and Oakley (2009), with permission from Wiley.   

trait is used in mate competition. Sexual dimorphism in antennae is also common in terrestrial isopods, where they most likely play a role in locating females (Lefebvre et al. 2000). Patterns of sexual dimorphism and the functional role of antennae in scramble mate competition are less well studied in other crustacean groups. Sexual dimorphism in antenna size has been documented in other peracarids (reviewed in Thiel 2011); however, patterns of sexual selection on antennae and their functional role in mating competition have not been revealed. In Hyalella amphipods, antennae are sensitive to resource stress and thus are expected to vary in size among males depending on their condition (Cothran et al. 2012a). This should provide plenty of phenotypic variation for selection, as antennae are expected to capture some of the variation associated with male condition (Rowe and Houle 1996). There are few studies documenting sexual dimorphism in antenna size or structure in other well-​studied groups of malacostracans (e.g., decapods; Thiel and Breithaupt 2011). An interesting exception is the hermit crab Pagurus middendorffii, where it has been confirmed that males have longer antennae than females (Morita and Wada 2018). Morita and Wada (2018) used ablation experiments with controls to assess whether antennae were used in mate competition. They discovered that males with ablated antennae were as successful in both scramble competition for females and in contest competition with other males over guarded females than males from the control groups. The authors suggest that the sexual dimorphism in

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Reproductive Biology antennae size observed in this species may be due to different ecological challenges experienced by the sexes (Shine 1989). Outside of the clasping antennae of copepods, branchiopods, and anostracans, patterns of sexual dimorphism in antennae are not well documented in other groups of crustaceans. Chemosensory structures are also located on the body surface and other appendages in some crustaceans (Kaufmann 1994). Interestingly, one such structure is the peracarid gnathopod. Perhaps this structure has a dual purpose as both a weapon in interference competition for access to females and a large surface area for the deployment of chemosensory structures that increase the efficiency of finding females (i.e., exploitative competition) or assessing the state of the female while forming precopulatory pairs or while in precopula (Hunte et al. 1985, Dick and Elwood 1989a). In addition to chemical cues, male crustaceans may use visual cues to find females. In Myodocopida ostracods, three independent origins of extreme eye sexual dimorphism have occurred (Oakley 2005; B in Fig. 11.4). The mechanism(s) driving the evolution of extreme sexual dimorphism in eye size in this group is still in question. Interestingly, the evolution of complex eyes does not necessarily correspond with the evolution of bioluminescence, which is also found in the Myodocopida (Oakley 2005). This is perhaps not surprising, given that males are the sex that use bioluminescence during courtship (Rivers and Morin 2008, Morin and Cohen 2010). However, males do respond to the bioluminescent displays of other males and use this information to employ sneaking strategies where they intercept receptive females (Morin and Cohen 2010). It would be interesting to explore whether the quality of bioluminescent displays and eye size trade off in males given that these traits are part of alternative reproductive tactics. Exaggerated eyes may also increase a male’s chances of seizing a receptive female that joins the bioluminescent swarm, which can be extremely male-​biased in terms of operational sex ratio (e.g., up to 176 males to each female has been observed in Vargula annecohenae swarms; Rivers and Morin 2008). Finally, male eye size has been found to improve a male’s chances of evading visual predators in non-​luminous species (Euphilomedes). Blindfolded males were more likely to be consumed by predatory fish than control males (blindfold present but not covering the lateral eye) and unaltered males (Speiser et al. 2013). Blindfolding had no effect on predation risk in females, which have rudimentary eyes. Larger eyes in males may be selected for because they spend much more time in the water column, where predatory fish are active (Speiser et al. 2013). Future comparative studies should address the relative contributions of male-​male interactions, mate searching, and ecological pressures on the evolution of male eyes in this group. Intersexual Selection Intersexual selection, typically in the form of female choice, occurs when same-​sex individuals vary in mating success due to the expression of mating preferences expressed by the opposite sex. The “choosy” sex is expected to receive either direct (i.e., benefits that increase the immediate fitness of the choosy individual) or indirect (i.e., benefits received by producing superior offspring) benefits for expressing mating preferences. I will briefly summarize some studies that have used crustaceans to explore questions related to intersexual selection, with a focus on the traits used to signal quality and the benefits associated with being choosy. A critical component of intersexual selection is that the choosy sex receives information about the quality of potential mates. Thus, signaling theory plays a central role in research on mate choice. Crustaceans use a variety of sensory modalities to transmit and receive information related to mating. Although the majority of research has focused on chemical communication, crustaceans also use visual and mechanical sensory channels to advertise to prospective mates (Thiel and Breithaupt 2011). These signals may represent an index by which the receiver can make decisions



Sexual Selection and Sexual Conflict in Crustaceans

about mate quality or may serve as handicaps that demonstrate an individual’s ability to function at a high level despite expressing an expensive or costly trait (Andersson 1994). By paying attention to such signals, the receivers are able to filter potential mates and make decisions that increase their own or their offspring’s reproductive success. Thus, choosy individuals are expected to have higher fitness than individuals that mate randomly (Kokko 2001). Visual signals are clearly involved in mating of several malacostracan crustaceans, with stomatopods and crabs being the best-​studied groups. Smasher stomatopods are often brilliantly colored and are capable of color vision (Christy and Salmon 1991, Marshall et  al. 1996). In the smasher stomatopod Haptosquilla trispinosa, males with manipulated first maxillipeds (so that they were unable to reflect brightly blue colored polarized light) had to court females longer, experienced shorter mating durations, and received increased aggressiveness from females compared to control males (Chiou et al. 2011, A in Fig. 11.5). This study clearly shows that female H. trispinosa use male coloration to guide their behavior when interacting with potential mates. However, the information that males are signaling and the benefits that females receive from using this information are unknown. The crabs have been relatively well studied with respect to potential visual signals, particularly with respect to coloration patterns. However, the majority of studies have addressed proximate mechanisms for color patterns (Caro 2018). Many species of crabs are brilliantly colored. Coloration in both anomuran and brachyuran crabs have many proposed functions, and some studies have confirmed that color is important in mate choice (Caro 2018). The best studied group

(A)

(C)

(B)

Fig. 11.5. Brilliantly colored crustaceans where mate choice based on color has been documented. (A)  Smasher stomatopod, Haptosquilla trispinosa. Arrows denote the first maxillipeds. Insets on the right show the maxilliped before (top) and after (below) treatment with a hot pin head to compromise the signaling patch. (B) Natural variation in the yellow and orange color of the enlarged claw of the fiddler crab Austruca mjoebergi. (C) Variation in the claw color of female blue crabs Callinectes sapidus. See color version of this figure in the centerfold. (A) From Chiou et al. (2011), with permission from The Taylor Francis Group; (B) from Detto (2007), with permission from The Royal Society Publishing; (C) courtesy of Jamie Fergus with permission.   

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Reproductive Biology of crabs with respect to use of visual cues and mate choice are fiddler crabs. These crabs are often colorful and use a claw-​waving display to communicate with other crabs. How crabs use information contained in body coloration has not been well resolved in most species. The species specificity of coloration points toward species recognition as the primary function of color patterns (Zeil and Hemmi 2006); however, in the well-​studied species Austruca mjoebergi, females use color in mate choice. Females of this species have been found to recognize the color patterns of conspecific males (Detto et al. 2006) and prefer males with yellow claws over those with grey claws (Detto 2007, B in Fig. 11.5). Females did not discriminate yellow claws that varied in brightness, even though considerable variation in this trait is present in A. mjoebergi populations. Females also prefer males with intact UV signals to males that had these signals blocked with sunscreen; however, the function(s) of these signals are still unclear. They may be informative for mate quality, species recognition, or increase mate conspicuousness (Detto and Backwell 2009). Another interesting case where color may be used to signal quality is in the California beach flea, M. californiana. In addition to having larger antennae and posterior gnathopods, males have redder antennae than females (C in Fig. 11.3). The hue of the male antennae is correlated with both body mass and antennal length. Therefore, this trait may contain information that females, and perhaps male rivals, can use to assess a male’s quality (Iyengar and Starks 2008). There is also evidence of color patterns being important in male mate choice. Male blue crabs, Callinectes sapidus, preferred females with red-​clawed dactyls over females with white-​and black-​ clawed dactyls (Baldwin and Johnsen 2009, C in Fig. 11.5). The function of the female claw color in this species remains unknown. It is possible that claw coloration identifies opposite-​sex individuals in this highly aggressive and sometimes cannibalistic species, signals female reproductive status, or is an ornament used to convey female quality. The latter may be especially important given that the pigmentation is derived from carotenoids, which may indicate foraging ability (Endler 1980) for a resource that is deposited in eggs and important in embryo development (Pérez-​Rodríguez 2009). A spectacular example of a visual courtship display occurs in bioluminescent cypridinid ostracods. At night, males of these normally benthic crustaceans swim into the water column and produce courtship displays formed by emitted light (caused by luciferase reacting with its substrate luciferin) that attracts the attention of females (Morin and Cohen 2010). Within the cypridinids, there is tremendous diversity in the pattern of the display, and much of this diversity appears to be explained by selection for species recognition (Morin and Cohen 2010). There is also variation in the luminescent signal within species (i.e., among males) suggesting that females and competing males (males sometimes employ a sneaking strategy where they intercept attracted females) may be able to gain information about the signaling male (Rivers and Morin 2008, Morin and Cohen 2010). The source of inter-​male variation in signal is currently unknown, as is whether females use the information in mate choice. The only study that has addressed investment costs of the signal discovered that the courtship display was less costly to produce than defensive displays (used against predators) during which males released 50 times more luminescence (Rivers and Morin 2012). Additional studies on visual signals in crustaceans have been performed in other decapods. In the rock shrimp, Rynchocinetes typus, dominant robustus males and females use primarily visual and chemical signals, respectively, to find each other and mate (Díaz and Thiel 2004). The mating system, composed of “neighborhoods of dominance,” favors females that use chemical signals to discover preferred dominant males, avoiding detection by subordinate males that may eavesdrop on female-​produced chemical signals. Once females are in their vicinity, dominant males use visual cues to locate receptive females. Females benefit from mating with robustus males, which provide protection of females during mating and increased fertilization success because they have larger sperm stores to fertilize eggs (Correa et al. 2003, Hinojosa and Thiel 2003). However, it is not clear whether males use any of the visual stimulation from females to choose among possible mates. Interestingly, a similar mating system is described in American lobsters, Homarus americanus,



Sexual Selection and Sexual Conflict in Crustaceans

although the visual component of communication is replaced by females chemically signaling to dominant males once in their vicinity (Atema and Cowan 1986, Bushmann and Atema 1997, Atema and Steinbach 2007). In the crayfish Austropotamobius pallipes, there is also evidence that males use both visual and chemical cues to locate females, but there is no evidence that males use these cues/​ signals in mate choice (Acquistapace et al. 2002). Male fiddler crabs are also well known for their claw-​waving displays and built structures that they use to attract mates (Christy and Salmon 1991). In Austruca annulipes, males that wave their enlarged claw faster are more likely to be selected as mates (Backwell et al. 1999). Males also use hoods or other built structures as sensory traps to attract and retain females (Christy et al. 2003, Christy 2007). The information females receive from such displays is not clear, and it is likely that females use this and several other characters (males size, claw size, color) when making mating decisions (Christy and Salmon 1991). Male ghost crabs and fiddler crabs (Ocypodidae) use acoustic signals in courtship (Salmon 1983, Lucrezi and Schlacher 2014). These signals are transmitted as substratum vibrations and are received by the females’ Barth myochordotonal organs. In some species, females select males based on size (Leptuca pugilator and Minuca rapax) and burrow position (L. pugilator), and it is possible that the acoustic signaling by males transmits information about the quality of a mate (Salmon 1983). However, links between acoustic signaling and mate quality have not been revealed. These signals also appear to be used in species recognition, but the fact that, at least in some species of Ocypode, males limit signaling overlap with conspecific males suggests that the signals may be used in intraspecific interactions as well (Salmon 1983). Acoustic signals are also produced in terrestrial crabs (Gercarcinidae and Grapsidae) and stomatopods, although whether they function in signaling mate quality is unknown (Salmon 1983, Patek and Caldwell 2006). While it is clear that the primary sensory channel used by most crustaceans is chemical (Thiel and Breithaupt 2011), evidence for the use of chemical cues or signals in mate choice is limited. There are several contributions to the use of chemicals in mate location (i.e., sex and species identification) in a wide variety of crustaceans (amphipods: Borowsky 1991, copepods: Kelly and Snell 1998, and decapods:  Cowan 1991, Bushman 1999, Correa and Thiel 2003); however, research on the use of chemicals by females to select among conspecific males is restricted to decapods. In the lobster H. americanus, and the rock shrimp, R. typus, females use chemical information to choose dominant males as mates (Bushmann and Atema 2000, Díaz and Thiel 2003). It is likely that females are using the same chemical information contained in the urine that males use to assess each other during agonistic interactions (Bushmann and Atema 2000, Breithaupt and Eger 2002, Bergman and Moore 2005). Theory predicts that females should receive benefits from mate choice that more than compensate for the costs associated with mate choice (Andersson 1994). In species where females receive direct benefits in the form of nuptial gifts or other resources, the benefits associated with mate choice are quite clear (Andersson 1994). Here female fitness is directly affected by her choice of a mate. Such benefits may be important in crustaceans. For example, in U. pugilator, females chose males with burrows that were located at higher elevation during high tide periods. In doing so, females were less likely to breed in a burrow that could collapse during tidal inundation (Christy 1983). However, males with better burrows were not consistently larger than other males, and male size is also important in determining male mating success in this and other fiddler crab species (Christy 1983, Backwell and Passmore 1996). It is unclear how females balance the benefits of mating with males based on size and burrow location, and ultimately their ability to choose may be compromised by the costs of mate searching (Christy 1983). Direct benefits can also be more cryptic in nature (Reynolds and Gross 1990). In Hyalella amphipods, females paired with large males are less likely to be consumed by predators (Cothran 2008b, Cothran et  al. 2012b). Given that precopulatory and postcopulatory mate guarding are

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Reproductive Biology common in crustaceans, this direct benefit of mate choice may be widespread. Also, in many decapods, and perhaps other groups, males attend females after copulation (see Chapter 6 in this volume). This is a form of postcopulatory mate guarding and it has been proposed to function in protecting females from predators and cannibals, although use of this behavior to guard against sperm competition seems to be better supported by the current evidence (Wilber 1989, Jivoff 1997). Regardless, it is possible that females that choose larger, more dominant males will be better protected than females paired with smaller males. Moreover, these males may be able to better protect females from injury during takeover attempts by rival males (Smith 1992). Females may also receive indirect benefits from mate choice through the production of superior offspring (Andersson 1994). In Hyalella amphipods, females allowed to choose their mate in the field produced male offspring that were more successful in mate competition than the male offspring of randomly mated females (Cothran 2008b). Whether indirect benefits of mate choice are important in explaining costly female mating preferences in other crustaceans is an area that warrants future research. Sexual Conflict Sexual conflict occurs when the evolutionary interests of individuals of the two sexes do not align (Parker 2006). Crustaceans have been relatively well represented in sexual conflict research. Sexual conflict can arise over mate-​guarding duration, sensory exploitation, and coercive mating tactics. Perhaps the area where crustaceans have been best studied with regard to sexual conflict is research over mate guarding. Sexual conflict over mate guarding occurs whenever the optimal guarding period for the sexes differs ( Jormalainen 1998). This can result in an overt behavioral conflict in which males and females fight over whether they enter the guarding phase. Mate guarding can either be precopulatory or postcopulatory, and both types of guarding can be a source of conflict between the sexes (Arnqvist and Rowe 2005). Precopulatory mate guarding is a consequence of time-​limited female receptivity to fertilization (because in many crustacean species eggs can only be fertilized after the molt) and is considered a male time-​investment strategy (Ridley 1983). Rather than searching for a female that is receptive to fertilization, males seize females and guard them until they become receptive (i.e., they molt). The benefits to the male are obvious, as he monopolizes access to the female, but the optimal guarding strategy from the male’s perspective is not that simple. If males spend too much time in precopula, they miss out on mating opportunities. Thus, a male’s investment in precopula should be sensitive to the prospects of finding additional mates if he continues to search as well as guarding costs (reviewed in Jormalainen 1998). Indeed, males in some crustaceans can sense how close females are to their molt and adjust guarding durations to the level of competition for mates (reviewed in Jormalainen 1998). For example, in the amphipod Gammarus pulex, males can simultaneously hold two females and select the higher quality female, based on time to the female molt and female size (larger females are more fecund), within a few seconds (Dick and Elwood 1989b). The benefits of guarding to females are less clear. Under cases where mate availability is low, guarding may ensure that females have access to a male during the critical period after the molt. Guarding may also provide females an opportunity to select high-​quality males and trade up if an even better option presents itself. For example, in the hermit crab Pagurus filhol, paired females delay copulation and in doing so provide more opportunity for takeovers by rival males (Yamanoi et al. 2006). There is also evidence that females “encourage” these takeovers by signaling to males using pheromones (Sneddon et  al. 2008, Okamura and Goshima 2010). In Gammarus pulex, females guarded for longer intervals had shorter intermolt intervals without a reduction in fecundity (Galipuad et  al. 2011). While the mechanisms behind this pattern are unclear, a shorter intermolt interval should translate to a higher mating rate and perhaps increased reproductive



Sexual Selection and Sexual Conflict in Crustaceans

success. However, these benefits must be weighed against the costs associated with guarding. In many crustaceans, males control the movement of the pair, which may limit foraging opportunities for females (reviewed in Jormalainen 1998). In the skeleton shrimp Caprella penantis, females exposed to male-​biased sex ratios were guarded for longer and had reduced growth and number of offspring (Takeshita et al. 2011). It is possible that this effect was the result of reduced foraging by females while paired, although energetic costs associated with deflecting male harassment may also explain the observed fitness costs. In the ostracod Eulimnadia texana, longer guarding durations were associated with decreased gut fullness in hermaphrodites, but not in the males that were guarding them (Benvenuto and Weeks 2012). In the isopod Idotea baltica, females suffered both an energetic cost and fecundity cost associated with precopulatory mate guarding ( Jormalainen et al. 2001). Pairing may also increase an individual’s susceptibility to predators (Cothran 2004), which may change male and female behaviors associated with mate guarding. In the amphipod Gammarus duebeni, females decreased investment in resistance behavior and males were less tenacious in their pair bond under perceived predation risk (Dunn et al. 2008). Although males will also incur costs associated with guarding, the cost-​to-​benefit analysis is likely more weighted on the benefit side for males. Moreover, if males are the mate-​searching sex, searching for females may be riskier than pairing when it comes to avoiding predation (Thiel et al. 2001, Cothran 2004). Postcopulatory mate guarding in crustaceans has been proposed to serve two functions, and the prospects for conflict between the sexes depends on which mechanism is most important in the species. In both stone crabs (Menippe mercenaria) and blue crabs (Callinectes sapidus), postcopulatory mate guarding duration increases under the threat of predation. This has been interpreted as males protecting recently molted females, as in many crustaceans molting and fertilization occur together in these species (Wilber 1989, Jivoff 1997). Moreover, female stone crabs were more likely to be consumed by blue crabs if they were guarded for shorter durations (Wilber 1989). However, in both of these species, guarding duration is even longer when males experience high mate competition. Thus, it appears that the strongest driver of postcopulatory mate guarding is likely avoidance of sperm competition. Whether females pay costs associated with guarding durations that are longer than necessary for protection during the vulnerable post-​molt period is unknown. Jormalainen (1998) provided a framework for understanding the compromised guarding durations we often observe in natural populations (Fig. 11.6). The conceptual model takes into account costs associated with guarding over the course of the female’s molt interval. Costs to females increase from tf (the optimal guarding duration for females) as guarding duration increases. Any of the aforementioned costs of guarding could contribute to this rising function of female guarding costs with longer mate guarding duration. For males, the costs of losing a female in an encounter increase from the male optimal guarding duration (tm) to the female molt (t = 0). This is because females closer to their molt require less time investment, increasing the opportunity for males to find additional females. Where the two cost functions intersect represents a compromised guarding duration (tc). Longer guarding durations within the zone of conflict can be considered as the male winning the contest over guarding duration, and shorter guarding durations as the females winning (represented by gray shading on arrows). Note that there are also areas where there is no conflict, represented by really short guarding durations (pays for both sexes to pair) and really long guarding durations (pairing is too costly for both sexes). Some of the predictions from this conceptual model have been tested in crustaceans. For example, in the isopod Lirceus fontinalis, males use female molt hormones to locate females, which may minimize missed opportunity costs and females effectively use resistance to avoid male guarding attempts (Sparkes et al. 2000). Moreover, studies that have used phenotypic manipulation to tip the scales in favor of one sex over the other in conflict over guarding duration have demonstrated that males and females disagree over guarding duration in natural populations of crustaceans

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Fig. 11.6. Jormalainen’s graphical model of sexual conflict over mate guarding duration. The model considers contest outcomes between females and males along a range of contest costs (solid lines) and the female molt interval (x-​axis). Labels on the x-​axis are time points in the female molt interval: “0” is the sexual molt, “T” is the start of the female molt cycle, and tf, tm, and tc are times during the female molt where the female optimal guarding criterion, male optimal guarding criterion, and compromised guarding criterion fall, respectively. t'c represents a case where males are twice as powerful as females in determining the outcome of the conflict over guarding duration. See text for further details. Redrawn from Fig. 2 in Jormalainen (1998), with permission from The University of Chicago Press.   

(amphipods:  Cothran 2008a, Cothran et  al. 2010, Cothran et  al. 2015, isopods:  Jormalainen and Shuster 1999, Miura and Goshima 2016, ostracods: Benvenuto and Weeks 2012). Another source of sexual conflict over mating is sensory exploitation. In this case, a signal is produced that exploits the sensory system of a receiver for the signaler’s benefit. Excellent examples of sensory exploitation occur in fiddler crabs, where males use visual signals to deceive females and increase the male’s chances of mating (reviewed by Christy and Rittschof 2011). In Leptuca terpsichores and other species, males build structures that draw females to areas they perceive to lower their predation risk. For example, in Leptuca beebei, experimentally increasing the perceived predation risk resulted in females increasing their preference for males with pillars (Kim et al. 2009). In this case females are deceived, but there is evidence that males that build structures are in better condition (i.e., good quality mates) and hence there may not be an evolutionary conflict associated with the deception. In Minuca pugilator, males court females near structures they build next to their burrow. When a female rejects a male and begins to move away, the male crawls atop the structure to produce a visual signal that startles the female, causing her to return to the male’s burrow. Whether such deception has negative consequences for female fitness is unknown. Perhaps the most overt form of sexual conflict over mating is coercive mating. In crustaceans, coercive mating includes cases where males forcibly overcome female resistance to mating or the initiation of precopula. There has been much debate as to whether females use physical resistance



Sexual Selection and Sexual Conflict in Crustaceans

to select males or if females incur a net fitness cost from these interactions, i.e., represent sexual conflict (e.g., Kokko 2005, Peretti and Córdoba-​Aguilar 2007). Examples of apparent coercive mating are common in crustaceans (e.g., Christy 1987, Jormalainen 1998, Sparkes et  al. 2000, Contreras-​Garduño and Córdoba-​Aguilar 2006); however, there has been little work on the fitness consequences of such interactions for females. In cases where females are vulnerable to predation or advancements by conspecific males (e.g., Wilber 1989, Jivoff 1997), physical resistance may ensure that females are “guarded” during this vulnerable period by large males that can offer superior protection. Females may also benefit indirectly through the production of manipulative male offspring that compensate for direct costs of resistance (Kokko 2005). While difficult to achieve in practice, combining fine-​scale behavioral observations and, more importantly, measuring the fitness consequences of male-​female interactions are important for understanding the relationship between sexual selection and sexual conflict in populations (Peretti and Córdoba-​Aguilar 2007, Kokko and Jennions 2014).

RELATIONSHIP BETWEEN SEXUAL SELECTION AND SEXUAL CONFLICT IN CRUSTACEANS Although male-​specific weaponry may evolve because such traits give their bearers an advantage in competition with other males over access to females, these traits can be used in other contexts as well. However, these traits may also be used “out of context” to coerce the opposite sex into mating. Female harassment by males is often cited in crustacean research (e.g., amphipods: Cothran 2008a, Takeshita et al. 2011, decapods: Thiel and Hinojosa 2003, ostracods: Benvenuto et al. 2009) and the claws and other exaggerated, sexually selected weaponry observed in males may give their bearer an advantage in overcoming female resistance to mating. For example, in Hyalella amphipods, males clearly use their exaggerated gnathopods in male-​female interactions (Cothran et al. 2010, Cothran et al. 2015) and as Darwin (1871) suggested, these traits appear to be used to seize females and manipulate them into the pairing position (Cothran, personal observation; A in Fig. 11.7). Females may counter evolutionarily in a number of ways. For example, populations for which pairing is more costly, because of the presence of positive, size-​selective predatory fish, tend to have females that are larger than males, whereas the reverse is true in populations without fish (Wellborn and Bartholf 2005; B in Fig. 11.7). These patterns of sexual size dimorphism may be the result of selection for larger female body size in populations where resisting male pairing attempts is critical for survival. Additionally, females have a “notch” on the pereon segment that males use for attachment with the sexually monomorphic first pair of gnathopods (C in Fig. 11.7). Whether females can position this notch to where it is unavailable to males and if there is variation across species or populations in notch shape are unknown. In some crustaceans, females use sexually selected weapons in mate choice. Berglund et  al. (1996) suggested that male weapons may be used by females to assess mates given that they will often be honest and tested indicators of fighting ability and overall male quality. Females that use morphological characteristics to assess mates may be deceived if the trait does not accurately indicate mate quality. Male fiddler crabs use their enlarged claws to display to and fight male rivals, and it has been shown that in some species females also prefer males with large claws (Reaney 2009, Bywater et al. 2014). Claw shape is important, and it has been shown that females prefer and male rivals are deterred by males with longer claws (Backwell and Passmore 1996, Jennions and Backwell 1996, Backwell et al. 2000). The weaponry of male fiddler crabs is fitted with tubercles on the inner margins of the claw that allow the male to deliver tremendous force, unexpected of the long shape of the weapon. This morphological and behavioral compensation affords males both a powerful weapon to use in combat and an attractive signal that can be used in mate choice (Dennenmoser

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Fig. 11.7. Possible traits used to resolve sexual conflict over mate guarding duration in Hyalella amphipods. (A) Scanning electron micrograph of the distal segments of the posterior gnathopod that is around 15 times larger in males than females. (B)  Patterns of sexual size dimorphism in Hyalella populations. Large ecomorph species live in habitats without fish and typically have males that are larger than females. Small ecomorph species live in habitats with positive size selective fish and often have females that are larger than males. (C) Scanning electron micrograph of the dorsal pereon of a female, showing the “notch” located on the second pereon segment. This notch is where the male attaches to the female using his sexually monomorphic anterior gnathopods to form a precopulatory pair. Insert shows the notch in greater detail. (A) Photo courtesy of Tom Harper with permission; (B)  from Wellborn and Bartholf (2005), with permission from Springer. (C) photo courtesy of Tom Harper with permission.   



Sexual Selection and Sexual Conflict in Crustaceans

and Christy 2012). When fiddler crab males lose their claws, they regenerate them. Although these claws are approximately the same size as the original claw, they contain less muscle and are less effective in combat (Backwell et al. 2000, Lailvaux et al. 2009). Males with dishonest signals appear to be able to deceive receivers and win contests they would have otherwise lost (Backwell et al. 2000, Lailvaux et al. 2009). Moreover, males with regenerated claws pay less of a metabolic cost, and thus the signal may be a poor indicator of male quality (Bywater et al. 2014). Collectively, these results suggest that females may be deceived if males invest in dishonest claw size (i.e., less muscle mass). The extent to which crustacean males use other sensory channels (e.g., chemical and acoustic) to deceive females during mate choice is unknown (Christy and Rittschof 2011). Ultimately, the environment determines the intensity of sexual selection in a population (Emlen and Oring 1977). The environment, i.e., ecology, that an organism experiences shapes the development of traits used in mating, filters existing variation in the population through selection, and determines the ecological and social interactions experienced by individuals, which affect patterns of selection. Therefore, understanding how sexual selection and sexual conflict shape the evolution of mating traits requires doing so in an ecological context. Crustacean male weaponry is known to be sensitive to resource stress and metabolically expensive (Allen and Levinton 2007, Cothran and Jeyasingh 2010, Cothran et al. 2012a, Bywater et al. 2014, Cothran et al. 2014). This suggests that food availability and stress may affect the distribution of male weapon size in a population. If these traits are used to coerce females, the severity of costs incurred by females may depend on the bottom-​up effects of resource availability. Sexually selected traits may also increase the conspicuousness of their bearers to predators (Andersson 1994). Natural selection may work against weapon elaboration and limit the costs imposed by females. Moreover, population density and sex ratio may affect the harassment females experience from poor-​quality suitors (Kokko and Rankin 2006). High levels of harassment by males may affect mate-​guarding durations and the frequency of mating experienced by females, both of which may be costly ( Jormalainen 1998, Thiel and Hinojosa 2003). Such costs may have important impacts at higher levels of biological organization given that a population’s health is most dependent on the productivity of females (Kokko and Jennions 2014).

CONCLUSIONS AND FUTURE DIRECTIONS Crustaceans have been well represented in the study of sexual selection and sexual conflict. This is particularly true for understanding the biology of animal weapons and sexual conflict over mate-​guarding behavior. Crustaceans also hold tremendous opportunity as model organisms for informing broader concepts in sexual selection. In the following paragraphs, I highlight gaps in our knowledge of sexual selection and sexual conflict in crustaceans, and some areas where research on crustaceans may add to our understanding of these areas of evolutionary ecology. When it comes to crustacean weaponry, we need more research that demonstrates weapons are indeed correlated with male reproductive success, controlling for the effect of body size. Such studies are important for understanding how selection on weapons, body size, and correlated selection due to allometry have affected the evolution of crustacean weaponry. Moreover, studies on weapons need to consider these as multipurpose traits that are going to be affected by multifarious selection. McCullough et al. (2016) suggested using a weapon-​display continuum to understand the functional ecology of crustacean weapons. However, weapons are also used in competition for food, subduing prey, and predator defense, and therefore understanding their evolutionary trajectories may be complex (Milner et al. 2010, Lane 2018). The ontogeny of weapon development and use may also provide insights into weapon evolution. In the caridean shrimp, R. typus, males transition from fighting intensely over food to fighting over females as they move through successive morphs (typus, intermedius, and robustus). Success in competition over food may be important in male

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Reproductive Biology development of behaviors and morphology that affect future success in competition for matings. Males that are more successful in contests over food during earlier developmental stages will have more resources to dedicate to growth and weapon development, which may impact success in agonistic interactions over females later in life (Dennenmoser and Thiel 2007). Future studies should carefully employ modern techniques to measure selection, ideally in natural populations, paired with manipulative experiments to understand how selection shapes weapon evolution across a variety of ecological contexts (Anthes et al. 2016). While crustaceans are often used to study courtship behavior and mate choice, studies that determine what males are conveying to females (e.g., condition, resource holding potential, resistance to parasites) are largely missing in the literature. Moreover, and this is true for all groups of animals, including crustaceans, more research on the fitness consequences of mate choice is needed. Do females benefit from mating with successful males, or due they incur a net cost from such interactions? This will allow us to determine how intersexual interactions may affect mating trait evolution and the consequences of these interactions at higher levels of biological organization. Many groups of crustaceans are found in a wide variety of habitats, making them excellent models for exploring how the ecological context shapes the evolution of mating traits. Understanding how varying ecology affects the evolution of male weapons, male sensory structures, male ornaments, female mating preferences, and traits used to resolve sexual conflicts over mating will be highly rewarding. Given the tremendous rate at which humans are changing environments and the sensitivity of sexual traits to such changes, research on crustaceans could provide critical insights into the evolutionary response to human activities (Snell-​Rood et al. 2015). Finally, there is a tremendous taxonomic bias when it comes to sexual selection research on crustaceans. While this chapter was not intended to be an extensive review of the topic, the majority of examples cited fall in two groups:  decapods and peracarids. Far less is known about sexual selection in other groups of crustaceans. Although there has been some work on ostracods, branchiopods, and copepods, these taxa are poorly represented in the literature. Next to nothing is known about sexual selection in other groups (e.g., branchiurans, thecostracans, and xenocarids), and these should be the focus of future studies.

ACKNOWLEDGMENTS Many thanks to the editorial assistants Miguel Penna, Miles Abdilla, Tim Kiessling, and Mika Tan for careful work during the development of this chapter. I  am also fortunate to have wonderful colleagues to bounce ideas off, especially Gary Wellborn and Puni Jeyasingh.

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12 MULTIPLE MATINGS AND SPERM COMPETITION

Carola Becker and Raymond T. Bauer

Abstract In polyandrous mating systems, females mate multiple times and males have evolved adaptations for sperm competition which increase the number and fitness of their offspring. Mate guarding is a widespread monopolization strategy in groups where female receptivity is temporally restricted and often associated with the molt. Precopulatory guarding occurs in branchipods, copepods, peracarids and decapods. Postcopulatory guarding is notable in numerous brachyurans with males protecting females until her exoskeleton has hardened. During copulation, male success in fertilization depends on an effective sperm transfer mechanism, the precise placement of ejaculates closest to where female gametes are fertilized. Male copulatory systems are highly diverse and strongly adapted to these tasks, especially the structures that interact with the female genital ducts. The elaborate tips of brachyuran gonopods are supposed to act in the displacement, possibly even in the removal of rival sperm masses; however, sperm removal is only evident in crayfish: males eat spermatophores previously deposited by other males. During copulation of several crustacean groups, males transfer secretions that harden and form a sealant. These sperm plugs, plaques and gel layers may protect their own sperm, prevent remating or seal off rival sperm from the site of fertilization. Several groups of isopods and decapods have internal insemination, elaborate sperm storage organs and some exhibit internal fertilization. The intensity of sperm competition increases with the latency between the processes of insemination and fertilization. This chapter gives on overview on mate guarding, male sealants and the anatomical adaptations to sperm competition in crustaceans. We also briefly discuss the consequences of multiple matings for the genetic diversity of broods, i.e., single vs. multiple paternities. There is still a lack of data for many crustacean groups. Moreover, it is often hard to assess how successful a male strategy to ensure paternity actually is as many studies focus on either the behavioral, anatomical, or molecular aspects, while comprehensive multi-level studies on crustacean sperm competition are virtually absent from the literature.

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Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.



Multiple Matings and Sperm Competition

INTRODUCTION Many crustaceans are promiscuous, and both sexes engage in multiple matings with different partners throughout their lifespan, often even within a single reproductive cycle (Bauer and Martin 1991, Duffy and Thiel 2007). Such sexually polygamous mating systems open the arena for sperm competition as a strong selective pressure is on male adaptations to ensure paternity in as many offspring as possible. On the one hand, multiple matings can lead to higher predation risk and energetic costs compared to sexually monogamous species. On the other hand, polygamy can increase genetic diversity and therefore prove beneficial for the adaptive potential of a population. Polygamy in crustaceans leads to sexual competition at different stages of reproduction, on the behaviorial, anatomical, and physiological level. Sperm competition starts with finding a suitable partner, which involves mate location, mate attraction, and mate choice. These traits certainly include very diverse and complex sexual behaviors (e.g., Christy 1987, Christy and Salmon 1991) and are the first step to assure paternity. Sexual selection and behavioral traits of inter-​male competition are explored in Chapter 11 of this volume, while this chapter will center on strategies directly associated with the process of sperm transfer during copulation (shortly before, during, and immediately after mating). Our primary focus is on mate guarding, sperm transfer, and the anatomical characteristics of crustacean reproductive systems that enable sperm competition and show adaptations for this task. Another focus is the outcome of sperm competition in broods. While multiple paternity provides direct evidence for sperm competition, single paternity can be a result of sperm competition as well and may then be interpreted as a very successful strategy by one male. It is generally the male that competes for the female in order to ensure his paternity of as many offspring as possible. Females, however, play an important role too, and female mate choice and the control of receptivity shape how males compete. Postcopulatory sexual selection is a very interesting area of study if females accumulate sperm from multiple matings (Zeh and Zeh 1997). This allows females to evaluate sperm quality and compatibility and directly influence which spermatozoa are used in fertilization (“cryptic female choice”; see Chapter 13 in this volume). Mating order and the placement of ejaculate in relation to the anatomical organization of the female reproductive system play a decisive role in determining which male achieves paternity (Zeh and Zeh 1997, McLay and López Greco 2011). Spermatozoa in a position close to the gonopore or oviduct opening have priority in fertilization. Depending on the architecture of female structures, the first or last male can achieve precedence in fertilization.

SPERM COMPETITION: BACKGROUND AND MAIN ADAPTATIONS Who Are the Protagonists? For many groups of crustaceans, our knowledge on reproduction is so poor that incidences of multiple matings and sperm competition are unknown, for example, in the Ostracoda. Sperm competition is probably absent or of low significance in the hermaphroditic Cephalocarida and Remipedia (Morrow 2004). In Anostraca (Branchiopoda), multiple matings have been demonstrated in the genus Artemia and sperm competition is likely (Morrow 2004). Sperm competition is more common and certainly better understood in animals that reproduce through copulation. But it also occurs in broadcast spawners that release gametes into the water. Some groups of corals are a famous example of synchronized spawning of both male and

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Reproductive Biology female gametes. To our knowledge, female crustaceans never release oocytes non-​directionally if a male is not nearby or some kind of previous pairing has taken place. There are, however, cases of males spawning their ejaculates into the open water, i.e., spermcast mating, in some species of free-​ living barnacles, which are an interesting group to study regarding sperm competition in broadcast spawners (Barazandeh et al. 2013, 2014). Male strategies to ensure paternity become elaborate in groups where females have the ability to store sperm. In some crustaceans, insemination (through copulation) and fertilization (at ovulation) are temporally uncoupled due to sperm storage, which results in an increased intensity of sperm competition. In many Malacostraca, males attach spermatophores externally on the female body, often at specific reception areas close to the gonopore where oocytes are extruded at ovulation. The most complex sperm competition strategies are found in groups of isopods and decapods with specialized sperm storage organs and internal fertilization. The Role of Spermatozoa, Spermatophores, and Male Secretions Sperm competition occurs whenever spermatozoa of two or more males compete in fertilizing female ova (oocytes) (Parker 1998). Sperm allocation can be shaped by sperm competition, and males can adjust ejaculate size to the intensity of inter-​male competition (Arundell et al. 2014; see Chapter 3 in this volume). In addition to quantity, the quality of gametes is crucial to succeed in fertlization. Gamete mobility plays an important role in flagellate spermatozoa; however, in many crustaceans, spermatozoa are aflagellate and thereby immotile ( Jamieson 1991). This is the case in Cephalocarida, Branchiura, Copepoda, Pentastomida, Ostracoda, and Malacostraca (Morrow 2004). Flagellate spermatozoa are considered the plesiomorphic character state and occur in Remipedia, Ascothoracida, Cirripedia, Branchiura, Mystacocarida, and Phyllopoda ( Jamieson 1991), but there is still a lack of data for many crustacean groups. In aflagellate, immotile sperm, a direct competition, as a race between single spermatozoa to reach the ova, is unlikely; however, flagellarity does not always go along with sperm mobility. Flagellate but immotile and aflagellate but otherwise motile sperm have been likewise reported (Pitnick et al. 2009). The loss of sperm motility shows some correlation to the absence of multiple matings and sperm competiton among crustaceans. Morrow (2004) therefore supposed that the reduction of energetically costly flagella has occurred in monandrous mating systems. Spermatoza of most crustaceans are enclosed in spermatophores during their transfer to the female. Spermatophores are of great structural diversity among crustaceans (Subramoniam 1993). Groups with internalized sperm storage, such as brachyuran crabs, have simple spherical spermatophores (e.g., Klaus et  al. 2009). In contrast, externally attached spermatophores can be very complex. Stomatopoda have sperm cords (Wortham-​Neal 2002), while Anomura and Achelata have species-​or taxon-​specific spermatophores (Subramoniam 1993, Tudge 1997). The role of spermatophore structure in sperm competition is not well understood, but whether intact spermatophores, free spermatozoa, or both are stored has important implications for sperm competition (e.g., Sal Moyano et al. 2010). Spermatophores are generally embedded in seminal fluids that play an important role in sperm transfer and storage, especially if secretions harden and act as a sperm plug or sealant in the female genital tract. The nature of a sealant can be defensive or ­protective, if it prevents remating or sperm loss by occluding the female genital ducts. Other sealants are rather aggressive, as spermatozoa from previous copulations become sealed off to foreclose their use in fertilization (Beninger and Larocque 1998). Sealants can also act against subsequent matings by merely reducing the space within the female storage organ.



Multiple Matings and Sperm Competition (A)

(B)

Fig. 12.1. Mate guarding. (A) postcopulatory mate guarding in terrestrial isopod Trachelipus rathkii. (B) Precopulatory mate guarding in flower crab, Charybdis feriata. (A) Photo courtesy of Ferenc Vilisics; (B) from Soundarapandian et al. (2013).   

Mate Guarding and Female Receptiveness Mate guarding is a male monopolization strategy in many animal groups (Parker 1974), including crustaceans (Ridley 1983), that is related to females being receptive for only a short period of time. An increased duration of mate guarding inevitably leads to a decrease in the number of mate encounters. Mate guarding is therefore only beneficial if the fitness gained from guarding is greater than from mating with more females (“missed opportunity costs”; Grafen and Ridley 1983). Among crustaceans, mate guarding is observed in branchiopods (Weeks and Benvenuto 2008), copepods (Todd et al. 2005), amphipods (Wellborn and Cothran 2007), isopods (A in Fig. 12.1; Jormalainen et al. 1999) and decapods (B in Fig. 12.1; McLay and Becker 2015). There is still a lack of data for groups in which mating is not easily observed. Precopulatory mate guarding is much more common than postcopulatory guarding and can be synchronized with the female molt, gonad maturation, or spawning. Males need to be able to assess or even predict female receptivity through pheromones related to these events. Whether mating is linked to molting has very important consequences for reproductive strategies in general and sperm competition in particular (Hartnoll 1969, McLay and Becker 2015; see Chapter 13 in this volume). In several decapods, females mate postmolt but top off sperm reserves during the intermolt (e.g., Elner and Beninger 1995). Postcopulatory mate guarding is mainly known from brachyurans and may serve different functions. First of all, it prevents female remating, which is particularly important if last male precedence occurs. Second, postcopulatory guarding may allow transferred sealants to harden and prove effective in protecting the male investment or preventing remating. Another important factor is the protection against predation through postcopulatory guarding of freshly molted, soft females. Jormalainen et al. (1999) argued that precopulatory guarding has no benefit for female isopods but instead leads to sexual conflict (see Chapter 11 in this volume). Sexual conflict can shape female traits, for example receptivity, ovary maturation, and sperm storage patterns ( Jormalainen 2007). In decapods, especially when guarding is linked to molting, females clearly benefit, especially from postcopulatory guarding, which often lasts until her exoskeleton hardens (Pardo et al. 2016).

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Reproductive Biology Male Arms Race: Copulatory Structures Male adaptations to ensure paternity can be observed in the structure of copulatory organs, which are adapted to precisely position the male seminal products (ejaculates) and minimize their loss during sperm transfer. To ensure paternity, males place ejaculates in a location where sperm is most likely to achieve paternity. This is usually the site of first contact of spermatozoa and oocytes, and thus where fertilization occurs. A  strong selective pressure lies herewith on the male structures that transfer sperm, and a great structural diversity of copulatory organs to their function in sperm transfer is present among crustaceans. In Malacostraca, either the penis or accessory modified appendages (pleopods or gonopods, uncommonly thoracopods) transfer the sperm to the female. Among decapod shrimps, lobsters, crabs, and many crayfish, two pairs of modified pleopods (gonopods) receive the ejaculate from the paired penis or gonopores and pass it onto the female. Both Anomura and Achelata show a tendency to reduce pleopods (Bauer 1986). The shared interest between the sexes in successful fertilization is expected to lead to confluence in the evolutionary responses of the sexes and maintenance of the functional integrity of the interaction between the different copulatory components in males (e.g., first and second gonopods) to reduce leakiness of sperm transfer. Multiple Paternity Paternity testing reveals the number of different fathers that sire female broods. Most studies have been conducted in important fisheries species. While earlier assessments were based on allozyme markers (e.g., American lobster Homarus americanus, Hedgecock et  al. 1977; edible crab Cancer pagurus, Burfitt 1980), more recent studies use microsatellite markers to estimate the diversity of non-​maternal alleles (e.g., snow crab Chionoecetes opilio, Urbani et al. 1998; H. americanus, Jones et  al. 2003). Multiple paternities occur in broods of females that store sperm from consecutive matings in specialized organs, but also in crustaceans with externally attached spermatophores and even in spermcast maters. The advantage of multi-​sired broods is hard to assess, because multi-​ generational breeding experiments would be necessary to demonstrate increased offspring fitness in comparison to single-​sired broods (Yockachonis 2016). A high genetic diversity of offspring is still regarded as beneficial for a species, as it increases the chances for the brood to have at least some individuals with good fitness (Bauer 1992). A  comprehensive overview on multiple paternity studies in crustaceans is presented in Dennenmoser and Thiel (2015). Several cases will be discussed as an outcome of mating strategies in general and sperm competition in particular.

MULTIPLE MATINGS AND SPERM COMPETITION IN CRUSTACEA Examples from Non-​Malacostracan Crustaceans Sperm competition in Copepoda has been demonstrated through observations of mate guarding and multiple paternity (Blades-​Eckelbarger 1991, Todd et al. 2005, Titelman et al. 2007). Both pre-​ and postcopulatory mate guarding can occur (Titelman et al. 2007). Spermatophores are deposited externally, sometimes to specialized areas: the coupling plates, genital atrium, or an associated seminal receptacle (Blades-​Eckelbarger 1991, Barthélémy et al. 1998). The storage sites in inseminated females can be fully occupied after one copulation and thus prevent remating (Barthélémy et al. 1998). Corni et al. (2000) assumed that the release of mate-​attracting pheromones is inhibited in already inseminated females in Centropages spp. (Calanoida). In some species, males can transfer two spermatophores per copulation. In this case, the second spermatophore is supposed to serve as a kind of sealant to prevent remating (Titelman et al. 2007).



Multiple Matings and Sperm Competition

Sperm competition has long been regarded of low significance in barnacles (Kelly and Sanford 2010) and mechanisms that assure paternity of broods are not well understood in this group; however, barnacles may be particularly interesting to study regarding reproductive traits and sperm competition since their mating systems are quite unusual. Most species are sessile but still copulate by means of an extraordinarily long penis (Vogt 2016). Many species are self-​fertilizing, but may additionally receive sperm from adjacent conspecifics, or through long-​distance broadcasting (Balanus glandula, Chthamalus dalli; Barazandeh et al. 2014). Recent studies reveal that multiple paternities actually occur, to a variable degree. In the barnacle Pollicipes polymerus, at least part of the egg batch in spatially isolated specimens was fertilized through spermcast mating, resulting in multi-​sired broods (Barazandeh et al. 2013). Unfortunately, it could not be determined in that study how many additional males were involved in fertilizing the broods. Multiple paternities were also found in around 25% of specimens in a population of the barnacle Tetraclita rubescens. The high ratio of single-​sired broods in this species can be interpreted as an indicator for either a lack of sperm competition or a very effective displacement of rival sperm (Kelly et al. 2012). High levels of multiple paternities were found in Pollicipes elegans (at 79%), with up to five males siring one brood (Plough et al. 2014). Mantis Shrimp (Stomatopoda) The knowledge on stomatopod reproduction is scarce, but behaviors seem to be diverse. Courtship can be initiated by the male or female (Dingle and Caldwell 1972). Male Squilla empusa do not guard females, but follow the pure-search strategy (Wortham-​Neal 2002). Females of several species can store sperm for at least a few weeks (Hatziolos and Caldwell 1983, Hamano 1988, Caldwell 1991). The reproductive anatomy has been studied in mantis shrimp S. empusa, in which females have a medial genital slit on the sixth thoracic sternite that is continuous with the gonopores and leads into a cuticular sperm storage organ (Wortham-​Neal 2002). Due to the complete cuticular lining, the contents of this storage organ are supposed to be shed with the molt. Sperm transfer is assumed to occur through the penis (Wortham-​Neal 2002). However, the first pair of pleopods is modified (Manning 1969) and might play a role in the copulatory embrace or in sperm transfer. The penes are asymmetric in S. empusa, with the left penis being longer than the right one. It has two distal openings, one is the ejaculatory duct, and the other is connected with accessory glands that are thought to produce a sealant, which is frequently found in the female sperm storage organ (Wortham-​Neal 2002). Sealants in stomatopods may prevent sperm loss from the female sperm storage organ, rather than having a function in sperm competition. Caldwell (1991) has proposed that Stomatopoda have internal fertilization, but there is no direct evidence to support this (Wortham-​Neal 2002). Amphipods and Isopods (Peracarida) Most information on reproduction is available for free-​living isopods and amphipods. Precopulatory mate guarding occurs in aquatic species of both groups. It can be regarded as a male monopolization strategy in response to the short period of female receptivity ( Jormalainen 2007) and is often synchronized with the (pubertal/​parturial) molt. Internal insemination and sperm storage in specialized organs are only known for isopods (Ridley 1983, Wilson 1991). In amphipods, the male attains a dorsal position and grasps the female with specialized thoracic appendages, the gnathopods (“pairing”; Wellborn and Cothran 2007). As sperm storage organs are absent, oocytes are fertilized during their release into the brood chamber, i.e., marsupium (Wellborn and Cothran 2007). Multiple matings and paternities can still occur if there is latency between spermatophore attachment and ovulation (Clark 2010). In the freshwater amphipod Gammarus pulex, males perform precopulatory guarding, but females remain receptive for a short period after pairs

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Reproductive Biology separate, hence subsequent matings with other mates occur (Birkhead and Pringle 1986). Paternity testing in this species revealed a high skew toward first male precedence, with 90% of offspring paternity (Sutcliffe 1992). A study on G. duebeni suggested that males respond to sperm competition by increasing mate guarding duration rather than ejaculate size (Arundell et al. 2014). Contact mate guarding in amphipods can result in higher or lower predation risks (compared to individuals that are not paired) depending on the type of predator in a habitat (Cothran 2004). Mate guarding and multiple matings are common in free-​living aquatic isopods (Sassaman 1978, Shuster 1989, Jormalainen et  al. 1999, Jormalainen 2007). Precopulatory mate guarding (“amplexus”) is linked to the peculiar biphasic molt of isopods. Females first molt the posterior body half, copulate, and then molt the anterior body half. In the marine isopod Ligia dentipes, the guarding male assists the female in removing her old exoskeleton during ecdysis (Santhanakumar et al. 2014). Once the posterior body of the female is molted, copulation takes place. Males then immediately start searching for new mates. Postcopulatory mate guarding is not oberserved in this species (Santhanakumar et al. 2014), it is generally rare and if present, only lasts briefly among isopods (A in Fig. 12.1). In the freshwater species Thermosphaeroma thermophilum of the otherwise marine family Sphaeromatidae, females are only receptive for a short period during the molt. Sperm is stored within the oviduct for one reproductive cycle until fertilization and oviposition occurs, but females need to remate in the following reproductive cycle. Multiple paternities are not common and the precopulatory guarding seems to be an effective strategy to prevent sperm competition ( Jormalainen et al. 1999). In most terrestrial oniscidean isopods, males do not guard females (but see Linsenmair 1989 and A in Fig. 12.1). Within Oniscidea, sperm storage organs have evolved and female receptivity is no longer time-​limited (Zimmer 2001). Specialized structures for sperm storage, referred to as either seminal receptacles or spermathecae, have also evolved in janiroidean Asellota and Sphaeromatidea, and those show a high degree of structural diversity (Wilson 1991, Longo et al. 1998). In most isopods, sperm is transferred into the ventral gonopore (oopore) and stored somewhere in the oviduct in more or less specialized cuticular or secretory areas. In Janiroidea, separate paired vaginae have developed on the dorsal surface of the female that lead through cuticular ducts into the sperm storage organs of the oviduct (Wilson 1991). Mating can hypothetically occur at any time in these groups. Sperm storage over several reproductive cycles and fertilization of several consecutive broods with the same ejaculate are possible in terrestrial isopods (Longo and Trovato 2008). As in most oniscideans, spermatozoa are stored in a specialized region at the transition of ovary and oviduct in Armadillidium vulgare (Suzuki and Ziegler 2005) and Porcellio laevis (Longo et al. 1998). The sperm storage organ in P. laevis is lined by a glandular epithelium that releases lipidic secretion, and stored spermatozoa can fertilize broods months after insemination (Longo et  al. 1998). The duration of sperm storage in oniscideans varies from three to four months in Trichoniscidae to up to 17 months in A. vulgare and correlates with sex ratio; sperm storage is especially long when the sex ratio is strongly skewed toward females (Longo and Trovato 2008). In Sphaeromatoidea, sperm storage has been observed in T. thermophilum, but sperm storage is in the oviduct instead of a specialized structure and restricted to the short period of time during copulation and ovulation ( Jormalainen et al. 1999). In A. vulgare, due to female refractory behavior, remating shortly after the first copulation, was demonstrated to result in lower paternity than remating after a certain delay in the next reproductive season (Moreau et al. 2002). Multiple paternities occur in several species of isopods ( Johnson 1982, Heath et al. 1990, Zeh and Zeh 1997). In the terrestrial isopod Venezillo parvus (as Venezillo evergladensis) ( Johnson 1982), first male precedence occurs despite spermatozoa from different males becoming mixed in the



Multiple Matings and Sperm Competition

sperm storage organ. Such sperm mixing may be an adaptation to reduce the probability of full-​ sibling matings in offspring ( Johnson 1982). In some species of sponge-​dwelling isopods, males guard harems of females (Wilson 1991). In Paracerceis sculpta, different male morphotypes exhibit alternative reproductive strategies (Shuster 1989). Large dominant males guard the entrance to their harem in the sponge; however, an alternative male morphotype, which is smaller than other males and resembles females or juveniles, manages to sneak inside the harem and inseminate females. In the male copulatory organs of isopods, paired penes and pleopods can be involved in the transfer of ejaculates (Asellota, Oniscidea, Valvifera) (Wilson 1991). The morphology of pleopods is highly variable, complex, and results in different sperm transfer mechanims. As in many other crustacean groups, gonopods are important taxonomic and phylogenetic characters of isopods. Some groups have a rod-​like appendix masculina on the second pleopod that is involved in sperm transfer. These appendices are so elaborate and specific that they are presumed to function in species recognition (Wilson 1991). In other isopods, the first pleopod forms a funnel that transfers the sperm. The Asellota have a so-​called “arm and hammer” system formed by the second pleopod: the exopod forms the “arm”, which is hooked and equipped with strong musculature. This hook grabs the endopod proximally, which functions as the “hammer” and forces the distal tip of the endopod with its sperm-​conveying structures into the female gonopore (Wilson 1991). Within the Asellota, Janiroidea have the most elaborate copulatory system, referred to as “pick hammer.” It involves the first pleopod, which stabilizes the second pleopod and takes part in the formation of a complete sperm channel that transfers the sperm from the fused penis into the female ducts. The strongly modified and complex reproductive systems of janiroidean isopods may either play a role in sperm competition or just represent an adaptation to precisely and effectively transfer sperm. Wilson (1991) suggested that the success of this group in deep-​sea habitats with low population densities may be related to their elaborate copulatory systems. Decapoda Ghost Shrimp (Axiidea) Multiple paternities of some broods (20%) have been demonstrated in a population of the callianassid Callichirus islagrande (Bilodeau et al. 2005). In this group, mating behavior is unknown due to the cryptic way of life inside burrows. Experiments with isolated females that failed to produce broods already suggested that internal sperm storage is absent in Callianassidae (Tamaki et al. 1996). More recently, Somiya and Tamaki (2017) conducted mating experiments and observed that spermatophores were externally attached in Nihonotrypaea harmandi. Shrimps (Sergestoidea, Penaeoidea, Caridea, Stenopodidea) Sperm competition is highly unlikely in stenopodidean shrimps, as these occur in monogamous pairs with strong pair fidelity ( Johnson 1977, Goy 2010, Gregati et al. 2014). In caridean shrimps, multiple matings have been observed in Palaemonetes pugio (Bauer and Abdalla 2001) and particularly in Rhynchocinetes typus (Thiel and Hinojosa 2003). Chow et al. (1989) observed two separate pairs of spermatophores attached to the posterior thoracic sternum of a female Macrobrachium latidactylus, showing that multiple copulations had occurred. Mating observations by Ra’anan and Sagi (1985) showed that matings of the same female by different males frequently occurred. In female penaeoid shrimps, the posterior two to three thoracic sternites and pereopodal coxae have

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Fig. 12.2. Genitalia of penaeoid and caridean shrimps. (A)  Ventral view of open thelycum of Litopenaeus stylirostris (Penaeidae), uninseminated on the left, with twin spermatophores attached on the right. (B) Closed thelycum of Farfantepenaeus subtilis (Penaeidae) showing twin plates covering the median spermatheca. (C) “­semi-closed” petasma of F. aztecus from (left) lateral view (ventral lobes folded together, natural position) and (right) interior view with flexible lateral lobes stretched open, as they might be in copulation to accept and transfer the spermatophores to the female. (D) “Closed” petasma of Sicyonia picta (Penaeoidea, Sicyoniidae) in which lateral lobes are rigidly folded against the dorsal lobes to form a tube-​like structure (proposed as a sperm injection device, e.g., Burkenroad 1934 but see Bauer 1996). (E) Male genitalia of a caridean, Rhynchocinetes albatrossae, thought to serve as spermatophores transfer and/​or female stimulatory devices in copulation. Left, endopod of pleopod 2 with appendix masculina and, right, endopod of pleopod 1 with appendix interna (not found on pleopod 1 in caridean females). Abbreviations: a = aperture between thelycal plates leading to median seminal receptacle; ai = appendix interna; am = appendix masculina; c4, c5 = coxa (basal segment) of pereopods 4, 5; LL = lateral lobe, ML = median lobe; sp = twin spermatophores. (A) From Pérez Farfante (1975); (B, C) from Pérez Farfante (1969); (D) from Pérez Farfante (1985); (E) from Chace (1997).   



Multiple Matings and Sperm Competition (A)

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Fig. 12.3. Mating and copulation in shrimps. (A) Litopenaeus setiferus (Penaeidae): 1, male chases female up in the water column; 2, courtship swimming; 3–​4, copulation. Male is the shaded individual. (B) Copulation in the caridean Palaemonetes pugio (Palaemonidae): 1, male grasps the newly molted female; 2, male dips below the female; 3, male attaches the spermatophore mass on the female posterior sternites. (A) From Misamore and Browdy (1996); (B) from Berg and Sandifer (1984), with permissions from © Journal of Crustacean Biology.   

depressions, protuberances, and setal groups termed the “thelycum” to which male spermatophores can be attached (“open thelycum”; A in Fig. 12.2), or which lead to apertures of a median (B in Fig. 12.2) or twin seminal receptacles (“closed thelycum”; A in Fig. 12.4) (Bauer and Lin 1993, Bauer 1994, Pérez Farfante and Kensley 1997). Orsi Relini and Tunesi (1987) found some females of Aristeus antennatus with two or three pairs of spermatophores attached externally to the female’s open thelycum, rather than the commonly observed one pair, showing multiple mating. However, this has not been observed in other penaeoids with external spermatophores and open thelyca, such as solenocerids or some penaeid species. Spermatophores are rarely observed in field collections of penaeids such as Litopenaeus species because, unlike A. antennatus, spawning and breaking up of the external spermatophores occur within a very short time after mating (Pérez Farfante 1975, Misamore and Browdy 1996).

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Reproductive Biology Insemination by multiple males and multiple paternities have been shown with molecular genetic techniques in broods of some caridean shrimps (Dennenmoser and Thiel 2015). Using polymorphic DNA microsatellite markers from brooded embryos, Yue and Chang (2010: Caridina ensifera), Bailie et al. (2014: Rhynchocinetes typus), and Jorquera et al. (2016: Acanthephyra pelagica) demonstrated two to several sires for broods incubated by females. Baragona et al. (2000: Palemonetes pugio) stated that 8 of 10 broods had multiple sires; Mathews (2007) showed a high rate of single paternity in broods of Alpheus angulosus. In two of these species (Palaemonetes pugio, Bauer and Abdalla 2001, Rhynchocinetes typus, Thiel and Hinojosa 2003), mating of females by more than one male has been observed. In Crangon crangon, multiple matings have been suggested through observations on reproductive morphology and copulation (Bodekke et al. 1991). The ideal situation in tests of multiple paternities is observation of mating by multiple males plus confirmation of multiple paternities through molecular genetic methods. Unfortunately, observation of mating behavior in laboratory situations is not possible in many species. In caridean and stenopodidid species, broods from a single spawning can be sampled for analysis, as these shrimps brood their embryos below the abdomen (Bauer 2004). However, in penaeoid (and sergestoid) shrimps, oocytes are spawned freely into the water; fertilization occurs as the oocytes emerge from the female gonopores with sperm released from attached spermatophores or from internalized seminal receptacles. Developmental time to hatching is short (less than a day in most species; Dall et al. 1990) so that larvae for genotyping can be obtained rather easily from laboratory-​spawning females, which is routinely done in penaeoid shrimp aquaculture. In the penaeoid Sicyonia brevirostris, an inseminated female with a mature ovary can be induced to spawn simply by placing it on top of a beaker of seawater where it will remain, releasing and fertilizing oocytes into the water below (Pillai et al. 1988); this is possible because of a cataleptic response by the shrimp when being lifted out of the water. The fertilized eggs can then be reared to hatching within a short time. Sicyonia spp. would be a good model species to test for multiple paternities with known sires. They are easily maintained and mate readily in the laboratory; Sicyonia is unusual among penaeoids in that females have internalized seminal receptacles for storing sperm, but Sicyonia males do not produce sealants (mating plugs) or other types of paternity assurance devices (Bauer 1992). Males can only inseminate one seminal receptacle per copulation, and even after repeated apparently normal copulations, may fail to inseminate a seminal receptacle. After a molt (when females mate in this genus), females will mate with multiple males repeatedly (Bauer 1992, 1996b). Thus, the stage for multiple paternities is set. Experiments in which spawned larvae are matched genetically with possible sires using molecular genotyping would verify multiple paternities (and sperm competition), in addditon to testing larvae produced from field-​collected females. In penaeoid shrimps, multiple males may court a female before copulation with a “following” behavior in which the male, using the rostrum prods the female from below in the genital area just posterior to the female gonopores (e.g., Sicyonia dorsalis, Bauer 1992, Litopenaeus setiferus and L. vannamei, Misamore and Browdy 1996, A in Fig. 12.3). After this courtship, the female allows one of the males to copulate. This process might allow females to select a male based on yet to be determined characteristics (cryptic female choice). In caridean shrimps, females always molt just before mating and after hatching a previously incubated brood if present (Bauer 2004). During copulation, the male seizes the female with its pereopods and, similarly to penaeoid shrimps, dips below the female. This situates the male gonopores on the basal segment of the last pair of pereopods in juxtaposition to the ventroposterior thorax or anterior abdomen just posterior to her gonopores, allowing spermatophore transfer to take place (B in Fig. 12.3). In some carideans at least, the female has to lower her first two pleopods so that the male can deposit the external spermatophores (Palaemon elegans, Höglund 1943, Heptacarpus sitchensis, Bauer 1976, Palaemonetes pugio, Berg and Sandifer, 1984, B in Fig. 12.3). A similar lowering of anterior female pleopods during copulation is also likely



Multiple Matings and Sperm Competition (A)

(B)

Fig. 12.4. Thelycum and sperm plug of penaeid shrimp Rimapenaeus similis. (A) Thelycum of unmated female without a sperm plug in the aperture (a) leading to the seminal receptacles (spermathecae) and (B) thelycum of mated female with sperm plug (p) in the aperture. From Bauer and Lin (1993), © Biological Bulletin.   

in stenopodidean and penaeoid shrimps. Thus, the female may reject the spermatophores of a male by not lowering the pleopods. In Rhynchocinetes typus, females may avoid fertilization of oocytes by subordinate males in various ways: evading them when a dominant male is not present, removing spermatophores placed by a subordinate male, and/​or delaying spawning until a dominant male is available (Thiel and Hinojosa 2003). In several penaeoid genera (e.g., Farfantepenaeus, Rimapenaeus, Parapenaeus, Xiphopenaeus), spermatophores are deposited within enclosed seminal receptacles (spermathecae) (Bauer 1991) whose apertures open on the female thelycum (genitalia) (B in Fig. 12.2; A in Fig. 12.4). Males of many penaeoid species seal or plug access to female seminal receptacles, indicating single paternity of subsequent spawns by the inseminated female (Burkenroad 1934, Bauer and Cash 1991, Bauer and Lin 1993; B in Fig. 12.4). These “paternity assurance mechanisms” seem to mechanically rule out the possibility that the female seminal receptacles can receive sperm from other males until after the next molt, when mating can again occur. Multiple spawnings occur between molts, apparently fertilized from the same male, given its paternity assurance mechanism. However, this needs to be verified by molecular genetic techniques since independent genotypic evidence that all stored sperm come from a single male is lacking. Microsatellite DNA analysis of sperm in female seminal receptacles might be used to detect multiple mating and sperm competition ( Jossart et al. 2014). Again, Sicyonia spp. would be ideal candidates for such a study, as mating by multiple males, with some failing to inseminate spermathecae in apparently normal copulations, has been shown through experimental methods (Bauer 1992, 1996b). Females could be collected from the field and allowed to spawn larvae in the lab. These larvae could then be genotyped and compared for multiple sires, and unused sperm in the seminal receptacles could by genotyped to assess which males were over-​or under-​represented in the resulting brood. In other penaeoid species in which females have sperm storage structures, it has been shown that captive females may spawn two to multiple times with stored sperm during the

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Reproductive Biology intermolt after a single insemination event (Scelzo 1991). In those species in which males apparently seal off female spermathecal apertures during insemination, the effectiveness of these putative paternity devices needs to be tested. After mating and before spawning in caridean shrimps, females pick at and groom the underside of the posterior female thorax and abdomen, where spermatophores are usually deposited (e.g., Höglund 1943, Bauer 1976, Thiel and Hinojosa 2003). In Heptacarpus sitchensis, this breaks apart the spermatophore and spreads sperm around the area where oocytes will pass during spawning, increasing the probability of sperm-​egg contact (Bauer 1976). Chow et  al. (1989) showed in Macrobrachium latidactylus that spermatophores from two inseminations were layered one below the other, so that perhaps postmating grooming might spread more sperm from the last insemination event than the previous one. In R. typus, Thiel and Hinojosa (2003) showed that females remove at least some spermatophores from a previous mating by a subordinate male before mating with a preferred dominant male. In this case, female choice, rather than direct sperm-​sperm competition, is involved. Male penaeoid shrimps have very complex gonopods (Bauer 1991, Pérez Farfante and Kensley 1997), which are assumed to transfer spermatophores (C and D in Fig. 12.2). The inner rami of the first pair of pleopods are joined together into a structure termed the petasma. The petasma has remarkable morphological variation among genera (Bauer 1991, 2013, Pérez Farfante and Kensley 1997), and may be equipped with spines or channel-​like tubes, may be asymmetrical, and in the genus Macropetasma, may be enormous in size, reaching from the abdomen to the anterior end of the shrimp! Burkenroad (1934) hypothesized about the function of male genitalia for several Gulf of Mexico genera. Based on morphology, he suggested that the petasma might be used to pick up spermatophores from the male gonopores and transfer them to the female in some species, or in others as hypodermic-​type devices for injecting sperm (Bauer 2013). However, no study has confirmed these speculations or the idea that these complex devices are lock-​and-​key copulatory organs that can be used in species recognition. Bauer (1996a) did the only experiments to date in which the petasma of a penaeoid species was manipulated by partial or complete ablation or blockage. Both the hypotheses that the petasma is a sperm-​injection device or a spermatophore-​ attachment device were rejected by these experiments. The results of Bauer’s (1996a) experiments on Sicyonia dorsalis suggested that males use the petasma to attach to the female genital area during copulation. Another hypothesis that needs to be tested is that the petasma of penaeoids is some sort of stimulatory or courtship device, in which the female may accept or reject the sperm/​spermatophore on the basis of its morphological or behavioral (usage) characteristics during copulation. Males of caridean species have relatively simple modifications to their anterior pleopods, which are assumed to function during copulation, i.e., serve as gonopods in spermatophore transfer (Bauer 2004)  (E in Fig. 12.2). Males of most species have an appendix masculina, generally a small, stalked spinous structure on the endopod of the second pleopod. The first pleopods may be linked by coupling hooks of appendix internae, which are not present in the female (E in Fig. 12.2). Some studies show that these modifications are important in sperm transfer (Bauer 1976, Berg and Sandifer 1984, Martinez and Dupré 2012) while other studies indicate that they may not be essential (Zhang and Lin 2004). It has been suggested that these male structures may also stimulate a female into accepting spermatophores (Bauer 2004). Thus, it is possible, as in penaeoids, that the caridean gonopods may serve primarily in sperm transfer, in female courtship, or for both functions. According to current knowledge, sperm competition seems possible in penaeoids only in the case of Sicyonia species, in which multiple mating and possible multiple insemination of one or both seminal receptacles has been shown (Bauer 1992). But how might sperm deposited by different males actually compete for egg fertilizations? In S.  dorsalis, deposited sperm appears as a single mass immediately after copulation (Bauer 1992)  and not in discrete spermatophores or layers. In this case, competition of the immotile sperm might only be possible at the sperm-​oocyte



Multiple Matings and Sperm Competition

interface, e.g., a more efficient mechanism of penetrating the egg membrane by one male’s sperm rather than another’s. In the caridean Crangon crangon, Bodekke et al. (1991) gave evidence that, unlike other caridean species studied, spermatophores are not applied externally to the female, but rather sperm is deposited directly within the female oviduct. Furthermore, the authors state that sperm is retained from previous inseminations by females and might be added to previous ejaculates before the next spawning event. If this is the case, direct sperm competition, as postulated for Sicyonia spp., might be possible. Crayfish (Astacoidea) Polyandry and multiple matings are common in crayfish (Dennenmoser and Thiel 2015). In the astacid Austropotamobius pallipes, females mate with up to five males (Ingle and Thomas 1974). Female receptiveness is not restriced to the molt, and precopulatory mate guarding does not occur (McLay and Van den Brink 2016). In several species, males fight over females with their chelipeds, which play an important role in mating success (Berrill and Arsenault 1984, Villanelli and Gherardi 1998, Aquiloni et al. 2008). Males with larger chelipeds win females over more frequently and are able to hold the copulatory position longer, which could be regarded as a kind of postcopulatory guarding reducing subsequent copulations (Snedden 1990). Different modes of sperm transfer are present in Astacoidea. In Astacidae and Cambaridae, two pairs of pleopods are adapted for sperm transfer (gonopods). Parastacidae lack first pleopods, and second pleopods are not specialized; sperm transfer is instead by penes. In some species, the fifth pair of pereopods assists. Spermatophores in the form of white threads are attached externally in most groups (McLay and Van den Brink 2016). In female Astacidae, spermatophores are deposited at a specialized receptive area, the spermatophoric plate (e.g., Rubolini et al. 2007). Only Cambaridae have internal sperm storage. The responsible structure, the annulus ventralis, is a cuticle invagination in sternite seven and is asymmetric due to its medially curved suture through which ejaculates are transferred (McLay and Van den Brink 2016). In mating experiments with Orconectes limosus, females were able to fertilize eggs for five months without remating (McLay and Van den Brink 2016). Sealants are common in species of Cambaridae (Berrill and Arsenault 1982, Baker et al. 2008, McLay and Van den Brink 2016). In O. rusticus, a sperm plug is present in the aperture of the annulus ventralis after mating (Villanelli and Gherardi 1998). This plug may protect the sperm from being exposed to water or may prevent subsequent copulations. As last male precedence occurs, sealants seem not to prevent remating successfully (Snedden 1990). Berrill and Arsenault (1984) suggested that the stiff and pointed tip of the gonopods in O. rusticus may function in sperm removal. It may as well serve to break through the sealant, which might explain last male precedence in this species (see Chapter 13 in this volume). As fertilization in crayfish is external, the outermost spermatozoa in the annulus ventralis are released from the suture first and should have priority in fertilizing ova. Multiple matings have also been observed in the cambarids Orconectes sanbornii and O. obscurus and result in multiple paternities of broods (Kahrl et al. 2014; see Chapter 13 in this volume). Very high levels of multiple paternities are found in the cambarid Procambarus clarkii (96.7%; Yue et al. 2010); it is, however, not known whether first or last precedence occurs. Multiple matings also occur in A.  italicus and A.  pallipes. Males that mate with inseminated females remove rival sperm by eating previously deposited spermatophores before attaching their own (Villanelli and Gherardi 1998, Galeotti et al. 2007). It has been suggested that last male precedence occurs (Galeotti et al. 2007). A study on the relationship between male claw asymmetry (due to autotomy), sperm removal, and ejaculate size in A. italicus provides evidence of sperm allocation. Chelipeds are important secondary sexual characters in this species. In males with claw asymmetry,

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Reproductive Biology sperm removal was inferior, probably due to a decreased performance in copulatory positioning. Thus, males increased ejaculate size to compensate for their deficit (Galeotti et al. 2007). Sperm removal by simply eating spermatophores of previous mates has also been observed in A. italicus (Galeotti et al. 2007). It is such an easy and effective strategy to ensure paternity that it seems surprising that other groups of crustaceans do not adopt it. Clawed Lobsters (Nephropoidea) Most studies available in this group have been conducted on commercially exploited species, for example, Homarus species and the Norway lobster Nephrops norvegicus. Females mate immediately after the molt, but also during the intermolt (Dunham and Skinner-​Jacobs 1978). Mate competition in H.  americanus involves agonistic behavior toward other (smaller) males and disrupting cohabitation with premolt females to monopolize several shelters for mating (Karnofsky and Price 1989). Copulation in N. norvegicus is initiated by a brief courtship, followed by the transfer of ejaculate, which takes only a few seconds (personal observation). Females store sperm in a single sperm storage organ (spermatheca) ventrally on the sternum (Fig. 12.5). It is lined with cuticle, and sperm is lost when molting. Sperm can be stored for up to three years in large female H. americanus if no molt occurs (Waddy and Aiken 1986). As in most decapods, gonopores are located ventrally on the coxae of third pereopods, and fertilization is external. The spermatheca has an aperture with a central slit through which spermatophores are transferred (B in Fig. 12.5, arrow) by the interacting two pairs of male pleopods (gonopods). In Homarus spp. and N. norvegicus, spermatophores are transferred together with vast amounts of seminal fluids. These harden to form a large sealant that occupies almost the entire spermatheca and thereby reduces the opportunity for remating. Experiments with H. americanus suggest that sealants can be long-​lived, as they outlast egg-​laying and still prevent remating (Aiken et al. 2004). In N. norvegicus, numerous spermatophores and different portions of sealants were identified, which are likely to originate from different males and demonstrate that sperm competition occurs (Fig. 12.5; Becker unpublished). Multiple matings in this species have also been shown through paternity testing. Multiple paternities were observed in more than 50% of a population, with two to three males contributing approximately evenly (Streiff et al. 2004). Multiple paternity has also been (A)

(B)

Fig. 12.5. Transverse sections through the spermatheca in Nephrops norvegicus stained with Masson Goldner. (A) Several spermatophores are located deep inside the spermatheca. (B) The sealant of the first male (1) fills out almost the entire spermatheca. A subsequent male has transferred a second sealant (2) and another spermatophore. Abbreviations: se = sealant; sp = spermatophore; spth = spermatheca; sw = spermatophore wall; sz = spermatozoa. Photos courtesy of C. Becker.   



Multiple Matings and Sperm Competition

demonstrated in H. americanus ( Jones et al. 2003), while broods of H. gammarus were found to be single-​sired (Ellis et al. 2015). Multi-​sired broods in H. americanus seemed to be related to fishing intensity. In Canada, multiple paternities were found in highly exploited populations, while females from healthier populations had single-​sired broods (Gosselin et al. 2005). A possible explanation is that lobster fisheries are male-​biased, which might lead to a lack of large males or sperm limitation in general and prompt females to mate more often or with smaller males to fertilize their brood. Spiny and Rock Lobsters (Achelata: Palinuridae) Knowledge of the reproductive biology of Achelata is scarce, especially for Scyllaridae and Synaxidae. The most information available is for Palinuridae, which are an interesting group to study since they show very distinct character states in the male copulatory organs and female spermatophore reception and storage areas among subgroups. With a higher complexitiy of the reproductive anatomy, the latency between insemination and fertilization increases and so does the opportunity for sperm competition. MacDiarmid and Sainte-​Marie (2006) state that female competition plays an important role in this group: it intensifies with greater reproductive synchrony and shorter durations of female receptivity. Some spiny lobsters possess stridulating organs that play a role in predator defense and escape (Patek 2001), but in Palinurus elephas, sounds produced by the female may attract males (Groeneveld et al. 2006). Copulation in Palinurus takes place in the intermolt stage (Berry 1969, Groeneveld et al. 2006), but it is unknown whether this is the case in all palinurids. Multiple matings prior to oviposition occur in several species (MacDiarmid 1988). Male pleopods are reduced in Palinuridae. Penile processes deposit paired spermatophores (“tar spots”) externally. Females lack internalized sperm storage organs, and fertilization is external (MacDiarmid 1988). In the species of Panulirus and Palinurus, sperm can be stored for up to four months (MacDiarmid and Sainte-​Marie 2006), and in Scyllarides deceptor for up to 10 months (Oliveira et al. 2008). Females of the genus Panulirus possess specialized, paired, and decalcified areas on the sternum (“soft windows”) that receive spermatophores (Vega Velázquez 2003) and may allow nutrients to pass through the body wall and maintain storage (MacDiarmid and Sainte-​ Marie 2006). In some species, several pairs of windows develop, and their number increases with female body size, allowing more spermatophores to be stored (George 2005). Spermatophores are rigid and longer-​lived in species of Panulirus, and the delay from attachment to fertilization is longer than in other palinurids (George 2005). The penile process of Panulirus can vary from a simple process to a complex, serrate, and setose structure, which may play a role in mate recognition, spermatophore attachment, or maybe even in removing rival spermatophores (MacDiarmid and Sainte-​ Marie 2006). The elaborate male penile processes of some Palinuridae may be used to assess the insemination status of females and adjust ejaculate size accordingly (MacDiarmid and Sainte-​Marie 2006). Females occasionally remove spermatophores from smaller males (MacDiarmid and Butler IV 1999), but there is no evidence that males remove spermatophores from rivals (MacDiarmid and Sainte-​Marie  2006). Anomura Male copulatory organs are very diverse in the Anomura, and several groups show a tendency to reduce gonopods. In galatheids, the fifth pereopod is involved in sperm transfer (Kronenberger et al. 2004). Anomura have external fertilization, and no specialized structures for sperm storage have been identified to date, nevertheless, sperm competition definitely occurs in this group. The mole crab Emerita emerita (as Emerita asiatica) (Hippidae) is a protandric hermaphrodite

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Reproductive Biology (Subramoniam 1981), with up to five dwarf males depositing spermatophores on a single female (Subramoniam 1977). Multiple paternities are very high in the galatheoids Munida rugosa and Munida sarsi, and broods are sired by at least three different males (Bailie et al. 2011). Cryptic female choice, forced copulations, and fishing pressure (resulting in sperm exhaustion and an increase of multiple matings) have been considered to cause such high rates of multiple paternity (Bailie et al. 2011). Brood survival was studied in M. sarsi, and multi-​sired broods showed higher survival rates in heat shock experiments, which is important in this species as it lives in intertidal habitats with extreme temperature fluctuations (Yockachonis 2016). Precopulatory behavior of hermit crabs involves rocking, tapping, and stroking of females prior to copulation. Several species fight over females, with larger males being more likely to win fights (Hazlett 1981). Sperm transfer is either by a penile process or by the aid of gonopods (Hess and Bauer 2002). Reproduction of king crabs (Lithodidae) has received some interest due to the commercial value of the species in this group. Paralithodes camtschaticus lacks sperm storage and mates only once per reproductive cycle (Vulstek et al. 2013). Furthermore, P. platypus has single-​sired broods (Stoutamore 2014). Sato et al. (2006) found slow recovery rates in ejaculate production and sperm supply to be limited in P. brevipes. Sperm allocation in larger males was positively correlated with female body size, demonstrating that males adjust the amount of sperm according to female sizes. However, smaller males could not increase the size of their ejaculate beyond a certain amount; thus, large females that mated with small males showed decreased fertilization rates in broods. In behavioral experiments using the stone crab Hapalogaster dentata, males increased the number of spermatozoa transferred when mating with larger females (Sato and Goshima 2007). Males also allocated larger ejaculates when sex ratios were skewed toward males and many rivals were present. Large females did not obtain enough sperm from small males to fertilize their whole broods and therefore preferred larger males and those that had not recently mated (Sato and Goshima 2007). Basically, lithodids show no indication of females mating multiple times, and sperm competition in this group is therefore rather unlikely. The studies mentioned here rather demonstrate that exploited lithodid species seem to be very vulnerable to sperm depletion. Brachyura Brachyura have internal insemination and sperm storage. In podotreme brachyurans with external fertilization, sperm is stored in cuticular spermathecae and therefore lost at the molt (Hartnoll 1975). Females of the spanner crab Ranina ranina were observed to mate during the intermolt, followed by a short period of postcopulatory guarding (Skinner and Hill 1987). Copulation of the sponge crab Dromia personata was also during the intermolt in captivity, despite field observations showing the highest numbers of impregnated females shortly after the molting season (Hartnoll 1975). No pre-​or postcopulatory mate guarding was observed in this species. Reproduction of podotreme brachyurans is generally not well studied; the only indication for sperm competition are the sealants found in females of some species after copulation (Hartnoll 1975; see later discussion in this chapter). Eubrachyuran crabs are probably the best-​studied crustacean group with regard to sperm competition. They have internal fertilization and long-​term sperm storage. Females can virtually accumulate sperm throughout their whole life (see Chapter  13 in this volume). The eubrachyuran seminal receptacle is also the site of fertilization, as oviducts lead directly therein. Seminal receptacles are ventrally lined with cuticle and dorsally by glandular epithelia, which produce secretions that promote sperm storage even beyond molting (Cheung 1968; see Chapter 13 in this volume). In the spider crab Inachus phalangium, sperm can be stored for up to six months and fertilize up to six broods without remating (Diesel 1989). In the snow crab Chionoecetes opilio, females



Multiple Matings and Sperm Competition

can fertilize broods from stored sperm for at least one year (Watson 1970, 1972). In the Tasmanian giant crab Pseudocarcinus gigas, females in captivity produced broods without remating for four years (Gardner and Williams 2002). Despite the ability to store sperm over extended periods, many eubrachyuran females remate and are highly polyandrous. Mate guarding has been intensively studied in Brachyura (reviewed in Bilodeau et  al. 2005, Guinot et  al. 2013, McLay and Becker 2015). It is often linked to females being receptive for a short time after the molt. Females mate in the soft-​shelled condition in Cancridae (Edwards 1966, Elner et al. 1985, Pardo et al. 2016), Geryonidae (Hilário and Cunha 2013), and several species of Portunidae (Spalding 1942, Berrill and Arsenault 1982, Jivoff 2003). Other portunids mate in the hard-​shelled intermolt condition (e.g., Thalamita sima; Norman 2009). Hymenosomatidae, Varunidae, and Ocypodidae can mate during the intermolt phase as well (McLay and López Greco 2011). In species of Chionoecetes (Oregonidae) with determinate growth, females mate immediately after the terminal pubertal molt (primiparous) but continue mating in the hard-​shelled condition afterward (multiparous) (e.g., Elner and Beninger 1995). In both pathways, mate guarding is of great importance. Before the primiparous mating, males guard and defend the premolt female for around a week, assist in ecdysis, and continue guarding after copulation for approximately eight hours (Watson 1970, 1972). In contrast to this, precopulatory guarding can last for two months in multiparous matings (Taylor 1985). Postcopulatory guarding is only observed in primiparous matings with soft-​shelled females and obviously resumed to defend the female (and thereby the male investment). Interestingly, males of C. opilio guarded females significantly longer when sex ratios were skewed in their favor (Rondeau and Sainte-​Marie 2001). Mate guarding is common in heterotremes, which exhibit a link between mating and molting (see Chapter 13 in this volume), but can also occur in thoracotremes. In the varunid Hemigrapsus sexdentatus, males intensively guard and defend receptive intermolt females and mate repeatedly until oviposition (Brockerhoff and McLay 2005). How mate guarding is initiated is not well understood. In the chereigonid Telmessus cheiragonus (Cheiragonidae), the precopulatory guarding is induced through pheromones released by the female. In experiments, males also guarded pieces of

(A)

(B)

sa

pq go

(C)

pq

go

G2

st

5 mm

2 mm

1 mm

Fig. 12.6. Sealants and other means of sperm competition in podotreme crabs. (A)  Sperm plaques in dromiid Austrodromidia octodentata spread over paired spermathecal apertures on the female sternum. (B)  Large plaque in Pseudodromia latens covering almost the entire female sternum. (C)  Broken-​off tip of the flagellate distal part of second gonopod occluding the female spermathecal aperture in Homolodromia robertsi. Abbreviations: G2 = second gonopod tip; go = gonopore; pq = sperm plaque; sa = spermathecal apertures; st = sternum. (A, B) From Guinot et al. (2013), with permission from Zootaxa; (C) from Guinot (1995) © Publications Scientifiques du Museum national d’Histoire naturelle, Paris.   

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(B)

(C)

Fig. 12.7. Sealants in eubrachyuran crabs. (A)  Sperm plug in Stenorynchus seticornis:  Histological transverse section through the vagina stained with Masson Goldner. (B) Sperm layering in the seminal receptacle of Metacarcinus edwardsii. The sperm portions (1, 2) received from consecutive copulations with different partners are separated by a gel layer. The sperm portion (2) closest to the oviduct orifice is most likely to fertilize the oocytes at ovulation. (C) Detail of the seminal receptacle and vagina of M. edwardsii. Next to the sperm layers (1, 2) separated by gel layers (white asterisks), a sperm plug is occluding the vagina. (B, C): Histological sections stained with Hematoxylin Eosin. Abbreviations:  gl  =  gel layer; gt  =  glandular tissue; lu  =  lumen of seminal receptacle; od = oviduct; ov = ovary; pl = sperm plug; sr = seminal receptacle; va = vagina. (A) Photo courtesy of Katja Kienbaum; (B, C) Luis Miguel Pardo © John Wiley and Sons.   

sponge impregnated with female urine, obviously containing the responsible pheromone (Kamio et al. 2000). Many male brachyurans transfer a hardening secretion to the female during copulation, ­referred to as a “sperm plug” (Guinot et  al. 2013)  or “sperm guards” (McLay and Becker 2015). We will herein use “sealants” as a collective term, which was introduced first by Beninger and Larocque (1998). A comprehensive overview on sealants among Brachyura is given in Guinot et al. (2013).



Multiple Matings and Sperm Competition

Depending on where and when sealants are placed, McLay and Becker (2015) have defined three different types: (i) sperm plaques, (ii) sperm plugs, and (iii) sperm gel layers (Figs. 12.6 and 12.7). Sperm plaques occur in podotreme crabs and cover the apertures of spermathecae in several members of Dromiidae (e.g., Dromia personata, Hartnoll 1975, Lauridromia intermedia, Sternodromia spinirostris, Guinot and Quenette 2005) and Raninidae (Ranina ranina, Symethis variolosa, Guinot and Quenette 2005). The sperm plaque is rather imprecisely spread over the sternum (A and B in Fig. 12.6) and can extend into the spermathecae. This sealant is presumably deposited after sperm transfer when gonopods are withdrawn (McLay and Becker 2015). Sperm plugs are deposited into the vagina of eubrachyuran crabs in similar fashion. Plugs are found after mating in female portunids (e.g., Spalding 1942, Ryan 1967, Bawab and El-​Sherief 1989, Wolcott et al. 2005, Tallack 2007), cancrids (Elner et al. 1985, Oh and Hankin 2004, Tallack 2007, Pardo et al. 2013; A and B in Fig. 12.7), geryonids (Elner et al. 1987, Melville-​Smith 1987), and goneplacids (Castro 2007). The plug can extend into the seminal receptacles as in C. pagurus (Tallack 2007) and also protrude externally and thereby indicate mating success. Sperm plugs are therefore important indicators to understand reproductive cycles. In Callinectes sapidus, several sperm plugs were present in 12.4% of females from a fished population in Chesapeake Bay ( Jivoff 1997). This indicates multiple matings and shows that a sperm plug cannot impede remating in this species. Sperm plugs were originally thought to prevent the loss of spermatozoa or the entry of seawater in impregnated females (see Becker and Scholtz 2017). More recent studies suggested a role in providing anti-​microbial protection or nourishing sperm (Oh and Hankin 2004, Becker et al. 2012, 2013), but sperm plugs certainly also play an important role in sperm competition by inhibiting remating. Sperm plugs are often only found in heterotreme eubrachyurans when mating is linked to molting and seem to be absent in thoracotremes (McLay and Becker 2015). The sperm gel layer is placed into the seminal receptacle of eubrachyurans before sperm is transferred (B and C in Fig. 12.7). Since the gel layer seals off sperm from previous copulations, it can be regarded as the most aggressive type of sealant. Diesel (1989, 1990, 1991) has laid down the groundwork on eubrachyuran sperm competition in his research on I.  phalangium. The seminal receptacle is divided into a dorsal sperm storage chamber and a ventral insemination chamber in this species. Both chambers are separated by a muscular velum that controls the release of spermatozoa from dorsally stored spermatophores into the ventral insemination chamber at the time of ovulation (Diesel 1989). Up to eight discrete sperm packets were observed in the sperm storage chamber (Diesel 1988). The ejaculates from different males appear stratified, as they are separated by sperm gel layers that seal off sperm from previous copulations before placing their own sperm (Diesel 1988, 1990). This strategy obviously favors last male precedence (McLay and López Greco 2011). A discrete storage of spermatophores and free spermatozoa in separate chambers has also been reported for C. opilio (Elner and Beninger 1992). Males of Metacarcinus edwardsii apply two different types of sealants. Ejaculates from different males appear stratified inside the seminal receptacle, as they are separated by sperm gel layers. Older ejaculates are pushed upward (dorsally) by more recent ejaculates deposited close to the ventral oviduct connection (B and C in Fig. 12.7; Pardo et al. 2013). Additionally, a sperm plug occludes the female vagina after copulation (B and C in Fig. 12.7; Pardo et al. 2013). The latter sealant seems to be a very successful strategy, as broods in M. edwardsii were shown to be single-​sired, probably through last male precedence (Pardo et al. 2016). Single paternity also occurs in C. pagurus (McKeown and Shaw 2008), but data on sperm storage are not available from the literature. Paternity in the ocypodid sand-​bubbler crab Scopimera globosa was studied using irradiation to fragment DNA (Koga et al. 1993). During the reproductive season, females copulate with several males above ground, followed by a last copulation inside an underground burrow. Last male precedence was over 90% and attributed to successful sperm displacement by the last male (Koga et al. 1993). Behavioral experiments combined with paternity testing revealed last male precedence in C. opilio, with a high skew in favor of the last male (Sévigny and Sainte-​Marie 1996).

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Reproductive Biology Substances that constitute any of the three different types of sealants may originate from the same source in the male reproductive system, either as a part of the seminal plasma produced in the vas deferens or as a product of rosette glands in the first gonopod (Beninger and Larocque 1998), or a combination of both (Spalding 1942, Diesel 1989). Female secretions play a role in the hardening of sealants inside the seminal receptacle. More externally placed sealants as plaques and sperm plugs are supposed to harden after contact with seawater (McLay and Becker 2015). How long this takes is unknown. Postcopluatory mate guarding may play an important role in this regard as it assures that sealants have time to harden before the female gets the chance to remate. The impermeability of sealants is achieved through a complex chemistry (Bawab and El-​Sherief 1989, Beninger and Larocque 1998). Plugs can be composed of distinct layers, some of which have chitinous properties (Spalding 1942, Bawab and El-​Sherief 1989). Bawab and El-​Sherief (1989) described the sperm plug in the vagina of Portunus sanguinolentus to be composed of two parts: a funnel structure which is at least in part constituted by secretions of the female seminal receptacle, and a matrix secreted by the male. Both parts of the sperm plug have cuticular properties and a high content of lipoprotein, and undergo phenolic tanning; the matrix is also rich in tyrosine. The durability of sealants determines their role in sperm competition by either preventing remating or making the sperm of rival males unusable for fertilization. Sealants are probably always temporary (McLay and Becker 2015). Plaques and plugs need to dissolve before spawning since they would otherwise prevent fertilization or egg extrusion. Gel layers inside the seminal receptacles of eubrachyurans may, however, last longer, as they are not necessarily affected by the molt. In C.  pagurus, sperm plugs were observed to protrude externally for three to eight weeks. The internal part, however, remained intact for a year and was displaced dorsally toward the seminal receptacle (Edwards 1966). Sperm plugs were present for approximately 180 days post-​mating in M. magister (as Cancer magister) (Oh and Hankin 2004). Elner et al. (1985) conducted mating experiments observing copulation and deposition of the sperm plug in C. borealis. After copulation, he removed the male and replaced it by a second male that was able to penetrate the sperm plug from the previous copulation with his gonopods and mate with the female. It remains unclear whether this was only the case because Elner et al. (1985) interrupted the mating process and hampered postcopulatory embrace, which might be necessary to allow the sperm plug to harden. It therefore remains unclear whether sperm plugs always prevent remating under natural conditions. Sperm transfer in brachyurans is always by two pairs of modified pleopods, the first and second gonopods, which receive the ejaculates from the penis arising from the gonopore. Gonopod morphology is highly diverse, and different mechanisms of sperm transfer have evolved (Fig. 12.8; McLay and Becker 2015). The first gonopod forms a tube in which the second gonopod is inserted during copulation. Depending on their relative length, one of the gonopod pairs actually transfers the sperm. In podotremes and heterotremes, either the first or second gonopods are longer than the other pair and interact with the female spermathecal aperture or vulva during sperm transfer. Among Thoracotremata, it is always the tubular first gonopod that forms the sperm channel and transmits the sperm. In this system, the second gonopod has an accessory function in the sperm transport within the tubular first gonopod and seals the proximal opening where the penis injects the sperm (Becker et al. 2012). The complex process of sperm transfer is not well understood across Brachyura. First gonopods of heterotremes and thoracotremes are so diverse and elaborate that they bear important characters for taxonomy. The distal tip of first gonopods is often equipped with processes, protuberances, spines and different types of setae (Fig. 12.8). The specific arrangement of structures is sometimes supposed to serve in species recognition and maybe even constitute a key-​lock mechanism with female vulvae to prevent interspecific mating attempts; however, possible corresponding structures in females are hardly studied. The distal setae in the first gonopods (e.g., B–​D, G in Fig. 12.8) may, at least in part, serve sensory functions and guide the gonopod into the optimal position (where released spermatozoa have the best chances in fertilization). There is



Multiple Matings and Sperm Competition

(C)

(B)

(A)

(E) (D)

(F)

(G)

(H)

Fig. 12.8. Scanning electron micrographs of brachyuran first gonopods. (A) Chionoecetes opilio. (B, C) Bathyrhombila furcata. (D)  Nepinnotheres pinnotheres. (E)  Mithraculus sculptus. (F)  Heikeopsis japonica. (G)  Lybia tesselata. (H)  Stenorhynchus seticornis. (A) From Beninger et  al. (1991) © Journal of Crustacean Biology; (B, C) from Hendrickx (1998), © Allen press; (D) photo courtesy of C. Becker; (E, H,) © John Wiley and Sons; (F) photo courtesy of Juliane Vehof with permission; (G) photo courtesy of Katja Kienbaum with permission.   

no evidence that gonopods can remove sperm from previous copulations, but from observations on the morphology of the first gonopod, some speculation on such a function is present in the literature (Beninger et al. 1991, Diesel 1991). The first gonopod in C. opilio is curved and equipped with robust setae (A in Fig. 12.8). The distal tip is pointed and oriented in a way that sperm removal (“cuvetting”) seems conceivable (Beninger et al. 1991, Elner and Beninger 1992, 1995). However,

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Reproductive Biology when comparing the structure of the vulva (Sainte-​Marie and Sainte-​Marie 1998)  with the first gonopod (Sainte-​Marie et al. 1997) in this species, it is likely that gonopods are only inserted superficially into the female vulva but do not actually reach the lumen of the seminal receptacle (Sainte-​ Marie et al. 2000). Based on anatomical studies on copulatory systems with long first gonopods, it seems improbable that gonopods are introduced deep enough to actually perform sperm removal. Diesel (1991), however, speculated that the pointed tip of the first gonopod of Portunus sanguinolentus may be able to penetrate a not fully hardened sealant and, thus, at least displace ejaculate from previous copulations. The often very long second gonopods of some heterotreme and podotreme crabs might actually represent better candidates to postulate a role in sperm competition. For example, the long second gonopod of the geryonid Chaceon maritae shows abrasions distally and the area around the female vulva does, too (Melville-​Smith 1987). In podotreme crabs of the groups Homolodromiidae and Dromiidae, the long flagellate second gonopod transfers sperm to the female. Broken-​off tips of second gonopods have been found in the narrow spermathecal aperture in some species (Pedro and Martin 1989, Guinot 1995, McLay 2001, Guinot and Quenette 2005, see C in Fig. 12.6). Based on this finding, McLay (2001) suggested a role of long second gonopods in sperm competition by either displacing ejaculates from previous copulations or by using the broken-​off tip as a substitute for a sperm plug. In spiders, broken-​off copulatory structures are considered low-​cost adaptations to sperm competition (Snow et al. 2006).

CONCLUSIONS AND FUTURE DIRECTIONS Anatomical studies of crustacean reproductive systems help to understand preconditions and possible mechanisms of sperm competition. Particularly, isopods and decapods have complex male copulatory organs and female sperm-​storage structures, which represent important phylogenetic characters and can be interpreted as adaptations in the context of sexual selection. Other traits such as mate guarding and sperm allocation can show a high degree of variability among closely related species, and sometimes the observed variation is related to alternative reproductive strategies within a single species. Reproduction is much better understood in crustaceans that are large-​sized, benthic, terrestrial, or of commercial interest, while our knowledge of less conspicuous species is still extremely scarce and often restricted to anatomical descriptions. Most research on sealants has been conducted on decapods. More studies are needed to better understand the origin, chemical composition, and function of sealants in relation to sperm competition. Sealants have not been documented in peracarids, which is surprising, especially with regard to terrestrial isopods, considering that other terrestrial arthropods such as spiders and insects have elaborate plugs (Choe and Crespi 1997). Whether rosette glands of decapods are responsible for the production of sealants and if isopods have such glands are important questions in this context. Sperm removal by competing males is only evident in crayfish and, here, not through gonopods but simply by eating rival spermatophores off the female body before depositing their own. The distal structures in brachyuran gonopods, which have previously been suspected to be involved in removing sperm, should be studied in more detail in the future, for example by examining gonopods for externally attached spermatophores and testing their origin with molecular methods. In many cases where sperm competition has been hypothesized or detected, our perspective is rather limited and does not encompass the whole picture. Studies often focus on a single approach, dealing either with anatomy, behavior, or the genetic outcome of sperm competition in broods (but see Jensen and Bentzen 2012, Pardo et al. 2016). Integrative approaches using molecular studies on the content of sperm storage organs, combined with paternity testing in species where detailed descriptions of their reproductive anatomy and sexual behaviors are available, will be necessary to advance our knowledge on sperm competition in the future.



Multiple Matings and Sperm Competition

ACKNOWLEDGMENTS The first author was funded by Seafish (UK) and Kilkeel/​W hitby Seafoods (UK). The images on Nephrops norvegicus sperm storage organs (Fig. 12.5) were produced during this project, and permission was kindly given to use them in this chapter. We thank Daniéle Guinot, Michael Hendrickx, Katja Kienbaum, Alison MacDiarmid, Luis Miguel Pardo, Juliane Vehof, and Günther Vogt for providing images. We would also like to thank the editors and Emma Gorman (Queen’s University Belfast, UK) for editing the final version of this manuscript. This is Contribution No. 201 of the Laboratory for Crustacean Research, University of Louisiana, Lafayette.

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Todd, C. D., R. J. Stevenson, H. Reinardy, and M. G. Ritchie. 2005. Polyandry in the ectoparasitic copepod Lepeophtheirus salmonis despite complex precopulatory and postcopulatory mate-​guarding. Marine Ecology Progress Series 303:225–​234. Tudge, C. C. 1997. Phylogeny of the Anomura (Decapoda, Crustacea): spermatozoa and spermatophore morphological evidence. Contributions to Zoology 67:125–​141. Urbani, N., B. Sainte-​Marie, J. M. Sévigny, D. Zadworny, and U. Kuhnlein. 1998. Sperm competition and paternity assurance during the first breeding period of female snow crab (Chionoecetes opilio) (Brachyura: Majidae). Canadian Journal of Fisheries and Aquatic Sciences 55:1104–​1113. Vega Velázquez, A. 2003. Reproductive strategies of the spiny lobster Panulirus interruptus related to the marine environmental variability off central Baja California, Mexico: management implications. Fisheries Research 65:123–​135. Villanelli, F., and F. Gherardi. 1998. Breeding in the crayfish, Austropotamobius pallipes: mating patterns, mate choice and intermale competition. Freshwater Biology 40:305–​315. Vogt, G. 2016. Structural specialties, curiosities, and record-​breaking features of crustacean reproduction. Journal of Morphology 277:1399–​1422. Vulstek, S. C., D. A. Tallmon, T. P. Linderoth, and J. R. Guyon. 2013. Spatio-​temporal population genetic structure and mating system of red king crab (Paralithodes camtschaticus) in Alaska. Journal of Crustacean Biology 33:691–​701. Waddy, S. L., and D. E. Aiken. 1986. Multiple fertilization and consecutive spawning in large American lobsters, Homarus americanus. Canadian Journal of Fisheries and Aquatic Sciences 43:2291–​2294. Watson, J. 1970. Maturity, mating, and egg laying in the spider crab, Chionoecetes opilio. Journal of the Fisheries Research Board of Canada 27:1607–​1616. Watson, J. 1972. Mating behavior in the spider crab, Chionoecetes opilio. Journal of the Fisheries Research Board of Canada 29:447–​449. Weeks, S. C., and C. Benvenuto. 2008. Mate guarding in the androdioecious clam shrimp Eulimnadia texana: male assessment of hermaphrodite receptivity. Ethology 114:64–​74. Wellborn, G. A., and R. D. Cothran. 2007. Ecology and evolution of mating behavior in freshwater amphipods. Pages 147–​166 in J. E. Duffy and M. Thiel, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, New York. Wilson, G. D. F. 1991. Functional morphology and evolution of isopod genitalia. Pages 228–​245 in R. Bauer and J. W. Martin, editors. Crustacean Sexual Biology. Columbia University Press, New York. Wolcott, D. L., C. W. B. Hopkins, and T. G. Wolcott. 2005. Early events in seminal fluid and sperm storage in the female blue crab Callinectes sapidus Rathbun: effects of male mating history, male size, and season. Journal of Experimental Marine Biology and Ecology 319:43–​55. Wortham-​Neal, J. L. 2002. Reproductive morphology and biology of male and female mantis shrimp (Stomatopoda: Squillidae). Journal of Crustacean Biology 22:728–​741. Yockachonis, T. J. 2016. Multiple paternity: a life-​history strategy for porcelain crabs in the face of rising temperatures. Ph.D dissertation, San Francisco State University. Yue, G. H., and A. Chang. 2010. Molecular evidence for high frequency of multiple paternity in a freshwater shrimp species Caridina ensifera. PLoS ONE 5:e12721. Yue, G. H., J. L. Li, C. M. Wang, J. H. Xia, G. L. Wang, and J. B. Feng. 2010. High prevalence of multiple paternity in the invasive crayfish species, Procambarus clarkii. International Journal of Biological Sciences 6:107–​115. Zeh, J. A., and D. W. Zeh. 1997. The evolution of polyandry. II: Post-​copulatory defenses against genetic incompatibility. Proceedings of the Royal Society B: Biological Sciences 264:69–​75. Zhang, D., and J. Lin. 2004. Fertilization success without anterior pleopods in Lysmata wurdemanni (Decapoda: Caridea), a protandric simultaneous hermaphrodite. Journal of Crustacean Biology 24:470–​473. Zimmer, M. 2001. Why do male terrestrial isopods (Isopoda: Oniscidea) not guard females? Animal Behavior 62:815–​821.

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13 DETECTING CRYPTIC FEMALE CHOICE IN DECAPOD CRUSTACEANS

Colin L. McLay and Stefan Dennenmoser

Abstract Decapod Crustacea (shrimps, lobsters, and crabs) employ a range of different reproductive mechanisms that affect paternity, but does it include cryptic female choice (CFC)? This chapter focuses on events surrounding the fertilization of an egg by a sperm and the opportunities where cryptic fertilization bias might occur. It presents a new model of decapod fertilization, defined in terms of space and time to fertilization. Females have several ways to store sperm and influence fertilization outcomes, which should be affected by (1) their growth pattern (indeterminate or determinate), (2) the link between molting and mating (soft-​shell or hard-​shell mating), (3) fertilization latency, and (4) how sperm are protected (no protection or storage is separate from the oviduct, or storage in a seminal receptacle is linked to the oviduct). Paternity data available for 26 decapods show that in 85% of species, females carry broods with multiple paternity and 15% have broods with single paternity. Therefore many (if not most) females mate with several males and so they certainly could make a choice. However, whether this pattern is due to CFC or merely reflects mating history is a matter of debate. At present, there are no unequivocal data that demonstrate CFC: outcomes caused by male mate guarding and sperm competition cannot be distinguished from female choice. The challenge is to understand what females might be choosing and how to detect that choice. Detecting CFC in field data is difficult, if not impossible, because both single and multiple paternities could be favored.

INTRODUCTION The occurrence of certain traits that are highly exaggerated or otherwise conspicuous invites an explanation based on mate choice by either or both sexes (Eberhard 1996). Such choice may be 364

Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.



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either or both precopulatory or postcopulatory. In the absence of choice, partners are assumed to mate randomly. The idea of cryptic female choice (CFC; see Thornhill 1983) encompasses female-​ controlled mechanisms during or following copulation, which might bias fertilization success of males with certain qualities. Cryptic female choice has been investigated as part of many insect mating systems and has become an important element in sexual selection theory (Eberhard 1996). However, despite its theoretical appeal, the covert nature of CFC and its possible symptoms have proved elusive and difficult to demonstrate (Firman et al. 2017). A prerequisite for CFC is for females to be able to mate and obtain sperm from multiple males. Recently, Dennenmoser and Thiel (2015) gathered evidence for polyandry and molecular data about multiple paternity in Crustacea with diverse mating patterns. They highlighted a range of possible postcopulatory sexual selection opportunities, which females might use to modify the outcome. Herein, we expand this discussion by concentrating on the effects of several structural and behavioral features on fertilization in decapod crustaceans. We explore CFC by starting at the fertilization endpoint and examine the course of events leading up to formation of the zygote, beginning at the time when the gametes are released. How do a sperm and an egg meet in the place where fertilization occurs? Do the females have opportunities to bias the fertilization outcome in favor of certain males? Many marine animals practice broadcast spawning wherein coordinated release of gametes occurs as a result of changes in solar (temperature) or lunar (tidal) events. Gametes are small and very numerous, and after fertilization, planktotrophic larvae disperse and settle in new places. Since there are no restrictions on gametes, we can assume that multiple paternity of a female’s brood is the norm: they are simply released into the water and fertilized by whatever sperm they encounter. Control over paternity is only possible when mating interactions occur between parents. Fig. 13.1 provides a conceptual definition of our fertilization model, encompassing both the spatial and temporal dimensions of how sperm and eggs arrive at the same place at the same time. It defines the domain in which mate choice can occur and thereby the space/​time in which CFC might be found. Whether we can define the boundaries of the CFC subset remains a challenge. Where gametes are transferred from male to female, coordinated development of gonads ensures that sperm can be delivered to females who advertise their receptivity. For the most part, crustaceans produce comparatively few gametes, and in the case of males, gametes are given more protection by being packaged in spermatophores (Subramoniam 1993)  that are transferred (via copulation) directly to the female. Spermatophores may simply be attached to the exterior of the female (pedunculate forms) or introduced by gonopods into some kind of storage organ. If gametes meet externally in the abdominal chamber that restricts dispersal of non-​motile gametes, then fertilization is external, but constrained. If eggs meet sperm in the storage organ (seminal receptacle), then fertilization is internal and even more localized. Multiple paternities are no longer the default option because all males do not have access to all of the eggs. How sperm are stored, and how long they are stored, will have an effect on which are used by the female for fertilization. The distribution of sperm storage patterns among almost 15,000 species in Decapoda (De Grave et al. 2009) are as follows: no storage 46.8%; thelycum/​annulus ventralis/​spermathecae 9.51%; and seminal receptacle 43.04%. Roughly speaking, there are similar proportions of species with some kind of storage as there are those without (53% compared to 47%). Hence, these decapods present a wealth of sperm storage modes and architectures that makes them an attractive study taxon to evaluate the feasibility of CFC through structural features of the female reproductive system.

FERTILIZATION IN DECAPOD CRUSTACEA What do we need to consider and incorporate into our explanation of paternity in decapod crustaceans? In these animals, all gametes are retained and transferred at the time of copulation, and

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Fig. 13.1. Conceptual model of decapod paternity. The model is symmetrical in the sense that both sexes are assumed to have the same properties, but not necessarily the same impact on paternity. There are two primary axes: time to fertilization is horizontal, and spatial proximity to fertilization is vertical. The diagonal axes represent sperm and eggs following tracks in space-​time that lead to fertilization (could be termed the “fertilization axis”). The space-​time area is divided into four domains, D1–​D4. These are D1, the gamete domain, in which sperm and eggs are spawned into the water: no decapods are a part of this domain, it is only included to allow out-​group comparison; D2, the mate choice domain where gametes are retained and transferred between chosen males and females, with fertilization occurring without delay; D3, gamete storage domain where they are stored externally and fertilization is external and delayed; and D4, gamete storage domain where they are stored internally and fertilization is internal and delayed. In whatever domain fertilization occurs, it is implicit that the factors of greatest importance are those immediately preceding fertilization, while others, more distant in space and time, rapidly diminish. Across these domains the physical dimensions of the “fertilization space” become smaller, but the temporal dimensions become larger because protection is provided and gametes survive longer. In the present context both sperm and eggs are stored by the female.   



Detecting Cryptic Female Choice in Decapod Crustaceans

mate-​choice is possible by either or both males and females. If fertilization occurs soon after, sperm competition is unlikely (Domain D2 in Fig. 13.1). If there is a delay, however, then sperm must be attached or stored by the female, making multiple partners and sperm competition a possibility (D3 in Fig. 13.1). When the female provides greater security for sperm by storing it internally (D4), there are new possibilities (Fig. 13.1). As a general principle, we employ the assumption that events with the closest space/​time distance from fertilization will be more important in determining the outcome than those more distant. Across these domains, the physical dimensions (s) of the “fertilization space” become smaller, but the temporal (t) dimensions become larger because protection is provided and gametes likely survive longer. We can define changes to the space/​time ratio along this axis as varying from Max (s/​t) → Min (s/​t). It is clear that in Domains D3 and D4, both CFC and sperm competition are possible and so are contenders to explain paternity. Here, we only directly address the search for CFC. In decapod crustaceans, fertilization occurs in roughly the same place as where the sperm are deposited, with the exception of species with a thelycum, annulus ventralis, or a spermatheca separate from the oviduct. In penaeoid shrimps, some freshwater crayfish and podotreme crabs’ sperm, respectively, are placed in these transitional storage sites and subsequently liberated, by unknown means, into the abdominal chamber, where fertilization occurs (Bauer 1994, Tavares and Secretan 1993). Central to understanding mate choice is how females might influence paternity. Fertilization in a particular decapod is affected by the following factors: (1) growth format (indeterminate [IDG] or determinate [DG]); (2)  link between molting and mating (intermolt hard shell or molt soft shell); (3) mate guarding by males (precopulatory or postcopulatory guarding, or both; (4) sperm guards used by males (spermatophores intact or burst, sperm plaque or sperm plug or gel layer); (5) delay between copulation and fertilization (sperm mixing is proportionate to latency); (6) the architecture of sperm storage, including capacity (see McLay and López Greco 2011 for theoretical background). We argue that these six factors provide the context in which we must look for CFC. We include growth format because female decapods that have indeterminate growth continue to molt and so lose all or part of their sperm reserves as they molt. In contrast, females who have determinate growth do not lose sperm after the terminal molt and instead may accumulate sperm across multiple mating cycles if they occur. When a female has indeterminate growth, some loss of stored sperm occurs during the molting process regardless of whether it is stored externally or internally. External attachment to chitin results in total loss, and security of internal storage depends on proportion of the receptacle lined with chitin (see Sainte-​Marie 2007, Fig. 9.1, and McLay and Lopéz Greco 2011, Fig. 3, for a more detailed discussion on the effects of growth format). Therefore, molting is an effective way of erasing mating history and can be used as such, in addition to other mechanisms (e.g., physically removing sperm from the body using limbs). Growth format is also related to mate attraction, which can be linked to molting (ancestral) or can occur during the intermolt (derived). For a long time, and because growth and reproduction (soft-​shell mating) were linked in some species, the release of molting hormones in mature female urine had been assumed to elicit mate attraction. Molting hormones were involved in the decalcification necessary to extract the new body from the old exoskeleton, but had an additional role in mate attraction. However, hard-​shell mating during the intermolt requires an alternative mechanism for females to attract males and obtain sperm because no growth occurs, and therefore no decalcification is needed. The signal could be released by the ovary to indicate that it has reached maturity (McLay and Sal Moyano 2016). Male mate guarding (precopulatory or postcopulatory) can become one of the main mechanisms used to control with whom a female copulates. Another determinant of paternity is the way in which males deposit various blocking devices, like sperm plugs, when the ejaculate is transferred. These devices are substitutes for

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Reproductive Biology guarding when the male is no longer present. The length of the delay (latency) between copulation and fertilization can influence the amount of sperm mixing that occurs in the storage organ. Sperm mortality will be higher when sperm are carried externally than if they are stored internally. Sperm must also have a shelf life that exceeds the length of the fertilization delay (McLay and López Greco 2011). Finally, the architecture of the sperm storage organ can have an important effect on which ejaculate fertilizes the majority of ova. In brachyuran crabs, the most important elements are where the oviduct enters the sperm storage organ and whether the chamber is divided into more than one semi-​autonomous section. The capacity for sperm storage also determines the need for a female to attract a male to copulate and replenish her sperm reserves. Structure of Thelycum, Annulus Ventralis, and Spermatheca The architecture of decapod sperm storage organs can be divided into those without a direct connection to the ovary (thelycum, annulus ventralis, and spermatheca) and those with a direct connection (seminal receptacle). The thelycum is a term applied to the genital area of the sternum of mostly penaeoid shrimp where spermatophores may be temporarily attached or stored for a prolonged period and where sperm-​free gel may be deposited by a male (Bauer 1994). We use the term spermatheca to refer to a pair of sperm storage chambers, opening on the sternum, formed by the last two thoracic segments of brachyuran podotreme crabs. We use these terms, in a sense, to be consistent with sperm storage morphology (Guinot et al. 2013). To demonstrate, Nephrops norvegicus has a thelycum involving sterna of the last two thoracic segments: the penultimate sternal plate forms a triangular shaped cavity, which is closed by a V-​ shaped structure on the following segment (Farmer 1974a). Viewed externally, they form an inverted Y-​shaped slit-​like opening (see A in Fig. 13.2). A sagittal section of the thelycum shows it filled with a hardened gel mass protecting sperm at the anterior end of the chamber (see B in Fig. 13.2) (Farmer 1974b). For many years there was a controversy about how female lobsters fertilized their eggs, with some people claiming that fertilization was internal (Farmer 1974b, Aiken and Waddy 1980). The controversy arose because lobsters could fertilize their eggs despite the presence of a sperm plug blocking the entrance to the thelycum. Aiken et  al. (2004) solved this problem by performing some elegant occlusion experiments on the thelycum of Homarus americanus (D in Fig. 13.2). They showed that fertilization could still occur when the entrance to the sperm storage chamber was occluded, because sperm was released from two grooves posterior to the entrance to fertilize eggs released from the coxal gonopores. In fact, the sperm did not retrace their entry route but followed an alternate exit, showing that fertilization was indeed external. The female expels sperm, as a result of muscular compression of the walls of the storage chamber. This is possible in these decapods because they have a mobile last thoracic segment. Experimental evidence from the spiny lobster Jasus edwardsii (Palinuridae) also shows that external fertilization is from spermatophores attached to the female sternum (MacDiarmid 1988). The annulus ventralis is found in some freshwater crayfish (Astacidea:  Cambaridae) and consists of a variously shaped chamber, lined with exoskeletal chitin, on the sternum of the seventh thoracic segment, which may or may not be blocked by a sperm plug (see C in Fig. 13.2, Orconectes limosus) (Andrews 1906). For our purposes, there is only one functional type:  ova released from coxal gonopores and sperm released from the annulus ventralis with external fertilization in the abdominal chamber. The female likely controls the meeting of both ova and sperm, with the last male to mate possibly having a fertilization advantage in some cases (McLay and van den Brink 2016).



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Fig. 13.2 (A) Ventral view of Nephrops norvegicus sternum. Gp  =  gonopore; Th  =  thelycum. Modified from Farmer (1974a), with permission from Taylor and Francis. (B) Sagittal section through N.  norvegicus thelycum. Entrance = entrance to thelycum; M = ejaculate; Sp = spermatozoa. Modified from Farmer (1974b), with permission from John Wiley and Sons. (C) Annulus ventralis of Orconectes limosus; Upper: empty; lower: showing plug projecting from entrance and spermatozoa stained black. Modified from McLay and van den Brink (2016). (D) Ventral view of Homarus americanus thelycum. OR = entrance to thelycum; PLG = posterolateral grooves separating plates on sterna of last two thoracic segments; 4th, 5th = pereopods four and five; arrows mark sperm exit routes from the thelycum. From Aiken et al. (2004), with permission from Oxford University Press.   

Structure of the Seminal Receptacle in Brachyura Ova released from the ovary must pass through the seminal receptacle, and the exposure to sperm is determined by the distance between the end of the oviduct and the beginning of the vagina. What exactly propels the ova along this path remains enigmatic, but the force must be entirely female-​ controlled. The seminal receptacle is literally the “playing field,” being a fertilization space defined by the female, but as we shall see, males have a number of ways to modify the game in their favor using various blocking devices. Our aim is to investigate whether females can also have a cryptic way to manipulate the outcome of fertilization.

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Reproductive Biology We illustrate the functional differences of seminal receptacles in a diagrammatic fashion (Fig. 13.3). The seminal receptacle is an inflatable “balloon-​ like” pouch whose wall is made of connective tissue. As more ejaculates are inserted, earlier ones are pushed further into the receptacle, normally in a dorsal direction, but could be anteriorly further away from the vagina. Internally, the receptacle is dorsally lined with glandular mesodermal epithelium and/​ or with a chitinous layer ventrally (Diesel 1991). McLay and López Greco (2011) concentrated on three kinds of seminal receptacles where the oviduct enters the chamber dorsally (DSR), ventrally (VSR), or at some intermediate point in between (ISR). Those previously referred to as DSR are now split into Types I–​III, VSR are split into Types V–​VI, and Types IV, VII, and VIII are referred to as ISR (Fig. 13.3). The ISR category includes seminal receptacles with and without an internal muscular velum. Kienbaum et al. (2017) recently questioned the interpretation of these apparent partitions. Here we recognize eight different seminal receptacles derived from a putatively ancestral receptacle whose inner wall was totally composed of chitin wherein the oviduct and vagina were at opposite poles (see McLay and López Greco 2011, Fig. 2) (Type I, Fig. 13.3). There are no known brachyurans who have this hypothetical ancestral state. The oviduct may enter dorsally into the receptacle lined with mesoderm up to half its surface, as in Callinectes sapidus (Type II, Fig.. 13.3; see Jivoff et al. 2007), or greater than half its surface, as in Arenaeus cribrarius (Type III; see Zara et al. 2014). With the same area of mesoderm, the oviduct may enter at some intermediate point as in Portunus sanguinolentus (Type I, Fig. 13.3; see Diesel 1991). Alternatively, the oviduct may enter ventrally with almost all the internal surface lined with mesoderm as in Chionoecetes opilio (Type V; see Sainte-​Marie et al. 2008) and Metacarcinus edwardsii (Type V, Fig. 13.3; see Pardo et al. 2013). The presence of a bursa can be added to this state, as in Metacarcinus magister (Type VI, Fig. 13.3; see Jensen et al. 1996). There are other species (Calappula saussurei, Calappidae; and Potamon fluviatile, Potamidae) with more complex seminal receptacle variations of the ventral type, which are not included in our analysis (Brandis et al. 1999, Ewers-​Saucedo et al. 2015). Finally, we recognize receptacles half-​lined with mesoderm and half with chitin, but divided into two chambers by a muscular velum or folds, with two variants differing as to whether the oviduct enters into the ventral chitin-​lined chamber, as in Inachus phalangium (Type VII, Fig. 13.3; see Diesel 1989), or the dorsal mesodermal-​lined chamber, as in Libinia spinosa and Leurocyclus tuberculosus (Type VIII, Fig. 13.3; see Gonzalez-​Pisani et al. 2012). In all the preceding cases, except for the ancestral condition, each can be separated into a mesodermal part (MSR) and an ectodermal (chitin) part (ESR). In eubrachyuran crabs, the fertilization site is the seminal receptacle (SR) where sperm are deposited and stored (McLay and Lopéz Greco 2011). The meeting place is a spot closest to where the oviduct enters the receptacle. We would like to know about the dynamics of the SR contents, controlled by the female, but so far this has not proved possible. It seems likely that the muscular walls may have a role in aiding the passage of ova through the SR, and into the vagina, so the same mechanism might manipulate its contents prior to fertilization. Given limited knowledge of female control over SR contents, we start at the endpoint and work backward so that we can place the role of CFC in proper sequence and context. Cryptic female choice can initially only be detected by failure of these other mechanisms, such as oviduct connection, that may lead to differential fertilization success. Ultimately, the best way to assess the role of CFC is by measuring paternity in an experiment where there is a clear null hypothesis (i.e., what we would expect if there were no CFC). What would we expect to find in each of these SR types? In females with Type I–​III seminal receptacles, we would expect first-​male precedence because the oviduct enters dorsally, but we have to remember that the eggs must traverse the whole SR to reach the vagina and so could be fertilized by other sperm encountered along the way. The fertilization opportunity is proportional to egg residence (transit) time in the SR (McLay and López Greco 2011). Residence time of ova in the SR ranges from several seconds in low-​fecundity females to less than one hundredth of a second in high-​fecundity portunid species (McLay and López Greco 2011). First-​male ejaculates would have



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VIII (ISR)

Fig. 13.3. Variation in the structure of eubrachyuran seminal receptacles. These are referred to as Type I to Type VIII, where DSR means that the oviduct enters dorsally opposite the vagina; VSR means that the oviduct enters ventrally adjacent to the vagina; and ISR means that the oviduct enters at some intermediate point in between. The black lining is ectodermal chitin; the grey lining is mesodermal tissue. Modified from McLay and López Greco (2011).   

the best chance to achieve paternity, but not exclusively so. By contrast, Type V and VI seminal receptacles would be expected to yield last-​male precedence with even better chances of paternity because eggs can take the shortest route to the vagina and not be exposed to sperm from any other ejaculates. The most complicated SR are Types IV, VII, and VIII, where the oviduct enters the SR at some point midway. In these receptacles, neither first nor last males are favored, but rather males who mated somewhere around midway in the sequence. We think that the rank order of uncertainty about paternity would be lowest in Types V and VI < Types I–​III < Types IV, VII–​VIII. We note that the effects of sperm mixing are not included because of the absence of such data. The other structural influence on paternity concerns the tissues lining the SR walls. The tissues in question are the mesodermal secretory tissue (usually dorsal), which may provide nutrition for sperm, and the chitinous layer (usually ventral), which is assumed to be a hazardous place for sperm

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Reproductive Biology because they could be shed when the female molts. The greater the amount of chitinous lining, the greater the loss of sperm during molting. In the ancestral Type I SR, there can be no trans-​molt sperm retention because the inner wall is chitinous throughout. We assume that the level of trans-​ molt sperm retention increases as the area of chitinous lining decreases (McLay and López Greco 2011). Finally, we must note that females with determinate growth, as in Chionoecetes opilio (Type V, Fig. 13.3), are sperm accumulators because they have no way of discarding sperm, while Cancer pagurus (Fig. 13.3), which has the same SR, can discard sperm and gather more because they have indeterminate growth. Despite having indeterminate growth, the Brazilian mangrove crab Ucides cordatus is also a sperm accumulator like Chionoecetes opilio because it apparently has no chitin lining of the seminal receptacle (see Sant’Anna et al. 2007). The tissue composition of the inner lining of the SR has been described in a few species, and the important role this plays in sperm retention has been recognized; this is an exciting frontier in crustacean CFC research.

DECAPOD MATING SYSTEMS The mechanisms that influence fertilization are mate guarding, sperm guarding, and sperm displacement by males, as well as sperm storage architecture, mating-​molting linkage, and fertilization delay by females. Table 13.1 lists 26 species of decapod crustaceans for which paternity data are available. The majority of the species (85%) show multiple paternities (MP), with only 15% showing single paternity (SP). Among these decapods, multiple paternities are the norm rather than the exception. We divide these species into six groups, each of which characterizes a different crustacean lifestyle and contrasting ways of storing sperm: shrimps, lobsters, crayfish, squat lobsters, anomuran crabs, and brachyuran crabs. Shrimps Many shrimps (Caridea) (Table 13.1) live in close association with other conspecifics, including heterosexual pairs, or sometimes with other animals who can collectively improve their chances of survival and reproduction (Thiel and Baeza 2001). Alpheid shrimps are of particular interest because they live cooperatively in a burrow, which they dig and maintain. Alpheus angulosus (A in Fig. 13.4) living in burrows on a Florida beach, in size-​matched heterosexual pairs, co-​defended their territory against other pistol shrimps of both genders. While males mated mainly with their partner, they also had extra-​pair copulations with neighboring females of greater reproductive value (closer to sexual receptivity) (Mathews 2002, 2007). Most broods were fathered by the female’s partner, but 31% were sired by another male. Male defense of the shared territory apparently does not always exclude interlopers. Males do not depart to search for other females once the female has laid her eggs, presumably because it is safer to stay in their shared territory. The reproductive success of male rock shrimp Rhynchocinetes typus (B in Fig. 13.4) depends on their ability to win fights over females and guard them against competitors (Correa and Thiel 2003, Thiel and Correa 2004). Females prefer to mate with large males (“robustus” stage), which are equipped with larger chelipeds and third maxillipeds, rather than smaller subordinate males (“typus” stage). Females can resist, but not avoid, mating with subordinate males, described as “convenience polyandry” (Thiel and Hinojosa 2003). Bailie et al. (2014) confirmed multiple paternities, which found that two to four males had sired 73.3% of broods. The possibility of CFC in this shrimp was indicated by the discovery that a female could selectively remove spermatophores from subordinate (“typus”) males, using her second pereopods, before mating with dominant (“robustus”) males (Thiel and Hinojosa 2003). Paternity distribution depends on the mating sequence: if the female mated with a “typus” male first and was unable to remove all his spermatophores, and subsequently

IDG

DG in males? IDG in females

Rhynchocinetes typus (Rhynchocinetidae)

M & M linked

M & M linked

Spermatophore external so not protected

Spermatophore external so not protected

Spermatophore external so not protected Male guards pre-​molt Spermatophore female for up to external so not 3h protected

No guarding

No?

M & M linked

Palaemonetes pugio (Palaemonidae)

Territorial monogamous pairs in burrows

M & M linked

Sperm Guarding

Male guards pre-​molt Spermatophore female for a few external so not days? protected

Mate Guarding

Alpheus angulosus IDG (Also known as Alpheus angulatus) (Alpheidae) Caridina ensifera IDG (Atyidae)

Mating –​ Molting Link

M & M linked

Growth Format

Acanthephyra pelagica IDG (Acanthephyridae)

Species (Family)

External sperm storage

External sperm storage

External sperm storage

Sperm Storage and Architecture of chamber External sperm storage

Short delay External sperm between storage mating and fertilization may be controlled by female.

2–​3 h

A few hours

A few hours

A few hours

Fertilization Delay

Table 13.1.  Features of the Mating System of Some Decapod Crustaceans Relevant to the Question of Paternity and CFC.

Skewness (60.3%) MP (2–​4 m) in 100% broods Skewness (94.4%) MP (2 m) in 31% of broods Skewness (35.4% MP (2–​11 m) in 100% of broods Skewness? MP in 80% of broods Skewness (54.8%) MP (2–​4) in 73.3% broods

Paternity and skewness (mean %)

(Continued)

Bailie et al. 2014

Baragona et al. 2000

Yue and Chang 2010

Mathews 2007

Paegelow 2014, Jorquera et al. 2016

Source

Growth Format

IDG

IDG

IDG

IDG.

Species (Family)

Homarus americanus (Nephropidae)

Homarus gammarus (Nephropidae)

Nephrops norvegicus (Nephropidae)

Orconectes placidus (Cambaridae)

Table 13.1 Continued

M & M not linked?

M & M linked

Sperm Guarding

No guarding?

No guarding

Spermatophore and sperm plug can be present.

Spermatophore and sperm plug

Spermatophore and sperm plug, but see text; Erkan and Ayun 2014

Shelter cohabitation Spermatophore and both pre-​molt and sperm plug, but post-​molt after see text copulation

Mate Guarding

M & M linked. Male attracts Gibson, 1967; also females to shelter intermolt mating; Guarding before, Waddy and Aiken and after mating 1991

Mating can occur post-​molt and inter-​molt

Mating –​ Molting Link

Sperm Storage and Architecture of chamber Open thelycum Sperm can remain viable for 3 years.

Several months?

Skewness? MP In 17.8% of broods

Skewness (69.5%) MP (2–​3 m) in 13% of broods

Paternity and skewness (mean %)

Gibson 1967, Debuse et al. 1999, Erkan and Ayun 2014, Ellis et al. 2015 Streiff et al. 2004

Gosselin et al. 2005

Source

Skewness (50%) MP (2–​3 m) in 54% of broods Annulus ventralis Skewness Walker et al. (82.7) MP. 2002 (2 m) in 60% of broods

Approx. one month Open thelycum

Variable delay 1–​24 months; Waddy and Aiken 1991 say female can fertilize two broods using stored sperm. Sperm may be held Open thelycum for up to a year; Debuse et al. 1999

Fertilization Delay

374

IDG

IDG

IDG

IDG?

IDG

IDG

IDG

Orconectes obscurus (Cambaridae)

Orconectes sanbornii (Cambaridae)

Procambarus clarkii (Cambaridae)

Callichirus islagrande (Callianassidae)

Munida rugosa (Galatheidae)

Munida sarsi (Galatheidae)

Petrolisthes cinctipes (Porcellanidae)

Probably have guarding

Probably have guarding

?

No guarding

No guarding?

No guarding?

M & M not normally No guarding linked

M & M not linked

M & M not linked?

?

M & M not linked

M & M not linked?

M & M not linked?

Several months?

Annulus ventralis Skewness (71.6%) MP (2–​3 m) in 100% of broods Spermatophore and Several months? Annulus ventralis Skewness sperm plug? (68.4%) MP (2–​3 m) in 100% of broods Spermatophores No 30 days? Annulus ventralis Skewness plug in AV access (74.2%) MP unguarded (2–​4 m) in 97% of broods Spermatophores ? External sperm MP (2–​3 m) storage in 20% of broods Spermatophores Probably a few days External sperm Skewness storage. (76.3%) MP (2–​4 m) in 86% of broods Spermatophores Probably a few days External sperm Skewness storage (55%) MP (2–​4 m) in 100% of broods Spermatophores About 1 hour External sperm MP (2–​4 m) storage in 80% of broods

Spermatophore and sperm plug?

(Continued)

Toonen 2004

Bailie et al. 2011

Bailie et al. 2011

Bilodeau et al. 2005

Yue et al. 2010

Kahrl et al. 2014

Kahrl et al. 2014

M & M linked

M & M linked

M & M linked

M & M linked

M & M linked

IDG

IDG

IDG

Paralithodes camtschaticus (Lithodidae) Paralithodes platypus (Lithodidae) Cancer pagurus (Cancridae)

Metacarcinus edwardsi IDG (Cancridae)

Metacarcinus magister IDG (Cancridae) [Oh and Hankin 2004]

Mating –​ Molting Link

Growth Format

Species (Family)

Table 13.1 Continued

2–​48 h

2–​48 h

Fertilization Delay

Sperm plug no intact Several months spermatophores

Sperm plug no intact A few months to spermatophores 15 months

Spermatophores

Spermatophore

Sperm Guarding

SP

Paternity and skewness (mean %)

Skewness (63.8%) MP (2–​3 m) in 40% of broods

External sperm SP storage Ventral SR SP without bursa (Type V) Ventral SR SP without bursa (Type V)

Sperm Storage and Architecture of chamber External sperm storage

Post-​copulatory Sperm plug. Several (6) months Ventral SR. with guarding for 3 days No intact Sperm can bursa (Type spermatophores? remain viable up VI) to 2.5 years.

Pre-​ and post-​molt guarding

Mate guarding pre-​ and post molt?

Pre-​molt guarding

Pre-​molt guarding

Mate Guarding

Rojas-​ Hernandez et al 2014, Pardo et al. 2013, 2015, 2016 Jensen and Bentzen 2012

Stoutamore 2014 McKeown and Shaw 2008

Vulstek et al. 2013

Source

376

DG

IDG

IDG

IDG

Chionoecetes opilio (Oregoniidae)

Dissodactylus primitivus (Pinnotheridae)

Ucides cordatus (Ucididae)

Uca mjoebergi (Ocypodidae)

M & M not linked

Burrow-​guarding ensures last-​male paternity.

?

Spermatophores and 3–​5 d free sperm No plug

Spermatophores and 2–​3 months free sperm No plug

?

Sperm plug but Several months up dissolves to a year after 5 wks. Intact spermatophores Pre-​and post-​ Spermatophores, gel 1–​72 h copulatory Sperm stratification guarding for 3–​6 d Contrib. of single male 90%–​60%; Sainte-​Marie et al 2008

Pre-​and post-​ copulatory guarding

M & M linked? More Male –​female pairs than 30 instars, co-​habit same with10+ being urchin host Mate post-​pubertal; guarding unlikely Pohle and Telford 1982 M & M linked “Andada” mating See Pinheiro season Dec–​May et al. 2005. Burrow-​linked

M & M linked + intermolt mating

M & M linked

Skewness (79.3%) MP (2 m) in 3.8%–​12% of broods; also SP in one study Skewness (85.8%) MP. (1–​6 m) in >60% of broods

Jossart et al. 2014

Urbani et al. 1998, Roy 2003, Sainte-​ Marie et al. 2008

Ventral SR, but Skewness?, MP Baggio et al. lacks chitinous (2 m) in 40% 2011, lining found in of broods Sant’Anna other Type V et al. 2007 females Ventral SR Skewness Murai et al. (probably (97.9%) MP 1987, Type V) (2 m) in 56% Kinnear of broods et al. 2009, Reaney et al. 2012

Ventral SR (probably Type V)

Ventral SR (Type V) [Paternity different in 3 studies]

Dorsal SR (Type Skewness Jivoff et al II) (none?) MP (2007); Hill (2+ m) 5.3% et al (2017) of broods

Notes: Skewness is the mean % paternity of major contributing male; IDG/​DG: determinate/​indeterminate growth; M&M linked: molting and mating linked; MP: multiple paternity; SP: single paternity; m: males.

DG

Callinecetes sapidus (Portunidae)

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Reproductive Biology mated with a “robustus” male, then multiple paternity could result; otherwise the “robustus” male was the sire. Receptive females were observed in the field to mate with up to five males within 10 minutes (Thiel and Correa 2004). In addition, female R. typus were able to delay ovulation, thereby increasing the possibility of mating with preferred males (Thiel and Hinojosa 2003). Larger males are better able to guard females and provide more sperm. Whether or not CFC was involved in determining the composition of the broods sampled by Bailie et al. (2014) is impossible to tell because the copulation sequences were not observed. Palaemonetes pugio is an estuarine shrimp that lives in dense groups. Berg and Sandifer (1984) have described mating behavior. Antennal contact by males allowed recognition of the female’s reproductive state. Males are only attracted to females within 24 hours before her molt, especially one hour beforehand. Video observations showed that copulations took place within one to three minutes of the molt. Mean duration of the period from the female molt to spawning was only 113 minutes, and during this period there was no evidence of guarding behavior (Bauer and Abdalla 2001). When females were held without males, the maximum time between molting and spawning, the only time when copulation can occur, was around 24 hours. Under such circumstances, we might expect few males contributing to fertilizations, but Baragona et al. (2000) found that 80% of broods had multiple paternities. Lobsters Females in this group possess a sternal structure specialized for sperm storage:  lobsters have a thelycum not connected directly to the oviduct (Table 13.1). Although all of the present examples are lobster-​like, the primitive podotreme crabs would also be included here if we had paternity data because they have spermathecae (Guinot et al. 2013). In these lobsters, the males often deposit a sperm plug to block the sperm entrance. In Homarus americanus and H. gammarus (C in Fig. 13.4), mating is linked to molting, where mate guarding occurs; so, a low level of MP would be expected. Intermolt mating is also possible; so, if females produce a second inter-​molt brood, then more than one male may be represented. The marine clawed lobster Nephrops norvegicus is similar, but males do not guard the female after copulating, so a higher level of MP might be expected: results are 54% of broods compared with only 0%–​18% in Homarus (Sørdalen 2012, and Ellis et al. 2015). In all of these species, there can be a fertilization delay of one to 24 months after mating. This means that when sampling ova for paternity analysis, it may be necessary to know whether the brood is first or second since copulation occurred. Crayfish The freshwater clawed crayfish Orconectes placidus, O. obscurus and O. sanbornii, and Procambarus clarkii (Cambaridae) (C in Fig. 13.4) have an annulus ventralis, which is a semi-​closed sperm chamber separate from the oviduct (Table 13.1). Unlike lobsters, mating is not linked to molting and there is no mate guarding, but a sperm plug has been reported in some species. In most of these species, there is a substantial fertilization delay (up to several months) after copulation (see, for example, Ingle and Thomas 1974, Galeotti et al. 2006, Aquiloni and Gherardi 2008). It is clearly not worthwhile for guarding males to remain in attendance. Like other cases of hard-​shell mating decapods, how females attract males remains a mystery, but a signal that advertises ovarian maturity seems most likely. The Cambaridae have high levels of MP, which is probably a consequence of the lack of guarding and long delay in fertilizing the eggs (Table 13.1). By contrast, the Astacidae have external sperm storage and males deposit spermatophores on the female sternum, but no paternity analyses have been done in this family. Ingle and Thomas (1974) reported that in Austropotamobius

(A)

(E)

(B)

(F)

(C)

(G)

(D)

(H)

Fig. 13.4. Examples of the decapod Crustacea from which paternity data were obtained and analyzed:  (A) Alpheus angulosus (Caridea:  Alpheidae); (B)  Rhynchocinetes typus (Caridea:  Rhynchocinetidae), mate guarding; (C)  Homarus gammarus (Astacidea:  Nephropidae); (D)  Procambarus clarkii (Astacidea:  Cambaridae); (E)  Munida rugosa (Anomura:  Galatheidae); (F)  Paralithodes camtschaticus (Anomura:  Lithodidae); (G) Chionoecetes opilio, (Brachyura: Oregoniidae); (H) Cancer pagurus (Brachyura: Cancridae). See color version of this figure in the centerfold. (A) Courtesy of Paulo P. G. Pachelle; (B) after Baeza et al. (2014), with permission from Oxford University Press; (D) courtesy of Duloup; (E) courtesy of Keith Hiscock; (F) courtesy of David Csepp; (H) courtesy of Hans Hillewaert.   

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Reproductive Biology pallipes, females mated with up to five males and that large males mated up to six times, so high levels of MP should be anticipated. However, A. italicus (Astacidae) males take radical steps during mating to modify fertilization outcomes by removing and eating many (average 77.2%) of the spermatophores deposited by earlier males. A third of the subsequent mating partners removed all of the first male’s sperm before depositing their own (Villanelli and Gherardi 1998, Galeotti et al. 2007). As noted earlier, Rhynchocinetes typus females will mate with subordinate males, but eventually remove their spermatophores before mating with a dominant male. Sperm removal has obviously evolved at least twice in both males and females, with each sex trying to skew paternity in their favor. Squat Lobsters Paternity data are available for two galatheid squat lobsters:  Munida rugosa (E in Fig. 13.4) and M.  sarsi (Table 13.1). Knowledge of growth and reproduction in these particular species is limited, but the results of research on other galatheid species are instructive. Pleuroncodes monodon, Agononida longipes, Munida gracilipes, M. constricta, M. flinti, M. forceps, and M. irrasa do not have a terminal molt (P. Hernáez, personal communication). Squat lobsters are often found in large aggregations, so mate availability is high. There are two contrasting mating strategies in squat lobsters (Thiel and Lovrich 2011, Thiel et al. 2012). Some species have males searching for receptive females and no guarding (e.g., M. gregaria and P.  monodon) or they have pre-​and postcopulatory guarding (e.g., Cervimunida johni and P.  planipes; Tulipani and Boudrias 2006, Espinoza-​Fuenzalida et  al. 2012). Female M.  gregaria mate during the intermolt (Perez-​Barros et al. 2011). Similarly, mating is not linked to molting in C.  johni and P.  monodon (Espinoza-​Fuenzalida et  al. 2012). Spermatophore transfer may involve both gonopods and the reduced pereopod 5 (P5). Females of C. johni use the P5s to mix the newly laid eggs with sperm from spermatophores in the abdominal “basket.” It is uncertain exactly how the ampullae are opened, but it may be by the female. Females produce successive broods without molting. Inter-​brood intervals are only a few days; male mate guarding in C. johni can last up to 72 hours and begins soon after post-​ovigerous females release their larvae (see photo of guarding pair, Fig. 13 in Thiel and Lovrich 2011). By contrast, P. monodon probably have a longer latent period, and fertilization occurs up to 144 hours after the release of the previous brood (Thiel and Lovrich 2011, Espinoza-​Fuenzalida et al. 2012). Whether or not female squat lobsters have multiple partners probably depends on density: if they live symbiotically on hosts, then the female may not have any choice about who to mate with, especially if density is low. So females could be either polygamous or monogamous depending on the number of males present. The most common scenario is probably polygyny. Bailie et  al. (2011) found that in M.  rugosa and M.  sarsi, 86%–​100% of broods had multiple paternity (two to four males). If females of these species use their P5s in the same manner as C.  johni to open spermatophores, then cryptic female choice may be possible. Crab-​Like Anomurans Crab-​like decapods (Table 13.1), for which we have paternity data, include Petrolisthes cinctipes. In porcelanid crabs, molting and mating may or may not be linked. Molenock (1975) observed that in P. manimaculis, mating was linked to molting and females laid eggs within a “few hours” of copulation. Brief (a “few hours”) precopulatory and postcopulatory male guarding occurred. However, in P. cinctipes, males mated only with hard females, accompanied by little guarding (Toonen 2004). Females laid their eggs about one hour after mating. Even though this species lacks sperm storage,



Detecting Cryptic Female Choice in Decapod Crustaceans

females may be able to accumulate spermatophores under the abdomen and produce multi-​sired broods. Toonen (2004) found that 80% of the broods of P. cinctipes had multiple paternities with two to four males involved. This crab lives in dense aggregations in the rocky intertidal zone of the northeast Pacific coast. In king crabs (Lithodidae), mating is linked to molting, and males perform precopulatory mate guarding that can last as long as one week. Fertilization occurs within a few hours after mating (Webb 2014). Males use their P5s to transfer spermatophore ribbons to the female sternum. Thus, we might expect MP to be low or nonexistent. Paralithodes camtschaticus (F in Fig. 13.4) and P. platypus have a similar reproductive pattern with external sperm storage (Powell and Nickerson 1965). Both species seem to have single male parent broods (Vulstek et al. 2013, Stoutamore 2014). Males clearly exercise tight guarding over the females they choose to mate with and need to provide sufficient sperm to fertilize the whole brood if they are to be the sole partner. Brachyuran Crabs Crabs belonging to the Eubrachyura have an internal sperm storage chamber linked to the oviduct, and the point at which the oviduct enters differs, creating eight different types of seminal receptacles (Fig. 13.3). Most paternity data available are for VSR of types V and VI (Table 13.1). The only exception is Callinecetes sapidus (DSR, Type II). The blue crab can fertilize up to six broods over two years without molting and remating, but have limited opportunities for multiple male partners that could result in MP (Hines et al. 2003). Seven of the eight species have mating linked to molting, and males can guard females both before and after copulation. The fertilization delay may be a few days or several months. On the one hand, we have several factors that could decrease the chances of MP, but this must be tempered by the fact that females can store sperm for long periods because it is not lost during molting. Cancer pagurus (H in Fig. 13.4) females (Type V) can fertilize up to three broods without remating (McKeown and Shaw 2008). Trans-​molt sperm retention means that males, which featured long ago in the mating history, can still fertilize eggs. Males of C. pagurus, Metacarcinus edwardsii, and M. magister can also deposit a sperm plug, deterring further mating partners. In C.  pagurus and M.  edwardsii (Type V), we find single paternity broods (McKewon and Shaw 2008, Pardo et al. 2016), but a high proportion (40%) of M. magister females have been found to have MP ( Jensen and Bentzen 2012). Moreover, in the case of M. edwardsii, SP broods are not necessarily the result of a female mating with one male. Pardo et al. (2016) compared brood paternity with ejaculates in the seminal receptacle and found that while there was only a single male represented in the brood, there could be three or more ejaculates in the receptacle, each of which could have come from different males. We can conclude that mate guarding by the last male to copulate ensured his paternity. Metacarcinus magister has more complex sperm storage with the addition of a bursa to the SR (Type VI). Bursal sperm is not used for fertilization and is not retained from one molt to the next. While the male whose sperm is in the bursa may not get any benefit for his efforts, the soft-​shell female may well gain from his protective postcopulatory guarding ( Jensen and Bentzen 2012). The Brazilian mangrove crab Ucides cordatus (Type V) has a similar suite of reproductive characters (Pinheiro et  al. 2005, Castilho-​Westphal et  al. 2013)  and level of MP as the cancrids. Baggio et al. (2011) found that 40% of broods had eggs fertilized by more than one male. There is a seasonal pattern of mating (known locally as the “Andada”) when both males and females emerge from burrows in the mangroves searching for mates. Mating occurs in burrows, but it is not clear whether there is any mate guarding. Spermatophores are transferred, but there is no sperm plug as found in the cancrids. An unusual feature of the seminal receptacles in this crab is that they do not have a chitinous lining, so in theory, females should accumulate sperm because none would be

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Reproductive Biology discarded when molting occurs (Sant’Anna et al. 2007). In other respects, the receptacles are the same as Cancer pagurus (Type V). Dissodactylus primitivus (Type V, assumed to be) is a pea crab symbiont on sea urchins and has a high level of MP (six fathers maximum and MP in more than 60% of broods) ( Jossart et al. 2014). The skewed parentage in 92% of multi-​parental broods is best explained by sperm competition. We do not know for sure whether mating and molting are linked in pea crabs, but to explain seminal receptacle contents for Pinnotheres pisum, it is necessary to assume that soft females mate in the last juvenile stage and then again during the intermolt hard mature stages (Becker et al. 2011, and C. Becker, personal communication). The same may apply to D. primitivus. There is no evidence of mate guarding, and growth in this species is indeterminate (Pohle and Telford 1982), but the number of post-​pubertal instars is uncertain. De Bruyn et al. (2009) found that these crabs were not socially monogamous and that both males and females are mobile between hosts. Crabs were found on hosts in all combinations of size and sex, making guarding unlikely. The mating system of D. primitivus involves a high rate of transfer between hosts, a pattern that might legitimately be called “bed-​hopping.” In Uca mjoebergi (Type V, assumed to be) there is no link between molting and mating. Unlike the previously mentioned species, it has hard-​shell mating, and MP was 56% with two males represented. There was a three-​to-​five-​day delay between mating and fertilization. Evidently, the burrow guarding may ensure last-​male precedence, but not 100% paternity. Reaney et  al. (2012) found that five out of nine (56%) burrow-​mated females produced offspring that were not fathered by the male guarding the burrow, but these interloper fertilizations were rare. The guarding male sired the vast majority (98%) of the eggs. Admittedly, this is a small sample size and the results should be viewed with caution. Trapping the female in a sealed burrow, until the eggs were laid, preventing her from remating, certainly paid dividends for the guarding male. The scope for CFC would seem small in this species. Similar levels of paternity were demonstrated for another burrowing crab, Scopimera globosa, using irradiated males (Koga et al. 1993). All of the species discussed up to this point have had indeterminate growth (IDG) but Chionoecetes opilio (G in Fig. 13.4; Type V) is a spider crab with determinate growth (DG). Crabs with this growth format are sperm-​accumulators. Seminal receptacles of females preserve the entire mating history because they cannot molt. Females mate first after the pubertal molt when they are soft (primiparous) and again after subsequent broods (multiparous) (Sainte-​Marie et al. 2002). Examination of C. opilio seminal receptacles showed up to 10–​12 ejaculates, which were neatly stratified when there were only a small or moderate number present, but disorderly and mixed when the sperm load was high (Saint-​ Marie et al. 2000). Having a VSR and with males providing pre-​and postcopulatory guarding, single paternity (by last male to mate) would be expected, but multiple paternities could occur when females copulate with many males, causing sperm mixing. Paternity of C. opilio broods has been investigated by three studies and the level of MP is low. Roughly speaking, detection of MP depends on sample size. A study that surveyed seven females found no MP, whereas studies surveying larger samples of females found 3.2% (n = 79) and 12.5% (n = 20) of females to have MP broods (Urbani et al. 1998, Roy 2003, Sainte-​Marie et al. 2008, respectively). Paternity data are also available for Callinectes sapidus with Type II DSR: mating is linked to molting, and growth is putatively determinate, so opportunities for mating with multiple males would appear to be limited, but a low level of MP (5.3%) has been found (Hill et al. 2017). Data are few, but a first guess might suggest that SR structure was not a primary factor in determining patterns of fertilization in these DG species (Table 13.1). In another DG species, Klaus et al. (2014) discovered a modified ventral seminal receptacle in the hymenosomatid freshwater crab Limnopilos naiyanetri, where the receptacle is lined by an epithelium, partially lined with secretory tissue, but lacked any chitinous lining often found in most crabs (also seen in U. cordatus; see Table 13.1). Furthermore, the vagina is divided into an unchitinized dorsal section, surrounded by a muscular epithelium, and a ventral chitin-​lined section with a small



Detecting Cryptic Female Choice in Decapod Crustaceans

bursa at the transition between the dorsal and ventral halves. In terms of our classification of SR, this species is similar to Type VI, as found in M. magister. Klaus et al. (2014) hypothesized that a female could exercise CFC by choosing which ejaculates could enter the seminal receptacle and directing the rest into the bursa. Given that L. naiyanetri has determinate growth and potentially many male partners, the small bursa (only 10% the size of the receptacle) would quickly fill with sperm, but the female could empty the bursa, employing the same musculature putatively used for selective entry to the receptacle. This species cannot molt to remove the bursa sperm because of its determinate growth format. A paternity analysis of L. naiyanetri would be valuable because it would allow a comparison of the effects of two different growth formats: M. magister IDG and L. naiyanetri DG. Meanwhile, the exact function of the bursa remains unknown. Either way, sperm in the bursa has a short shelf life because the female cannot provide any nourishment, such as that found in the receptacle, where most of the lining is secretory. For the moment, the bursa can be regarded as a dead-​end.

EXPLANATION OF PATERNITY The data used to explain paternity are summarized in Table 13.2. These include growth format, molting-​mating link, mate guarding, sperm guarding, fertilization latency, and sperm storage. We divide the species into three groups according to how they store sperm: (1) external sperm storage (n = 11), (2) thelycum/​annulus ventralis (n = 7), and (3) seminal receptacle (n =8 ), and compare brood paternity in relation to these characters. We compare paternity in terms of the level of MP, the number of males represented, and skewness (mean skewness is measured using data for the maximum % sired by one male in each brood which shows MP). External Sperm Storage In this group, mainly carideans and anomurans, the delay between copulation and fertilization is short, and mating/​molting/​mate guarding are employed and linked. Females receive intact spermatophores, which are either attached to their body or temporarily enclosed in the abdominal brood chamber where fertilization will occur. Latency in fertilization is shortest in this group, apparently because the spermatophores have very little protection and limited prospects of survival. Without protection, the shelf life of spermatophores is going to be much shorter, so they must be used quickly. External sperm storage should lead to low levels of MP. Moreover, these crustaceans (except squat lobsters) use sperm that has been collected during the short interval between when the female has molted and lays eggs, which should result in less opportunity for MP. However, the average putative number of males is 3.1 and the percentage of broods with MP is 74.5% (range 31%–​100%), suggesting that the males are not particularly effective in defending their partners. The lithodid crabs are the exceptions here. Paralithodes camtschaticus (F in Fig. 13.4) and P. platypus both show single paternity, as found in some cancrid crabs (Table 13.2). Mean skewness is the lowest of all the three groups at 63.1 %. Thelycum or Annulus Ventralis In this group, mainly lobsters and crayfish, a lower level of MP (mean = 63.1%; range 13%–​100%) is found. These crustaceans provide some protection for spermatophores, but without any direct connection between the storage site and the oviduct (Table 13.2). Here we can contrast marine lobsters with freshwater crayfish. Both use sperm plugs and have a fertilization delay of several months, but

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Reproductive Biology Table 13.2  Summary of Mating System Data for Decapoda. Character

External Sperm Storage (n = 11)

Growth Format Mating & Molting Linked

IDG 11/​11 6/​9 = 67%

Fertilization Delay A few hrs to a few (latency) days.

Thelycum (n = 3) or Annulus Ventralis (n = 4) IDG 7/​7 Linked in marine lobsters, but not in freshwater crayfish Marine lobsters can be 1–​24 months, FW crayfish normally several months Only in Homarus spp.

Seminal Receptacle (n = 8) IDG 6/​8 DG 2/​8. 6/​7 = 85.7% (where known) Several days to several months (could be several years)

Mate Guarding

71.4%

Sperm Guarding

Spermatophores only

Spermatophores and normally a sperm plug

Brood Paternity

MP: ​74.5% SP: ​25.5% 3.25 (11)

MP:​  63.1% SP: ​36.9% 2.5 (4)

7/​8 = 87.5% (where known) Spermatophores and plug/​gel (6/​8), spermatophores only (2/​8) MP: ​37.1% SP: ​60.4% 2.5 (6)

Mean = 63.1% (35.4–​94.4)

Mean = 73.1 (68.4–​82.7)

Mean = 81.7% (63.8–​97.9)

Mean # Males Detected in Brood (max) Mean Skewness (range)

Notes: Female mechanisms are Sperm Storage, Mating & Molting linkage and Fertilization Delay. Male mechanisms are Mate Guarding and Sperm Guarding. Performance measures are Brood Paternity, # Males Represented and Skewness. Growth Format is a shared character since it is the same for both sexes. (Mean skewness is measured using data for the maximum % sired by one male in each brood which shows MP.)

only lobsters have mating and molting linked and mate guarding. Contrasting the levels of MP, we find that lobsters only have 28.8%, but crayfish have 89.3%, which probably reflects dislocation of the link between molting and mating and the absence of mate guarding. Lobsters have a level of MP that is less than crabs (37.1 %), but the crayfish have MP that is greater than decapods, which provide no sperm protection (74.5%). Overall mean skewness is intermediate at 73.1%. Seminal Receptacle These are the eubrachyuran crabs which have internal seminal receptacles as part of the reproductive tract. They provide the most secure environment for spermatophores and in some cases provision the sperm for long-​term storage. Mating and molting are often linked, followed by mate guarding, and often a sperm plug is employed to protect the ejaculate. What is significant about this group is that they have something that none of the other decapods have, namely, trans-​molt sperm retention, which means that sperm can be stored for several years, although the delay between copulation and fertilization is normally a few days to several months (Table 13.2). This high level of



Detecting Cryptic Female Choice in Decapod Crustaceans

sperm protection and conservation might lead us to expect a high level of MP because of possible sperm mixing, but in fact we find the lowest level of MP (mean = 37.1%; range 0%–​60%). In fact, SP is found in Metacarcinus edwardsi and M. pagurus. Mean skewness is the lowest of the three groups at 37.1%. Some caveats are needed because the sample of eight species listed in Table 13.1 does not encompass the whole breadth of variation among crabs; however, they do allow us to compare one species with a DSR with the other seven having a VSR and to contrast two species with a DG with six species with IDG. In Callinectes sapidus, eggs must traverse the entire receptacle, whereas in Chionoecetes opilio (G in Fig. 13.4), the oviduct and vagina are in close proximity, meaning that eggs may only be exposed to sperm from the last male to copulate. MP is lower in Callinectes sapidus (5.3% vs. 12%, respectively) but skewness is much higher (none vs. 79.3%) in Chionoecetes opilio, suggesting that the VSR may facilitate greater paternity bias within a brood. Lack of skewness in Callinectes sapidus could reflect sperm mixing. Comparing growth format, those with DG show an average of 8.7% MP whereas the IDG species have 46.5%, but skewness is similar (79.3% vs. 82.5%). To get a better idea of what is going on in crabs, we need paternity data for females with SR of Types IV, VII, and VIII, which might favor males mating midway rather than first or last. This data might well show higher levels of MP but lower levels of skewness. If it occurs, sperm mixing could be lowest when the male inserts a gel-​layer or sperm plug before/​after the spermatophores and conversely highest when these obstructions are not used, especially if the sperm arrives free of the spermatophore. Given that crustacean sperm is immotile, the only way that it can mix is by disturbance caused by males over-​filling the SR, or alternatively, females could “massage” the SR contents if the wall is sufficiently muscular, although this has never been demonstrated. Sperm displacement by males could be counterproductive if early ejaculates are pushed into a more favorable location ( Jensen and Bentzen 2012).

CRYPTIC FEMALE CHOICE Promiscuity promotes sperm competition and could also facilitate CFC. Once the female has gathered sufficient sperm, how she uses it is largely up to her, because in many cases, the male has long since gone. It is difficult to devise a simple test that could be used to detect CFC, in part, because we do not know which fertilization strategy might be chosen. The choice is between bet-​hedging (MP) versus literally “placing all the eggs in one basket” (SP). MP is certainly evidence that the female has mated with more than one male, from which a choice could be made, but as to whether any female choice occurs is more difficult to ascertain. It is also possible for CFC to result in MP or SP. Single paternity could be the ultimate result for a female because she was somehow able to eliminate all other sperm than the one that sired her entire brood. But without more information, we are left wondering whether SP is the product of shortage of males (only one mate), very efficient mate guarding by the male, or of CFC. Assuming the aim of CFC was to favor one particular male, a possible measure of success is the skewness of the maximum percentage sired by one male: we find that for species with external sperm storage, it is 63.1% (+/​–​8.8 SE), for species with a thelycum or annulus ventralis it is 73.1% (+/​–​2.3 SE), and for species with a seminal receptacle it is 81.7% (+/​–​6.1 SE) (Table 13.2). So one might conclude that greater sperm protection facilitates greater female control of which male is chosen (i.e., higher potential for CFC). However, greater male monopolization of the brood could result from mate guarding. Earlier we noted a marked difference in MP between marine lobsters and freshwater crayfish that we attributed to the absence of mate guarding in crayfish, but this is not reflected in brood skewness. Although those data are very limited, we find that Homarus americanus has skewness of 69.5%, whereas crayfish have 74.2% (+/​–​2.6 SE).

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Reproductive Biology What is a null-​hypothesis that we could test to detect CFC? Eberhard (1996) defined CFC as a female-​controlled mechanism that can bias fertilization success of certain males. Cryptic female choice implies that the distribution of brood paternity does not reflect expectations given the mating history. Mating may be random, but fertilization could be non-​random. If a female mated with n-males, who transferred the same sized ejaculates to an unstructured SR, then if sperm were used indiscriminately, each male should be represented in 1/n of her brood. This is what you would expect from pure sperm competition based on sperm numbers. But if males used behavioral (e.g., guarding) and structural devices (e.g., plugs, gel layers) to interfere with rival sperm, then our expectation would be different, depending on the SR structure. The other component to keep in mind is the nature of the “playing field” provided by the female, namely the structure of the seminal receptacle. We might call this the “static” female component and look at whether there might be any “active” female component as well, such as CFC. When we are testing whether females manipulate paternity outcomes, we need to first see if the paternity distribution matches expectations given what we know about the seminal receptacle. The problem is that given the current techniques, we have to try to detect how much variation cannot be explained by sperm competition in the receptacle and then attribute the remaining variation to CFC. How big a difference between observed and expected paternity does there have to be to conclude that CFC was at work? The best example of female bias is the work on Rhynchocinetes typus (B in Fig. 13.4) (Thiel and Hinojosa 2003). Females prefer to mate with “robustus” males and can use their second pereopods to remove spermatophores, deposited earlier by “typus” males, before mating with the dominant males and then fertilizing their eggs. Multiple paternities have been confirmed by Bailie et  al. (2014), who found that two to four males sired 73.3% of broods (n = 11/​15). Superficially, it would appear that female choice is not very effective in achieving the preferred outcome (SP), but paternity was usually skewed in favor of one male. What we would like to know is whether these favored males were “robustus” or “typus” sires. Experimentally controlled mating is required. We can see that some kind of female manipulation of paternity is going on, but whether it is effective remains to be measured. In contrast to this case of female manipulation of sperm on her own body is the case of Austropotamobius italicus males removing sperm from their female partner before copulating with her. There are no brood paternity data to measure how effective this might be in producing SP for this crayfish. In both these cases, the aim of the behavior of both sexes is to bias paternity to only one male. For decapods with sperm storage, sorting out who the male competitors are and manipulation of their chances of winning are more complicated because neither sex has direct access to the SR. To detect CFC, we need to be able to compare the paternity of the contents of the SR with the paternity of the brood carried by the female. Two studies, in which brood paternity was compared to genotyped ejaculates in the SR, allow us to test whether we can account for brood paternity using SR structure or whether CFC could be involved. Primiparous Chionoecetes opilio (G in Fig. 13.4) females have stratified ejaculates, in a Type V seminal receptacle, each of which is large enough to be genotyped. Urbani et al. (1998) found, in lab-​mated females, that when the delay between copulations was less than four hours and mate guarding was interrupted, the last male fathered all or most of the offspring, but when the delay was greater (8–​20 hours) and accompanied by extended mate guarding, it was the first male that was successful. Sainte-​Marie and Gosselin (2008) outline a range of options females can take, depending upon sperm supply, but none of them points toward CFC. Genotyping stored sperm and brood paternity of Metacarcinus magister, which have Type VI seminal receptacles, also confirms last-​male precedence and that sperm lodged in the bursa, by secondary males, do not fertilize any eggs ( Jensen and Bentzen 2012). Field-​caught ovigerous female M. edwardsii have multiple ejaculates in storage, but broods only have single paternity (Pardo et al. 2013, Pardo et al. 2016). This is believed to be the result of female mate guarding by the male. Thus,



Detecting Cryptic Female Choice in Decapod Crustaceans

the two studies that allow us to see if CFC could be happening do not provide any data that cannot be accounted for by female structure and male mating strategy. Although the seminal receptacle contents were not checked to establish the number of males represented, the case of the fiddler crab Uca mjoebergi might be included here because we know the provider of the last ejaculate, who has to be the guarding male in the sealed burrow, and the paternity of the brood (Reaney et al. 2012). The guarding male fathered around 98% of the brood, so there is little likelihood of CFC. We need to note here that the female may well have “chosen” to enter the burrow of the particular male, so female choice may well be involved, but it was overt rather than covert.

CONCLUSIONS ABOUT CFC AND FUTURE RESEARCH There are no studies that provide conclusive evidence of CFC in decapod crustaceans. The focus has been on detecting multiple paternities in broods, but by itself, such data do not shed much light on the question. Genotyping broods for paternity and being able to characterize all male ejaculates in the SR or wherever they are stored are essential prerequisites when questions of CFC are asked of other species. The characters that we used in our analysis were growth format, mating-​molting link, sperm storage, fertilization delay (latency), mate guarding, and sperm guarding. In some cases, there is overlap between them in that some may share the same evolutionary force, a central one being the mode of sperm storage, which is a female character that improves reproductive security. Decapods with a seminal receptacle (i.e., crabs) have the highest level of single paternity (see Table 13.2). Mate history is what we are trying to interpret, when asking whether females have exercised a choice by screening paternity of “chosen” males. An important part of this work will be to investigate dynamics and spatial structuring of stored sperm. Is it possible that female crabs could use the muscular wall of the seminal receptacle to “massage” the contents, thereby disrupting mate order and defeating the efforts of males to be the last/​first to mate? Besides structural effects, we have highlighted several other factors like mate guarding and fertilization delay which, by themselves, are often able to explain paternity patterns in field data, possibly obviating the need to investigate further. A productive approach would be to experimentally remove these factors from captive crabs. For example, we could compare broods laid by multiply-​ mated females, with and without male mate guarding, to see which sperm were used by the female to fertilize her eggs. Does male mate guarding ensure paternity, or could something else like CFC be at work? Additional paternity data about other decapod species, of which we already have good knowl­ edge concerning their reproduction or morphology, should be collected, in particular crabs that have IDG and mating not linked to molting. Possible examples are Danielethus crenulatus (Platyxanthidae) (Farias et al. 2014, Farias et al. 2017), Hemigrapsus sexdentatus (Brockerhoff and McLay, 2005)  (MEPS), Neohelice granulata (Sal Moyano et  al. 2017)  (Varunidae), Johngarthia lagostoma (Hartnoll et al. 2010), Cardisoma guanhumi (Shinozaki-​Mendes et al 2013) (Gecarcinidae), Calappa pelii (Ewers-​Saucedo et  al. 2015)  (Calappidae), or any other species in these families. Females of these species mate during the intermolt, when hard-​shelled, and so they have a better chance to escape from male guarding and gather sperm from other males. These are the species in which female choice would be maximized. The challenge of detecting CFC could be framed as follows: first, define what might be the best evolutionary strategies for females, and then, use performance data to measure their success. The measures used in our analysis were: (1) level of SP/​MP broods, (2) number of males contributing to each brood, and (3) brood paternity skewness (Table 13.2). Females could exercise CFC by either

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Reproductive Biology achieving monogamy or polygamy. We are using the same performance measures to evaluate both males and females because both can manipulate the outcome. Our challenge is to partition and measure the contributions made by each sex.

ACKNOWLEDGMENTS We would like to acknowledge the helpful and valuable advice provided by Patricio Hernáez Bove, Anson (Tuck) Hines, Pam Jensen, and Bradley G. Stevens.

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14 ENVIRONMENTAL INFLUENCES ON CRUSTACEAN SEX DETERMINATION AND REPRODUCTION: ENVIRONMENTAL SEX DETERMINATION, PARASITISM, AND POLLUTION

Alison M. Dunn, Thierry Rigaud, and Alex T. Ford

Abstract This chapter reviews the influences of environmental factors on sex determination, sex ratios, and reproductive behavior in the Crustacea, focusing in particular on amphipod and isopod examples. A  range of abiotic and biotic environmental factors influence reproduction in Crustacea, including temperature, day length, pollutants, and parasites. Individual crustaceans may benefit from these environmental influences, but in other cases, reproductive biology responses to biotic and abiotic environments may be detrimental to individual fitness. Environmental Sex Determination (ESD) falls into the former category. ESD is an adaptive mechanism of sex determination that is rare, but has evolved in diverse taxa. Evidence from gammarid amphipods is used to explore the evolution of ESD in response to a patchy environment. While ESD is an adaptive mechanism of sex determination, the impact of other environmental factors can be very costly. Parasitic castrators can lead to a reduction or total cessation of reproduction in crustacean hosts, driving population declines. In contrast, parasitic feminizers convert male hosts into females, enhancing maternal parasite transmission but also leading to sex ratio distortion in the host population. The chapter discusses parasite-​host coevolutionary conflict and reviews evidence that selection on the host in response to parasitic sex ratio distortion has led to altered mate choice in amphipods, and to the evolution of a novel system of sex determination in isopods. Human-​ induced environmental influences can also be seen in Crustacea, and the chapter discusses how parasites, ESD, and endocrine-​disrupting chemicals can each affect sex determination and lead to abnormal intersex phenotypes. It ends by highlighting areas for future research on the diverse world of crustacean reproduction.

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Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.



Environmental Influences on Crustacean Sex Determination

INTRODUCTION Reproduction in the Crustacea is under the influence of a range of environmental factors that affect sex determination, sex ratios, and reproductive behavior. In this chapter, we review the impact of environmental factors on Crustacea, focusing in particular on amphipod and isopod examples. The majority of crustaceans, including amphipods and isopods, reproduce sexually and have separate sexes, with the sex of an individual being genetically controlled. However, in some species of gammarid amphipods, sex is not solely genetically determined, but instead is determined by the environmental conditions experienced during development (Environmental Sex Determination, or ESD). In the first section of this chapter, we discuss this unusual method of sex determination, its advantages, and its evolutionary significance. Crustacean reproduction is also influenced by other biotic and abiotic environmental factors, in particular, parasitism and pollution. In contrast with ESD, which is an adaptive mechanism of sex determination, these other environmental influences on reproduction are often costly. Parasitic castration is widespread in crustaceans and is very costly, as it can lead to partial or complete loss of reproduction, and we describe the mechanisms of castration, and the evolutionary significance for the parasite and its crustacean host. Amphipods and isopods are also hosts to parasites that change the sex of their host. These parasitic sex ratio distorters are only transmitted by female hosts and have evolved to feminize their hosts, thereby increasing their own transmission. We compare parasitic sex ratio distortion by bacteria and microsporidian parasites that infect isopod and amphipod hosts, and review the evolutionary conflict between sex ratio distorters and their hosts. Crustaceans are the most successful taxonomic group of aquatic invaders globally (Karatayev et al. 2009), with widespread impacts on biodiversity, and we consider situations where parasite manipulation of host reproduction may influence the success and impact of biological invasions. Intersexuality is the abnormal condition where individuals from gonochoristic species have both male and female characteristics; it is widespread in the Crustacea, and we highlight the different types of intersexuality and the environmental factors that lead to intersex phenotypes. We review evidence for multiple causes of intersexuality including incomplete male development under ESD, partial feminization by parasites, and the effect of endocrine-​disrupting pollutants.

ENVIRONMENTAL SEX DETERMINATION IN THE AMPHIPODA The most common system of sex determination among gonochoristic species is genetic sex determination, exemplified by the XX (female), XY (male) system found in mammals. However, a few species display Environmental Sex Determination (ESD). ESD is a mechanism of sex determination in which sex is determined after conception in response to environmental conditions experienced by the developing offspring. Although it is rare, ESD has evolved in diverse taxa; it has been documented in species from several phyla including chordates (fish and reptiles; Conover 1984, Warner and Shine 2008), nematodes, annelids, and arthropods (crustaceans; Adams et  al. 1987, Korpelainen 1990). It may occur in one species but be absent from closely related taxa (Korpelainen 1990), and populations within a species may differ in the presence or absence and prevalence of ESD (Dunn et al. 2005, Duffy et al. 2015). What factors drive the evolution and maintenance of this unusual mechanism of sex determination? For some species, the selective forces behind ESD remain a matter of debate. Theoretical work by Charnov and Bull (1977) proposed that ESD should be selected over genetic sex determination

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Reproductive Biology in situations where offspring enter a patchy environment, and when patch quality has a differential effect on the fitness of male and female offspring. By using environmental cues for sex determination, offspring are able to develop into the sex that will benefit more from the patch type in which it was born. Empirical evidence for the adaptive significance of this mode of sex determination has been well illustrated for some species of vertebrates. Among the invertebrates, ESD is known in a few species belonging to diverse crustacean groups (Amphipoda, see references in the following; Copepoda, see Becheikh et al. 1998, and Cirripedia, see Hoeg et  al. 2016). The example of the extensively studied amphipod Gammarus duebeni illustrates the adpative significance of ESD (Bulnheim 1978, Naylor et al. 1988, Dunn et al. 2005). In G. duebeni, sex determination is cued by the photoperiod and temperature experienced by the developing young three to four weeks after release from the mother’s brood pouch (Bulnheim 1978, Naylor et al. 1988, Dunn et al. 2005). As a result, most of the young produced early in the breeding season become male, and young produced later in the breeding season become female (Dunn et al. 2005). ESD is adaptive in G. duebeni because the environment is temporally patchy: animals born earlier in the breeding season achieve a larger adult size, and size affects the fitness of both males and females but has a greater effect on males (Adams et al. 1987, McCabe and Dunn 1997). This size advantage is evident during precopulatory mate guarding. A male will guard a female for several days before her molt, using his anterior gnathopods to carry her beneath his ventral surface until she oviposits, which is when copulation takes place. Guarding has evolved in response to a male-​biased operational sex ratio (Grafen and Ridley 1983); males are able to mate at any point (other than when they are molting), but female oogenesis is synchronized with the molt cycle, and oocytes are released into the brood pouch at molt. By guarding a female for the days leading up to her molt, the male ensures that he is able to copulate with her when she molts and lays her eggs into the brood pouch. Males compete for the females they guard in precopula (Naylor and Adams 1987), and larger males can guard larger females (that produce more eggs), while small males may fail to mate (McCabe and Dunn 1997). In contrast, although fecundity is size-​dependent, females suffer less from being of a small size as they are still able to find mates, while very large females may fail to mate if there is only a small pool of males large enough to guard them (Hatcher and Dunn 1997, McCabe and Dunn 1997). Hence, it is more advantageous for offspring released early in the season to become males than females. Under ESD, temperature and day length are used to cue sex determination and hence, to match an individual’s sex to its potential size-​related fitness. ESD in Gammarus duebeni is thus an adaptive response to a temporally patchy environment. In contrast, ESD in the parasitic copepod Pachypygus gibber is an adaptive response to a spatially patchy environment and to sexual selection. This copepod feeds on plankton filtered by its sea squirt (Ciona intestinalis) host and has three sexual morphs: females, typical males, and atypical males, with only atypical males able to swim between hosts. In this species, sex determination is cued by food availability and social cues (mate availability and intrasexual competition). When resources are plentiful, female sex determination is cued, although typical males may develop if a female is already present in the host, thus increasing the likelihood of finding a partner. Under poor resources, males are produced. Furthermore, atypical, swimming males are more likely to occur in the presence of other males, an adaptive response to avoid local mate competition (Becheikh et al. 1998). These parallel examples illustrate the flexibility of ESD as a response to maximize reproductive success in a patchy environment. The mechanism of ESD in crustaceans has not been elucidated. In Crustacea, male sexual differentiation is under the control of the androgenic gland (Charniaux-​Cotton and Payen 1985, Katakura 1989, López Greco 2013). In G. duebeni, the time window of three to four weeks post-​release, during which the young are responsive to environmental cues for sex determination, corresponds to the period of androgenic gland differentiation, suggesting that environmental cues modify androgenic gland differentiation (Naylor et al. 1988).



Environmental Influences on Crustacean Sex Determination

There have been few studies that tested for ESD in other amphipods. ESD cued by photoperiod has been demonstrated for G. zaddachi (Bulnheim 1978) and Echinogammarus marinus (Guler et al. 2012), but Bulnheim (1978) found no evidence for ESD in G. locusta, suggesting that this strategy of sex determination may have evolved multiple times among amphipods. There is also strong evidence for between-​population variation in both the degree of ESD and in the cues used for sex determination in G. duebeni: while sex is cued by photoperiod alone in some populations, animals from more northern populations respond to an interaction between day length and temperature (Dunn et al. 2005). This variation among populations reflects local adaptation to the different environments experienced during the breeding seasons by these populations. In northern populations, where the breeding season is short and there are no overlapping generations, low temperatures and short day length at the start of the breeding season induce male-​biased sex ratios. This is adaptive, because early-​born males will maximize the advantages of long growth. In other populations, with a longer reproductive season, selection for ESD is less strong as females produced early in a given year can reach sexual maturity during the same year and can mate with males born during the previous year (Dunn et al. 2005). A similar pattern is observed in the fish Menidia menidia, in which the level of temperature-​controlled sex determination is also driven by the length of the growing season (Duffy et al. 2015).

PARASITISM, SEX DETERMINATION, AND REPRODUCTIVE BEHAVIOR The environment in which individuals are living is not restricted to abiotic factors such as temperature or photoperiod. A major component of the environment is other species, and, among these interacting species, parasites represent a major selective pressure on the organisms they infect. There is now growing evidence that parasitism may influence sex determination and reproduction, and this has been extensively demonstrated among the Crustacea. In this section, we explore the impact of parasitic castrators and of parasitic sex ratio distorters and the conflict between parasite and crustacean host for sex determination and reproductive behavior. Parasitic Castration in Crustacea Numerous parasites are able to prevent or block the reproduction of their hosts (reviews in Reinhard 1956, Baudoin 1975, Lafferty and Kuris 2009). Since the publication of the seminal papers of Kuris (1974) and Baudoin (1975), castration has been considered an adaptive trophic strategy of the parasite, in which the parasite partially or wholly eliminates host reproduction to acquire energy and nutrients (Lafferty and Kuris 2009). In other words, a parasitic castrator will prevent host reproduction and will hijack the energy normally invested in the host’s reproduction for its own growth and reproduction. However, an alternative hypothesis is that reduced reproduction may be an adaptive host strategy that reallocates the remaining available energy from reproduction to maintenance (limiting the damage from infection) or longevity, increasing the probability for future reproduction following recovery from the infection (Hurd 2001). In this section, we review the mechanisms, evolutionary significance, and ecological impact of parasitic castration. Parasitic castration has been reported in the majority of crustacean taxa, and the parasite taxa causing castration are also very diverse, ranging from bacteria to other crustaceans (Table 14.1). Indeed, the diversity of parasites is probably greater than reported here, since, with a few exceptions, such as the commercial Decapoda or Paguroidea, the species composition of parasites in most crustacean taxa is not well studied. The intensity or nature of castration varies. In most reported cases, total castration is associated with infection (Table 14.1), with parasite growth or multiplication, resulting in gonad degeneration or destruction. In other cases, infected individuals reproduce but their fecundity is lowered (referred to as “reduction in fertility or fecundity” in Table 14.1). Finally,

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Copepoda Oncaea sp. Amphipoda Corophiidea Corophium volutator

TPC

RF

Gynaecotyla adunca

Trematoda

RF

Blastodinium mangini

Halipegus occidualis

Dinoflagellata

Trematoda

Ostracoda Cypridopsis sp.

TPC

TPC TPC?

Fungi, Chytridiomycota Polycaryum leave Microsporidia Flabelliforma magnivora Pasteuria ramosa

TPC RF

Flamingolepis liguloides Flamingolepis flamingo

Cestoda Cestoda

Bacteria

Type of Castration

Parasite Species

Parasite Taxa

Daphnia magna

Hosts Taxa and Species Branchiopoda Anostraca Artemia parthenogenetica Artemia parthenogenetica Cladocera Daphnia pulicaria Daphnia magna

The reduction of host fecundity is intensity dependent.

Reduction of host fecundity is intensity dependent; hosts have an increased longevity.

Infection induces gigantism; impacts population dynamics of the host.

Comments

McCurdy et al. (1999)

Skovgaard (2005)

Zelmer and Esch (1998)

Johnson et al. 2006 Decaestecker et al. (2005) Ebert et al. (2004); Decaestecker et al. (2005)

Sanchez et al. (2012) Sanchez et al. (2012)

References

Table 14.1.  Overview Of Crustacean Host Taxa That Are “Victims” of Castration and Their Castrator Parasite Taxa (Examples of Species Are Given; in Most Taxa, More Species Are Involved).

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Cyathocephalus truncatus RF, BC

Unknown

Cestoda

Trematoda

Acanthocephala

Isopoda, Dajidae

Isopoda, Bopyridae

Isopoda, Bopyridae

Isopoda, Bopyridae

Aselotta Asellus aquaticus

Euphausiacea Stylocheiron afine

Decapoda Thalassinidea Upogebia pugettensis

Dendrobranchiata Parapenaeopsis stylifera

Caridea Lysmata amboinensis Parabopyrella sp.

Epipenaeon ingens

Orthione griffenis

Oculophryxus bicaulis

Acanthocephalus lucii

RF

TPC

TPC

TPC

TPC?

RF, BC?

TPC, BC

Gammarus pulex Isopoda Anthuridea Cyathura carinata

Polymorphus minutus

Acanthocephala

RF, BC

Gammarus pulex

Pomphorhynchus laevis

Acanthocephala

Gammaridea Gammarus pulex

Shields and Gomez-​ Gutierrez (1996)

Brattey (1983)

Ferreira et al. (2005)

Calado et al. (2006)

Gopalakrishnan et al. (2009)

Invasive parasite; may Dumbauld et al. (2011) cause host population collapses.

Fewer ovigerous females are found among infected than uninfected females.

Bollache et al. (2001, 2002) Bollache et al. (2001, 2002) Galipaud et al. (2011)

TPC TPC

Castrated males behave like females (e.g., brooding behavior).

Comments

McDermott et al. (2010) McDermott et al. (2010)

McDermott et al. (2010)

e.g., Rubiliani and Payen (1979); Kristensen et al. (2012)

Van Wyk (1982)

References Calado et al. (2005) Bellon-​Humbert (1983)

TPC: total physiological castration (no clutch, either destruction or disruption of gonad functioning, mostly in females); RF: reduction in fertility or fecundity (partial castration); BC: behavioral castration; ?: the nature of castration is uncertain.

Clistosaccus paguri Nectonema agile

Fecampia erythrocephala

Paguroidea Pagurus bernhardus

Pagurus bernhardus Anapagurus hyndmanni

TPC

Sacculina carcini

TPC?

TPC

Aporobopyrus muguensis

Fecampiida (plathelminthes) Rhizocephala Nematomorpha

Type of Castration TPC TPC?

Parasite Species Eophryxus lysmatae Fecampia erythrocephala

Hosts Taxa and Species Parasite Taxa Lysmata seticaudata Isopoda, Bopyridae Palaemon serratus Fecampiida (Plathelminthes) Anomura Pachycheles rudis Isopoda, Bopyridae Brachyura Carcinus maenas Rhizocephala

40



Environmental Influences on Crustacean Sex Determination

“behavioral” castration has been reported, where infected individuals show a dramatically reduced inclination to pair or mate, although no obvious damage of gonads was observed. The type of castration is often very specific to the host-​parasite association. A single host species may be castrated differently according to the parasite species it harbors, even if these parasites are phylogenetically closely related. For example, the cestodes Flamingolepis flamingo and F. liguloides are both castrators of the intermediate host, the brine shrimp Artemia parthenogenetica; in contrast, F. tadornae does not affect Artemia reproduction (Sanchez et al. 2012). The same kind of specificity in the nature of castration has been observed between two acanthocephalan parasite species infecting the same amphipod host, Gammarus pulex; female hosts infected by Polymorphus minutus suffer total castration, whereas those infected with Pomphorhynchus laevis show only reduced fecundity (Bollache et al. 2002). Mechanisms of Parasitic Castration With a few exceptions, mechanisms of parasitic castration remain poorly understood. The most obvious way for a parasite to castrate a host is to directly destroy or consume the gonads. Such a mechanism is known in anther-​smut fungus infecting plants (where the fungi spores replace host gametes) and in trematodes infecting snails (e.g., Jokela et al. 1993, Sloan et al. 2008), but has not been demonstrated in crustacean hosts. This could be due to the difficulty of discriminating between direct consumption of the gonads by parasites and indirect manipulation that diverts host resources away from the gonads (Lafferty and Kuris 2009). Energy drain by parasites is another possible mechanism of castration. Both hosts and parasites face resource limitation, and, by definition, a parasite diverts energy from the host for its own growth or reproduction. Since reproduction is an energetically demanding process, it may be the first physiological trait of the host affected by the parasite, resulting in castration. Examination of castration in the cladoceran Daphnia magna by its bacterial parasite Pasteuria ramosa (an obligate killer, therefore more a parasitoid than a parasite) revealed a progressive but rapid and irreversible cancellation of reproduction in Daphnia, associated with an increased growth rate (hence inducing gigantism; Ebert et al. 2004). Resource diversion from host to parasite may be general, or may be targeted such that resources are diverted from reproductive organs of the hosts. Lafferty and Kuris (2009) proposed that parasites may specifically disrupt the biochemical mechanisms of vitellogenesis (in female hosts), allowing the redirection of nutritive yolk for their own benefit. Such a mechanism has been proposed for the acanthocephalan parasite Polymorphus minutus in its gammarid host Gammarus pulex (Bollache et  al. 2002). Here, vitellogenesis disorders were observed, as well as abnormal maturation of the few developing oocytes (Fig. 14.1). Since gammarids transfer only astaxanthin to their eggs among all available carotenoids and because the parasite selectively accumulates astaxanthin from the host (Gaillard et al. 2004), redirection by the parasite of a specific host resource used in reproduction is a reasonable hypothesis for explaining castration. Different degrees of castration have been observed among acanthocephalan species that infect the same host species (Bollache et al. 2002), and the various species of acanthocephalans infecting G. pulex differ in their carotenoid contents (Perrot-​Minnot et al. 2011), probably reflecting differences in the carotenoid uptake. Although a link between parasite species differences in the carotenoid uptake and variation in castration has not yet been tested, it is tempting to make a parallel between these two phenomena. Energy draining or energy reallocation, however, does not explain cases of irreversible degeneration of gonads. Such degeneration is better explained by specific humoral manipulation of the host endocrine system by parasites. This has been demonstrated in rhizocephalan parasites infecting various decapods. Crabs (e.g., Carcinus maenas) infected by rhizocephalans (e.g., Sacculina) cease

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Fig. 14.1. Cystacanth stage of the acanthocephalan parasite Polymorphus minutus (left) and of the castrated ovary dissected from the Gammarus pulex female where the parasite was found (right). The white arrow denotes a zone of the ovary where oocytes are welded in a single shapeless mass. The black arrow denotes a zone of the ovary where no developing oocytes can be distinguished. Between these two zones, distinguishable oocytes are of an abnormal blue color, contrasting with the brownish color of developing oocytes in an uninfected female. These oocytes will never be laid. See color version of this figure in the centerfold. Photo courtesy of Yann Bailly and Thierry Rigaud, Laboratory Biogéosciences, Dijon, France.   

reproduction following infection. Parasite organs called “roots” invade the general cavity and most organs of their hosts. In infected male crabs, spermatogenesis stops and the testes degenerate. These castrated males progressively differentiate feminized morphology; they acquire a broader and longer abdomen where the parasite’s externa will develop in place of crab eggs (Kristensen et al. 2012). In parallel, infected males begin to exhibit behaviors of brooding typically exhibited by non-​parasitized females (migrating where brooding females are present, and grooming the externa; Sloan 1984 and references therein). All these changes are due to disruption of the neuroendocrine system by a specific parasite product released by the parasite’s roots (Rubiliani and Godette 1981, Rubiliani 1985). Evolutionary Significance of Parasitic Castration Two contrasting evolutionary strategies have been proposed to explain the reduction or prevention of host reproduction by a parasite infection: a “parasite strategy,” where the energy dedicated to host reproduction is diverted to parasite survival and fecundity (Baudoin 1975), or a “host strategy” of resource reallocation (Hurd 2001). Host strategies could include a reallocation strategy, where, in theory, the energy remaining after parasite demand could be reallocated in the host from reproduction to survival (Hurd 2001) if



Environmental Influences on Crustacean Sex Determination

host defenses involve the redirection of host resources away from reproduction and toward survival (Bonds 2006). Furthermore, when a host is infected by a castrating parasite, selection should favor reallocation of resources to reproduction in the period before parasitic castration takes effect, a strategy termed fecundity compensation. For example, Daphnia magna infected by the microsporidian Glugoides intestinalis produced first broods that were 40% larger than the first broods of uninfected controls. There is also strong empirical evidence for castration as a parasite strategy. Daphnia magna infected by the bacterium Pasteuria ramosa (Ebert et al. 2004, Jensen et al. 2006) show castration associated with host gigantism. These traits benefit the parasite, because host reproductive resources are “converted” into the parasite’s transmission stages. In addition, Duneau et al. (2012) showed that male and female Daphnia represent different environments for the parasite:  host castration led to an increased carrying capacity for parasite proliferation in female but not male hosts. Here, castration evolved as an adaptation to exploit female hosts, the most abundant “resource” available for the parasite (D. magna are mostly parthenogenetic). Observations of behavioral and morphological changes induced by rhizocephalan parasites all suggest advantages for the parasite, but not for the decapod host (Sloan 1984, Kristensen et al. 2012). The development of a broader abdomen allows the parasite’s externa to have more space, and grooming behavior allows the externa to be oxygenated. To our knowledge, however, no firm experimental evidence for this has been provided. The two hypotheses of host or parasite strategies are not mutually exclusive. For example, it appears that both parasite strategy and host compensation strategy occur in a Corophium/​trematode relationship depending on host age (McCurdy et al. 1999). Older (already mated) females newly infected by trematodes often aborted and ate their young. This phenomenon is inconsistent with a host-​compensation strategy because these old, over-​wintering females will die shortly after releasing their offspring, and the phenomenon likely reflects parasite manipulation. In contrast, young, non-​ovigerous females that were newly infected shortened the onset of their reproduction, a response compatible with fecundity compensation by the host to maximize reproduction before the onset of castration (McCurdy et al. 1999). Ecological Consequences of Parasitic Castration Because of their effect on host fecundity or survival, parasites are expected to suppress host population growth, density, or both (Anderson and May 1979, Dobson and Crawley 1994). Owing to their strong effect on host reproduction, this should be true for castrating parasites. An assemblage of eight parasites, all of which reduce the host’s fecundity, decreased population density of their host, Daphnia magna, and the magnitude of this decrease was correlated with overall endoparasite prevalence (Decaestecker et al. 2005). Dumbauld et al. (2011) showed that the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America may be caused by a sudden epidemic of an exotic, castrating bopyrid isopod parasite. The lack of co-​evolutionary history between the host and this newly introduced parasite may explain why host populations suffer to such a great extent through castration by this parasite. The effects on population dynamics of castrated hosts may also have cascading effects on other species in the ecological community, including consequences for competition between host species. The invasive American brine shrimp Artemia franciscana is known to outcompete European species such as A. parthenogenetica. Sanchez et al. (2012) showed that one important factor explaining this competitive advantage is the large impact of cestode parasites on the native, but not the invading species. In particular, the most prevalent parasite species, Flamingolepis liguloides, castrates A. parthenogenetica but not A. franciscana, contributing to the competitive advantage of the invasive A. franciscana. This example of parasite-​driven apparent competition, as well as the previous example of the mud shrimp, illustrates the importance of parasitism on the outcome of biological invasion success (Dunn 2009).

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Reproductive Biology Parasitic Sex Ratio Distortion in Crustacea In addition to castrating their host, parasites may influence host sex determination and differentiation to increase the parasite’s fitness. By doing so, their impact on crustacean reproductive biology is important at both ecological and evolutionary scales. Reproductive parasites are microparasites that manipulate the reproduction of the host (Bandi et al. 2001). Although this group of parasites is taxonomically diverse, they all are vertically transmitted from generation to generation of hosts via the gametes. Hence, in contrast with parasitic castrators, reproductive parasites rely directly on host reproduction for transmission via the oocytes to the next generation of hosts. Due to the difference in the size of male and female gametes, such transmission is mainly or solely maternal. As a result of this maternal transmission, a range of strategies have evolved among reproductive parasites, including cytoplasmic incompatibility and sex ratio distortion (by the means of parthenogenesis induction, male killing, and feminization), all of which benefit the parasite by increasing the relative frequency of female (transmitting) hosts. Among crustacean hosts, parasite-​induced feminization is common and induced by parasitic fungi in the phylum Microsporidia in amphipod hosts and by bacteria of the genus Wolbachia in isopod hosts. Feminizing Microsporidia were first described in the amphipod Gammarus duebeni (Bulnheim and Vavra 1968). Two species of Microsporidia have been well studied and shown to cause feminization in this host: Nosema granulosis (Terry et al. 1999a) and Dictyocoela duebenum (Terry et al. 2004). These parasites are characterized by low virulence, which is adaptive as the parasite depends on successful host reproduction to ensure transmission to the next generation of hosts. However, they cause feminization of the host, converting male offspring into females (Fig. 14.2). Such feminization is adaptive for the parasite as males are a transmission dead end (parasites are not transmitted via sperm). By converting male offspring into females, the parasite enhances its likelihood of transmission (via the oocytes) to the next host generation (Fig. 14.3).

100 90 80 Percentage male offspring

404

70 60 50 40 30 20 10 0

N. granulosis

Dictyocoela duebenum

Uninfected

Fig. 14.2. Mean sex ratios of offspring produced by Gammarus duebeni females infected with Nosema granulosis, females infected with Dictyocoela duebenum, and uninfected females. Survival did not differ between infected and uninfected broods. The heights of the bars indicate the mean percentages of male offspring produced by females in each category. The error bars indicate ±1 SE. Modified from Ironside et al. (2003), with permission from John Wiley and Sons.   



Environmental Influences on Crustacean Sex Determination (A)

(B)

Fig. 14.3. Vertically transmitted parasites are transmitted from parent to offspring via the gamete. Males are gray and females are black. Difference in gamete size between sexes means that vertical transmission is usually only maternal, and that males are a transmission dead-​end for the parasite (A). By converting male offspring to females, feminizing parasites increase the relative frequency of the transmitting (female) sex (B).   

Prevalence of these feminizing parasites varies between populations with N. granulosis prevalence ranging from 0% to 50% and D. duebenum from 7% to 45% in populations surveyed in the United Kingdom and France (Ironside et al. 2003). It also appears that the strategy of feminization is widespread among amphipod/​microsporidian associations. A survey of amphipods from northern Europe detected vertically transmitted Microsporidia across all 16 amphipod species sampled, and sequences from 11 distinct parasite species were found. In five out of eight parasite species tested, infection was more frequent in female than male hosts, suggesting sex ratio distortion (although this has been experimentally tested and confirmed for only two of these five parasite species). Phylogenetic reconstruction revealed that these potential sex ratio distorters occurred in diverse lineages of the Microsporidia, suggesting that sex ratio distortion has independently evolved several times in Microsporidia/​crustacean systems (Terry et al. 2004, see also Haine et al. 2004, Haine et al. 2007). In the terrestrial isopod Armadillidium vulgare (woodlouse), populations exhibit strong female-​ biased sex ratios. In fact, numerous A. vulgare females produce highly female-​biased broods without differential mortality between sexes. The causative agents of this maternally inherited sex-​ratio distortion are Wolbachia endosymbionts (Bouchon et al. 1998). Embryos that inherit Wolbachia develop a female phenotype regardless of their sex chromosome genotype (typically ZZ are males, and ZW are females; Howard 1942, Rigaud 1997). One important outcome of Wolbachia infection is the counter-​selection of the W sex chromosome in populations harboring Wolbachia, because feminized ZZ individuals produce excess females without transmitting a W chromosome (Rigaud 1997, Caubet et al. 2000). In populations where Wolbachia is highly prevalent, this results in the absence of W sex chromosome, and sex determination is under the control of Wolbachia: individuals inheriting Wolbachia develop as females, whereas males are uninfected individuals. Thus, the A. vulgare/​Wolbachia model may be considered as an example of cytoplasmic sex determination (Cordaux et al. 2011). Different A. vulgare populations have been shown to harbor three Wolbachia variants, each exhibiting different transmission and/​or feminization intensities (Cordaux et  al. 2004, Verne et al. 2012). Furthermore, in addition to the Wolbachia, another non-​Mendelian feminizing element (termed “f-​factor”) is present in various A.  vulgare populations, also producing excesses of females, but with a very complex pattern of inheritance and/​or expression ( Juchault et al. 1992, Rigaud et al. 1999a). It has been proposed that the f-​factor could be a fragment of the

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Reproductive Biology Wolbachia chromosome carrying the bacterial feminizing information that has been inserted into the woodlouse genome ( Juchault and Mocquard 1993). Recently, Leclerc et al. (2016) identified a 3-​Mb insert of the feminizing Wolbachia genome transferred into the A. vulgare nuclear genome, confirming this hypothesis. Populations of A. vulgare are not all entirely infected by Wolbachia bacteria, and, when the infection is present, a polymorphism of infection is always observed among females (Rigaud et al. 1999a, Verne et al. 2012). Conflict between parasite and host for control over host sex determination has led to the co-​evolution of host resistance. Autosomal host gene(s) occur in some A. vulgare populations that confer resistance to Wolbachia transmission (Rigaud and Juchault 1992) or reduce the feminization efficiency of both f-​factor and Wolbachia (Rigaud and Juchault 1993). The very complex sex determination in A. vulgare woodlice is thus an example of nucleo-​cytoplasmic sex determination, and ultimately, theoretical models predict that the interplay between feminizers and autosomal resistance genes could lead to the evolution of sex chromosomes, autosomal chromosomes becoming new sex-​determining chromosomes (Caubet et al. 2000). To sum up, the ancient infection by feminizing Wolbachia bacteria in A. vulgare induces nucleo-​cytoplasmic conflicts and also creates evolutionary novelty, thus having a profound impact on the evolution of the isopod genetic sex determination. Broadly, many isopods, as well as other crustaceans, carry Wolbachia symbionts (Bouchon et al. 1998, Cordaux et al. 2001, Cordaux et al. 2012, Zimmermann et al. 2015). Feminization is strongly suspected or demonstrated in some species (e.g., Bouchon et al. 1998, Rigaud et al. 1999b), with some documented cases of strongly female-​biased population sex ratios (e.g., Moreau and Rigaud 2003; Fig. 14.4). However, for many infected species, reproductive modifications leading to sex ratio distortion remain to be investigated (Cordaux et al. 2012, Zimmermann et al. 2015). Parasite Transmission and Feminization Feminizing parasites are under conflicting selective pressures with respect to parasite burden within the host. Selection should favor parasite replication to increase chances of infecting oocytes and subsequent transmission to new hosts, and to induce feminization of the new host (Terry et al. 1997,

60 OSR (% males)

60 Sex Ratio (% males)

406

40

20

0

40

20

0 20

60

% Wolbachia

100

10

30

50

70

90

% Wolbachia

Fig. 14.4. Population sex ratio (left) and operational sex ratio (OSR, i.e., the proportion of males vs. females receptive to mating) (right), as a function of Wolbachia prevalence (proportion of infected females) among populations of the terrestrial isopod Philoscia muscorum. High prevalence of Wolbachia is linked with strong deficits in males, but due to high mating capacity of males, all receptive females were inseminated. Redrawn from Moreau and Rigaud (2003).   



Environmental Influences on Crustacean Sex Determination

Dunn et al. 1998). However, these parasites rely on host reproduction for transmission, and so selection should favor low replication and hence low burden-​associated virulence (Bandi et al. 2001). As a result of these conflicting selective pressures on burden and virulence, feminizing parasites have evolved elegant strategies to target host tissues, yet cause low virulence. Studies of two species of microsporidian feminizers, N. granulosis and D. duebenum, infecting their amphipod host, G. duebeni, revealed that these parasites are localized in the gonadal tissue of the adult host (Dubuffet et al. 2013). Proliferation of the parasites and development of the infective spore occurs in the follicle cells (Fig. 14.5) that transfer components to the developing oocyte (López Greco 2013); spores then invade secondary oocytes during their maturation (Dubuffet et al. 2013). These feminizing parasites also target specific cell lineages during embryogenesis (Dunn et al. 1998, Weedall et al. 2006). Only merogonic (vegetative) stages of the parasite have been observed in embryos (Terry et al. 1997), and so the targeting of host tissues is not a result of parasite spore germination. However, the localization of parasites within the perinuclear zone and their close association of parasite meronts with host microtubules suggest that they segregate with the spindle microtubules at host cell mitosis (Terry et  al. 1999b). This is likely to benefit both parasite and host, as the exclusion of the parasite from the spindle zone will ensure that nuclear division is not disrupted. In contrast with feminizing Microsporidia in amphipods, Wolbachia bacteria do not target reproductive tissues of woodlice during embryogenesis (Sicard et al. 2014). Although bacteria show the highest multiplication rate in ovarian tissue (Fast et al. 2011), they also colonize tissues as diverse as fat bodies, gut epithelium, nerve cord, brain, and haemocytes (Dittmer et al. 2014). It is possible that bacterial colonization of somatic tissues contributes to some potential for horizontal transmission (Sicard et al. 2014). Furthermore, in the isopod A. vulgare, the higher multiplication rate of Wolbachia in the germ line is not anarchic and massive. It is also fine-​tuned, as observed for Microsporidia in gammarid amphipods. A progressive enrichment of Wolbachia-​infected oocytes in the course of ovary maturation is observed (Fig. 14.6), suggesting either a secondary colonization of previously uninfected oocytes or the preferential development of infected ones (Genty et al. 2014). The precise molecular mechanism(s) of parasite-​induced feminization are not known, but it appears that parallel mechanisms of feminization may be employed by the phylogentically distinct feminizers that infect the amphipod G. duebeni (parasitic fungi of the phylum Microsporidia) and

Fig. 14.5. A Gammarus duebeni follicle cell containing Dicytocoelum duebenum spores (arrow) is visible in the vicinity of a maturing oocyte (bracket). Oocyte yolk (bracket) is lightly autofluorescent. See color version of this figure in the centerfold. From Dubuffet et al. (2013), with permission from the American Society for Microbiology.   

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Reproductive Biology the terrestrial isopod A. vulgare (bacteria of the genus Wolbachia). It appears that these parasites act by manipulating the hormonal control of sex differentiation of the host. In crustaceans, male sexual differentiation is controlled by the extragonadal hormone androgenic gland hormone (AGH) that is secreted by the androgenic gland located at the distal end of the vas deferens (Charniaux-​Cotton and Payen 1985, Cerveau et al. 2014). In the absence of androgenic gland differentiation, female development occurs (Katakura 1989). Rodgers-​Gray et al. (2004) found that N. granulosis-​infected (feminized) G. duebeni had fully developed ovaries and an undifferentiated androgenic gland, identical to that found in true (uninfected) females. Furthermore, while AGH was produced by males, it was absent from uninfected females and infected feminized individuals, suggesting that N. granulosis manipulates host sex by preventing androgenic gland differentiation and AGH production and, consequently, male differentiation. Similarly, Wolbachia appears to prevent androgenic gland differentiation during sexual differentiation of A. vulgare (reviewed in Rigaud et al. 1997). The cue for sex determination and differentiation in A. vulgare appears to be the “male” gene(s), which controls the development of the androgenic gland. Wolbachia could therefore target these “male” gene(s), resulting in an absence of the development of the androgenic gland and leading to female sex differentiation. It is interesting to note that such diverse parasite taxa (Microsporidia and Wolbachia) show convergent evolution, each leading to sex ratio distortion by manipulation sex differentiation in their crustacean hosts.

Fig. 14.6. Wolbachia distribution in an infected ovary of an Armadillidium vulgare female, illustrating the apparent progressive colonization of oocytes during their maturation. Wolbachia (in red) appear are mostly distributed around the oocyte nuclei. The germarium, where oocytes are differentiating, is on the left side. Most of the young, recently differentiated, oocytes are uninfected (*), medium-​sized oocytes are weakly infected (**) and mature oocytes are highly infected (***).See color version of this figure in the centerfold. Figure from Genty et al. (2014), Creative Commons license.   



Environmental Influences on Crustacean Sex Determination

Ecological Impacts: Sex Ratio Distorters and Biological Invasions Invasive species are a major driver of biodiversity loss globally, and understanding what makes a successful invader is key to predicting and managing invasions. Successful invaders tend to be larger, more fecund, and more abundant in invaded areas compared to their original ranges (Parker et al. 2013). One hypothesis to explain the success of these invasive species is that they benefit from escaping their natural enemies:  for example, analysis of data from 26 invasive species including mammals, reptiles, amphibians, birds, fish, mollusks, and crustaceans revealed lower parasite diversity in the invasive than in the native range for the majority of species (Torchin et al. 2003). Loss of parasites may be driven by sampling effects (infected individuals may be absent in introduced propagules) and by selective effects (infected individuals may be less fit, and initial host density during the colonization phase may be insufficient to sustain a parasite population; Torchin et al. 2003, Colautti et al. 2004). However, vertically transmitted parasites do not experience the same selective pressures, as their transmission is not dependent on parasite burden, and they typically cause little virulence (Bandi et al. 2001, Dunn and Smith 2001). Hence, they are less likely to be lost during the invasion process (Mitchell and Power 2003, Galbreath et al. 2004). Evidence from plant pathogens supports this prediction; invasive plants were more likely to show release from fungi than from viruses that are often seed-​transmitted (Mitchell and Power 2003), although evidence from animal pathogens is more equivocal (reviewed in Hatcher and Dunn 2011). Vertically transmitted sex ratio distorters have in fact been predicted to enhance invasion success as they may increase population growth through over-​production of females (Slothouber Galbreath et al. 2010). For example, although invasive populations of the amphipod Crangonyx pseudogracilis have undergone a genetic bottleneck, Slothouber Galbreath et al. (2010) found no evidence for enemy release, but found that two vertically transmitted parasites had been co-​introduced. One of these, the microsporidian feminizer Fibrillanosema crangonycis, was prevalent in all populations, suggesting that the production of excess females facilitated amphipod population growth (Slothouber Galbreath et al. 2010). Similarly, a study of the invasive amphipod Dikerogammarus villosus in Europe found no evidence of either a genetic bottleneck or of enemy release. However, this invader had acquired two microsporidian parasites within its invasive range that are related to the feminizer N.  granulosis and which may therefore facilitate the ongoing D. villosus invasion (Wattier et al. 2007). Parasitism and Crustacean Reproductive Behavior In addition to directly disrupting sex determination and differentiation, parasitism can affect behavioral traits with diverse consequences, including determining mating success, affecting patterns of assortative pairing, altering mate choice, and changing investment of resources to sperm. Parasites with an indirect life cycle can induce dramatic changes in the anti-​predator behavior of their hosts, thereby increasing trophic transmission to the parasite’s final hosts (Hughes et al. 2012). These behavioral changes may also disrupt patterns of assortative pairing. For example, the trematode Microphallus papillorobustus causes its amphipod host, Gammarus insensibilis, to move to the surface of the water column, thereby increasing the likelihood of predation by the definitive bird host. This change in micro-​habitat selection also increases the encounter rate with other infected individuals, thus generating assortative pairing by parasite prevalence (Thomas et al. 1996). In contrast, Gammarus pulex infected by the acanthocephalans Pomphorhynchus laevis and Polymorphus minutus show a decreased probability of pairing (Bollache et al. 2001, Bollache et al. 2002). This is unlikely to benefit the parasite, as predation by fish (the definitive hosts for these parasites) may be higher on paired than single amphipods (Cothran 2004). However, it may reflect parasite

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Reproductive Biology manipulation of the host, diverting energy allocation from mating behaviors to traits that increase transmission (i.e., behavioral manipulation). This hypothesis has not yet been tested. Fecundity compensation is an adaptive host response that reduces the lifetime fitness cost of parasitic infection by increasing reproductive effort in the initial stages of infection (see earlier section “Evolutionary Significance of Parasitic Castration”). For example, the trematode Gynaecotyla adunca manipulates the anti-​predator behavior of its amphipod host Corophium volutator. Once the trematode develops to the infective stage, it makes the host crawl on the surface of a mudflat, where it is vulnerable to predation by the final host (sandpipers, Calidris pusilla). Interestingly, male Corophium compensate for future parasite-​induced predation by showing increased mating and ejaculate size in the period post-​infection but before parasite manipulation occurs (McCurdy et al. 2001). Parasitic Sex Ratio Distortion and Crustacean Reproductive Behavior Owing to the transmission route of sex ratio distorters, selection on the parasite could favor reduced virulence, but also manipulation to increase its own reproductive success, whatever the impact on the host fitness (Bandi et al. 2001). For example, infection by the microsporidian feminizing parasites N. granulosis and D. duebenum is associated with slightly reduced survival and fecundity in the amphipod host, G. duebeni, but feminization compensates this fitness cost and parasite transmission remains high (Terry et al. 1998, Ironside et al. 2003). In contrast, selection on the host should favor any behavior that reduces the potential cost of sex ratio distortion. Mating with infected feminized hosts is likely to be disadvantageous, as in some systems, these hosts suffer reduced fecundity. Furthermore, under female-​biased sex ratios (as a result of infection), individuals that invest in male offspring will have higher fitness (Fisher 1930). In the isopod Armadillidium vulgare, males prefer to mate with “real” females relative to Wolbachia-​ reversed females (Moreau et al. 2001). In the amphipod G. duebeni, males invest less time guarding infected than uninfected females (Kelly et al. 2001). In addition, both amphipod and isopod males allocate more sperm to uninfected females (Rigaud and Moreau 2004, Dunn et al. 2006). This could result from strategic sperm allocation (in G. duebeni, uninfected females produce more eggs than infected ones), or could be a consequence of a lower attractiveness of infected females in A. vulgare (Moreau et al. 2001). This reduction in sperm allocation has negative consequences for female fertility (Rigaud and Moreau 2004, Dunn et al. 2006), which may, in turn, limit the spread of parasitic feminizers in host populations. Parasite-​induced sex ratio biases may also underpin between-​ species differences in mating capacity: in isopod species infected by feminizing bacteria, males have evolved an increased ability to inseminate more females (in response to strong female-​biased population sex ratios), relative to species infected by closely related non-​feminizing Wolbachia (Moreau and Rigaud 2003).

INTERSEXUALITY IN CRUSTACEA Intersexuality is the abnormal condition whereby gonochoristic individuals display both male and female characteristics. In contrast with hermaphrodite species, intersexuality in gonochoristic species results from abnormal development, and intersex individuals suffer a fitness cost in comparison with males or females. Intersexes are widely reported in gonochoristic crustaceans, and several mechanisms have been proposed for its occurrence (Ford 2008), including incomplete environmental sex determination (Dunn et al. 1996), incomplete parasite-​induced feminization (Kelly et  al. 2004), and the impact of environmental pollutants (Ford 2008, deFur and Williams 2015).



Environmental Influences on Crustacean Sex Determination

In some instances, intersex characteristics can be observed externally in the form of both male and female appendages (external genitalia and gnathopods), while in others it is only revealed by careful examination of gonadal structures or histology of the testicular or ovarian tissues. Within the literature, some authors have classified intersex specimens into intersex male or intersex female when characteristics of one sex are more predominant. With so many examples of sequential and simultaneous hermaphrodites in crustaceans (Yaldwyn 1966, Baeza et al. 2009; see also Chapter 8 in this volume), there has been confusion as to whether accounts of intersexuality in the literature are correct, or whether these specimens simply had a poorly understood life history (Ford 2012). The first known published accounts of “intersex” in a crustacean was a specimen of “a hermaphrodite lobster” presented in a report to the Royal Society in 1729 (Nicholls 1729) that described a specimen which was male on one side and female on the other. Ford (2012) highlighted that this was more likely an example of bilateral gynandromorphism and not hermaphroditism, which has since been reported in many crustaceans. Subsequently, many cases of gynandromorphy have been reported in lobsters (Chase and Moore 1959) and other crustaceans across many classes (Bowen and Hanson 1962, Farmer 1972, Johnson and Otto 1981, Taylor 1986, Micheli 1991, Olmstead and Leblanc 2007). Bilateral gynandromorphism is a condition that is thought to arise when genes (e.g., governing sex determination) are altered during the bilateral developmental of an embryo, resulting in one side appearing male and the other female (Levin and Palmer 2007). Mosaic gynandromorphism can also occur whereby individuals demonstrate a more patterned (mosaic) formation of phenotypic characters (e.g., coloration) and is best understood in the insects (Michez et al. 2009). In most cases, such gynandromorphs are thought to arise early in embryonic development during midplane formation (Wolff and Scholtz 2002, Levin and Palmer 2007). Under the current definitions, gynandromorphs might be considered a form of intersexuality in that they are abnormal and occur in gonochoristic species. As opposed to sexual gynandromorphs, which might be considered to have more of a developmental underpinning, the causes of intersexuality are multifaceted and may occur due to disturbances in sex determination or sexual differentiation. Intersexuality is certainly not a new phenomenon. An intersex fossil crab has been reported from the upper Cretaceous dating back to about 70 million years ago (Bishop 1973). Despite the outlined confusion, intersexuality (including gynandromorphs) has been reported within the literature among a wide variety of taxa, including Anostraca (Bowen and Hanson 1962, Decapoda (Yaldwyn 1966), Copepoda (Moore and Stevenson 1991, Gusmão and McKinnon 2009), Mysidacea (Mees et  al. 1995), Isopoda (Rigaud and Juchault 1998), Cladocera (Mitchell 2001), Anomura (Turra 2004), and Amphipoda (Ford and Fernandes 2005a). A  considerable body of literature now exists for the incidences and phenotypes of intersexuality in the Amphipoda and Isopoda (Table 14.2). Within both these groups, reports exist for both intersex males and intersex females. While at this stage the causal factors are unclear, Ford and Fernandes (2005a) speculated that separate sexual phenotypes may be due to environmental and/​or parasite-​induced disruption around critical periods in sex determination. Environmental Sex Determination and Intersexuality Environmental sex determination (ESD) is an adaptive strategy found in diverse taxa including some amphipod species, which allows individuals to match their sex to their future size-​related fitness (see previous section “Environmental Sex Determination in the Amphipoda”). Crustacea develop as male when the androgenic gland differentiates and produces androgenic gland hormone, or become female in the absence of androgenic gland differentiation, and it has been proposed that, in amphipods with ESD, the environmental cues stimulate androgen gland differentiation. There is evidence that intersexes can result from incomplete sexual differentiation under ESD. Higher

411

Order Amphipoda

Prevalence 5%–​20%

~1% 60%–​100%

0.5%–​10%

0.8%–​8%

-​

-​

Species Echinogammarus marinus

Gammarus chevreuxi Gammarus minus

Gammarus duebeni

Gammarus fossarum

Gammarus tigrinus

Gammarus pulex

Table 14.2.  Intersexuality in Amphipod and Isopod Crustacea.

-​

-​

Hynes (1955)

Sexton (1939)

Ladewig et al. (2002)

Intersex ♀

Intersex ♂ and intersex ♀

Sexton (1924) Miller and Buikema (1976); Buikema et al. (1980) Bulnheim (1965); Dunn et al. (1990)

Intersex ♂ and intersex ♀ Intersex ♀

Sexual Phenotype Reference Intersex ♂ and intersex ♀; Ford et al. (2003); Yang et al. (2008) internal intersex ♂ also reported

Attributed to infection with vertically transmitted microsporidian parasites Unknown; “component of water” reported in causality although parasite infection was not recorded ( Jungmann et al. 2004) Intersex male recorded by Ford and Fernandes (2005); unknown cause Intersex females reported by Ford and Fernandes (2005); unknown cause

Notes Causes considered multiple although evidence points to infection with microsporidian and/​or paramyxean infections in some populations along with speculation on pollution (Short et al. 2015) Unknown cause Unknown cause

412

Intersex ♂ and intersex ♀ -​

-​ -​ -​ 1%–​15% -​ -​ -​ 0%–​8.5%

-​ -​

Ampelisca sp. Jassa sp. Jassa falcata Orchestia gammarellus

Orchestia mediterranea

Orchestia aestuarensis

Tmetonyx similis Corophium volutator

Eulimnogammarus obtusatus Gammarus oceanicus

-​ Intersex ♂ (type i & ii) and intersex ♀

Intersex ♂ and intersex ♀

Intersex ♂ and intersex ♀

Intersex ♂ Intersex ♂ Intersex ♂ Intersex ♂ and intersex ♀

Intersex ♂

-​

-​

-​

-​

-​

-​

-​

-​

-​

Gammarus pungens padanus Ampelisca brevicornis

Gammarus pulex subterraneus Gammarus pseudolimnaeus Gammarus lacustris

Sanderson (1973) Sanderson (1973) Sanderson (1973) Ginsburger-​Vogel (1975) Ginsburger-​Vogel (1991) Ginsburger-​Vogel (1991) Sexton (1911) Barbeau and Grecian (2003); McCurdy et al. (2004) Ford and Fernandes (2005) Ford and Fernandes (2005a)

Maccagno and Cuniberti (1956) Hastings (1981)

Hynes and Harper (1972) Ökland (1969)

Anders (1957)

Large sexually undifferentiated specimens

Unknown cause

Unknown cause Unknown cause

Unknown cause

Unknown cause

Speculated that metacercaria from digenean parasites may have caused castration but unlikely given current knowledge Unknown cause Unknown cause Unknown cause Unknown cause

Intersex ♂ and intersex ♀ reported by Ford and Fernandes (2005); unknown cause Unknown cause

Unknown cause

Unknown cause

Isopoda

Order

Prevalence -​ 26%

-​ -​

-​ -​ 2%

-​

-​

Species Echinogammarus pirloti

Dikerogammarus haemobaphes

Asellus communis Asellus aquaticus

Asellus aquaticus Asellus aquaticus

Mesidotea sibirica

Porcellio dilatatus and P. laevis

Armadillidium vulgare

Intersex ♀

Intersex ♀

Intersex ♀

Intersex ♀ Intersex ♀

Intersex ♀ Intersex ♀

Intersex ♂ and Intersex ♀

Sexual Phenotype -​

Notes Large sexually undifferentiated specimens High infection with microsporidian parasites in females and intersexes indicates probably cause Smith (1977) 1 from 253 specimens Munro (1953) Drew attention to acanthocephalan parasites among intersexes but refrained from suggesting causal factor Unwin (1920) Unknown cause Needham (1942 Suggested though hybridization with A. meridianus Korcynski (1985, 1988) 1 from 50. Parasitism considered plausible explanation as extracellular protozoan found within population Juchault et al. (1991) Intersexuality inducible through infection by a virus (injection of cytoplasm from infected specimens) Juchault et al. (1991) Intersexuality inducible through infection by a virus (injection of cytoplasm from infected specimens)

Reference Ford and Fernandes (2005a) Green Etxabe et al. (2015)

41

-​

Sphaeroma rugicauda

Chaetophiloscia elongata

Ligia oceanica

Idotea balthica

15%

Armadillidium vulgare

Intersex ♂

Intersex ♀

Intersex ♀ Intersexuality is inducible through bacteria (Wolbachia) and its conflict with masculinizing host genes, and their interaction with the environment Martin et al. (1994) Intersexuality is linked with intracytoplasmic bacterial infection (Wolbachia) Mocquard et al. (1978) Intersexuality is inducible by variation in the environment Martin et al. (1974) Intersexuality is linked with intracytoplasmic bacterial infection Dalens (1968) Unknown cause

Rigaud and Juchault (1993, 1998)

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Reproductive Biology intersex frequency has been reported in G. duebeni populations where the level of ESD is high, and intersexes were found to be more common in months when environmental cues lead to male-​biased sex ratios. Similarly, amphipods reared in the lab under conditions that cue males were more likely to show intersex characteristics than those raised under female-​determining conditions, suggesting that one cause of intersexuality was incomplete androgenic gland differentiation and hence male sexual differentiation under ESD (Dunn et al. 1993, Dunn et al. 1996). Thus, the risk of intersexuality may be due to the cost of the delayed and flexible sexual differentiation that is a hallmark of ESD. Parasite-​Induced Intersexuality Intersexuality can also result from incomplete feminization by sex ratio–​distorting parasites (Kelly et al. 2004). Rodgers-​Gray et al. (2004) found that 97% of intersex G. duebeni amphipods from a population in Northumberland, United Kingdom, were infected by the microsporidian feminizer N. granulosis (prevalence in females was only 38%). These intersexes showed both male and female external sexual characteristics. Their gonads included an ovary and oviduct and a vestigial androgenic gland, identical to the morphology of females, but a vestigial vas deferens was also present (Fig. 14.7). Males have also been shown to prefer mating with females than with intersex females, and intersex females also had reduced fecundity (Kelly et  al. 2004). Therefore, intersexuality is likely to be disadvantageous to both the host and the parasite, which relies on host reproduction for transmission to future host generations. Intersexes are also found, sometimes at high numbers, in populations of the terrestrial isopod Armadillidium vulgare ( Juchault et al. 1992). Two kinds of intersexes are found, with contrasting functional phenotypes. First, some individuals show functional male gonads (and mating behavior), but non-​functional, tiny vas deferens that open on the female genital apertures. These intersexes function as males and result from the conflict between the feminizing “f ” sex factor (probably from bacterial origin) and an autosomal gene restoring the male sex. Here, the intersex phenotype (with female gonopores) is a trace of an incomplete restoration of the male sex (Rigaud

oviduct ovary

vestigial vas deferens

Fig. 14.7. Line drawing of the gonad of a N. granulosis-​infected intersex Gammarus duebeni. Structures shown are ovary, oviduct, and vestigial vas deferens. Redrawn from Rodgers-​Gray et al. (2004), with permission from Elsevier.   



Environmental Influences on Crustacean Sex Determination

and Juchault 1993). Other intersex phenotypes in this species are variable, with all intermediate stages between fertile females with gonads showing non-​functional vas deferens and male genital papillae (intersex females, iF) to sterile individuals with gonads showing characteristics of non-​ functional testes with hypertrophied androgenic glands (intersex males, iM). These phenotypes are the expression of delayed feminization induced by Wolbachia (Rigaud and Juchault 1993). Longer delays increase the probability of a sterile iM phenotype. Delayed feminization can be induced by an autosomal repressor of feminization or by the detrimental effect of high temperature on the multiplication of Wolbachia bacteria (Rigaud and Juchault 1993, 1998). Such dysfunction of parasite-​ induced feminization therefore leads to high proportions of sterile intersexes, which are disadvantageous for the population growth of both the woodlouse host and bacteria. Pollution and Sex Determination Since the early 1990s, there have been concerns that pollutants termed endocrine-​disrupting chemicals (EDCs) have the capacity to cause reproductive abnormalities in wildlife (Colborn et al. 1996, Norris and Carr 2005, deFur and Williams 2015). Many of these reproductive abnormalities were reported in vertebrates, including fish ( Jobling et al. 1998), reptiles (Crain and Guillette 1998), and amphibians (Hayes et al. 2002). Several of these reproductive aberrations manifest themselves as an intersex condition in which organisms “abnormally” display characteristics of both males and females (as opposed to sequential hermaphrodites in transition between sexes or simultaneous hermaphrodites). The chemicals involved vary from natural and synthetically produced estrogens to industrial contaminants such as pesticides, hydrocarbons, and polychlorinated biphenyls (PCBs). Toward the very end of the twentieth century, there was more emphasis on the potential impacts of EDCs on invertebrates (Oetken et al. 2004). Until this time, the only well-​documented case of endocrine disruption was “imposex” in gastropod molluscs caused by tributyltin (TBT)-​ based paints (Bryan et al. 1986). Imposex referred to the imposition of one sex genitalia on another. In this instance, the female gastropods developed a penis and vas deferens, blocking the oviducts and causing sterility. Sometimes the term “imposex” has been wrongly used in crustaceans and might have been more appropriately called intersexuality (e.g., Takahashi et al. 2000). As a result of the focus on pollution potentially impacting sex determination and differentiation, the number of published incidences of intersexuality in invertebrates, including crustaceans, began to rise (Ford 2012). A number of studies have highlighted correlations between pollution and intersexuality in Crustacea (Moore and Stevenson 1991, 1994, Takahashi et al. 2000, Barbeau and Grecian 2003, Vandenbergh et  al. 2003, Jungmann et  al. 2004, Ford et  al. 2004, Ayaki et  al. 2005). While there has been speculation that individual cases of bilateral gynandromorphs might have been caused by pollutants disrupting sexual development, this has not been substantiated by thorough field and laboratory studies. Research from the field has mainly focused on intersex individuals that display an array of external or internal male and female characteristics as a result of feminization/​defeminization or masculization/​demasculinization. For example, Moore and Stevenson (1991, 1994) reported an elevated number of intersex copepods around sewage effluent discharge, although a follow-​up study found no correlation between intersexuality and distance from the pollution discharge (Moore and Stevenson 1994). Takahashi et al. (2000) found high prevalence (34%–​63% males with gonopores, and 12%–​28% females with penis-​like appendages) of intersex freshwater crabs in contaminate compared to none in “clean” Japanese rivers. However, although a large number of possible pollutants were measured, none was correlated with the observed intersexuality, nor were parasites implicated as a causal factor. Ayaki et al. (2005) similarly found high numbers of intersexuality (8%–​32%) in male crabs from Japanese freshwater streams, but could not identify a causal factor, speculating that chemicals from agricultural runoff were the cause. Jungmann et al. (2004) found that when amphipods (Gammarus fossarum) collected from streams

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Reproductive Biology with a low prevalence of intersexuality were caged in streams with high levels of intersex, or were kept under laboratory conditions in water from high-​intersex streams, a greater proportion became intersexed than if kept in “low-​intersex” stream water. However, the role of parasites could not be ruled out, nor was any specific chemical contaminant identified. The only laboratory-​confirmed cases of intersexuality caused by chemical contamination are studies conducted on Daphnia following exposure to a pesticide. Olmstead and LeBlanc (2002) found that the terpenoid hormone methyl farnesoate (MF) is a sex-​determining factor in Daphnia and that elevated concentrations of MF or MF synthetic analogues resulted in all-​male broods. The same authors also demonstrated that exposing Daphnia to MF in the laboratory can induce sexual gynandromorphism (Olmstead and LeBlanc 2007). Methyl farnesoate is structurally similar to juvenile hormones (III) in insects, and these researchers also found that increased temperature, synergized with pesticides based on juvenile hormone analogues, caused elevated numbers of intersex progeny. Therefore, it is conceivable, based on laboratory studies, that man-​made pesticides could disrupt sexual development in crustaceans. In a study exposing amphipods to 17α-​ethinylestradiol, Vandenbergh et  al. (2003) found that first-​generation males had smaller gnathopods, intersex testes, and disrupted spermatogenesis, although the potential role of parasites in the observed results was unclear (Ford and Fernandes 2005b). Pollution might increase the prevalence of feminizing parasites in crustaceans, thus causing a form of “indirect” endocrine disruption (Ford et al. 2006). High numbers of intersex amphipods (Echinogammarus marinus:  ~30%) were recorded around industrially polluted bays in Scotland, while relatively low numbers (~3%–​5%) were recorded at reference locations (Ford et al. 2004). The intersexuality correlated strongly with microsporidian infections that were identified using histological methods (Ford et al. 2006) and later confirmed to be the feminizing microsporidium Dictyocoela duebenum. Yang et al. (2008, 2011) highlighted another phenotype of intersexuality in the amphipod E.  marinus in which ovotestes were observed internally in males but no external feminized features were observed. These internally intersexed specimens were not associated with any known feminizing parasites (Short et al. 2012), thus opening the possibility of pollution and parasite-​induced intersexuality. Using high throughput sequencing technologies to compare the transcriptomes, the parasite-​infected external intersex and the uninfected internal intersex specimens had broadly similar gene expression (Short et al. 2012, Short et al. 2014). Interestingly, Short et al. (2014) reported that despite a substantial up-​regulation of female-​related genes in intersex male amphipods, there was no concomitant decrease in male-​related genes as demonstrated in vertebrate species. Conversely, Li (2002) found that intersexuality in Taiwanese crabs (Grapsus albolineatus) decreased with contamination, with 80% intersexuality observed at reference sites and only 30% intersexuality close to a municipal landfill. In this instance, the intersexuality referred to was the feminization of appendages (claws and abdomens) caused by rhizocephalan parasites, and it was speculated that the parasite larvae might be susceptible to poor water quality. Therefore, to date, despite a large number of studies highlighting intersexuality within the Crustacea, few have demonstrated that intersexuality can be induced experimentally through exposure to pollutants, or have linked intersex phenotypes to pollution in the field. With the relative plasticity of sex determination found throughout crustaceans, it seems possible that some compounds could interfere with the process of sex determination or differentiation. With the advent of affordable genomic and transcriptomic sequencing, the ability to search for sex-​determining genes and those involved in downstream sexual differentiation is now possible in non-​model organisms. This is rapidly expanding our knowledge of crustacean developmental biology and should enable us to gain a better understanding of the impacts of pollution on sex-​determining mechanisms.



Environmental Influences on Crustacean Sex Determination

CONCLUSIONS Crustacea show a wide range of environmental effects on their reproduction. These range from the evolutionary adaptive environmental sex determination, through manipulation of individual sex determination and population sex ratio by parasites and pollutants, to catastrophic parasite-​ induced castration. The examples reviewed here reveal a high degree of plasticity in sex determination, reproduction, and behavior. It appears that the neuroendocrine control of sex determination in Crustacea is key to this plasticity. On the one hand, this sex determination system underlies the evolution of adaptive sex determination in response to environmental factors such as sex-​specific fitness (ESD) or sex ratio biases. However, it may also explain the vulnerability of these organisms to manipulation by parasites and altered development due to pollutants. The conflict between crustacean hosts and their reproductive parasites provides some elegant examples of co-​evolution in action, and studies to date suggest that such phenomena may be widespread among crustaceans. Future studies of these fascinating interactions should explore the mechanism of action. Parasites infecting crustaceans come from divergent taxa, prokaryotes (Bacteria) feminize isopods, and eukaryotes (Microsporidia) feminize amphipods; are the mechanisms responsible for feminization the same, reflecting the vulnerability of crustacean sex determination to manipulation, or are there contrasting mechanisms leading to evolutionary convergence? Another interesting question to explore would be the evolution of sex ratio manipulation. Are the dynamics of sex ratio evolution the same among crustacean/​parasite pairs? For a given host species, what is the diversity of feminizing parasites, and, more broadly, are there different degrees of specificity among host/​parasite species? Data exist for some models (Wolbachia/​Armadillidium vulgare and microsporidia/​Gammarus duebeni), but other parasite/​host couples remained too overlooked to build a general picture. Anthropogenic factors including pollution are also likely to impose increasing pressures on Crustacea. Crustacea play key roles in aquatic communities, hence the impact of pollutants on reproductive development and thus crustacean population dynamics could have profound ramifications to energy flow and the structure of aquatic communities. Laboratory evidence suggests that it is conceivable that pollutants can impact sexual differentiation/​development in crustaceans, with field-​based studies highlighting correlations between contamination and intersexuality. Future studies need to address the interaction between ESD and environmental contamination on crustacean reproduction and development. This will require a better fundamental knowledge of the mechanisms of sex determination and differentiation. The advent of affordable sequencing technologies now makes these fundamental research questions achievable, which will ultimately benefit by giving adequate responses to the applied questions related to environmental quality, fisheries, and climate change.

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15 ALTERNATIVE REPRODUCTIVE TACTICS

Shawn Garner and Bryan Neff

Abstract Alternative reproductive tactics (ARTs) describe variation among individuals of a single sex in the tactics used to obtain mating opportunities. In crustaceans, ARTs have been observed in multiple taxa and take a variety of forms. ARTs are most commonly observed in males and are generally associated with intense competition among males to monopolize access to breeding females. ARTs frequently involve a guard tactic that competes with other males to monopolize access to females, while a second usurper tactic foregos competition with other males and instead obtains mating opportunities through sneaking behavior. Guard and usurper tactics may be expressed conditionally based on a male’s ability to guard a female (e.g. his body size, the abundance of competitors), or may be expressed as discrete phenotypes that can also include morphological differentiation. For example, in Jassa amphipods the guard tactic is associated with large body size and an enlarged “thumb” on the claw that is used in aggressive interactions with other males, while the usurper tactic is associated with small body size and a reduced thumb. The usurper tactic can take two forms in a marine isopod: small males (gamma) use sneaking behavior to avoid competition with large males (alpha), whereas intermediate-​sized males (beta) use female mimicry to avoid competition. Overall, ARTs are well-​represented in crustaceans, with many opportunities for continued study to better characterize these unique adaptations.

INTRODUCTION Sexual selection, which acts on variation in breeding success among individuals, is a key process that contributes to phenotypic diversity both between and within sexes (Andersson 1994). Females typically have higher parental investment than males due to the high energetic cost of producing and incubating eggs, which leads to longer latency between reproductive bouts and more males Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology than females being reproductively active at a given time (i.e., the operational sex ratio is male-​biased; Trivers 1972, Emlen and Oring 1977). Consequently, females are not typically limited by their ability to secure mates, whereas for males, reproductive success and number of mates are tightly linked (Bateman 1948). Male fitness thus tends to be more dependent on mating success than female fitness, which means that males face more intense sexual selection than females and competition for mates occurs primarily among males (Clutton-​Brock and Parker 1992, Kvarnemo and Ahnesjo 1996). Intense sexual selection that acts predominantly on a single sex has long been recognized as a cause of sexual dimorphism in which that sex develops armaments or ornaments that are absent in the other sex (Darwin 1859). For example, sexually dimorphic armaments are common in fiddler crabs (genus Uca), in which males have a large claw used in competitions with other males and a small claw used for feeding, whereas females have two small claws (Swanson et  al. 2013). A second outcome of intense sexual selection, and the focus of this chapter, is alternative reproductive tactics (ARTs), in which intense sexual selection acting on a sex instead contributes to phenotypic diversity within that sex. ARTs occur when individuals of one sex use discrete tactics to obtain reproductive success (Gross 1996, Oliveira et al. 2008). This definition has two key elements. First, ARTs must occur within a single sex, and thus exclude the many differences in reproductive tactics between males and females. A special case whose inclusion is less clear under this definition occurs when a species is hermaphroditic, but some individuals specialize on the reproductive functions of a single sex. For completeness, we have included these cases here in our discussion of ARTs. Second, ARTs must be discrete (i.e., discontinuous in expression), such that continuous variation in reproductive tactics is not included within the framework of ARTs. Under this definition, at one extreme ARTs can occur as little more than behavioral variants, which differ in the tactics that they use to obtain mates. At the other extreme, ARTs can occur as complex phenotypic variants, which involve not only behavior, but also differences in morphology, physiology, development, and life history. ARTs have been observed across a wide range of animal taxa, and can take many forms even within a single taxon, such as the crustaceans (reviewed in the following and summarized in Table 15.1; for additional examples, see Shuster 2008). It should also be noted that the diversity of ARTs is perhaps matched only by the number of unique terms used to describe those tactics. Where possible we have endeavored to include species-​specific terminology while also classifying tactics within more general classes of ARTs.

SURVEY OF ALTERNATIVE REPRODUCTIVE TACTICS IN CRUSTACEANS Guard and Usurper Tactics Female reproduction is linked to molting in most crustaceans (Thiel and Duffy 2007). Females typically become receptive to mating for only a brief window following molting, which can lead to intense competition among males to mate with the small proportion of females that are sexually receptive at any given time. Male crustaceans have evolved a number of adaptations in response to this competition, which largely focus on monopolizing access to receptive females to avoid sperm competition (here termed guard tactics). One of the most common ARTs in crustaceans occurs when some males forego intrasexual competition to monopolize access to females and instead use some other tactic to obtain mating opportunities (here termed usurper tactics because they typically involve avoiding confrontations with guarding males). In the following we describe several examples that fall within the general class of guard and usurper tactics.

Table  15.1. Summary of  the Crustacean Alternative Reproductive Tactics Discussed in This Chapter. Taxon Malacostraca Amphipoda

Decapoda

Species

Alternative tactics

References

Jassa falcata, Jassa marmorata, likely in most Jassa spp. Neohelice granulata

• Major (thumbed) male: guards females • Minor (thumbless) male: mates by sneaking • Guard male: constructs a burrow for mating, guards female • Usurper male: mates outside of burrow, does not guard • Underground-​mating male: captures a female then mates in his burrow, guards female • Surface-​mating male: mates outside his burrow, does not guard • Underground-​mating female: captured by male, mates and releases eggs in his burrow • Surface-​mating female: mates on surface, releases eggs in her burrow • Blue-​claw male: large claws and body size, courts and guards female • Orange-​claw male: intermediate claws and body size, intermediary stage with low mating success • Small male: small claws and body size, mates by sneaking • Guard male: engage in dominance contests with other males, courts then guards a female • Usurper male: mates by sneaking when guard males are distracted

Borowsky (1985); Clark (1997); Conlan (1989, 1990); Kurdziel and Knowles (2002) Sal Moyano et al. (2012); Sal Moyano et al. (2016)

Scopimera globosa

Scopimera globosa

Macrobrachium rosenbergii

Rhynchocinetes typus, likely in Rhynchocinetes brucei, Rhynchocinetes durbanensis

Henmi et al. (1993); Koga and Murai (1997)

Henmi et al. (1993); Koga and Murai (1997)

Kuris et al. (1987); Ra’Anan and Sagi (1985)

Bailie et al. (2014); Correa et al. (2000); Correa et al. (2003); Thiel et al. (2010)

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Taxon Isopoda

Branchiopoda Spinicaudata

Species Paracerceis sculpta

Alternative tactics References • Alpha male: large size, Shuster (1987, 1989) defends a sponge cavity where females breed • Beta male: intermediate size and resembles a female, can enter a sponge cavity without provoking alpha male • Gamma male: small size, avoids alpha male in sponge cavity by hiding or rapid movement

Eulimnadia texana • Hermaphrodite: male Sassaman and Weeks sexual function through (1993) self-​fertilization • Male: specializes on male sexual function, uses claw-​like appendage to facilitate spermatophore transfer to hermaphrodites

In the amphipod genus Jassa, males can adopt one of two morphotypes upon reaching their final instar (Conlan 1990). Major males have large body size and an enlarged “thumb” on the claws of their second pereon, whereas minor males have small body size and a reduced thumb (see Fig. 1 in Kurdziel and Knowles 2002). In multiple species these morphotypes have been shown to be associated with guard and usurper tactics (Borowsky 1985, Conlan 1989, Clark 1997, Kurdziel and Knowles 2002). Major males use a guard tactic in which they defend reproductively active females to exclude male competitors. The strongly developed thumb of major males appears to function both as an armament in aggressive interactions with other males, and as an ornament that is displayed to other males as a signal of dominance (Kurdziel and Knowles 2002). In contrast, minor males use a usurper tactic to mate with spawning females, in which they use sneaking behavior to avoid detection by the major males. The burrowing crab Neohelice granulata has guard and usurper tactics that are associated with male size (Sal Moyano et al. 2012). Large males use a guard tactic in which they construct complex burrows that include a chamber for copulation. Large males mate with females in the copulation chamber, and then guard the female to prevent her from mating with another male. In contrast, small males construct simple burrows that are used only as shelters. Small males gain mating opportunities by using a usurper tactic in which they mate with females they encounter outside of burrows, after which they do not guard the female to prevent her from mating with other males.



Alternative Reproductive Tactics

Small males will claim unoccupied burrows that contain copulation chambers, but do not use guard tactics when occupying these burrows (Sal Moyano et al. 2016). Guard and usurper tactics associated with burrow usage are also seen in the sand-​bubbler crab Scopimera globosa. In the underground mating tactic, a male captures a female on the surface, carries her to his burrow, then plugs the entrance to the burrow until the female releases her eggs (Henmi et al. 1993, Koga and Murai 1997). This guard tactic allows the male to be the last to copulate with a female before her eggs are released, and thus to achieve high paternity through last-​male sperm precedence (Koga et al. 1993). The female then incubates her eggs in the male’s burrow. In the surface mating tactic, a male copulates with a female on the surface and does not guard her to ensure paternity. Usurper males may fertilize eggs either through sperm competition with a guard male, or by the female releasing and incubating eggs in her own burrow in the absence of a guard male (Koga and Murai 1997). Males using the guard tactic tend to be larger than males using the usurper tactic, with individual males switching between tactics as they grow (Koga and Murai 1997). The giant freshwater prawn Macrobrachium rosenbergii provides another example of guard and usurper tactics (Ra’Anan and Sagi 1985, Kuris et  al. 1987). Mature male prawns belong to three morphotypes that are distinguished by body size and the color and relative length of their claws. Blue-​claw males have dark blue claws, the largest body size, and the longest claws. Orange-​claw males have orange claws, intermediate body size, and intermediate claw length. Small males have translucent claws, the smallest body size, and the shortest claws. The blue-​claw morphotype uses a guard tactic, in which the male uses courtship behaviors to attract females (providing grooming and protection during the vulnerable molting period) and responds aggressively to other males to defend his territory. For mating to occur, the blue-​claw male inverts the female to place her abdomen in an upright position and then attaches his spermatophore to her abdomen. In contrast, the small morphotype uses a usurper strategy in which the small male gains mating opportunities using sneaking behavior to avoid aggressive interactions with blue-​claw males. Small males actively search for females, and upon finding a female, will attempt to evade larger males and attach a spermatophore to the female’s abdomen. Unlike the larger blue-​claw males, small males can invert themselves, rather than the female, to attach a spermatophore, facilitating a sneaking tactic. The orange-​claw morphotype appears to be largely a transitionary life stage characterized by rapid growth and low reproductive success. Orange-​claw males are generally smaller than blue-​claw males, and even when their body size is similar to a blue-​claw male, their claws are smaller and they are subordinate (Barki et al. 1992). Orange-​claw males are thus unable to effectively employ the guard tactic, although these males will compete with each other for access to females in the absence of a blue-​claw male (Ra’Anan and Sagi 1985). Orange-​claw males are also too large to effectively employ a usurper tactic. Similar to blue-​claw males, they must invert the female to attach a spermatophore, rather than inverting themselves as small males do. All individuals have the ability to irreversibly progress from small to orange-​claw to blue-​claw morphotypes, with the transitions apparently governed by both age and the abundance of the alternative morphotypes in a population (Cohen et al. 1981). In rock shrimp Rhynchocinetes typus, male guard and usurper tactics are associated with social cues (Correa et  al. 2000, Correa et  al. 2003). Male rock shrimp ontogenetically progress through three morphotypes. Initially, small males are morphologically similar to females (typus morphotype). Males then progress through a number of molts associated with increasing body size (intermedius morphotype) before reaching a final stage that has powerful claws and an elongated pair of third maxillipeds (robustus morphotype). In the absence of other males, all three morphotypes use a guard tactic that is associated with a typical breeding sequence (Correa et al. 2000). The male first captures a female and holds her beneath his body, then engages in courtship behavior, followed by spermatophore transfer, and finally guards the female through the end of her period of sexual receptivity. When two males encounter a sexually receptive female, the males will

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Reproductive Biology first aggressively compete for dominance, with the subordinate male fleeing and the dominant male then proceeding to use a guard tactic and the typical breeding sequence (Correa et al. 2003). Large body size and the associated weaponry confer greater success and quicker resolution to dominance contests (Correa et al. 2003). When an extended dominance contest occurs, the usurper tactic may be expressed by a third male who is not engaged in the contest. These usurper males take advantage of the brief lapse in the dominant male’s defense of the female to quickly transfer spermatophores to the female without courtship or subsequent guarding (Correa et al. 2003, Dennenmoser and Thiel 2008). The three morphotypes documented in rock shrimp have also been found in the closely related dancing shrimp Rhynchocinetes brucei and R. durbanensis, although the use of a usurper tactic has not been formally described in these species (Thiel et al. 2010, Prakash et al. 2015). Multiple species of freshwater crayfish from the family Cambaridae show discrete male morphotypes at maturity that in many ways resemble the morphological variants associated with guard and usurper tactics (Guiasu and Dunham 1997, Gherardi and Daniels 2003, Laufer et  al. 2005, Tierney et al. 2008, Stewart et al. 2010). Males of the form I morphotype have enlarged claws and prominent ischial hooks on the walking legs that facilitate sperm transfer. In contrast, males of the form II morphotype have smaller claws and reduced or absent ischial hooks. Consistent with guard and usurper tactics, in Orconectes rusticus form I males are more aggressive than form II males (Tierney et al. 2008); however, differences in aggressive behavior between form I and form II males are not seen in either Cambarus robustus or Procambarus suttkusi (Guiasu and Dunham 1997, Stewart et al. 2010). Rather than ARTs, male forms in the Cambaridae appear to represent reproductive (form I) and non-​reproductive (form II) morphotypes, with males able to transition between morphotypes during their lifetime (Laufer et al. 2005). Males typically alternate between morphotypes during successive molts (Laufer et  al. 2005), with the timing of these transitions leading to high frequencies of the form I morph when breeding females are abundant (Scudamore 1948). Females may also experience a similar alternation between morphotypes in successive molts, which appear to again represent reproductive (form I) and non-​reproductive (form II) morphotypes, with higher growth rate during the form II phase (Buřič et al. 2010). It is possible that male morphotypes are associated with as yet undocumented ARTs in cambarid crayfish, as the reproductive behavior of form II males is poorly characterized, and form II males have been observed attempting to copulate with females in at least one study (Tierney et al. 2008), but there is currently little data that would indicate the presence of ARTs in this family. Guard, Usurper, and Female Mimic Tactics A notable extension to systems with guard and usurper tactics occurs when there is also a third tactic that avoids confrontation with guard males not by sneaking, but by mimicking a female phenotype. Female mimics are then able to enter the territory of a guarding male and gain access to females without prompting the aggressive response typically directed toward male competitors. Across the animal kingdom, guard, usurper, and female mimic tactics have been prominently described in only a few species. In crustaceans, the isopod Paracerceis sculpta provides a well-​known example of a species that uses guard, usurper, and female mimic tactics (Shuster 1987, 1989). Paracerceis sculpta breeds in the large central cavities of marine sponges. Males belong to three unique morphotypes, each of which uses a different tactic (Fig. 15.1). Alpha males are the oldest and largest individuals, and possess a pair of elongated horn-​like appendages (uropods) that are used in aggressive interactions with other males. Alpha males use a guard tactic, in which they defend a sponge cavity from other males while allowing females to enter the cavity. Once inside the cavity, females molt, become sexually receptive for a single day, and then begin an extended pregnancy that eventually leads to the female’s death. Alpha males can differ substantially in reproductive success, and will defend harems whose sizes have been observed to range from zero to 11 females



Alternative Reproductive Tactics

Fig. 15.1. Three male alternative reproductive tactics in the marine isopod, Paracerceis sculpta. Shown are alpha males, which compete with other males to defend breeding territories in sponge cavities; beta males, which mimic females to gain access to cavities without provoking an aggressive response from the alpha male; and gamma males, which gain access to cavities by evading detection by alpha males. See color version of this figure in the centerfold. Photo courtesy of Stephen Shuster.   

(Shuster 1987). Beta males are of intermediate age and size and do not possess elaborate uropods. Instead, beta males phenotypically resemble females and use a mimic tactic. Beta males fool the alpha male into thinking that another female has entered his sponge cavity, and thereby avoid provoking the typical aggressive response toward other males. Gamma males are the smallest in size and use a usurper tactic. These males enter nest cavities and attempt to avoid aggressive interactions with alpha males by hiding and moving rapidly. In the laboratory, none of the three morphotypes has been found to grow or molt, so within its lifetime, a male isopod appears to adopt a single reproductive tactic. Female Alternative Reproductive Tactics In crustaceans, ARTs have been best described in males. This finding is in many ways unsurprising, as the greater sexual selection typically experienced by males is thought to be key to generating conditions that favor the evolution of ARTs (Shuster and Wade 2003). Nevertheless, although they are rare, there are examples of female ARTs, particularly in insects where female tactics appear to function largely to reduce costs associated with male mating attempts (Cordero 1990, Svensson et al. 2005, Hardling and Bergsten 2006). In crustaceans, precopulatory mate guarding by males is known to incur costs to females, which leads to sexual conflict over optimal guarding duration that is frequently associated with female resistance to male mate-​guarding attempts ( Jormalainen 1998). Female reproductive tactics in crustaceans might thus take the form of variation in acceptance of mate guarding. One example that appears to meet the criteria for discrete female reproductive tactics occurs in the sand-​bubbler crab. These crabs are characterized by two male ARTs: an underground-​mating male captures a female on the surface and guards her in his burrow until she breeds, whereas a

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Reproductive Biology surface-​mating male copulates with females on the surface without mate guarding (Henmi et al. 1993, Koga and Murai 1997). Females that mate on the surface may subsequently pair with an underground-​mating male and release eggs in his burrow, but may also release eggs in her own burrow, thereby avoiding mate guarding by a male (Koga and Murai 1997). Females that accept underground mating receive a resource (burrow) but may have limited opportunity for mate choice, whereas females that resist underground mating receive no resources but may have greater opportunity for mate choice. The expression of these female mating tactics appears to be related largely to body size, with females that breed in a male’s burrow being smaller on average than females that breed in their own burrow (Henmi et al. 1993). This size difference may reflect both the greater ability of large females to resist capture by underground mating males, as well as the greater success of large females in defending a burrow against takeover by another individual (Henmi et al. 1993, Koga and Murai 1997). Hermaphrodite and Single-​Sex Tactics One of the more unique examples of ARTs in crustaceans occurs when some individuals reproduce as hermaphrodites, while others specialize on the sexual function of a single sex. For example, in the conchostracan shrimp Eulimnadia texana, some individuals are self-​compatible hermaphrodites and others specialize on male sexual function (Sassaman and Weeks 1993). These specialist males develop a claw-​like appendage that allows them to grasp hermaphrodites and transfer a spermatophore, whereas hermaphrodites are able to engage in male sexual function only through self-​ fertilization. Hermaphrodites and specialized males thus represent ARTs within males, although if self-​fertilization is rare, these tactics may in many ways be more similar to two sexes. The caridean shrimps (genus Lysmata) represent another interesting sexual system that has been described as protandrous simultaneous hermaphroditism: individuals first mature as a male, then become hermaphroditic, and finally become female (Bauer 2000). However, because hermaphrodites lack the ability to self-​fertilize in these shrimps, they do not represent a true ART. Instead, hermaphrodites gain female reproductive function using the same tactic as single-​sex females, and gain male function using the same tactic as single-​sex males.

EVOLUTION OF ALTERNATIVE REPRODUCTIVE TACTICS Game theory and the concept of evolutionarily stable states provide a useful framework for understanding the evolutionary dynamics of ARTs (Dawkins 1976, Maynard Smith 1982). Within this framework, strategies represent the rules that determine which reproductive tactic (phenotype) is expressed by an individual (Gross 1996). A pure strategy is associated with a single reproductive tactic. For example, one pure strategy may lead an individual to adopt a guard tactic, whereas a second pure strategy leads an individual to adopt a usurper tactic. A mixed strategy leads to multiple tactics with fixed probabilities (e.g., adopt a guard tactic with probability 0.6 and a sneak tactic with probability 0.4). Individuals using a mixed strategy select a tactic by essentially flipping a weighted coin, with that selection possibly occurring once before the onset of reproduction or at random for each reproductive opportunity. A conditional strategy leads individuals to express the tactic that has the greatest fitness given their relative condition (e.g., large males use a guard tactic, and small males use a usurper tactic). Both pure and conditional strategies have received theoretical and empirical support, whereas support for mixed strategies has been largely limited to theoretical models (e.g., Flaxman 2000). In particular, empirical support for mixed strategies is limited by the need to definitely exclude conditional strategies as an explanation (i.e., by demonstrating that individuals that use different tactics do not differ in any aspect of condition). Under specific conditions, both



Alternative Reproductive Tactics

pure and conditional strategies may be evolutionarily stable. Following Maynard Smith (1982), an evolutionarily stable state occurs when the genetic composition of a population will be restored by selection following moderate disturbance, and an evolutionarily stable strategy exists when a single strategy is adopted by all members of a population and is resistant to invasion by any alternative strategy. When ARTs are determined by pure strategies, two conditions are required for the tactics to be evolutionarily stable. First, at least one of the tactics must be subject to negative frequency-​ dependent selection; that is, at least one tactic must enjoy increased fitness when it is rare. Second, the tactics must have equal fitness when the strategies are at their equilibrium frequencies. Given these conditions, the frequency-​dependent fitness functions for the alternative tactics will intersect and the strategies will move toward an equilibrium that is an evolutionarily stable state (A in Fig. 15.2; Gross 1996). If the tactics have equal fitness but are not subject to negative frequency-​ dependent selection, populations will be prone to lose strategies through random drift as neither offers a fitness advantage (B in Fig. 15.2). If the tactics experience negative frequency-​dependent selection but there is no frequency at which the fitness of the tactics are equal, then one tactic will have higher fitness at all frequencies and will eventually reach fixation, whereas the alternative tactic will be lost from the population (C in Fig. 15.2). Although a population composed of a mixture of individuals expressing different pure strategies may achieve an evolutionarily stable state, the presence of multiple strategies at equilibrium means that there is not an evolutionarily stable strategy for that population. When ARTs are instead determined by a conditional strategy, the fitness of the tactics need not be equal at equilibrium for an evolutionarily stable state to be reached. Instead, in the simplest case there must be a relationship between condition and fitness for at least one tactic, and the fitness functions for different tactics must intersect at some level of condition (Fig. 15.3; Gross 1996). This level of condition then represents the switch point at which individuals should shift between tactics, as an individual maximizes its fitness by using one tactic below this point and the other tactic above it. The tactics need not have equal fitness for a conditional strategy to reach an evolutionarily stable state because all individuals use a similar decision rule (i.e., there is an evolutionarily stable strategy). Even though the fitness of individuals using the inferior tactic may be lower than individuals using the superior tactic, individuals using the inferior tactic are maximizing their fitness given their low condition (i.e., making the best of a bad job; Gross 1996). As a result, condition itself is likely to be under strong directional selection, but because condition is a complex trait that can be influenced by many factors (e.g., age, environment, genetic variation), variation in condition, and thus reproductive tactics, is likely to persist. The condition at which individuals switch between tactics may itself be subject to heritable variation that enables populations to evolve toward the evolutionarily stable state, and subsequent extensions to the theory of conditional strategies have explicitly incorporated polygenic effects, liability models for threshold traits (in which multiple factors contribute to liability, with the transition between alternative tactics determined by a liability threshold), and the reliability of cues that individuals use to assess their condition (Hazel et al. 1990, Tomkins and Hazel 2007, Roff 2011). Given the differing predictions about the fitness of alternative tactics governed by pure and conditional strategies, a common experimental approach to distinguish between these hypotheses has been to first quantify the fitness of different tactics, and if the fitness of different tactics is equal, to conclude that a pure strategy is likely (or at least possible), whereas if the fitness of different tactics is unequal, to conclude that a conditional strategy is likely. For example, this approach was applied in digger wasps (Sphex ichneumoneus), where the approximately equal fitness of the two tactics led to the conclusion that the tactics were governed by pure strategies (Brockmann et al. 1979). In side-​ blotched lizards (Uta stansburiana), two guard tactics and a usurper tactic all have approximately equal fitness over time, and were further shown to be subject to negative frequency-​dependent

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Fig. 15.2. Evolutionary stability of pure strategies governing alternative reproductive tactics. Plots show the relative fitness of two reproductive tactics as a function of the frequency of the first tactic. In panel (A), tactic 1 is subject to negative-​frequency dependent selection and the fitness of the tactics are equal when the proportion of tactic 1 is 0.4, which represents an evolutionarily stable state (ESS). In panel (B), neither tactic is subject to frequency-​ dependent selection, and one tactic will eventually be lost via drift. In panel (C), there is no frequency at which the fitness of the tactics is equal, and tactic 1 will eventually be lost via selection. Modified from Gross (1996).   



Alternative Reproductive Tactics

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Fig. 15.3. Evolutionary stability of a conditional strategy governing alternative reproductive tactics. Plotted is the relative fitness of the two reproductive tactics as a function of male condition. An individual’s optimal tactic is determined by its condition, and the intersection of the two fitness functions marks the condition at which individuals would be expected to switch between tactics. Modified from Gross (1996).   

selection with a rock-​paper-​scissors dynamic among the three tactics (Sinervo and Lively 1996). In crustaceans, this approach has been most notably applied to the alternative tactics in the marine isopod Paracerceis sculpta, which as previously described consists of alpha, beta, and gamma males. Over the course of two years, sponge cavities were sampled to determine the abundance of the different male tactics and the frequency with which different numbers of females were present in spawning aggregations (Shuster and Wade 1991). Shuster and Wade (1991) then applied paternity allocation rules based on separate parentage analyses to assign reproductive success to each male in a spawning aggregation. For example, a male of any tactic would be assigned 100% paternity if he was the only male present with a female, whereas if one alpha and one beta male were present, the alpha would be assigned 40% paternity and the beta 60% paternity. Using these rules and their field data on spawning aggregation composition, Shuster and Wade (1991) showed that reproductive success was equal for the three tactics and was consistent with pure strategies controlling the development of the different tactics. Studies of tactic frequencies within families represent another approach for distinguishing between pure and conditional strategies. This approach was applied to the marine isopod Paracerceis sculpta, and revealed that males of all three tactics overproduced male offspring that shared their tactic (Shuster and Sassaman 1997). The ratios of tactics within families were consistent with autosomal Mendelian inheritance in which tactics were determined by a single gene with three alleles and strict dominance relationships: the allele associated with the beta tactic was dominant to the alpha and gamma tactic alleles, and the gamma tactic allele was dominant to the alpha tactic allele (Shuster and Wade 1991, Shuster and Sassaman 1997). Further genetic analyses in this species showed that the tactic-​determining gene and the gene for the enzyme phosphoglucomutase are in linkage disequilibrium (i.e., located on the same chromosome), as within families different phosphoglucomutase alleles are associated with different male tactics (Shuster and Sassaman 1997). The phosphoglucomutase gene itself is unlikely to be the tactic-​determining gene because different alleles at this gene were not associated with male tactics at the population level, meaning that the tactic-​determining gene itself has not yet been characterized in this species. In contrast, family analyses in the amphipod Jassa marmorata identified no relationship between the tactic used by a male and the tactic used by

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Reproductive Biology his male offspring, suggesting that in this species tactics are controlled by neither simple Mendelian inheritance nor another heritable genetic mechanism (Kurdziel and Knowles 2002). Demonstration of genetic control of ARTs has in general been rare, although additional examples can be found outside the crustaceans. For example, the ruff (Philomachus pugnax) is characterized by two male tactics, and these tactics appear to be controlled by a single gene with two alleles: a dominant allele associated with the usurper tactic and a recessive allele associated with the guard tactic (see also Lank et al. 1995, Lank et al. 2013). In a cichlid (Lamprologus callipterus) with guard and usurper tactics, pedigree analysis showed that sons always shared the reproductive tactic of their father, consistent with genetic determination of reproductive tactic by a gene with two alleles located on the Y-​chromosome (Ocana et al. 2014). Despite the low frequency in which such family analyses have identified clear inheritance patterns associated with ARTs, studies of tactic frequencies within families represent a powerful experimental approach and can provide some of the strongest evidence in support of pure strategies. Conditional strategies, in contrast, have been frequently supported, including in multiple crustaceans (Roff 2011, Shuster 2008, Neff and Svensson 2013). Conditional strategies can be most easily demonstrated when individuals are able to use multiple tactics within their lifetime. If an individual can use either a guard or usurper tactic depending on context, then those tactics must not be genetically determined by discrete pure strategies. Given the relative ease of demonstrating conditional strategies, studies of conditional strategies often focus on identifying the aspect of an individual’s condition that determines its reproductive tactic. Body size and ontogenetic stage frequently affect conditional strategies, with individuals typically using a usurper tactic at a small body size, then switching to a guard tactic at larger body size. Such is the case in the giant freshwater prawn, in which individuals initially have a small body size and reduced claws that are associated with a usurper tactic. As the prawns progress through several molts, they develop a larger body size and elongated claws that are associated with a guard tactic (Cohen et al. 1981, Ra’Anan and Sagi 1985, Kuris et al. 1987). Conditional strategies may also be determined by the quality of the environment experienced by an individual. In the amphipod Jassa marmorata, whether a male adopts a guard or usurper tactic is determined by the quality of his diet (Kurdziel and Knowles 2002). Males fed a high-​ quality diet that is rich in protein and fatty acids predominantly developed into the morphotype associated with the guard tactic, whereas males fed a low-​quality diet deficient in these nutrients predominantly developed into the morphotype associated with the usurper tactic. This conditional strategy presumably maximizes the fitness of each male given his diet. This assumption was explicitly tested in male dung beetles (Onthophagus taurus), which have been shown to develop horns and use a guard tactic when food is abundant at the larval stage, and to not develop horns and use an usurper tactic when food is limited at the larval stage (Hunt and Simmons 1997, Moczek and Emlen 2000). Quantifying the fitness function for each tactic revealed that individual males were maximizing their fitness by adopting the appropriate morphotype and tactic given their size (Hunt and Simmons 2001).

DISTRIBUTION OF ALTERNATIVE REPRODUCTIVE TACTICS AMONG CRUSTACEAN TAXA The distribution of ARTs is non-​random with respect to phylogeny in crustaceans. Specifically, guard and usurper tactics have been described most frequently in the class Malacostraca, and in several cases similar ARTs have been described in multiple species within a family or genus (see Table 15.1). These phylogenetic patterns may represent either common evolutionary origins of ARTs in shared ancestors, or convergent evolution in response to similar selection pressures. Understanding



Alternative Reproductive Tactics

the relative contribution of these two processes to phylogenetic patterns can help to illuminate the factors that favor or constrain the evolution of ARTs. The frequent occurrence of guard and usurper tactics in Malacostraca almost certainly has resulted from multiple independent evolutionary origins. These tactics are seen in at least three orders, which are separated by considerable phylogenetic distance and many intermediate taxa that do not share these tactics. Guard and usurper tactics also take a variety of forms in Malacostraca that include distinct morphological and behavioral specializations, making it unlikely that these tactics share a single origin. Instead, properties of the Malacostraca that have favored the evolution of mate guarding (e.g., brief periods of female reproductive activity, male-​biased operational sex ratios) have likely enabled the repeated emergence of usurper tactics in response to intense sexual selection. Similar guard and usurper male ARTs have been described in multiple species in the amphipod genus Jassa (Table 15.1). These ARTs are associated with distinct morphotypes, with major males (guard tactic) having large body size and enlarged thumbs, and minor males (usurper tactic) having small body size and reduced thumbs. Despite some variation in thumb morphology among species, thumbs (and the associated guard tactic) are ubiquitous in Jassa and likely share a common evolutionary origin (Conlan 1990). In contrast, data on the presence of minor males within Jassa are incomplete, with many species described based on a single major male (Conlan 1990). It is thus difficult at this time to infer if the minor morphotype is the result of multiple evolutionary transitions, or if it has a single origin. Regardless, intense sexual selection associated with male mate guarding (including morphological specializations in major males) likely provided the conditions that favored the evolution and maintenance of a usurper tactic in multiple species of Jassa. In crustaceans, perhaps the best data concerning evolutionary transitions associated with ARTs come from Rhynchocinetes and Cinetorhynchus shrimps. In Rhynchocinetes typus, males engage in intense competitions to monopolize access to females, and the robustus morphotype, with powerful claws and an elongated pair of third maxillipeds, has emerged as an adaptation that increases success in these competitions (Correa et al. 2000, Correa et al. 2003). In response to this intense competition, some males use a usurper tactic to sneak copulations (Correa et al. 2000, Correa et al. 2003). Although the presence of this behavioral tactic has not been assessed in closely related species, data on the presence or absence of the robustus morphotype is available. Baeza et al. (2014) plotted these data on a phylogeny, showing that there have been multiple evolutionary transitions

Rhynchocinetes uritai Rhynchocinetes brucei Rhynchocinetes durbanensis Rhynchocinetes typus Cinetorhynchus cf. rigens Cinetorhynchus hendersoni ‘slender’ Cinetorhynchus hendersoni ‘bulky’

Fig. 15.4. Phylogenetic tree showing the presence (filled circles) or absence (open circles) of the robustus morphotype in Rhynchocinetes and Cinetorhynchus shrimps. Data are from Baeza et al. (2014) and are redrawn to exclude species with incomplete information.   

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Reproductive Biology associated with the robustus morphotype (Fig. 15.4). Specifically, the most parsimonious explanation would be that the robustus morphotype was present in a common ancestor, but was subsequently lost in two species. How this pattern translates into the expression of a usurper tactic remains to be determined, but it does demonstrate differences in the intensity of sexual selection among closely related species that would be predicted to affect the relative fitness of a usurper tactic.

FUTURE DIRECTIONS Several characteristics of crustaceans make these animals an excellent choice for studying ARTs: ARTs have already been described in many species of crustaceans; those ARTs take a variety of forms; and ARTs are known to be controlled by either pure genetic strategies or conditional strategies in different species. Many crustaceans with ARTs also have small body size and short generation times, which enable experimental approaches such as family pedigree analyses and replicated microcosms that are less tractable in other taxa. Self-​fertilizing hermaphrodites and single-​sex specialists represent a unique breeding system, and one that has been largely unexplored within the framework of ARTs. Despite these desirable characteristics, we feel that ARTs in crustaceans are largely under-​studied relative to other taxa. There are clearly opportunities to not only better characterize the diversity of ARTs in this group, but also to advance the larger field of ART research. A genetic basis of ARTs has been identified in a number of studies (e.g., Lank et al. 1995, Shuster and Sassaman 1997). However, the specific gene variants that lead to different tactics are largely unknown. One exception is the white-​throated sparrow (Zonotrichia albicollis), in which ARTs have been linked to a chromosomal inversion (Thomas et al. 2008, Davis et al. 2011, Huynh et al. 2011). The isopod Paracerceis sculpta seems an ideal system to explore this question, as Mendelian inheritance at an autosomal gene with three alleles has already been implicated, while linkage disequilibrium between the tactic-​determining gene and the phosphoglucomutase gene suggests a chromosomal location that could narrow the search for a candidate gene (Shuster and Sassaman 1997). Genomic resources for this species are currently limited, but advances in high-​throughput sequencing techniques have made such resources increasingly available in non-​model organisms (reviewed by Ellegren 2014). A second question surrounds the role of ARTs as a source of sexual conflict. When females prefer to mate with large males, as in many crustaceans, males that use usurper tactics may override female mate preferences. Indeed, female rock shrimp appear to prefer guard males and bias paternity against usurper males by actively removing spermatophores that were deposited by sneaking (Thiel and Hinojosa 2003). Consequently, despite high rates of multiple mating, cryptic female mate choice is associated with a strong bias in paternity toward a single male (Bailie et al. 2014). In extreme cases, usurper males may even promote interspecies hybridization by undermining female mate preferences and normal courtship behaviors (Garner and Neff 2013, Stewart et al. 2017). The interaction between ARTs and female mate choice, as well as the fitness consequences of mating with males that use alternative tactics, remains a rich area for further study.

SUMMARY Alternative reproductive tactics (ARTs) occur when individuals of a single sex use discrete tactics to obtain reproductive success. ARTs take multiple forms in crustaceans and are most frequently observed in males. The most common form of ARTs consists of a guard tactic and a usurper tactic, in which guard males are large and often have enlarged claws that they use in competitions with other males to monopolize access to females, and usurper males are small and use sneaking to



Alternative Reproductive Tactics

access females while avoiding conflict with guard males. A notable extension to guard and usurper tactics occurs in a marine isopod, in which some males use a female mimic tactic to avoid conflict with guard males. ARTs are less frequently observed in females, but may occur in crustaceans when females differ in their response to male mate guarding. A unique form of ARTs seen in crustaceans occurs when some individuals are self-​compatible hermaphrodites and others specialize on the sexual function of a single sex. ARTs may be genetically determined by pure strategies or by a conditional strategy in which individuals have the potential to adopt any tactic. To reach an evolutionarily stable state, pure strategies require that the tactics are subject to negative frequency dependent selection and have equal fitness at equilibrium, whereas conditional strategies instead require individuals to use the tactic with the greatest fitness given their underlying condition. There is strong evidence that ARTs in crustaceans are associated with both genetic determination of pure strategies and conditional strategies. ARTs have multiple independent evolutionary origins in different crustacean taxa, and are often associated with the presence of mate guarding and intense sexual selection on males.

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16 CRYPTIC DIVERSITY AND SEXUAL SELECTION

Matthias Galipaud, Loïc Bollache, and Clément Lagrue

Abstract Recent advances in molecular and genetic techniques have revealed tremendous hidden genetic diversity in plants and animals. Crustaceans are no exception and, in fact, present one of the highest levels of cryptic diversity among the metazoans. Beyond the importance of such discovery and its multiple implications for taxonomy and ecology, it is now timely to investigate the potential causes of cryptic diversity. This chapter reviews the theoretical and experimental literature, seeking evidences for a relationship between sexual selection and cryptic diversity in crustaceans. It proposes three scenarios for the role of sexual selection on the origin and maintenance of pre-​ mating isolation and genetic divergence among crustacean populations, and suggests ways to discriminate among them experimentally or using existing data. Assuming that taxonomic identification is largely based on differences in sexually selected morphological traits, it also reviews evidence for a cryptic action of sexual selection on crustacean phenotypes. Specifically, if sexual selection acts primarily on chemical, visual, or behavioral traits, it is likely that allopatric crustacean populations remain morphologically similar even when they are reproductively isolated. This review shows that the strength of sexual selection likely differs among allopatric populations but does not seem to consistently induce pre-​mating isolation (e.g. as in copepods and amphipods). Research is now needed to try to identify general patterns and determine the role of sexual selection on pre-​mating isolation after secondary contact between populations, through reinforcement and reproductive character displacement.

INTRODUCTION The notion of species is one of the most basic, and yet critically important, classification levels in biology, with far-​reaching implications on conservation, ecology, and evolution. Morphology Reproductive Biology. Edited by Rickey D. Cothran and Martin Thiel. © 2020 Oxford University Press. Published 2020 by Oxford University Press.

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Reproductive Biology is the original and has long been the primary tool biologists have used to identify species (Mayr 1949). However, we now know that a significant part of natural diversity is morphologically cryptic and has therefore evaded morphological identification (Bickford et al. 2007). In closer examination and with recent developments and the democratization of modern molecular analyses, we can now identify such hidden diversity (Ladner and Palumbi 2012). One obvious way is to look at the genetic make-​up of populations. Molecular approaches can detect genetic structuring within so-​called morphological species and help identify Molecular Operational Taxonomic Units (MOTUs; Floyd et al. 2002). MOTUs are groups of genetically similar individuals divergent from others of the same morphological taxon. These groups are defined exclusively on the basis of genetic differences using arbitrary divergence thresholds. Numerous methods have been proposed for MOTU identification, ranging from simple divergence levels based on DNA barcoding (Smith et  al. 2005)  to complex multigene phylogenetic approaches (Yang and Rannala 2010). The revelance of each method is debated (Carstens et al. 2013) and will not be discussed here. Generally, rapid progress in molecular techniques shows that morphological identification underestimates the number of evolutionarily divergent phylogenetic lineages within species (Bickford et al. 2007). So-​called cryptic species have now been identified in almost all metazoan taxa (Pfenninger and Schwenk 2007), but their prevalence varies greatly among phyla (Pérez-​Ponce de León and Poulin 2016). As a result, recent studies have recommended that taxonomy now includes voucher DNA sequences to complement morphological descriptions (Ladner and Palumbi 2012). It was even suggested that morphology be replaced altogether by a database of DNA sequences (i.e., molecular taxonomy) to avoid problems with cryptic diversity (Ratnasingham and Hebert 2013). This has sparked heated debates around the definition of taxonomy itself (Tilley et al. 2013).

WHAT IS CRYPTIC DIVERSITY? Cryptic species are basically those that are difficult to distinguish using traditional methods of taxonomy (Knowlton 1993). They are most often defined as two or more distinct species initially classified as a single one due to their morphological similarity (Bickford et  al. 2007, Trontelj and Fišer 2009). There is, however, a lack of methodological and theoretical uniformity when delimiting and identifying cryptic species (Pérez-​Ponce de León and Nadler 2010, Tilley et al. 2013), and the definition of the term even varies among researchers (Bickford et al. 2007). Here, we instead have chosen to use the term cryptic diversity, defined as follows:  the occurrence of individuals that are genetically divergent but morphologically identical or nearly identical, whether among or within populations (i.e., allopatric, occupying different areas separated by an ecological barrier, or sympatric, occupying the same area, respectively). Diversity is cryptic in the sense that it depends on the human observer’s ability to accurately distinguish among organisms. It is therefore unrelated to whether or not it has been uncovered by molecular techniques. This admittedly makes our definition somewhat subjective. But morphological species are identified from differences that human observers are capable of perceiving with no, or limited technological help (e.g., magnifying glasses or microscope). Detecting subtler differences among organisms using technological tools to magnify our senses requires extra effort, time, and often funding. Such effort is yet rarely, if ever, made when there is no initial suspicion that populations may have genetically and/​or phenotypically diverged. This, and the fact that many organisms are often small and difficult to examine, partially explains the high level of cryptic diversity uncovered in virtually every taxon (see Fig. 16.1 for an example of a morphological cryptic diversity in a crustacean).



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Fig. 16.1. Three sympatric ecomorphs (A, B, and C) of the North American crustacean amphipod Hyalella azteca. Although the subtle differences in color patterns observed in live individuals (top row) are a match to molecular markers used to distinguish them, preserved specimens (bottom row) are virtually indistinguishable using morphology (Wellborn and Cothran 2004). Figure adapted from Cothran et al. (2013a).   

Cryptic diversity has profound implications for evolutionary biology, biogeography, ecology, and conservation. For example, the mosquito Anopheles gambiae, a major malarial vector, consists of seven cryptic species. Some attack only wildlife, posing no threat to human health. If eradication could focus on human-​specific species, resources would be spent more strategically, without impacting non-​target species (Bickford et al. 2007). Another major issue is to understand the causes of such diversity. But there is an obvious logical flaw here! Cryptic diversity and its causes cannot be studied if overlooked or unsuspected in the first place, which it is by definition. This tautology incites researchers to proceed step by step. First, we must unravel previously hidden diversity. As stated earlier, this is, to a certain extent, done or in the process of being done, thanks to new molecular tools. Second, we can study the ecological and evolutionary causes of its origin and maintenance, about which we still know very little. This timely endeavor should, in turn, help us predict where and what to look for to discover new taxa.

WHAT CAUSES CRYPTIC DIVERSITY? Levels of cryptic diversity vary widely among animals (Pérez-​Ponce de León and Poulin 2016, Poulin and Pérez-​Ponce de León 2017). To explain such variation, Pfenninger and Schwenk (2007) tested the hypothesis that cryptic diversity is greater in more extreme climates as a result of selection for morphological stasis. They, however, found no effect of biogeographical realms on the number of MOTUs within morphological species. Habitats with higher degrees of fragmentation, and thus more geographical barrier to gene flow, may also harbor greater levels of cryptic diversity. Accordingly, cryptic diversity was more often observed in highly fragmented freshwater habitats, compared to marine or terrestrial habitats (Poulin and Pérez-​Ponce de León 2017). Incidentally, such fragmentation also occurs at high rates in freshwater habitats. As a result, populations split somewhat often on an evolutionary time scale, which leads to a high probability of observing incipient speciation, and therefore cryptic diversity, rather than complete speciation leading to well-​ defined morphological taxa. Beyond habitat, specific characteristics of organisms, such as their life history adaptations, their reproductive strategies, or their body size, may affect the potential for cryptic diversity. For

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Reproductive Biology instance, cryptic diversity has been hypothesized to be higher in parasites because of their shorter generation time, rapid evolution, and high rate of host specialization, which are thought to promote speciation. However, no relationship between life strategies (parasitic versus free-​living) and levels of cryptic diversity was found (Poulin and Pérez-​Ponce de León 2017). Whether caused by environmental factors or by organisms’ characteristics, observed variation in cryptic diversity among animals is still poorly understood.

CRYPTIC DIVERSITY IN CRUSTACEANS Cryptic diversity is very common in crustaceans. Evidence suggests that crustaceans contain comparatively more cryptic diversity than expected based on species richness and research effort (Pérez-​Ponce de León and Poulin 2016). Genetic divergence among haplotypes (i.e., the proportion of pair-​wise nucleotide substitutions between haplotypes) from individuals belonging to the same morphological species frequently exceeds 10%. For example, in Mesopodopsis slabberi, a common mysid species along the Atlantic and Mediterranean European coasts, divergence among haplotypes ranges from 0.22% to 19.43% (Remerie et al. 2006). In the amphipod species complex Gammarus pulex/​Gammarus fossarum, genetic divergence ranges from 3% to 27.9% (Lagrue et al. 2014). The prevalence of cryptic diversity also varies widely among crustacean taxa. For example, 13 distinct MOTUs from 121 haplotypes were found based on the analysis of only 657 specimens of the G. pulex/​G. fossarum complex (Lagrue et al. 2014). In the snapping shrimp Alpheus armillatus, at least 19 MOTUs were described based on mitochondrial and nuclear DNA from 67 individuals (Matthews and Anker 2009, Fig. 16.2). In deep-​sea phoxocephalid amphipods, an astonishing 49 MOTUs from 4,100 individuals were identified (Knox et al. 2012). However, nearly 60% (29/​49) of these MOTUs were present at only one location and represented by a single specimen. Typically, MOTUs are groups of genetically similar individuals (see earlier discussion), and identifying a MOTU based on a single individual may be inappropriate. Such MOTU diversity would thus need confirmation. We demonstrated the prevalence of cryptic diversity in crustaceans using an ISI Web of Science internet search between 1986 (year of the first scientific publication mentioning the polymerase chain reaction, or PCR, technique) and 2016 (Fig. 16.3). In total, 8,097 articles contained cryptic diversity keywords (Fig. 16.3). Among those, 6.3% (507 articles) also included at least one keyword of the crustacean search field (including fields 1 and 2 in the search, Fig. 16.3). Cryptic diversity has been found in every contemporary crustacean class except horseshoe shrimps (i.e., Cephalocarida). Taxa for which research effort is greater are also those where more cryptic diversity is reported (Fig. 16.4; Table 16.1). After controlling for species richness and research effort in each taxon, most crustacean taxa showed levels of cryptic diversity in the expected range (Fig. 16.4; Table 16.1). However, mantis shrimps (i.e., stomatopods) and amphipods seemed to present higher levels of cryptic diversity than expected, while barnacles and mysids presented lower levels of cryptic diversity than expected (Fig. 16.4; Table 16.1). Such variation in reported cryptic diversity among crustaceans remains to be explained. In this chapter, we discuss the potential link between cryptic diversity and sexual selection in crustaceans, as sexual selection is thought to be a major evolutionary process triggering speciation in other animal taxa (Turelli et al. 2001, Kirkpatrick and Ravigné 2002, Ritchie 2007). In our literature search, only about 2% (157 articles) of cryptic diversity papers also included at least one keyword from the sexual selection search field (when including fields 1 and 3 in the search, Fig. 16.3). Comparatively, articles referring to sexual selection (search field 3) represented about 10% (1,612 articles over 15,702) of the total number of articles referring to speciation in general (search field: speciation AND *evolution*). References to sexual selection are almost nonexistent among

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(K)

(J)

(L)

(N)

(O)

Fig. 16.2. Representatives of major color pattern types in the snapping shrimp Alpheus armillatus species complex. The A. armillatus complex includes at least 19 putative divergent lineages, with coloration being typically the most pronounced phenotypic character distinguishing them; substantial biodiversity remains concealed by morphological similarity (Mathews and Anker 2009). Cryptic species complexes are generally very common in the genus Alpheus, indicating widespread genetic diversification with little or no morphological change. Figure adapted from Mathews and Anker (2009).   

452

Reproductive Biology 800 cryptic diversity... ...and crustaceans 600

Number of articles

...and sexual selection

400

200

0

19 8 19 6 8 19 7 8 19 8 89 19 9 19 0 9 19 1 9 19 2 9 19 3 9 19 4 95 19 9 19 6 9 19 7 9 19 8 99 20 0 20 0 01 20 0 20 2 0 20 3 0 20 4 05 20 0 20 6 07 20 0 20 8 0 20 9 1 20 0 11 20 1 20 2 13 20 1 20 4 1 20 5 16

452

Publication year

Fig. 16.3. Number of articles published per year with a reference to cryptic diversity, cryptic diversity and crustaceans, and cryptic diversity and sexual selection. Results were obtained from the ISI Web of Science searching engine. Selected keywords were searched within the title, abstract, and keyword sections of articles and were included in three search fields connected by the logical conjunction AND (which means that at least one keyword of every search field necessarily appears in selected articles). The search fields were as follows: (1) the cryptic diversity search field:  “cryptic species” OR “sibling species” OR “cryptic diversity” OR “cryptic speciation” (the logical operator OR means that at least one of the keyword is found in the article), (2) the crustacean search field: *crustacea* OR maxillopod* OR ostracod* OR malacostrac* OR branchiopod* OR remiped* OR cephalocarid* OR *crab* OR *shrimp* OR *decapod* OR *amphipod* OR *isopod* OR *copepod* (where we included names of the major classes of crustacean as well as well-​studied taxa) and (3) the sexual selection search field: “sexual selection” OR “mate choice” OR “mating preference*” OR “competitiveness.” Three searches were performed, which included search field (1)  only, search fields (1)  and (2), and search fields (1) and (3), respectively.   

the 507 articles dealing with cryptic diversity in crustacean, as only 5 articles (16% genetic divergence), with the exception of a few cases where males were non-​choosy, which led to asymmetric mating preferences (Galipaud et al. 2015a). Similar patterns of incomplete pre-​mating isolation and asymmetric preferences may be prevalent among crustacean

459

460

Reproductive Biology 1.0

Proportion of unpaired males

460