Neuroendocrinology of Behavior and Emotions: Environmental and Social Factors Affecting Behavior (Masterclass in Neuroendocrinology, 16) 3031511115, 9783031511110

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Masterclass in Neuroendocrinology 16

Heather K. Caldwell H. Elliott Albers   Editors

Neuroendocrinology of Behavior and Emotions Environmental and Social Factors Affecting Behavior

Masterclass in Neuroendocrinology Volume 16 Series Editors Mike Ludwig, Centre for Discovery Brain Sciences The University of Edinburgh, Edinburgh, UK Rebecca Campbell, School of Biomedical Sciences University of Otago, Dunedin, New Zealand

Masterclass in Neuroendocrinology is published in collaboration with the International Neuroendocrine Federation (INF) https://www.inf-neuroendocrinology. org/. This series aims to illustrate and promote the use of the latest and most impactful technologies in basic and clinical research in the exciting field of neuroendocrinology. Neuroendocrinology is defined as the study of the control of endocrine function by the brain and the actions of hormones on the brain. The series is made up of volumes that highlight different topics in neuroendocrinology that are of current interest and encompass the study of both normal and abnormal function, and the developmental origins of disease. They include the study of neural networks in the brain that regulate and form neuroendocrine systems, and also include the study of behaviours and mental states that are influenced or regulated by hormones. They also necessarily include the study of peripheral physiological systems that are regulated by neuroendocrine mechanisms. Some recent examples include: Developmental Neuroendocrinology, Neuroendocrine Clocks and Calendars, and Neuroanatomy of Neuroendocrine Systems. Each book • is edited by leading experts in the field • is written by a team of internationally respected researchers • is focused on an area of neuroendocrinology research • demonstrates the present state of knowledge and understanding in the field of neuroendocrinology and highlights the translation of such knowledge to improve human health and well-being • includes assessments of different experimental approaches both in vivo and in vitro, and of how the resulting data are interpreted. The Series is aimed at a wide audience, as neuroendocrinology integrates neuroscience and endocrinology. It is intended for established scientists, clinicians and early-career researchers. Founding Series Co-Editors: William E. Armstrong and John A. Russell The series is indexed in Scopus.

Heather K. Caldwell  •  H. Elliott Albers Editors

Neuroendocrinology of Behavior and Emotions Environmental and Social Factors Affecting Behavior

Editors Heather K. Caldwell Department of Biological Sciences Kent State University Kent, OH, USA

H. Elliott Albers Center for Behavioral Neuroscience Georgia State University Atlanta, GA, USA

ISSN 2662-2068     ISSN 2662-2076 (electronic) Masterclass in Neuroendocrinology ISBN 978-3-031-51111-0    ISBN 978-3-031-51112-7 (eBook) https://doi.org/10.1007/978-3-031-51112-7 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Paper in this product is recyclable.

Series Preface

This series began as a joint venture between the International Neuroendocrine Federation and Wiley-Blackwell, and now is continuing with Springer Nature as publisher for the federation. The broad aim of the series is to provide established researchers, trainees, and students with authoritative, up-to-date accounts of the present state of knowledge, and prospects for the future, across a range of topics in the flourishing field of neuroendocrinology. The series is aimed at a wide audience as neuroendocrinology integrates the disciplines of neuroscience and endocrinology. We define neuroendocrinology as the study of how endocrine function is controlled by the brain and the actions of hormones on the brain. It encompasses the study of normal and abnormal function, and the developmental origins of disease. It includes investigation of the neural networks in the brain that regulate and form neuroendocrine systems, and it also includes the study of behaviors and mental states that are influenced or regulated by hormones. In addition, neuroendocrinology encompasses the understanding and study of peripheral physiological systems that are regulated by neuroendocrine mechanisms. While neuroendocrinology embraces many issues of concern to human health and wellbeing, research in reductionist animal models is usually required to fully understand these issues. Contemporary research in neuroendocrinology involves a wide range of techniques and technologies, from the subcellular and systems level to the whole-­ organism level. A particular aim of the series is to provide expert advice and discussion about experimental or technical protocols in neuroendocrinology research, and to further advance the field by giving information and advice about novel techniques, technologies, and interdisciplinary approaches. To achieve our aims, each book focuses on a particular theme in neuroendocrinology. For each book, we recruit editors, who are leaders in their field, to engage an international team of experts to contribute chapters in their individual areas of expertise. The mission of each contributor is to provide an update of current knowledge and recent discoveries and to discuss new approaches, “gold-standard” protocols, translational possibilities, and future prospects. Authors are asked to write for a broad audience, to use references selectively, and to consider the use of video clips and explanatory text boxes; each chapter is peer-reviewed and has a glossary.

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Series Preface

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The masterclass series is open-ended; books in the series published to date are: • Neurophysiology of Neuroendocrine Neurons (2014, ed. WE Armstrong & JG Tasker) • Neuroendocrinology of Stress (2015, ed. JA Russell & MJ Shipston) • Molecular Neuroendocrinology: From Genome to Physiology (2016, ed. D Murphy & H Gainer) • Computational Neuroendocrinology (2016, ed. DJ MacGregor & G Leng) • Neuroendocrinology of Appetite (2016, ed. SL Dickson & JG Mercer) • The GnRH Neuron and its Control (2018, ed. AE Herbison & TM Plant) • Model Animals in Neuroendocrinology (2019, ed. M Ludwig & G Levkowitz) The first books of the series published by Springer Nature are: • • • •

Neurosecretion: Secretory Mechanisms (2020, ed. JR Lemos & G Dayanithi) Developmental Neuroendocrinology (2020, ed. S Wray & S Blackshaw) Neuroendocrine Clocks and Calendars (2020, ed. FJP Ebling & HD Piggins) Glial-Neuronal Signaling in Neuroendocrine Systems (2021, ed. JG Tasker, JS Bains, & JA Chowen) • Neuroanatomy of Neuroendocrine Systems (2022, ed. V Grinevich & A Dobolyi) • Neuroendocrine-Immune System Interactions (2023, ed. JP Konsman & TM Reyes) • Cardiovascular Neuroendocrinology (2023, ed. T Cunningham & G Yosten) In development are Neuroendocrinology of Pregnancy and Lactation (ed. P Brunton & D Grattan) and Evolutionary and Comparative Neuroendocrinology (ed. V Grinevich & R Oliveira). Feedback and suggestions are welcome. Series Editors International Neuroendocrine Federation—https://www.inf-­neuroendocrinology.org/ Edinburgh, UK Dunedin, New Zealand 

Mike Ludwig Rebecca Campbell

Preface

Animals are inherently social. Whether their social interactions are restricted predominately to times of reproduction or whether they live in complex social groups, all animals engage in social behaviors and many of these behaviors are critical for their survival. While there is a biological drive to have sex, fight, flee, and eat, the way that behaviors manifest between individuals and in groups can vary widely across species and sexes. Thus, the nuanced way an individual, or group of individuals, behaves is ultimately shaped by numerous factors, including temperament, social experience, and the environment. All these factors affect the neuroendocrine system, which serves as the biological “currency” for the neural regulation of behavior. Sitting at the interface of the environment and brain, the neuroendocrine system is sensitive to sensory input and affects behavioral responses by mediating behavioral plasticity, allowing for dynamic responses to varying contexts, both social and environmental. With this as the backdrop, this volume presents the current state of knowledge in three areas of behavioral neuroendocrinology: Part I—Social Relationships, Part II—Social Behaviors and their Regulation, and Part III—Environmental Influences on Neuroendocrine Systems and Behavior. This collection from experts in the field challenges readers to think deeply about the complexity of social interactions and the ways in which there are similarities and differences across species as well as how social factors and environmental factors directly affect social behavior. Part I focuses on relationships. Chapter 1 walks through what is known about coordinated acoustic displays in songbirds, which are a complex form of animal communication. Tobiansky and Price discuss the roles that estrogens and androgens play in both signal perception and production, which are required for duets, and highlight the need for more research in this area. Chapter 2 by Manca and Bales discusses the different types of social bonds that primates experience, from pair bonds to coalitions. The purpose of each bond is explored as well as what is known about its regulation. Chapter 3 examines human cooperation and parental care and the neuroendocrine mechanisms that support these behaviors. Rilling reviews the human data ranging from peripheral hormone measures to fMRI and brings together disparate datasets to evaluate what is known and what is needed for the field to move forward. The theme for Part II is social behaviors and their regulation. The first two chapters in this section are more focused on the neuroendocrine regulation of specific vii

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Preface

behaviors, whereas the latter two chapters are more focused on factors involved in the regulation of the neuroendocrine system and behavior. Chapter 4 discusses what is known about the neuroendocrine regulation of maternal behavior in rodents, which is critical for species survival. Sanson and colleagues also dive into how altered neuroendocrine transmission can disrupt the maternal brain and can result in maternal neglect. Chapter 5 by Veney and Caldwell discusses the complexity of the neural regulation of behavior by the oxytocin and vasopressin systems, with an eye toward sex differences. Chapter 6 examines neural plasticity in adults, specifically neurogenesis. Jorgensen and Wang walk through the most recent research in this area and link changes in neurogenesis to impacts on the neuroendocrine system and ultimately social behavior. Chapter 7 takes a sweeping view across taxa to look at neuroendocrine contributions to reproductive decision making. Elson and colleagues highlight how reproductive decision making can vary widely across species even if the neural circuits that underlie reproductive decision making, and which interface with the neuroendocrine system, may be conserved. Part III focuses on how the environment affects neuroendocrine systems and behavior. Chapter 8 by Kareklas and Oliveira looks at how social isolation impacts the oxytocin system, such that motivational and cognitive functions are altered. Chapter 9 discusses how animals are bombarded by man-made chemicals in our environment and considers their effects on neuroendocrinology and behavior. In this chapter, Patisaul highlights the impact of endocrine-disrupting chemicals on human health and in particular their linkage to the etiology of neurodevelopmental disorders. The neuroendocrine system is complex as are the behaviors that it helps to regulate. While there appears to be some conservation in terms of the brain regions involved across species, the behavioral output is often sex- and species-specific. Beyond this, the life history of an individual, social context, and the physical environment also affect the neuroendocrine system and shape behavioral responses. We hope readers are excited by the breadth and depth of the topics covered in this collection. Further, we hope that many are inspired to develop new ideas and engage in research that will continue to move this exciting field forward. Kent, OH, USA Atlanta, GA, USA 

Heather K. Caldwell H. Elliott Albers

Contents

Part I Social Relationships 1

 Neuroendocrine Modulation of Coordinated Acoustic Signals ������������   3 Daniel J. Tobiansky and J. Jordan Price

2

 Adult Social Relationships in Primates����������������������������������������������������  27 Claudia Manca and Karen L. Bales

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Neuroendocrinology of Human Cooperation and Parental Care ������������������������������������������������������������������������������������������������������������  57 James K. Rilling

Part II Social Behaviors and Their Regulation 4

 Neuroendocrine Basis of Impaired Mothering in Rodents��������������������  83 Alice Sanson, Luisa Demarchi, and Oliver J. Bosch

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Oxytocin, Vasopressin, and Sex Differences in Social Behavior. It’s Complicated!���������������������������������������������������������������������������������������� 109 Sean L. Veney and Heather K. Caldwell

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Adult Neurogenesis and Social Behavior: A Reciprocal Relationship������������������������������������������������������������������������������������������������ 131 Claudia Jorgensen and Zuoxin Wang

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Neuroendocrine Mechanisms Underlying Reproductive Decision Making Across Taxa ������������������������������������������������������������������ 157 Mary R. Elson, Nora H. Prior, and Alexander G. Ophir

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Part III Environmental Influences on Neuroendocrine Systems and Behavior 8

 Oxytocin and Social Isolation: Nonapeptide Regulation of Social Homeostasis������������������������������������������������������������������������������������������������ 195 Kyriacos Kareklas and Rui F. Oliveira

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Dirty Minds: How Endocrine Disrupting Chemicals (EDCs) and Other Pollutants Affect the Neuroendocrinology of Behavior and Emotions���������������������������������������������������������������������������������������������� 217 Heather B. Patisaul

Glossary�������������������������������������������������������������������������������������������������������������� 251

About the Editors

Heather  K.  Caldwell  received her B.A. and M.S. from the University of North Carolina at Greensboro and her Ph.D. from Georgia State University. She went on to work with Dr. W. Scott Young at the National Institute of Mental Health at the National Institutes of Health for her postdoctoral training. She is currently Professor and Chair of the Department of Biological Sciences at Kent State University. Her work has focused on the contributions of oxytocin and vasopressin to the neural regulation of behavior, both in early development and adulthood. H. Elliott Albers  received his B.S. from the University of Nebraska in 1974 and his Ph.D. from Tulane University in 1979. He did postdoctoral training at Harvard Medical School and the Worcester Foundation for Experimental Biology. After serving on the faculty of the University of Massachusetts Medical School, he joined Georgia State University in 1986. Currently, he is the Director of the Center for Behavioral Neuroscience and Regents Professor of Neuroscience at Georgia State University. Dr. Albers’ research program focuses on behavioral neuroendocrinology with studies focused on neurochemical signaling in brain circuits regulating social behavior and biological rhythms.

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Part I Social Relationships

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Neuroendocrine Modulation of Coordinated Acoustic Signals Daniel J. Tobiansky

and J. Jordan Price

Abstract

Coordinated acoustic displays, in which two or more individuals combine their sounds to produce collaborative signals, are among the most remarkable and least understood forms of animal communication. While many studies have focused on the evolution and potential functions of coordinated displays, especially the male–female duets of many songbird species, relatively little is known about the underlying neural and hormonal bases of acoustic coordination. Here, we use our current understanding of the neuroendocrine mechanisms involved in signal perception and production—with a focus on songbirds—to explore the roles that these mechanisms might play in coordinated acoustic displays. Recent research suggests that brain regions of the song control system play important roles in processing salient social cues during signal coordination to correctly modulate the timing of appropriate motor responses by signaling partners. These regions associated with signal coordination are particularly sensitive to steroid hormones in songbirds and other taxa that display coordinated acoustic behaviors. In this chapter, we focus on estrogens and androgens—the two “sex” steroids that play an oversized role in communicative behavior in birds. Decades of research suggests that these steroid hormones regulate the development and modulate the activity of brain regions important for vocal and non-vocal coordinated sonations. However, our understanding of these systems has been limited D. J. Tobiansky (*) Department of Biology, St Mary’s College of Maryland, St Mary’s City, MD, USA Program in Neuroscience, St Mary’s College of Maryland, St Mary’s City, MD, USA e-mail: [email protected] J. J. Price Department of Biology, St Mary’s College of Maryland, St Mary’s City, MD, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 H. K. Caldwell, H. E. Albers (eds.), Neuroendocrinology of Behavior and Emotions, Masterclass in Neuroendocrinology 16, https://doi.org/10.1007/978-3-031-51112-7_1

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by a disproportionate research focus on male brains and relatively few previous studies of female brains and behavior. We discuss what we have yet to understand, and we offer some potential avenues for future research. Keywords

Animal communication · Coordinated signals · HVC · Male–female duets · Social cues · Sex steroid hormones

1.1 Introduction Many social animals coordinate their signaling behavior to produce complex acoustic displays. Coordinated signals are unlike other forms of communication in that the timing and types of signals contributed by participants may be modulated in response to other signaling individuals. In a vocally duetting pair of birds, for instance, each member of the pair may rapidly alter its vocalizations based on the sounds produced by its interacting partner (Farabaugh 1982; Hall 2009). This is unlike the situation for lone, individually vocalizing birds, in which the order, tempo, and structure of sounds in a series may follow a predetermined and relatively invariant pattern. The mechanisms underlying the development and production of stereotyped vocal displays have been well studied, especially in oscine passerine species (i.e., songbirds) that learn their songs, and especially in male songbirds (Marler and Slabbekoorn 2004; Catchpole and Slater 2008). However, the neural and hormonal mechanisms involved in the complex signal coordination of duetting birds have only recently garnered significant attention (Fortune et al. 2011; Benichov et  al. 2016; Elie et  al. 2019; Hoffmann et  al. 2019; Coleman et  al. 2021; Brenowitz 2021). Coordinated acoustic displays presumably involve special neurophysiological mechanisms beyond those involved in perceiving, learning, and/or producing stereotyped songs (Rivera-Cáceres and Templeton 2019). Signal coordination appears to be associated with cortical enlargement or specialization (Cerkevich et al. 2022). Moreover, these coordinated signals, like many behaviors that tend to occur primarily during the breeding season, are modulated by steroid hormones such as androgens (e.g., testosterone) and estrogens (Brenowitz et al. 1985; Brenowitz and Arnold 1989). Hormonal modulation of these signals is regulated through regions of the central nervous system and the skeletal muscle output that produces these signals (Tobiansky et al. 2018, 2020b; Tobiansky and Fuxjager 2020). In this chapter, we discuss coordinated acoustic signals, with a particular focus on songbirds. We focus on songbird taxa because of the number and variety of well-­ documented coordinated vocal signals in this group (Hall 2009; Dahlin and Benedict 2014; Logue 2021), the broad literature on how the brain controls oscine bird song (Marler and Slabbekoorn 2004; Catchpole and Slater 2008), and our understanding of how hormones (particularly steroids) modulate these signals (reviewed by Rose et al. 2022). Specifically, we discuss the evolution of signal coordination, the neuroanatomy and neuroendocrine signaling involved in song perception and production

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in males and females, and putative neuroendocrine mechanisms modulating acoustic coordination. Finally, we use the backdrop of our knowledge about these topics to explore what we have yet to understand.

1.2 The Evolution of Intersexual Acoustic Coordination Some of the best-studied and most impressive examples of coordinated acoustic signaling are the male–female duets of many songbird species (Farabaugh 1982; Hall 2009; Logue and Krupp 2016). Duetting can be defined as the coordination of vocalizations by two individuals such that their elements alternate or overlap with a degree of temporal precision (Farabaugh 1982). Species vary widely in the coordination and complexity of their duets, from pairs that loosely overlap or alternate parts of their songs (Mennill and Vehrencamp 2005; Odom et al. 2017) to species that perform elaborate, rapidly alternating (i.e., antiphonal) duets or choruses in which the songs of two or more individuals are combined with such precision that they sound like a single bird singing (Mann et al. 2006, 2009; Fortune et al. 2011; Templeton et al. 2013). Male–female duets are generally thought to be cooperative behaviors, largely based on evidence that these coordinated displays are more effective in defending territories than displays produced by single individuals (Hall and Magrath 2007; Mennill and Vehrencamp 2008; Templeton et al. 2011). Vocal duetting tends to be found in non-migratory species (Logue and Hall 2014), which are typically tropical breeders that defend year-round territories, engage in long-term monogamy, and have convergent sex roles (Slater and Mann 2004; Garamszegi et  al. 2008). The primary functions of male–female duetting appear to be joint territory defense and signaling pair-bond stability (Hall 2004; Dahlin and Benedict 2014; Keenan et al. 2020). Consistent with this idea, a recent comparison of duetting species showed that levels of duet coordination and precision are associated with breeding season length, presumably reflecting levels of cooperation and commitment between partners (Keenan et al. 2020). Pairs tend to get better at duetting with experience (Hall and Magrath 2007), suggesting that long-term social relationships play an important role in the development of highly coordinated displays (Rivera-Cáceres et al. 2018; Rivera-Cáceres and Templeton 2019). Although most studies of vocal duetting have focused on songbirds, male–female duets are also known to occur in a variety of other avian groups (Farabaugh 1982; Malacarne et al. 1991), including owls (Odom and Mennill 2010), parrots (Wright and Dahlin 2007), barbets (Soma and Brumm 2020), and waterfowl (Kraaijeveld and Mulder 2002). Coordinated acoustic displays can also involve forms of non-­ vocal sonations such as coordinated drumming by territorial pairs in some woodpecker species (Schuppe et al. 2016). These coordinated displays ostensibly serve many of the same functions for communication as the vocal duets of oscine songbirds (Hall 2004, 2009). Singing by both sexes is widespread in passerines, and phylogenetic analyses show that females sang in the ancestors of all modern songbirds (Odom et al. 2014).

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Comparative evidence suggests that female singing may be a precursor for the evolution of duetting in some avian groups (Odom et al. 2015). However, evidence also suggests that the production of complex vocalizations by females and the coordination of those sounds with a male partner are separate behaviors that have evolved independently under different but largely overlapping selective pressures (Mitchell et al. 2019; Price et al. 2023). Vocal coordination between the sexes is widespread, in non-passerines as well as passerines, and it is therefore possible that coordinated acoustic communication evolved in the earliest birds.

1.3 The Evolution of Intrasexual Acoustic Coordination Precise signal coordination can also occur between members of the same sex. For example, in some lekking manakin species (genus Chioxiphia), pairs of males collaborate to produce matching songs virtually in unison to attract females (DuVal 2007; Maynard et al. 2012). Coordinated male–male duets are more attractive to females than displays produced alone (DuVal 2007; Maynard et al. 2012) suggesting that the evolution of precise signal coordination has been driven by female mating preferences. Males in these long-term partnerships do not have identical interests: dominant males benefit in the short term by gaining access to mating opportunities, while subordinate males increase their probability of eventually achieving dominant status (DuVal 2007). Male pairs with better frequency matching tend to attract more females, and duet performance improves over years (Trainer et  al. 2002), suggesting that social learning and repeated practice are important. Thus, in many ways, these male–male manakin displays are analogous to the coordinated territorial duets produced by mated male–female pairs in many other avian species (Hall 2009). Another, more common form of male-male vocal coordination occurs during vocal interactions among territorial neighbors. In many songbird species, competing neighboring males appear to signal dominance or aggression by overlapping or matching the acoustic structure of their rivals’ sounds (Beecher et al. 2000; Todt and Naguib 2000; Mennill et al. 2002; Naguib and Mennill 2010; Price and Yuan 2011; Logue 2021). Such rapid matching in the timing and/or sound patterns of songs may serve as an indicator of aggressive intentions toward rivals, suggesting the likelihood of ensuing aggressive behavior (Vehrencamp 2001). Alternatively, birds may coordinate their sounds with rivals to showcase their relative vocal performance abilities, potentially acting as a display to other listeners (Price et al. 2006; Logue and Forstmeier 2008; Logue 2021). While these interactions between rival males are seldom referred to as “duets,” the attentiveness and precision required for acoustic overlapping and rapid pattern matching bear similarities to the mechanisms involved in coordinated male-female duets. This suggests that the same neural and hormonal pathways may be engaged. Despite the lack of extensive research on the neuroendocrine mechanisms underlying song overlapping and song type matching (Logue 2021; but see Prather et al. 2008), this area presents a promising direction for future studies.

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Same-sex vocal coordination among females is an unexplored domain. However, considering the prevalence of female song in passerines (Odom et al. 2014), such coordination probably occurs. Growing focus on female singers will likely unveil new insights into the crucial roles females play in coordinated acoustic displays (Riebel et al. 2019). Female song is not just a rare curiosity, but a widespread phenomenon (Odom et al. 2014). Females engage in singing behaviors for various reasons (Price 2009), much like their male counterparts. These can range from territorial defense to mate attraction, providing a rich context in which same-sex vocal coordination could conceivably occur. Given the broad range of functions that singing serves for female passerines, it seems plausible that such coordination would provide additional communicative advantages.

1.4 Neuroendocrinology of Acoustic Signal Perception and Production Relatively little is known about the underlying neural structures and endocrine signaling that regulate duets or rapid counter-singing in birds (Hall 2009; Logue 2021). However, there is a significant literature base describing the structures and neural functions of the song system in songbirds, including in duetting species. In this section, we introduce brain regions that are integral in auditory perception and vocal and non-vocal acoustic production in both male and female birds. We then tie this information together with the little that is known about the functional neuroanatomy of coordinated acoustic behaviors and the hormones that regulate the neural circuitry responsible for producing these behaviors. Much of this previous research has focused on males, but the neuroendocrinology of female brains is earning increasing attention (Riebel et al. 2019; Brenowitz 2021; Rose et al. 2022). Here, we devote special attention to these recent findings.

1.4.1 Basic Neuroanatomy Driving Acoustic Displays The song control system in songbirds and neural regions that control other vocal and non-vocal sonations have been extensively mapped and studied in a wide variety of bird taxa over the past half-century. Coordinated vocal displays inherently require a functional auditory processing circuit and a vocal control pathway. Starting with the auditory processing circuit, a listening bird will transduce auditory information through the basilar papilla, similar to auditory hair cells in mammals (Fischer 1992). Comparative analyses of these cells in songbirds versus more distantly related lineages (i.e., chicken and emu) suggest that the efferents of the basilar papilla of songbirds have evolved to be myelinated (Köppl 2001). The myelinated efferents allow the signal to be relayed faster to integration and processing centers required for the precise timing necessary in coordinated acoustic behaviors. The remaining auditory relay and processing circuits are evolutionarily conserved and have been reviewed in detail elsewhere (Bolhuis et  al. 2010; Petkov and Jarvis

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2012). In brief, the signal is relayed through the cochlear ganglion to the cochlear nucleus in the hindbrain. Auditory signals are then processed in the superior olive, lateral lemniscus, and dorsal lateral nuclei of the mesencephalon. From there the information is relayed to the L2 subdivision of field L in the forebrain through the nucleus ovoidalis in the thalamus. Finally, the auditory information is processed by other subregions of field L, the caudomedial and caudolateral mesopallium (CMM and CLM, respectively), the HVC (proper name), the caudomedial nidopallium (NCM), and the robust nucleus of the arcopallium (RA). These regions project to one another and several also project back to thalamic and midbrain auditory nuclei to process and regulate environmental, conspecific, and interspecific auditory information. In birds that do not learn their songs, several of these regions are not well defined or are completely missing, such as the HVC and RA (Schuppe et al. 2022a), but closely related non-passerine birds that learn vocalizations (e.g., parrots and hummingbirds) have regions that are homologous to these oscine-specific circuits (Davenport and Jarvis 2023). Importantly, when the birds hear songs of conspecifics, the CLM, CMM, shelf of the HVC, and cup of the RA are more active (Gobes et al. 2010; Arneodo et al. 2021; McGregor et al. 2022; Davenport and Jarvis 2023), suggesting that these regions are specific to song processing and thus perhaps vocal duetting. The other circuit required for coordinating acoustic signals is the song production system, which has also been extensively mapped out and reviewed in detail (Brenowitz et al. 1997; Mooney 2009). In short, the song system can be divided into two parallel and overlapping pathways: the vocal motor pathway and the anterior forebrain pathway. Lesion and tract-tracing studies have shown that the vocal motor pathway is responsible for song production and involves the HVC, RA, interfascicular nucleus of the nidopallium (Nif), nucleus uvaeformis (UVa), nucleus avalanche (Av), Area X of the striatum (Area X), ventral tegmental area (VTA), dorsal medial nucleus of the thalamus (DM), tracheosyringeal portion of the nucleus hypoglossus (nXIIts), and the retroambiguus (RAm) (Nottebohm 2005; Davenport and Jarvis 2023). The UVa and other auditory processing nodes project to the HVC via the Nif and L2 subregion of the nidopallium (Jarvis et al. 2005). During song production, the HVC is highly active and sends its signal to the Av and the RA (Akutagawa and Konishi 2010). The Av is also active during song production, but its projections and function are not as well understood as those of the RA. A recent study suggests that the HVC projects song information to the Av which in turn relays vocal motor signals to the auditory system during song learning, acting as a sort of feedback system that allows the bird to adjust temporal components of the song (Roberts et al. 2017). Concurrently, the RA is essential for song production (Ashmore et al. 2005, 2008) and is highly active during this behavior. This neural node controls syllable production, trill bandwidth stereotypy, and other acoustic modulations (Alward et  al. 2017). This nucleus projects to two brainstem nuclei—the nXIIts and the RAm, innervating the trachea and syrinx and the muscles that control respiration, respectively. These projections give the RA direct control over syringeal muscle actuation to produce different songs and fine motor control of the timing in respiration.

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Moreover, the RA innervates the DM, which regulates call and song patterns also through direct innervation of the nXIIts and RAm (Fukushima and Aoki 2000) and feedback projections to the UVa (Ashmore et al. 2005). The anterior forebrain pathway is the other primary and parallel circuit involved in song learning and vocal and non-vocal acoustic production. This pathway shares the neural nodes Area X, HVC, and RA with the vocal motor pathway. The anterior forebrain pathway also includes the dorsal lateral nucleus of the medial thalamus (DLM) and lateral magnocellular nucleus of the anterior nidopallium (lMAN). Signal production and learning are modulated by this circuit, such that auditory information and vocal output processing that occurs in the HVC then projects to Area X, which forms a feedback loop with the DLM and lMAN (Area X→DLM→lMAN→Area X). Finally, this modulatory information is sent to the vocal motor pathway through lMAN projections to the RA. During bouts of acoustic production (e.g., singing), the regions of these feedback loops (Area X, HVC, and lMAN) are neuronally active, along with the RA which is the output nucleus for the pathway. This pathway is also heavily involved in the song-learning process, which has been well-established and extensively reviewed (Jarvis 2004; Petkov and Jarvis 2012; Davenport and Jarvis 2023). Learning is almost certainly also involved in development of the precise coordination observed in many male-female duets (Rivera-Cáceres and Templeton 2019); however, this topic and aspects of the associated pathway are beyond the scope of this chapter.

1.4.2 Sex Differences in Neuroanatomy Based on most previously studied passerine species, the most obvious difference in the developmental neuroanatomy of male and female brains is that males develop significantly larger song system nuclei than females. For example, in adult Zebra Finches (Taeniopygia guttata), the HVC is at least four times larger and much more well-defined in males than it is in females (Shaughnessy et al. 2019). Moreover, the paraHVC, an HVC-adjacent neural node important in song production, is completely lacking in female Zebra Finches (Olson et  al. 2011). Similarly, in Marsh Wrens (Cistothorus palustris), males in western populations produce larger song repertoires and have larger HVC and RA volumes than males of eastern populations, while females do not sing and show no detectable geographic differences in these neuromorphological measures (Brenowitz et al. 1994). Previous studies have focused disproportionately on songbird species in which only males sing, providing a potentially biased perspective on the neuroanatomy of a “typical” songbird brain (Riebel et al. 2019; Rose et al. 2022). Female song is much more widespread than previously thought and, furthermore, singing by both sexes appears to have been the ancestral state in passerines (Price et al. 2009; Odom et al. 2014). Consistent with this idea, both males and females develop equivalent neural song production systems during early embryonic development, which subsequently atrophy in females of species that lack female song (Konishi and Akutagawa 1985). Thus, differences between the brains of adult males and females in most

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songbirds appear to be largely a product of selection against these neuroanatomical structures in females rather than selection favoring them in males. Comparisons of neuroanatomy among songbird species have shown that song control region volumes in the brains of adult males and females roughly correlate with their relative vocal outputs and complexity (MacDougall-Shackleton and Ball 1999). Males and females have similar song nuclei volumes in species in which both sexes have similar song repertoire sizes, whereas females have much smaller regions in species in which they sing less than males (Brenowitz and Arnold 1986). In duetting Rufous-and-white Wrens (Thryophilus rufalbus), for instance, females produce song repertoires with significantly fewer song types than do males and likewise have song control nuclei that are roughly half as large (Brenowitz and Arnold 1986). Sexual dimorphisms in neuroanatomy may largely reflect differences between the sexes in their vocal behaviors, which likely depend on their roles in territorial defense and mate attraction (Riebel et al. 2019; Rose et al. 2022). Nevertheless, this relationship between neuroanatomy and relative vocal complexity appears to be more intricate than some of the previously mentioned studies suggest. In some duetting species where males and females produce song repertoires of similar size and complexity, females nevertheless have significantly smaller song nuclei (HVC and RA) than do males, including smaller and fewer neurons (Gahr et al. 1998). Despite evidence that female song nuclei tend to be larger in species in which females sing, multiple studies have found little correlation between the degree of sexual dimorphism in brain nuclei and the song output or repertoire sizes of females (Gahr et al. 1998; Jawor and MacDougall-Shackleton 2008; Hall et al. 2010; Lobato et al. 2015). Even in taxa in which females sing more than males, such as Streak-backed Orioles [Icterus pustulatus (Price et al. 2008)], males still have significantly larger song nuclei compared to females relativized to body size (Hall et al. 2010). Thus, although a threshold in song nuclei size is presumably necessary for song production, comparative evidence suggests a minimal direct relationship between the sizes of neural nodes and vocal complexity across species (Lobato et al. 2015). Singing appears to involve similar brain centers in males and females, but we still have much to learn about how fine-scale similarities and differences in these macro- and microstructures between the sexes and across species affect the behaviors of males and females (Rivera-Cáceres and Templeton 2019).

1.4.3 Endocrine Modulation of Neural Function Involved in Acoustic Signaling In most species that use acoustic signals, avian and otherwise, individuals exhibit seasonal changes in their rates of signal production (Bradbury and Vehrencamp 2011). For example, male Song Sparrows (Melospiza melodia) are more likely to sing during the breeding season (early spring) compared to other times of the year (Smith et al. 1997a). This seasonality occurs in large part due to environmentally induced hormonal changes—particularly steroid hormones such as androgens and estrogens. These steroids are present in both males and females of most if not all

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vertebrates that vocalize. Steroids have two mechanisms of action at the cellular level. First, many steroids have membrane-bound steroid receptors that are responsible for rapid modulation of neural excitability in steroid receptor-rich brain regions (O’Connell and Hofmann 2012; Tobiansky et al. 2018). Second, cytoplasmic and nuclear steroid receptors act as transcription factors, thereby affecting the expression of thousands of genes and altering wide-ranging molecular cascades and cell signaling pathways. This second mechanism of action is typically slower (hours to days) and tends to cause longer-term organizational changes in these cells (Heimovics et al. 2015). Steroids have important and well-documented influences on neural function through the organization of the brain during development to “masculinize” or “feminize” the brain and behavior (Cooke et  al. 1998; Schwarz and McCarthy 2008; Balthazart et al. 2009; Peper and Koolschijn 2012). This early organization of the brain in songbirds is more complicated and less reliant on steroids than brain development in mammals and other taxa (Gurney and Konishi 1980; Konishi and Akutagawa 1985; Arnold and Breedlove 1985; Gahr 2007). In adult songbirds, steroids can influence neural organization and function by affecting the size of song nuclei (Thompson et al. 2007) and directly modulating neuronal activity in adulthood. Circulating gonadal and adrenal steroids cross the blood–brain barrier and affect steroid-sensitive brain regions, and steroid concentrations in turn are affected by seasonality. For example, in White-crowned Sparrows (Zonotrichia leucophrys), a temperate songbird, testosterone alters the size of Area X, HVC, and RA (Thompson and Brenowitz 2010). However, many temperate bird species show socio-sexual acoustic behaviors outside of their breeding seasons, suggesting either a limited role for steroid hormones or a separate pathway of steroid synthesis that is not reliant on the gonads. The latter hypothesis has garnered a lot of support, as there is increasing evidence suggesting that steroids are created from precursors or de novo in the brain (neurosteroids) and other extragonadal tissue (Soma et al. 2003; London et al. 2006; Tobiansky et al. 2018, 2020a; Tomm et al. 2022; Schuppe et al. 2022b), which can have significant effects on motivation and territoriality (e.g., Tomm et al. 2022). Regardless of whether it is a species where just one sex (typically the male) sings, or if both males and females combine their songs in a duet, the song nuclei and actuator muscles in both sexes are highly sensitive to steroid hormones (Frankl-Vilches and Gahr 2018; Tobiansky et al. 2020b; Tobiansky and Fuxjager 2021). The two main steroid families that modulate socio-sexual behaviors such as bird song are androgens and estrogens, with the two most bioactive steroids from these families being 5α-Dihydrotestosterone (DHT; a metabolite of testosterone) and 17β-estradiol (E2), respectively. In male birds with well-defined breeding seasons, gonadal androgen production significantly increases at the beginning of the breeding season, which generally coincides with longer photoperiods (Smith et al. 1997b). This increase in gonadal androgens increases acoustic territorial behaviors, which is associated with mate attraction and mate guarding (reviewed in Soma 2006; Soma et al. 2008; Frankl-Vilches and Gahr 2018). The androgenic effect on singing behavior has been well described, with century-old research showing that androgens can

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induce singing in female Domestic Canaries (Serinus canaria domestica) (Leonard 1939). John Wingfield and colleagues have repeatedly demonstrated that androgen levels are sufficiently high during the breeding season to maintain breeding behavior, but androgen levels will increase even further during times of social instability or territorial challenges, which then invigorates the singing response and other aspects of territorial aggression (Wingfield et al. 1990; Goymann et al. 2007). This phenomenon is known as the “challenge hypothesis” and has also been shown to explain aspects of avian female-female competition as well and is still an active area of research (Wingfield et al. 1990; Rosvall et al. 2020; Lipshutz and Rosvall 2020). The challenge hypothesis predicts that a transient increase in steroids should be “sensed” by brain nuclei that are responsive to small changes in local steroid concentration. Therefore, the neural nodes involved in territorial (and possibly coordinated) behavior should have high concentrations of genomic and non-genomic steroid receptors. This hypothesis would also account for differences in steroid receptors between regions and explain why they might fluctuate throughout the breeding and non-breeding seasons (Soma et al. 1999; Schlinger 2015; Wingfield et al. 2018). For example, female birds that sing often show a similar increase in song during the breeding season when androgens and estrogens are at their peak (Rouse 2022), and females of some species will also sing outside of the breeding season in response to female intruders (Cain and Langmore 2015). Together, these studies suggest that steroids affect coordinated acoustic behavior by modulating the function of steroid-sensitive brain nuclei that are central nodes of the song control system. Indeed, both estrogen and androgen receptors (ERs and ARs) have been identified throughout the neural nodes of the song control system as well as the auditory processing nodes in male and female birds. In both circuits, most neural nodes contain ARs and ERs. Specifically, they have been found to be expressed in the medial geniculate body, inferior colliculus (ICo), RA, lMAN, Area X, and NCM (Gahr 2001; Frankl-Vilches and Gahr 2018). Furthermore, both steroid receptors are expressed in the adult and developing HVC, and they are thought to play a key role in the development of the HVC (Brenowitz 2004). By contrast, the lMAN does not appear to express any form of the estrogen receptor (neither ERα nor ERβ); however, it does robustly express the androgen receptor (Ball et  al. 1999; Perlman et al. 2003). The distribution and concentrations of steroid receptors exhibit significant sexual dimorphism across various brain regions in avian species. Generally, AR concentrations are notably higher in male birds than in their female conspecifics. This sex-­ specific disparity in AR concentrations could potentially be attributed to the differential exposure to testosterone during developmental stages and throughout adulthood (Gahr and Metzdorf 1997; Soma 2006; Fraley et al. 2010). In particular, the HVC, RA, and lMAN (i.e., the principal nodes of the song system) of male birds exhibit elevated AR concentrations compared to that of female birds, suggesting a possible role of testosterone in modulating song production and learning (Metzdorf et al. 1999; Gahr 2001). In particular, the paraHVC, a region important for song reproduction, has been shown to be highly concentrated with ERs, suggesting a

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significant role for estrogens in reproducing the partner’s song (Häring 2012). In addition to these major nodes, other parts of the song control system, such as Area X, the Uva, and the DM-ICo, also show sexual dimorphism in the distribution of steroid receptors (Gahr 2007). For instance, Area X has higher concentrations of ARs and ERs in males compared to females (Frankl-Vilches and Gahr 2018). Importantly, these sex differences have been found in all taxa that have been examined in the class Aves. These findings suggest a complex interplay between steroids, steroid receptor concentrations, and their distribution in the avian brain, which appears to be intricately linked to the control of song production, learning, and behavioral coordination. Specifically, males are likely more sensitive to fluctuations of systemic and local steroids in brain regions associated with coordinated acoustic behaviors compared to females, even in species where females sing.

1.5 Functional Neuroanatomy and Neuroendocrinology of Acoustic Coordination While rigorous examination of the oscine song system has greatly informed our understanding of vocal learning and avian signaling in general, researchers have rarely studied this system in the context of coordinated acoustic behaviors (Hall 2009; Logue 2021). The research that has been done has focused on the neural nodes associated with temporal coordination of acoustic behaviors. In this section, we discuss the specific regions that play a direct role in duetting or other coordinated sonations. So far, research has revealed little about how endocrine signaling modulates these behaviors. Therefore, we focus on how steroid signaling modulates the development and activity in the regions known to control coordinated behaviors.

1.5.1 Functional Neuroanatomy Brain nuclei in both the song production and auditory processing systems are necessary for intersexual, and presumably intrasexual, coordinated acoustic behaviors. The most studied, and perhaps most important, brain regions for coordinated vocal behavior are the HVC and directly afferent brain regions. The production and timing of vocal coordination is regulated by the HVC and descending forebrain projections. For example, although Zebra Finches are not known to duet, both males and females produce simple, alternating vocalizations that are important during intersexual social interactions. In a study of vocal coordination, Benichov et al. (2016) used a precisely controlled, call-producing robot bird to explore how disruptive masking (i.e., “jamming”) with well-timed artificial vocalizations affects the timing and interplay of male and female calls. The researchers found that both males and females can learn to anticipate the disruption and adjust their timing within minutes of being exposed to this stimulus. However, a complete bilateral transection of descending connections from the HVC to the RA in Zebra Finch causes a loss of precision and anticipation in both sexes. Moreover, bilateral lesions of the RA

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decrease both sexes’ abilities to anticipate the jamming signal and call precision (Benichov et al. 2016). In duetting species, neurophysiological recordings in the song control regions of males and females have revealed complex neural mechanisms mediating the production of precise, antiphonal duets (Fortune et  al. 2011; Coleman and Fortune 2018; Hoffmann et al. 2019; Coleman et al. 2021). In wild, freely moving Plain-­ tailed Wrens (Pheugopedius euophrys), for example, the HVC becomes active while both males and females are signaling during a duet but are inhibited while listening to the partner’s song (i.e., “heterogeneous feedback”) (Coleman et  al. 2021). However, if the bird’s own song is played back to them during a duet (i.e., “autogenous feedback”) this inhibitory effect is only present in females, suggesting sex specificity in duetting circuitry. Similar findings have been reported by Hoffmann et al. (2019) in free-living White-browed Sparrow-weavers (Plocepasser mahali). With these technological innovations to measure neural activity in pre-motor regions in free-living birds, we now have a better (but still incomplete) understanding of the role that the HVC plays in regulating coordinated vocal behavior. Other regions appear to be involved in coordinated acoustic behaviors in birds, but their exact roles are not as clear as the examples given above. Along with the HVC, the other neural nodes of the song control network seem to play an outsized role in vocal coordination and duet learning. For example, directed singing (singing toward a conspecific) in Zebra Finch has a different ZENK expression profile in the anterior forebrain pathway (i.e., Area X, DLM, and lMAN) compared to undirected singing (singing in the absence of conspecifics) (Jarvis et al. 1998). These results suggest that the anterior forebrain pathway is responsible for mediating directed songs, which are essential for harmonizing intricate duets and ensuring proper synchronization of the performance, leading to a blend of both signals. Furthermore, adaptive auditory processing is also required for the receiver to engage in coordinated acoustic behaviors (see Elie et al. 2019 for review). However, other research must be done to determine how other nuclei involved in sensory integration and song modulation act during these intersexual coordinated behaviors (Rivera-Cáceres and Templeton 2019). Similar regions seem to be involved in non-vocal acoustic coordination in other avian taxa outside of oscine passerines. Recently, Schuppe et  al. (2022a) have shown that an lMAN-like area is highly active during drumming behavior in Downy Woodpeckers (Dryobates pubescens). Drumming in woodpeckers is a form of territorial behavior but also serves as a contact signal between the individuals of a breeding pair (Schuppe et al. 2016). To determine the role of this region in coordinated acoustic behaviors, Schuppe et  al. (2022a) examined transcription of an immediate early gene Egr1 (used as a proxy for neural activation) after a simulated territorial intrusion, and the homology of the lMAN-like region was determined by transcriptional markers seen in the lMAN of Zebra Finch and other well-studied songbirds. Another bird, the suboscine Bearded Manakin (Manacus spp), also exhibits coordinated non-vocal sonations. They are a lekking species, whereby colorful males perform acrobatic mating courtship displays and produce unique firecracker-­like sounds called the jump-snap and rollsnap (Tobiansky et al. 2020b;

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Fuxjager et al. 2022). To produce this rollsnap, they bang their wrists together at a rate of up to 70 Hz. This acoustic behavior rolls through the lek once a female is spotted, cascading from the first male to those farther away (personal observation). However, these suboscines lack many of the brain structures that are present in songbirds that duet. Accordingly, Day et al. (2011) found that male Golden-collared Manakins (Manacus vitellinus) did not have evidence of a pre-motor RA-like region in the male arcopallium; yet males do have larger arcopallium relative to overall brain size compared to females. Furthermore, correlational data across taxa in the family Pipridae (including Manacus) suggest that males show an increase in relative brain size as display complexity increases (Lindsay et al. 2015; Day et al. 2021). To our knowledge, these studies did not find or analyze any HVC- or lMAN-like regions in these birds, but these findings do not preclude the possibility that other brain regions are acting as functional homologs—they may yet exist but remain undiscovered. Given the difficulty of a neuroethological approach with these birds, there is a significant gap in our knowledge on cellular and systems neuroscience of rollsnap behavior in Manacus and drumming behavior in woodpeckers.

1.5.2 Neuroendocrinology Neuroendocrine signaling likely plays a significant role in modulating coordinated acoustic behaviors. For example, administration of exogenous androgens can provoke male and female song in the duetting White-browed Sparrow-weaver (Voigt and Leitner 2013). But the relationship between song and androgens is convoluted, as exogenous androgens tended to elicit a male-like song in the females of this species. Moreover, very little is known about how hormones modulate relevant neural circuits within the context of these behaviors. The obvious nuclei to examine first are the HVC and RA (Benichov et al. 2016; Coleman et al. 2021). In a comparative study of steroid receptors across passerine clades by Frankl-Vilches and Gahr (2018), there was nothing particularly unique about the distribution of ERs and ARs in the HVC or RA of duetting species (e.g., White-browed Sparrow-­weaver) compared to non-duetting songbirds. The researchers instead argue that species-specific song stems from unique patterns of hormonal regulation and regional genomic sensitivity (species differences in transcriptional regulation) to steroids (Frankl-Vilches and Gahr 2018). While the direct action of steroids in the HVC and RA in birds that coordinate their acoustic behavior is poorly understood, we can glean insights into how steroids affect these behaviors by examining how steroids influence the function of the male and female song control system. In canaries, for example, blocking AR in the HVC increases variability in syllable sequence, thereby disrupting temporal fidelity of the song, whereas blocking it in the RA leads to an increase in variation in song stereotypy (Alward et al. 2017). Chronic and acute systemic testosterone increases spontaneous firing rate and soma size in the RA and directly impacts song stereotypy (Meitzen et al. 2007; Thompson et al. 2007). Moreover, exposing RA neurons to the AR antagonist flutamide prevented the increase in firing rate and

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soma size that was induced by testosterone. This suggests that activation of ARs in RA is permissive for RA to respond to the neurotrophic signal arriving from HVC.  These findings are consistent with other studies that show that the size of these song nuclei responds to increases in circulating androgens (Tramontin et al. 2003), and spontaneous RA activity is higher during the spring breeding season in songbirds when androgens are at their peak (Meitzen et al. 2009). These findings suggest that androgens in the HVC and RA directly affect vocal plasticity necessary for precise timing in coordinated acoustic behavior. Similarly, estrogen signaling in the song control circuit likely plays a pivotal role in modulating coordinated sonations. While much focus has been on the effects of circulating and exogenous androgens on song, researchers have repeatedly shown that the HVC and NCM (a node of the auditory processing circuit) are sensitive to estrogens. These regions also express the steroidogenic enzyme aromatase [i.e., CYP19A1 (Soma et al. 2003; Heimovics et al. 2012)], which converts androgens into estrogens locally. Systemic and intracranial aromatase inhibition alters the frequency, duration, and composition of directed song or vocalizations in male and female Canaries (Alward et  al. 2016), Song Sparrows (Soma et  al. 1999), Zebra Finch (Choe et al. 2021), and a wide range of other songbirds and non-passerines (reviewed in Cornil et al. 2015; Spool et al. 2022). Further research has repeatedly shown aromatase and neuroestrogens (local estrogen synthesis catalyzed by aromatase) are central to the function of the songbird song circuit by acting as rapid, hyperlocal neuromodulatory signals in the NCM and HVC (Vahaba and RemageHealey 2018). Neuroestrogen signaling in the NCM affects song selectivity and song preference (Remage-Healey and Joshi 2012), which is essential for song coordination. In a similar vein, Meitzen et al. (2007) take it a step further and state that estrogen signaling (and perhaps neuroestrogens) in the HVC likely also regulates “syllable-type usage variability, syntax, and temporal aspects of trills.” Furthermore, they have proposed that androgens and estrogen signaling in the HVC leads to the generation of neurochemical signaling that acts on neurons in the RA. Importantly, they posit that sufficient AR binding in RA allows for the signal from the HVC to exert its effect on song output. This is likely the case for songbirds that also engage in coordinated vocal behaviors such as duetting. Taken together, these studies, along with others (e.g., Soma et al. 1999) suggest that androgens and estrogens work synergistically in controlling vocal behavior and perhaps coordinated acoustic behaviors.

1.6 Conclusion Coordinated acoustic signals are among the most complex forms of animal communication, involving more than just the combining of motor patterns between individuals. Duetting songbirds, for example, appear to adjust their notes with rapid precision in response to those of their duetting partner (Fortune et al. 2011; Coleman and Fortune 2018; Hoffmann et al. 2019; Coleman et al. 2021), essentially functioning as a flexible neural song control system spanning two individuals (Elie et al.

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2019). Studies are just beginning to reveal the neural structures and endocrine pathways underlying acoustic coordination (Benichov et  al. 2016; Elie et  al. 2019; Rivera-Cáceres and Templeton 2019; Coleman et al. 2021). Yet, we still have much to learn. Although studies have investigated the role of the HVC during signal coordination (e.g., Coleman et al. 2021), the importance of other brain regions during counter-singing or duetting is virtually unknown and should be a focus of future investigations. Future studies should likewise focus on the role of neurosteroids and the expression of steroid hormone receptors in the brain regions involved in these behaviors. We are also just beginning to understand how these pathways might differ between the sexes. Widespread evidence has revealed sexual dimorphisms in the neuroanatomy of species in which both sexes regularly sing, including duetting songbirds (Gahr et al. 1998; Jawor and MacDougall-Shackleton 2008; Hall et al. 2010; Lobato et al. 2015), but questions still remain. Do males and females employ different hormones and neural circuitry to produce identical sounds? Does the neural circuitry involved in signal perception also differ between the sexes? Moreover, given evidence that learning is involved in the development of well-coordinated displays (Hall 2009; Rivera-Cáceres et  al. 2016, 2018; Rivera-Cáceres and Templeton 2019) do males and females learn in similar ways? Addressing these and other questions will undoubtedly provide exciting new insights into the mechanisms underlying behavioral coordination, in birds and perhaps in humans too. Key Literature 1. Leonard (1939), is one of the earliest studies showing that androgens can induce singing in female Domestic Canaries. This finding laid the groundwork for understanding the hormonal control of bird song. 2. Soma et al. (1999), was one of the first studies to provide evidence for the role of locally produced steroids (i.e., neurosteroids) in modulating the function of steroid-­sensitive brain nuclei that are central nodes of the song control system. This work has contributed to our understanding of how hormones influence bird song. 3. Coleman et al. (2021), was one of the first studies to investigate neuronal activity in freely moving duetting birds by implanting electrodes in the HVC of wild-­ caught male and female songbirds. 4. Benichov et al. (2016), is key as it is the first evidence of the role of the forebrain song system in mediating predictive call timing in both male and female zebra finches, suggesting a shared, predictive mechanism for vocal coordination. This work is particularly relevant to understanding the neural mechanisms underlying duetting and other coordinated vocal behaviors in birds. 5. Gahr et al. (1998), was the first paper to describe sexual dimorphism in brain nuclei that control song (HVC and robust nucleus of the arcopallium) in duetting songbirds. They find that, similar to non-duetting songbirds, these neural nuclei are significantly larger in males even though there is no sex difference in vocal repertoires.

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Adult Social Relationships in Primates Claudia Manca and Karen L. Bales

Abstract

Like other animals, primates tend to live in social groups where they communicate with one another and interact in both agonistic and affiliative ways. Primates are capable of forming various social bonds that can impact the individual’s health and well-being. Social behavior is flexible and dynamic, and the social organization of primates is complex. Primates of different species form various types of bonds with conspecifics. These relationships include pair bonds, friendships, coalitions, and other bonds among kin. Social relationships are a critical component of group life, where affiliative or aggressive interactions can have fitness consequences on the individual. In mammals, these different types of social relationships are regulated by different hormonal systems such as the oxytocin and vasopressin systems. The goal of this chapter is to provide a deeper understanding of different types of adult social relationships in primates by reviewing the variation in primate social behaviors and the neurobiology underlying it.

C. Manca Department of Psychology, University of California, Davis, CA, USA e-mail: [email protected] K. L. Bales (*) Department of Psychology, University of California, Davis, CA, USA Department of Neurobiology, Physiology, and Behavior, University of California, Davis, CA, USA California National Primate Research Center, Davis, CA, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 H. K. Caldwell, H. E. Albers (eds.), Neuroendocrinology of Behavior and Emotions, Masterclass in Neuroendocrinology 16, https://doi.org/10.1007/978-3-031-51112-7_2

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Keywords

Social behavior · Primates · Neurobiology · Pair bond · Coalitions · Friendships

2.1 The Large Variety of Adult Social Relationships in Primate Societies Social interactions are a key component of group-living in primate societies. Interactions between individuals, especially interactions with others in a non-­ agonistic manner and affiliative manners, have fitness consequences (Ellis et  al. 2019). In fact, well-connected individuals can live longer and produce more offspring than less well-connected individuals (Mitani et al. 2012). There are various ways in which sociality develops, depending on individual differences within primate societies and differences between species (Mitani et  al. 2012). Aspects of diversity include spacing, mating patterns, and grouping, as well as variability in patterns and quality of social relationships (Kappeler and van Schaik 2002). Many group-living primates develop species-typical systems of hierarchical interactions organized around social dominance (Pereira 1995). In African and Asian monkeys and apes, socioecological models of female social relationships are focused on competition around feeding resources (Sterck et al. 1997). However, one of the most distinct features of animals is their ability to cooperate with one another to reach common goals such as hunting, protection of young, and reproduction (Van Schaik et al. 2006; Higham and Maestripieri 2010). When individuals form coalitions, we witness an additional subset of cooperative behaviors between members (Higham and Maestripieri 2010). Some of the most astonishing coalitions have been observed in nonhuman primates, and are therefore extensively studied in this group (Higham and Maestripieri 2010). In contrast to theories based on female competition, there is evidence that in many primate species females form cooperative relationships. Female baboons, macaques, and vervets present a remarkable example of the complex adaptive design of social relationships in primates (Silk 2007). Females can discriminate among potential partners and exhibit strong biases in favor of close maternal kin and other females close to their dominance rank and age (Silk et al. 2006a, b). Some female primates form mutualistic coalitions with nonrelatives, as these coalitions produce stable nepotistic hierarchies (Pereira 1995; Sterck et al. 1997). There is also evidence that female baboons form relationships that fulfill most of the characterizing criteria for friendship (Silk et al. 2006a, b). Female baboons are also able to form strong bonds with close maternal and paternal kin, age mates, and other females who possess similar ranks but are not maternal kin (Silk et al. 2006a, b). The social organization of a species sets the background for the development of intra-species relationships. The vast majority of primates live in bisexual groups with three adults or more, which sets them apart from other mammals in which permanently bisexual groups are much less common (Van Schaik and Kappeler 1997). Accordingly, polyandrous, polygynous, multimale, and multifemale groups have been distinguished (Crook and Gartlan 1966; Eisenberg et  al. 1972;

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Clutton-­Brock and Harvey 1977). Variation in group size is another aspect of diversity in the social organization of group-living primates (Kappeler and van Schaik 2002). Interestingly, as a group, primates also have a higher proportion of species characterized as monogamous (~15%), compared with other mammals (between 3 and 5%) (Kleiman 1977; Munshi-South 2007; Díaz-Muñoz and Bales 2016). Here, social units consisting of one adult male and one adult female constitute the predominant social organization (Van Schaik and Kappeler 2003). Male and female dyads in socially monogamous species often form pair bonds (Carp et al. 2016). Pair bonding is a key behavioral concept that has been well studied particularly in behavioral neuroendocrinology (Bales et al. 2021). Various types of social relationships are unpinned by several interacting hormonal systems (Ziegler and Crockford 2017). The study of neurobiology along with behavioral studies is critical to deepening our understanding of the various social relationships that primates are capable of forming.

2.2 Pair Bonding 2.2.1 Behavioral Studies In species where they occur, pair bonds (selective attachments between two individuals) are among the most critical social relationships for health and well-being (Bales et al. 2017). Pair-bond relationships are usually observed in pair-living species that are also socially monogamous (Tecot et al. 2016). Pair bonds are stable adult attachments and are characterized by spending time in extended physical contact and physical proximity with a pair mate (Carter et al. 1995). Most definitions of pair bonds agree that a pair bond is a selective association between two adults of the same species (Kleiman 1977; Black 1996; Nowicki et al. 2020; Bales et al. 2021). The quality of a pair bond is strongly associated with important survival outcomes including lower mortality rates (Coyne et  al. 2001; Kiecolt-Glaser et  al. 2003), faster recovery from injury (Kiecolt-Glaser et al. 2005), and decreased risk from infection (Robles and Kiecolt-Glaser 2003; Bales et al. 2017). Behaviors identified in pair bonds include a preference for their partner compared to alternative mates [e.g., titi monkeys (Carp et al. 2016) and prairie voles (Cho et al. 1999)], proximity, shared territory, joint display, and certain types of affiliation such as allopreening or allogrooming (Bales et  al. 2021). Mating behavior and sometimes even sexual exclusivity are included in some definitions of pair bond, as well as aggression toward strangers, or territorial defense (Bales et al. 2021). Within the order of primates, scientists have suggested that behaviors that accompany pair bonds would involve bond-reinforcing species-specific behaviors such as duetting, partner contact behaviors, mutual displays (Anzenberger 1988; Palombit 1999), and other behaviors like food sharing and grooming (Fuentes 2002; Bales et al. 2021). According to a definition of a primate pair bond by Fuentes (1998), there are only a few species of primates that demonstrate pair bonds: genuses Callicebus and Plecturocebus (titi monkeys), genus Aotus (owl monkeys), Indri indri (indris), and Avahi laniger (the eastern woolly lemur). Bales et  al. (2021) proposed in their

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article a new definition of pair bond and provided a list of behaviors that may be used as a guide to identify species that may form pair bonds. They defined pair bonding as a psychological construct that can be measured only through behavioral observations or physiology. They argued that a pair bond must include at least some affective component such as arousal, attraction, motivation, and aversion (Bales et al. 2021). Furthermore, a pair bond must continue for a relevant duration of time, specifically the relationships between two individuals must persist longer than one reproductive cycle (Bales et al. 2021). In addition, they proposed that pair bonds must have some degree of strength or quality that can be measured, that both individuals must be sexually mature and that the bond must be specific to a certain individual (Bales et al. 2021). According to their definition, pair-bonded individuals may engage in sexual behavior with each other, nor does a sexual relationship need to be exclusive (Bales et al. 2021). Additionally, parenting, or the lack thereof, is not viewed as essential to the pair bond, as parenting involves a relationship outside of the pair bond (Bales et al. 2021). It is important to mention that not all putatively pair-bonding species will display all the behaviors listed by Bales et  al. (2021), rather they presented this list as a guide to identifying species that are capable of forming pair bonds. In laboratory settings, patterns of social attraction are measured using a behavioral paradigm called the partner preference test (Carp et al. 2016; Rothwell et al. 2020). This test has been widely used in rodents and involves a three-chambered testing arena in which the focal animal’s partner and an unfamiliar opposite-sex stranger are restricted to two outside chambers (Carp et al. 2016). The focal animal is then placed in a central “neutral” chamber and allowed to interact with the animals in the two outside chambers or to stay in the neutral chamber of the apparatus (Williams et al. 1992; Carp et al. 2016). Behaviors such as proximity and physical contact are measured, as well as other affiliative or aggressive behaviors exhibited by the focal animal (Carp et al. 2016). One critical component of this test is that the focal animal chooses to spend time in proximity to their partner even when given the choice to spend time alone or with a stranger (Bales et al. 2021). In order to provide evidence of a pair bond, during tests of separation distress, the behavioral or physiological response shown needs to be specific to the pair mate and not eliminated by another familiar figure or a familiar environment (Mendoza and Mason 1986). Furthermore, the ability to buffer stress should also be specific to the partner (Hennessy et al. 2009). The relationship between social structure and pair bonding is complicated; most pair-bonding species are socially monogamous, but not all socially monogamous species demonstrate pair bonds and many have not been studied for the characteristics of pair bonding described in the previous paragraph (Bales et al. 2021). There have also been several mammalian species that were thought to be monogamous and pair bonding but have later been shown to display polygyny and sexual promiscuity under different conditions (e.g., wild vs. captivity) (Cavallini 1996; Tardif et al. 2003). One group of primates that has generated considerable debate are the marmosets and tamarins (family: Callitrichidae) (Bales et  al. 2021). While older literature claimed that marmosets are socially monogamous and form pair bonds,

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recent research agrees there is variability in wild marmoset and tamarin group structure, which may have implications for the development of pair bonds (Díaz-Muñoz 2016; Garber et al. 2016). Callitrichid social structure may be monogamous, polygynous, or polyandrous depending on the different circumstances and history of the group (Garber et al. 2016). Many species of gibbons (family: Hylobates) also demonstrate preferential pair living and pair behavior (Choudhury 1990; Cheyne 2010), but there have also been documented cases of fluid sociosexual structure which tend to be influenced by resource availability (Savini et al. 2009). There is also mixed information on whether sakis (genus: Pithecia) form pair bonds, as some studies found them to form preferential close relationships with their mates (Porter et al. 2015; Thompson 2016) while others debated whether they exhibit enough of the essential pair-bonding behaviors (e.g., mate guarding) to be considered pair bonding (Thompson and Norconk 2011; Porter et al. 2015; Thompson 2016). Some species of lemurs have also been proposed as pair bonding (Tecot et al. 2016). The red-bellied lemurs (Eulemur rubriventer) exhibit different intrapair behaviors that stipulate the possibility of a pair bond such as pair-specific vocalizations, territorial defense, and other pair-specific behaviors (Tecot et al. 2016; Grebe et  al. 2021). However, Grebe et  al. (2021) examined the distribution of oxytocin (OT) and vasopressin (AVP) in two monogamous and five non-monogamous Eulemur species in the brain and found that OT and AVP receptor distribution differed only minimally. This finding was unexpected given the striking differences in OT and AVP receptors between monogamous and non-monogamous voles (Insel and Shapiro 1992), and between monogamous titi monkeys and non-monogamous rhesus monkeys (Freeman and Young 2016). This suggests that perhaps lemurs might not form pair bonds, or alternatively that there could be a distinctive neurobiological mechanism underlying pair bonds in lemurs (Bales et al. 2021). In summary, pair bonds are stable adult attachments that have been demonstrated to be present only in a few primate species that share many behavioral features. Many species have not been sufficiently studied to either prove or disprove the existence of a pair bond. Exploring the neurobiological mechanisms regulating these behaviors is critical to better understand the underpinnings of pair bonds in primates.

2.2.2 Neurobiology/Endocrinology OT and AVP are evolutionarily conserved neuropeptide hormones involved in mammalian reproduction and implicated in the regulation of mammalian social behavior (Campbell 2008; Declerck et al. 2010). These two hormones are highly conserved across species in terms of function and structure (Campbell 2008). Therefore, it is thought that they are related to the development and maintenance of affiliative social relationships in many animal species (Massen et al. 2010b). In general, AVP has been studied for modulating several behaviors exhibited at higher frequencies by males, although this may also partly reflect a bias in the literature (Goodson and Bass 2001). Pharmacological blockade of either neuropeptide in either sex resulted in loss of the pair bond in prairie voles (Cho et al. 1999).

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Peripherally, OT regulates uterine contractions and milk production during lactation, while central OT acts as a neuromodulator (Campbell 2008). Central release of OT can be induced by reproductive and sexual stimuli such as olfactory stimuli, copulation, genital, and breast stimulation, and by non-sexual stimuli such as grooming and exposure to offspring (Campbell 2008). Both OT and AVP appear to be key mediators of mammalian pair bonding (Dębiec 2007) and their importance has been well established in prairie voles (Microtus ochrogaster) (Aragona and Wang 2004; Ross and Young 2009), despite recent evidence that knockout of OT receptors does not eliminate pair bonding in prairie voles (Berendzen et al. 2022). Moreover, OT and AVP are known to play roles in human sexual behavior, but they are also important for several nonsexual features that differentiate pair bonds from other sexual relationships (Bales et  al. 2017). For example, studies have shown higher plasma OT levels in newly formed couples than in single participants (Schneiderman et al. 2012, 2014; Ulmer-Yaniv et al. 2016), with new couples with higher plasma OT levels having higher interactive reciprocity including affectionate touch, positive affect, social focus, and synchronized dyadic states (Schneiderman et al. 2012). Research in nonhuman primates has been able to deepen our understanding of neural circuits involved in pair bonding (Bales et al. 2021). Relationship formation in titi monkeys (Plecturocebus cupreus) is supported by the dopaminergic reward system, with newly paired males showing higher levels of D1 receptors in the lateral septum (Hostetler et al. 2017), as well as increased activity in the nucleus accumbens (NAc) and ventral pallidum (Bales et al. 2007, 2021; Maninger et al. 2017). The dopamine (DA) system also plays a role in prairie vole and human pair bonding (Bales et al. 2017). DA is released in the NAc in response to mating in prairie voles, and this increase is essential for the formation of a pair bond (Aragona et al. 2006). The use of a D2 (but not D1) receptor antagonist is enough to prevent the formation of a pair bond in prairie voles (Gingrich et al. 2000), suggesting the importance of D2 receptors in the formation of pair bonds (Bales et al. 2017). On the other hand, D1 receptors are upregulated in the NAc following the establishment of the pair bond, and their activity contributes to the maintenance of the bond by causing aggressive behaviors in bonded prairie voles toward opposite-sex strangers (Aragona et al. 2006). In titi monkeys, D1 receptors are also important for maintaining a pair bond as they regulate mate-guarding behaviors, suggesting that the dopaminergic reward system plays a critical role in the agonistic components of pair-bonding maintenance (Rothwell et al. 2019). In addition to the neurotransmitters mentioned above, literature on mammalian social attachments supports the importance of opioids for the formation and maintenance of pair bonds (Bales et al. 2017). Due to their role in affective responses, activation of μ and κ opioid receptors may assist different features of pair bonds in monogamous species (Bales et al. 2017). A study suggested that μ opioid receptors could be important for the formation of a pair bond in prairie voles due to the regulation of pleasant affective responses (Resendez et  al. 2013). Affiliative behaviors such as grooming and invitations to be groomed naturally released β-endorphin, and

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overactivation of μ opioid receptors decreases the need for further grooming in primates (Keverne et al. 1989). On the other hand, activation of κ opioid receptors may be responsible for pair bond maintenance due to their role in producing unpleasant affective responses to stressors (Bales and Rogers 2022). This means that κ opioid receptors may mediate the dysphoric effects of separation from a partner (Resendez et al. 2016). Endocrine responses to separation from and reunion with a pair mate may help demonstrate emotional attachments exclusive to the pair mate (Huck et al. 2020; Bales et al. 2021). The maintenance of a pair bond also requires mate guarding, which is associated with novel social stimuli that are processed as aversive (Resendez et  al. 2012). Resendez et al. (2012) showed that κ opioid receptors within the NAc shell are also important for this behavior in prairie voles, as the blockade of κ but not μ opioid receptors mediated mate guarding in both sexes. Both κ and μ opioid receptors located in the limbic regions are likely important for various aspects of pair bonding in nonhuman primates as well (Ragen et al. 2015). Specifically, the striatum, the mediodorsal thalamus, and the cingulate gyrus may play various roles in attenuating emotional responses during pair bond formation (Bales et al. 2017). The presence of both κ and μ opioid receptors in the cingulate gyrus, which is an important region for emotion regulation, may help regulate differing responses to a pair mate versus an unfamiliar individual (Bales et al. 2017). In essence, opioid receptors may help regulate both hedonic and dysphoric aspects of pair bonding (Bales et al. 2017). There is also evidence from titi monkeys that disruptions to opioidergic activity through separation from a pair mate result in physiological and behavioral changes including the activation of the hypothalamic–pituitary–adrenal (HPA) axis (Ragen et  al. 2013). Acute administration of μ agonists reduces cortisol concentration in humans (Zis et al. 1984) and macaque monkeys (Broadbear et al. 2004), while naloxone (an opioid antagonist) and naltrexone raise cortisol concentrations in humans (Wand et  al. 1998) and nonhuman primates (Fabre-Nys et  al. 1982). In male titi monkeys, an increase in cortisol was seen in response to naloxone (Ragen et  al. 2013). This increase in cortisol was greater when the animal was tested alone compared to when he was tested with his pair mate (Ragen et al. 2013). These results suggest that having a pair mate present provides a source of social buffering decreasing the aversive components of naloxone (Ragen et al. 2013). There is accumulating evidence that bond partners may moderate the perception of a stressor as well as the physiological stress response modulating the reactivity of the HPA axis (Crockford et  al. 2018). The presence of a mate acts as a buffer against potentially adverse effects associated with prolonged or repeated HPA axis activation (Crockford et al. 2018). A large body of literature has found the neuroendocrine systems, including OT, AVP, DA, and opioids, to underlie the formation and maintenance of pair bonds (Bales and Rogers 2022). Despite evidence for some commonalities in the neurobiology of pair bonding across mammal species, there is still relatively little information from primates, providing many questions for future research (Bales et al. 2021).

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2.3 Family Relationships that Continue into Adulthood 2.3.1 Behavioral Studies Across one’s lifespan, personal relationships provide an important framework for individual well-being and development (Noack and Buhl 2004). Peer relationships can be temporary, while relationships with family are the most durable (Laursen and Bukowski 1997). Over time, the family goes through a variety of transitions that demand adaptive efforts by its members (Parra et  al. 2015). During infancy, the social setting and especially one’s family composition can have a great influence on the individual (Brent et al. 1997). In certain species, different family members such as aunts, grandmothers, and older siblings may influence the opportunity for social interaction, learning, survival, and future access to the group (Fairbanks 1993). Family composition and relationships in nonhuman primate species are influenced by which sex disperses at maturity. In some nonhuman primate species, males tend to leave the group at puberty, and do not usually associate with female relatives even when they do not disperse (McDonald Pavelka 1994). Females, on the other hand, are usually philopatric (e.g., Japanese monkeys, and Macaca fuscata) (Nishikawa et  al. 2014). The social structure of Japanese monkeys is characteristic of most Cercopithecidae; they live in female-bonded groups from which males tend to disperse (McDonald Pavelka 1994). They are sometimes referred to as female-bonded groups because the primary bonds holding the group together are those between related females (McDonald Pavelka 1994). These groups usually consist of mothers, grandmothers, daughters, sisters, nieces, aunts, and so on; with connections between mothers and daughters enduring throughout the lives of the animals (McDonald Pavelka 1994). In these matrilocal primate species, mothers usually form close and enduring ties with their offspring; even when mothers wean one infant and produce another, they still associate with their older offspring (Silk 2009). In vervet monkeys, mothers continue to preferentially associate with their daughters after their daughters have reached adulthood (Fairbanks and McGuire 1986). Fairbanks and McGuire (1986) also found that mothers had an influence on their daughters’ social relationships and reproductive success in their vervet colony, with the presence and support of a living mother doubling the chances for infant survival during the early years of reproduction. In rhesus monkeys (Macaca mulatta), close associations with the mother ensure tight associations with the mother’s associates such as older siblings and mother’s siblings, which shapes the bias toward kin as frequent partners in all forms of social interactions (Bernstein et  al. 1993). Even in chimpanzees, a species in which females disperse, juveniles of both sexes continue to associate frequently with their mothers for years after they are weaned; they observe and participate in social behavior, gaining her support or reassurance in agonistic confrontations with other individuals (Pusey 1983). Some Central and South American monkey species (e.g., Titi monkeys, Plecturocebus cupreus) form small family groups centered around a male-female pair, where offspring of both sexes can remain with the parents until adulthood even

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beyond the age of reproductive maturity without aggression, and in which both sexes of offspring eventually disperse (Mayeaux et al. 2002). Titi monkey offspring form a strong attachment bond with their father, and a weaker bond with their mother; separation from the father, but not the mother, results in behavioral and physiological signs of distress (Hoffman et  al. 1995). In contrast, parents do not form emotional bonds with their offspring and do not respond to separation from their offspring (Mendoza and Mason 1986). Common marmosets (Callithrix jacchus) can also live in small family groups where offspring can remain with the parents indefinitely and where multiple group members including older siblings participate in the care of other dependent infants (Mills et al. 2004). Unlike titi monkey offspring, common marmoset offspring showed no depression reaction during removal of either parent (Arruda et al. 1986). In humans, although the affiliation between parents and minor offspring is to some extent obligatory, there is great variability in the degree to which parents and children remain interconnected during early adulthood (Laursen and Collins 2009). One study explored the organization of attachment hierarchies of young adults (Trinke and Bartholomew 1997). In this study, participants who did not have a close romantic partner ranked their mothers most highly, followed by fathers, and finally peers (Trinke and Bartholomew 1997). A second study found that mothers remain important attachment figures throughout adolescence and even into adulthood, regardless of whether or not participants reported having romantic partners (Markiewicz et al. 2006). This study suggests that mothers generally continue to play an important role in providing a basic sense of security and availability throughout this age range (Markiewicz et al. 2006). On the other hand, fathers were chosen much less often than mothers, but when chosen they served as a secure base component of attachment across adolescence and early adulthood (Markiewicz et al. 2006). Parenting and parent–child relationships can also impact relationship quality with other family members, such as siblings (Feinberg et al. 2012). In humans, harsh and authoritarian parenting is linked to more conflicts between siblings (McHale et al. 2000), while having parents who were able to use mediation strategies to solve disputes was related to more harmonious sibling relationships (Siddiqui and Ross 2004). In general, sibling relationships are the longest-lasting relationships in most people’s lives, yet they have received very little research attention past young adulthood (Stocker et al. 2020). Stocker et al. (2020) found sibling relationships among older adults were characterized by high levels of warmth and low levels of parental favoritism and conflict, suggesting the importance of sibling support later in life. In nonhuman primates, such as chimpanzees, Sandel et al. (2020) found that adolescent and young adult males develop association and proximity bonds with their older maternal brothers. A 10-year study of maternal kin biases among a group of capuchins (Cebus capucinus) found that females selectively groomed and associated with their mothers, daughters, and maternal sisters (full and half-sisters) (Perry et al. 2008). Ring-tailed lemur (Lemur catta) groups also show nepotistic biases in affiliative behaviors, although coalitionary aggression is rare (Nakamichi and Koyama 1997; Sauther et al. 1999). Across the primate order, kinship plays a critical role in structuring the evolution of primate social systems and the consequent

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development of social relationships in primate groups (Silk 2009). Biological kinship has emerged as a primary organizing force in the evolution of primate social organization, with primates being able to distinguish kin from non-kin, and form relationships with their offspring, and other relatives as well (Silk 2009).

2.3.2 Neurobiology/Endocrinology Among primates, the mother is generally the primary target of the infant’s solicitation of care, but in some primate species other group members are also responsive to infants (Fernandez-Duque et al. 2009). In females, mechanisms regulating maternal behavior may originate from processes involved in birth and/or lactation which can cause sudden changes in progesterone, estrogen, OT, and prolactin (Fernandez-­ Duque et al. 2009). A few of the same hormones involved in maternal behavior also appear to be involved in paternal behavior. Although prolactin is not one of the first candidates in paternal care, some studies show fluctuations in prolactin with the event of fatherhood. For instance, among some Central and South American primates that display paternal behavior, adult reproductive males show changes in prolactin levels associated with fatherhood (Schradin et al. 2003). In marmosets and tamarins, fatherhood is associated with increases in prolactin to prevent weight loss during the infant care period and perhaps motivate initiation of infant carrying and contact (Storey and Ziegler 2016). A better candidate for involvement in paternal care is AVP. In male prairie voles, AVP is elevated after mating, promoting partner protection and territoriality (Winslow et al. 1993). Kozorovitskiy et al. (2006) provide evidence for significant structural reorganization in the prefrontal cortex of infant-carrying marmoset fathers and a parallel enhancement in the abundance of AVP V1a receptors. In humans, men who exhibited more stimulating play with their infants had higher plasma AVP levels than other fathers (Apter-Levi et  al. 2014). Another hormone associated with reproduction and infant care is testosterone. There is substantial evidence that testosterone is antagonistic to infant care in many species, and males may have trade-­ offs between parental care and mating (Wingfield et  al. 1990; Ketterson and Nolan 1999). Mothers, and sometimes fathers, continue to furnish support, protection, and comfort for many years after weaning their offspring (Reddy and Mitani 2019). Hormonal changes involved in social interactions between mothers (sometimes fathers) and offspring are also involved in other close relationships (Ziegler and Crockford 2017). In some primate species, offspring of the non-dispersing sex continue to share mother–offspring bonds throughout life, such as mother–daughter relationships in chacma baboons (Silk et al. 2009), and mother–son relationships in bonobos (Surbeck et  al. 2011). To ensure the continuation of nurturing, bonded relationships between offspring of both sexes and their mothers (Curley and Keverne 2005), mechanisms for OT release have likely evolved beyond the known triggers of its release (e.g., labor and suckling), which could explain how adult individuals are able to sustain stable, platonic social ties (Ziegler and Crockford 2017).

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2.4 Friendships 2.4.1 Behavioral Studies Both humans and group-living animals are more inclined to associate and cooperate with some individuals than others (Massen et al. 2010b). As we know, humans are able to form deep intimate relationships with others, and scientists interested in behavior have started investigating close social relationships in animals that could resemble human friendships. If we are interested in using the term friendship to identify certain kinds of social associations in nonhuman primates, it might be helpful to first define what we mean when we use this word to describe human friendships. There is a general agreement that friendships are supportive, intimate, and egalitarian relationships (Silk 2002). In the human literature, some researchers have described different positive features of good friendships that include pro-social behavior, loyalty, self-esteem support, and intimacy, plus other positive features (Berndt 2002). Compatibility is also another important component of friendship, but friends could also experience some degree of tension and conflict between them (Silk 2002). To identify friends in humans, researchers can simply ask the participants who they consider friends. This can provide a picture of the differentiation of relationships from the asked participant’s perspective (Massen et  al. 2010b). However, every individual has a somewhat subjective definition of friendship and who their friends are, therefore a friendship can vary between individuals and across cultures. On the other hand, questionnaires are impossible with animals, therefore researchers studying animal behavior are mostly confined to observational methods (Massen et  al. 2010b). Behavioral experiments that can test cooperation between familiar individuals and non-familiar individuals exist and have been tested in chimpanzees (Engelmann and Herrmann 2016), as well as in other species (Asakawa-Haas et al. 2016; Kozma et al. 2019; Shin and Ko 2021). The different methods used to measure and study friendship in humans and in animals make it more difficult to draw conclusions about differences and similarities between human friendships and animal friendships, although there are general measures of friendship suggested by primate research (Massen et al. 2010b). Researchers interested in the prominence of strong ties between certain pairs of adult females and males in savanna baboon groups were among the first to use the term friendship in describing social associations between nonhuman primates (Silk 2002). A number of other researchers have started using the term friendship to describe close male–female relations that continue beyond the mating period in macaques (Maestripieri 2000), chimpanzees (Hemelrijk et al. 1999), and baboons (Palombit et al. 1997; Silk 2002). According to Silk (2002), primatologists use the term “friendship” in a more general way to describe close and affiliative relationships, which may include same- or other-sex partners. Definitions of friendship in nonhuman primates rely on the frequency and patterning of social interactions through observational methods (e.g., collecting information about the content, quality, and frequency of interactions among individuals)

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(Silk 2002). Grooming and proximity are behavioral measures often used to determine the quality of social relationships in nonhuman primates. There is abundant evidence that physical touch plays an important role in human relationships as well (Massen et al. 2010b). Humans frequently exhibit physical touch in various forms which include cuddling, patting, petting, and similar to animals these types of physical touch are confined to intimate relations (Dunbar 2010). There is some evidence that proximity as a measure is positively correlated with more frequent affiliative interactions and negatively correlated to aggression (Silk 2002). Although these correlations could be related to other variables such as kinship or rank, grooming may be used as a useful index of the nature of social relationships (Silk 2002). Besides looking at the frequency of interactions to identify friends, researchers have also begun to explore methods to assess the quality of social bonds (Silk 2002). Rates of self-directed behaviors such as scratching, yawning, and self-grooming are elevated when monkeys are undergoing a stressor in naturalistic situations (Maestripieri et al. 1992; Castles et al. 1999). Self-directed behavior may provide information about the quality of social bonds between group members (Silk 2002). For example, Castles et al. (1999) compared the rates of self-directed behavior by females when they were near neighbors that were higher ranking or lower ranking than themselves. On average, the rates of self-directed behaviors were 40% higher when the neighbor near them was higher ranking than when the nearest neighbor was lower ranking (Castles et  al. 1999). Their results indicate that self-directed behaviors may be useful to assess relationship quality, although more research is needed to determine whether this measure is valid across taxa (Silk 2002). Friendships also seem to require some degree of selectivity and discrimination, as in many groups not all individuals interact with each other (Silk 2002). For instance, female baboons in Moremi groomed on average only 8 of the other 18 adult females in the group, and half of these females reserved the majority of their grooming to one another female (Silk et al. 1999). So how does one pick friends? Silk (2002) proposed that friendship should be reserved for non-kin relationships that are characterized by frequent participation in affiliative interactions (often including grooming); involvement in coalitionary aggression, such as defending a partner; high rates of association; collective responsibility for maintaining proximity; reciprocity in nonaggressive activities such as food sharing and grooming; continuity across time and context; high degrees of tolerance (for example, around co-feeding), loyalty, and compatibility; and a low degree of stress when together. This definition excludes certain relationships such as females that groom mothers to gain access to an infant, as well as allies (Silk 2002). Male baboons usually form alliances with specific individuals, but do not necessarily spend much time together (Noë and Sluijter 1995), and are not inhibited about fighting with each other or forming coalitions against a previous ally (Noë and Sluijter 1995). Associations between males and estrous females also do not form friendships if the association terminates when the female is no longer receptive (Silk 2002). Silk’s (2002) definition also excludes relationships among kin. According to this definition, if friends are nonrelatives, then friendship would have to be the product

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of reciprocal altruism, which requires a conditional exchange of benefits (Silk 2002). The tit-for-tat rule, in which one begins with behavior benefitting the other and subsequently behaves in the same way as the partner (Axelrod and Hamilton 1981), is one of the simplest rules that results in reciprocal altruism, suggesting animals only give a favor when a favor can be expected in return (Massen et  al. 2010b). Studies of reciprocity in nonhuman primates suggest that immediate contingencies do facilitate altruistic behavior (de Waal 1997a, b, 2000). For instance, chimpanzees are more likely to share food with individuals who have recently groomed them (de Waal 1997b), and capuchins are more likely to reciprocate sharing food with others who have recently shared their food with them (de Waal 1997a, 2000). It is currently unknown how nonhuman primates track these contingencies and are able to maintain reciprocal relationships (Silk 2002). Some researchers have argued that keeping score of reciprocal obligations with different individuals would be a computationally intensive burden on memory, and that it may be beyond the abilities of most animals (Stevens and Hauser 2004; Barrett et al. 2007). Schino and Aureli (2009) argued that animals may use something less cognitively demanding, called emotional bookkeeping, an emotion-based mechanism that would allow animals to keep track of benefits exchanged. This mechanism may be the basis of the primate’s ability to reciprocate over time (Schino and Aureli 2009). Emotional bookkeeping would resonate with evidence that social bonds are associated with trust and relaxation and mediated by reinforcement (Brent et al. 2014). Unexpectedly, reciprocity is not a requirement in human friendships, as it may even jeopardize the friendship (Silk 2002). Clark and Mills (1979) argued that there are two discrete categories of social relationships: exchange relationships and communal relationships. In exchange relationships, the benefits are given with the expectation that they will subsequently be repaid (Clark and Mills 1979). In communal relationships, which characterize family members and friends, each member is more concerned with the other’s welfare and benefits directed to others, not creating the obligation to reciprocate (Clark and Mills 1979). Animals can also show pro-sociality, for instance benefiting another individual without direct reciprocation (Massen et al. 2010b). Pro-social behavior without apparent cost has been shown in various primate species such as the capuchin monkey (Cebus apella) (de Waal et al. 2008); common marmoset (Callithrix jacchus) (Burkart et al. 2007) and long-tailed macaque (Macaca fascicularis) (Massen et  al. 2010a). The scientific study of friendship is still in its early stages, and future studies will be able to improve our understanding of affiliative interactions such as friendships (Brent et  al. 2014). Friendship is a distinctive feature of human behavior, but research is weakening the idea that we are unique in our ability to form friendships and suggests that friendship could be a product of natural selection that served an adaptive function in social animals (Brent et al. 2014).

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2.4.2 Neurobiology/Endocrinology Having friends can enhance physical and psychological well-being and survival (Massen et al. 2010b). In humans, psychological well-being seems to be positively related to friendship activity (McDonough and Munz 1994). There is evidence that having non-kin, platonic friendships can also provide reproductive benefits, such as offspring survival, in nonhuman primates, as well as in other mammals (Seyfarth and Cheney 2012). Beyond parental behavior and pair bonding, nonreproductive social bonds are less studied, perhaps because they are more nuanced (Caldwell 2021). However, some major biochemical systems are believed to be responsible for regulating friendships, including OT, serotonin, endorphins, DA, and the HPA axis (Brent et al. 2014). OT is a major contributor to behaviors involving sociality and friendship, in particular, feelings associated with closeness to others and social bonding (Tarsha 2022). OT has been implicated in behaviors known to be significant for friendships such as generosity (Zak et al. 2007; Barraza and Zak 2009), and social support (Heinrichs et al. 2003; Buchheim et al. 2009). In wild chimpanzees, grooming with a “bond partner” resulted in higher urinary OT levels following grooming, regardless of genetic relatedness (i.e., a friend) (Crockford et al. 2013). AVP plays a role in enhancing recognition of emotional states (Guastella et  al. 2010) and is also involved in social recognition (Bielsky and Young 2004). In rhesus macaques, friendships predicted later concentrations of plasma AVP and OT in sexand friendship-specific ways (Weinstein et al. 2014). In females, OT concentrations were related to both reciprocal and play friendships, while in males, higher plasma AVP was significantly associated with a greater number of friendships (Weinstein et al. 2014). Based on animal studies, it has also been proposed that OT stimulates DA release in the nucleus accumbens and therefore regulates activity in the mesolimbic reward system (Depue and Morrone-Strupinsky 2005; Declerck et al. 2010). Consequently, some researchers proposed that OT can facilitate social activities by associating it with the ability to experience rewards from social interactions (Campbell 2008; Declerck et al. 2010). DA contributes to the formation of social memories and social preferences as a part of the ventral tegmental area-dopamine projection system (Depue and Morrone-Strupinsky 2005; Scerbina et al. 2012). In addition to OT and DA, β-endorphin is also involved in reward processes and has been associated with social behavior, particularly in primates (Dunbar 2010; Keverne et  al. 1989). β-Endorphin may be crucial to the formation and maintenance of social bonds (Depue and Morrone-Strupinsky 2005; Dunbar 2010, 2012). Taken together, these studies suggest that OT, DA, and endorphins contribute to the formation and maintenance of social bonds, such as friendships (Brent et al. 2014). Social relationships may also have an effect on how individuals deal with a conflict, which is usually a stressful event (Massen et al. 2010b). The stress response, produced by activation of the HPA axis, alerts animals that homeostasis has been disrupted and mobilizes energy to restore a homeostatic state (McEwen 2000). Several species, including humans, show smaller increases in cortisol levels during exposure to adverse stimuli when a friend is present compared to when alone

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(DeVries et al. 2003). Female baboons with a large, close social circle of grooming partners have healthy cortisol levels and usually deal better with stressful situations (Saltzman et al. 1991; Crockford et al. 2008; Wittig et al. 2008). In primates, grooming reduces heart rate (Aureli et al. 1999), which could be interpreted as a response to the fulfillment of a social need with a negative feedback between endorphins, OT, and HPA axis likely playing a part (Brent et  al. 2014). Chronic activation of the stress response is known to have negative health and reproductive consequences (Cohen et al. 1992; Cameron 1997) which can negatively impact evolutionary fitness (Brent et al. 2014). To summarize, hormonal and neuronal patterns exhibit a complex system that strengthens sociality and that is shared across species, suggesting that this system is highly conserved and serves similar functions in animals and humans (Massen et al. 2010b).

2.5 Coalitions 2.5.1 Behavioral Studies Coalitions and alliances are core features of human behavior (Flinn et al. 2012). All societies recognize alliances among communities and aggression between groups is pervasive, often deadly, and can have devastating effects on human welfare (Flinn et al. 2012). Coalitions and alliances between animals are found in a variety of different taxa, but some of the most extraordinary coalitions are found among nonhuman primates, and have been studied more extensively in this group (Higham and Maestripieri 2010). Coalitions can be defined as coordinated attacks by at least two individuals on one or more targets, and they may serve to protect against attacks by more powerful individuals, to defend or obtain access to resources, or to earn the dominant rank, or the targeted individual (van Schaik et al. 2006). Coalitions are usually formed by individuals of the same sex, although intersexual coalitions may also occur (e.g., Watanabe 1979). It is common in large primate groups containing several adults of both sexes, that males and females compete over different limited resources: food and shelter for females, fertilizations for males (van Schaik et al. 2004). Coalitions may occur in many configurations (Chapais 1995), in many different combinations, and not always in support of the same partners or directed at the same target (Silk 1993; van Schaik et al. 2006). At times they occur spontaneously or as interventions in ongoing conflicts (de Waal et al. 1976), and some of them beat their opponent(s) while others end in a deadlock (van Schaik et al. 2006). It is difficult to identify the underlying strategic goals behind coalitions, but the main general intent may be an increase in fitness gains (van Schaik et al. 2006). In some species, coalitions help facilitate males’ access to important resources (Silk 1993). For instance, male baboons sometimes form coalitions as they strive to disrupt other males’ consortships with receptive females (Packer 1977; Bercovitch 1988). Males who are part of coalitions are often successful in disrupting consortships, and coalitions provide a means for middle- and low-ranking males to establish consortships with receptive females (Silk 1993). Male chimpanzees often form

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coalitions with one another and use them to manipulate the ranks of their rivals and enhance their own dominance positions (de Waal 1982). Chapais (1995) divided coalitions in primates into three types: (1) conservative coalitions where all coalition members are all higher ranked than the target; (2) bridging coalitions, where at least one coalition member is of high rank and at least one member is of lower rank than the target; and (3) revolutionary coalitions, in which coalition members are all of lower rank than the target. Later, Van Schaik et al. (2006) separated both bridging and revolutionary coalitions into “leveling” and “rank-changing” coalitions. Along with these models, various studies have made predictions about different features that should predispose primate males toward forming coalitions with each other (Noë and Sluijter 1995). Males seem more likely to form coalitions: among individuals of greater familiarity and that had been in a group together for a long time (Smuts 1985; Noë and Sluijter 1995); among friends (Smuts 1985); among individuals of similar fighting abilities (Bercovitch 1988; Noë and Sluijter 1990); among kin (Wrangham 1982). There is considerable evidence of nepotism in support among adult male primates (Silk 1993). For example, after dispersal, male vervet monkeys and rhesus macaques transfer into groups that contain maternal kin as well as previous members of their natal groups (Meikle and Vessey 1981; Cheney and Seyfarth 1983). Following dispersal, male rhesus monkeys selectively approach, sit nearby, and support their brothers (Meikle and Vessey 1981). There is also evidence of coalition formation among non-kin. For example, Schülke et  al. (2010) found that maternally unrelated Assamese macaque males formed coalitions against competitor males and rose in dominance rank, resulting in increased paternity success. Male chimpanzees that share close social bonds with other non-kin males also form coalitions against dominant males to gain access to fertile females (Duffy et al. 2007). Males usually have linear dominance relationships that can change rapidly and due to their dispersal patterns, often cannot rely on kin to assist them in conflicts (MacKinnon and Fuentes 2011). For this reason, males sometimes need to form associations with other males or females in order to negotiate dominance disputes (MacKinnon and Fuentes 2011). Adult female–male coalitions are rarely kin-based and consequently reflect possible opportunities for reciprocal altruism to take place (MacKinnon and Fuentes 2011). Females may receive male assistance in dominance contests, while males might receive social benefits like increased social interactions or grooming, while both sexes may receive reproductive benefits but also suffer reproductive costs from such alliances (MacKinnon and Fuentes 2011). Coalitions involving relatives are usually more common among females (Waal and Hooff 1981). For example, cross-­ sectional analyses demonstrate that female baboons have the strongest bonds with close relatives such as mothers, daughters, maternal sisters, and paternal sisters (Silk et al. 1999, 2004, 2006a; Smith et al. 2003). Female coalitions are observed almost exclusively in female-philopatric species, where females stay with their natal groups (Smith et al. 2010; Sterck et al. 1997). Although females may enhance their inclusive fitness benefits by forming alliances with relatives, they can also benefit directly from creating relationships with non-kin females who provide them with benefits (Silk et  al. 2006b) In fact, females can also show preferences for

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unrelated partners who are close to their dominance rank and age (Silk et al. 1999, 2006a). Females’ preferences for particular partners in baboons (Papio cynocephalus) seem to be influenced by the quality of their interactions (Silk et al. 2006b). Females who were groomed most equitably had the strongest and lasting social bonds (Silk et al. 2006b). For female baboons, which are characterized by female philopatry and form groups composed of several matrilines, social integration enhances their fitness and females were more likely to rear their infants successfully than socially isolated females (Silk et al. 2003). In several species, females form coalitions to defend themselves against male harassment (Sterck et al. 1997). There is also evidence of Central and South American monkeys forming coalitions. In ursine howler monkeys, coalitions of males cooperate to take over small groups of females or to defend access to them from other males (Fernandez-Duque et  al. 2012). Among the cebids (e.g., white-faced capuchins) close cooperation among males may be promoted by the high incidence of parallel dispersal, which could translate into fitness benefits and increase survivorships (Jack and Fedigan 2004). In Bolivian squirrel monkeys, males emigrate together, and alliance members support each other as they compete with males in other groups and attempt to join new groups during immigration events (Mitchell 1994). In summary, coalitions occur if they are both feasible, i.e., lead to a fitness benefit for all members, and profitable, i.e., can beat the target (van Schaik et al. 2006). Coalitions are formed by several species and can occur among kin and non-kin and the nature of the coalition can vary across species, although some of the main goals of coalitions include obtaining access to food for females and fertilization for males.

2.5.2 Neurobiology/Endocrinology Humans usually respond to mental and physical challenges with complex endocrine responses (Wagner et al. 2002). In men, cortisol and testosterone are typically elevated in anticipation of competition, and winners have higher testosterone than losers (Mazur and Lamb 1980; Elias 1981). In some nonhuman primates, males sometimes cooperate in dominant interactions (Wagner et al. 2002). For instance, in male baboons testosterone and cortisol levels are very sensitive to social stimuli, especially in situations dealing with dominance competition where successful males have higher testosterone levels than lower-rank males (Sapolsky 1991, 1992). Testosterone is an androgenic steroid hormone secreted from the testes in men and the ovaries in women (Casto and Edwards 2016). Across vertebrates, males exhibit elevated testosterone levels when competing for mates, during mating season or territorial defense, and lower levels during periods of paternal care (Wingfield et al. 1990; Hirschenhauser and Oliveira 2006; Muller 2017; Grebe et  al. 2021). For instance, prior research has shown that male chimpanzees display high levels of testosterone when they compete for estrous females in their own community (Muller and Wrangham 2004; Sobolewski et al. 2013). Glucocorticoid steroids (frequently cortisol in primates) are also involved in regulating social behavior, including in contexts relevant to nurture and social bonds

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(Rincon et  al. 2020). Glucocorticoid release is regulated by the HPA axis and is responsive to actual or perceived stressors (Sapolsky 2002). Being able to count on others for social support and being socially integrated may help to regulate the HPA axis activity even in the absence of a stressor (Rosal et al. 2004; Wittig et al. 2016). A first condition for cooperative behaviors to occur is that the individual shows a predisposition to approach other potential partners and tolerate their presence (Soares et al. 2010). Hormones are likely to affect levels of helping in different ways as they have activational and organizational influence on general social behavior (Soares et al. 2010). For example, bonding mechanisms may be necessary to avoid aggression against partners and may modulate the perception of pay-offs and consequently facilitate cooperative behavior (Soares et al. 2010). The building blocks of cooperation have been suggested to be: tolerance toward others, social recognition, assessment of the social environment, social learning and memory, temporal discounting, social bonding, and partner choice (Soares et al. 2010). Primate social life routinely utilizes a similar skill set, even outside of mother-offspring or pair-­ bonded relationships (Ziegler and Crockford 2017). Most of these features are underpinned by the OT system, which is arguably a key facilitator of cooperation (Ziegler and Crockford 2017). It has also been hypothesized that OT as well as AVP may influence basic emotional mechanisms that regulate social approach and social aversion (Porges 2001). According to this hypothesis OT, acting on the hindbrain parasympathetic system, should stimulate pro-social behavior, while AVP acting on sympathetic pathways should stimulate social withdrawal and/or aggression (Porges 2001; Soares et al. 2010). Hormones can also influence learning processes, and because cooperation and conflict are often contingent on individual recognition and memory of the partner (or opponent), hormone-modulated learning may play a critical role in establishing social relationships (Soares et al. 2010). Moreover, social interactions may also be rewarding (Krach et al. 2010) and thus lead to additional interactions with the same individual. The rewarding value of social interactions proposes that their valence and salience might be coded by the mesolimbic dopaminergic pathway, the circuitry involved in reward learning (Soares et  al. 2010). Importantly, the dopaminergic reward pathways in the brain are also influenced by AVP and OT as seen in prairie voles where OT and AVP interact with DA receptors in their reward centers (Young and Wang 2004). Coalitions and cooperation, like other social behaviors, appear to be modulated by various hormones such as OT, AVP, and DA, as well as testosterone and glucocorticoids.

2.6 Perspectives Social behavior is an essential component of primate societies. As seen in this chapter, primates can form and maintain various social relationships such as pair bonds, friendships, coalitions, and relationships among kin (Fig. 2.1). A few species, such as titi monkeys, are able to form and maintain pair bonds, a stable adult attachment characterized by many behavioral features. Other primate species could be capable

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Fig. 2.1  Characteristics of different adult primate social relationships. The authors would like to thank Sophia Rogers for providing us with this figure

of forming friendships, an ability once thought to be unique to humans. Relationships among kin that tend to last into adulthood and play a key role in structuring the evolution of primate social systems have surfaced as a central force of social organization in primates. Finally, we reviewed coalitions that can occur among kin and non-kin, where the nature of coalitions can vary across species but will usually lead to certain fitness benefits for all members. We also reviewed the importance of different hormonal systems underlying these bonds such as the OT and AVP systems, and other neuroendocrine responses such as the HPA axis. The scientific study of some of these relationships is still in its early stages. Many primate species have not

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been sufficiently studied to prove or disprove the existence of a pair bond, or to provide an understanding of the neurobiological mechanisms underpinning these bonds. More studies are needed to improve our understanding of friendship in primates and its evolutionary role, as well as addressing gaps in the literature on neurobiology and social relationships regarding friendships. Future studies will also need to address gaps in the literature concerning family bonds, specifically parent– offspring and sibling relationships once the offspring have entered adulthood. Key Literature Massen JJM, Sterck EHM, de Vos H (2010b) Close social associations in animals and humans: functions and mechanisms of friendship: This article discussed important findings on the central-neural regulation of social bonds and concluded that human friendship and animal close social association are beneficial. Silk JB, Altmann J, Alberts SC (2006) Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds: The article discussed the role of female bonds in baboons which play a vital role in females’ lives and their fitness. Silk JB (2002) Using the “F’-word in primatology: The paper discussed several implications of using the word “friendship” to describe social bonds in nonhuman primates. Bales KL, Ardekani CS, Baxter A, et al. (2021) What is a pair bond? The article defined pair bonding across taxa and reviewed previous definitions. Soares MC, Bshary R, Fusani L, et al. (2010) Hormonal mechanisms of cooperative behaviour: This paper examined the role of neuroendocrine mechanisms on the regulation of the expression of cooperative behaviors. Ziegler TE, Crockford C (2017) Neuroendocrine control in social relationships in non-human primates: Field based evidence: This article reviewed the impact of the neuroendocrine system on social interactions in field studies.

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Neuroendocrinology of Human Cooperation and Parental Care James K. Rilling

Abstract

Human parental care appears to rely on the same neuroendocrine mechanisms that support parental care in other species, and other types of human prosocial behaviors may also depend on the same neuroendocrine systems. Research has examined associations between peripheral hormone levels and parental behavior or parental brain function using fMRI. Other studies have experimentally manipulated hormone levels by exogenous administration and examined the impact on brain function and parental behavior. These studies suggest that oxytocin acts on midbrain dopamine circuits to promote parental motivation in both human mothers and fathers. Oxytocin also suppresses the amygdala response to infant crying, potentially rendering infant cries less aversive. On the other hand, high levels of testosterone appear to interfere with direct caregiving activities, although indirect caregiving activities may be supported by low to moderate levels of testosterone. A smaller body of research has investigated the role of vasopressin and prolactin in human parental care. Similar approaches have been used to study human cooperation. Oxytocin facilitates cooperation, but only in specific contexts and in individuals with particular personality types. In response to cooperative interactions, oxytocin modulates activity within components of the midbrain DA system, but these effects differ starkly by gender, perhaps due to nonlinear J. K. Rilling (*) Department of Psychology, Emory University, Atlanta, GA, USA Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA, USA Center for Behavioral Neuroscience, Emory University, Atlanta, GA, USA Emory National Primate Research Center, Emory University, Atlanta, GA, USA Center for Translational Social Neuroscience, Emory University, Atlanta, GA, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 H. K. Caldwell, H. E. Albers (eds.), Neuroendocrinology of Behavior and Emotions, Masterclass in Neuroendocrinology 16, https://doi.org/10.1007/978-3-031-51112-7_3

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dose–response relationships. There is also emerging evidence that vasopressin and testosterone support cooperation in some contexts. More research is needed to replicate many of the reported findings, but current evidence is consistent with considerable overlap in the neuroendocrine mechanisms that support parental care and cooperation in humans. Keywords

Parental behavior · Cooperation · Oxytocin · Vasopressin · Testosterone · fMRI · Human

3.1 Introduction Parental caregiving is particularly well developed in mammals, and specific neuroendocrine mechanisms have evolved to support it. The available evidence indicates that human parental caregiving relies on the same mechanisms that support parental caregiving in other mammals. Parental care may be the most ancient and fundamental form of prosocial behavior. Therefore, other forms of prosocial behavior, such as cooperation, may have evolved by utilizing pre-existing neuroendocrine mechanisms already in place for parenting. This chapter presents evidence from humans relevant to this hypothesis.

3.2 Parental Care 3.2.1 Oxytocin 3.2.1.1 Oxytocin in Human Mothers Research in non-human animals has established a fundamental role for the neuropeptide oxytocin (OT) in parental behavior. Specifically, OT facilitates the onset and maintenance of parental behavior by acting within the medial preoptic area (MPOA) and the mesolimbic dopamine (DA) system to stimulate DA release in the nucleus accumbens, providing the motivation to deliver parental care (Numan 2020; Numan and Stolzenberg 2009). In recent years, researchers have investigated whether the same mechanism is involved in human parental care. Although human researchers lack the methodological tools to explore this model in comparable detail, considerable evidence indicates that human and non-human mammalian parental brain circuitry have extensive overlap. Research on human parental brain function is limited by the difficulty of measuring and manipulating OT levels in the human brain. Although OT can in principle be measured in cerebrospinal fluid of the brain, this is a highly invasive procedure and is rarely done. Instead, researchers have measured OT in the periphery and attempted to relate it to observed parental behavior. The blood–brain barrier has limited permeability to OT (Kang and Park 2000; Mens et  al. 1983), so that

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peripheral and central OT systems are considered to be largely independent (Leng and Ludwig 2016). Nevertheless, positive correlations between central and peripheral levels have been reported in some human studies (Carson et al. 2014; Martin et al. 2018; Wang et al. 2013) suggesting that peripheral levels may have behavioral relevance. Mothers with higher plasma OT levels spend more time gazing at their infant’s face, express more positive emotions toward their infant, and affectionately touch their infant more often. They also produce more motherese vocalizations (i.e., baby talk), and show better temporal coordination between their own and their infant’s positive emotion. In other words, they are better synchronized with their infant’s emotions (Feldman et al. 2011). Peripheral OT levels increase in mothers who touch and gaze at their infants with high frequency, but not in other mothers (Feldman et al. 2010; Kim et al. 2014). Further evidence for an association between OT and human maternal care is provided by research showing that mothers with a specific allele of the oxytocin receptor gene (OXTR), the GG genotype at SNP rs53576, exhibit greater maternal warmth and sensitivity (Bakermans-Kranenburg and van Ijzendoorn 2008; Klahr et al. 2015). Research in non-human animals has led to the hypothesis that decreased OT signaling explains the low levels of parental motivation and high levels of anxiety characteristic of post-partum depression (PPD) (Numan 2020). Mothers with PPD show negative alterations in maternal behavior that include lower levels of maternal sensitivity, more anger and intrusiveness, and fewer positive interactions with their infant (Bernard et  al. 2018; Brummelte and Galea 2016; Lovejoy et  al. 2000; Pawluski et al. 2017). Greater PPD symptoms are associated with lower plasma OT levels (Mah 2016; Thul et al. 2020). PPD is also more common in women who do not breastfeed and therefore have less endogenous OT release (Hamdan and Tamim 2012; Miksic et al. 2020; Oyetunji and Chandra 2020), although the direction of causality linking PPD and breastfeeding is unclear. Increasing OT levels in women with PPD has been considered as a strategy to normalize maternal behavior. This can be done via intranasal oxytocin (INOT) administration. Intranasally administered OT appears to reach the brain in functionally significant amounts that can influence behavior (Quintana et al. 2021). Mothers with PPD reported a more positive relationship with their infant following INOT compared with placebo (Mah et al. 2013). Among mothers with PPD, INOT also increased maternal protective behaviors in the presence of an intrusive stranger (Mah et al. 2014). However, INOT did not affect maternal sensitivity in mothers with PPD in one study (Mah et al. 2017). Maternal brain function has been investigated in humans using functional magnetic resonance imaging (fMRI), which detects changes in regional cerebral blood flow as mothers view infant pictures or videos, or listen to infant crying. This research has provided tentative evidence that OT acts on similar neural circuits in human and non-human mothers. Mothers with higher levels of peripheral OT show stronger neural activation to viewing pictures of their infants within both the nucleus accumbens and the hypothalamus (Strathearn et al. 2009). Other studies have experimentally manipulated OT levels by administering exogenous, intranasal OT and measuring the impact on brain function with fMRI. One study showed that INOT

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increased the maternal neural response to pictures of crying infants within the ventral tegmental area (VTA) (Gregory et al. 2015), the source of the mesolimbic DA neurons. Another showed that INOT decreased the amygdala response to infant crying among nulliparous women, interpreted to reflect decreased feelings of anxiety and aversion to the crying infant (Riem et al. 2011).

3.2.1.2 Oxytocin and Human Fathers Although OT was initially investigated in mothers and is generally considered a maternal hormone, it is also now known to be involved in paternal caregiving, in both non-human animals and humans. For example, when male mandarin voles become fathers, they experience an increase in both the number of neurons that produce OT within the hypothalamus as well as the number of oxytocin receptors (OTRs) in the NA (B. Wang et al. 2015; Yuan et al. 2019). Human fathers have higher levels of plasma OT compared with non-fathers (Mascaro et al. 2014). Paternal levels increase over the first 6 months of fatherhood (Gordon et al. 2010a), and reach levels that are equivalent to baseline maternal levels outside of breastfeeding bouts (Gordon et al. 2010a). Fathers with higher plasma OT levels engage in more stimulatory parenting, which includes stimulatory touch, object presentation, and moving the infant through space (Gordon et  al. 2010a; Morris et al. 2021). The specific cues that stimulate paternal OT release are not known, but recent studies point to tactile contact as being important. Paternal OT levels increase after 30–60 min of skin-to-skin contact with their pre-term infants. These OT responses may contribute to father–infant bonding, since fathers who show larger increases in OT following skin-to-skin contact engage in more sensitive and responsive care with their infant on the next day (Cong et al. 2015; Vittner et al. 2018). Paternal OT responses are not limited to pre-term infants. OT levels increase by about 20% in first-time fathers after they hold their newborn infant for the first time (Gettler et al. 2021). In play sessions, fathers who physically stimulate their infants at high levels show increases in peripheral OT, whereas other fathers do not (Feldman et al. 2010). To investigate a potential causal impact of OT on paternal care, several studies have examined the effect of INOT on human paternal behavior. INOT increases the amount of time fathers spend touching their infants, as well as the amount of social reciprocity they show toward their infants. Infants of OT-treated fathers, in turn, spend more time looking at their father’s face and more time manipulating objects, and their endogenous OT levels increase (Weisman et al. 2012) (Fig. 3.1). Fathers treated with INOT also encourage more learning and exploration in their toddler children, and they show less impatience and discontent (Naber et al. 2010). INOT treatment has been combined with fMRI to demonstrate OT modulation of paternal neural responses to infant and child stimuli. In fathers of toddler children, INOT augmented the BOLD response to viewing pictures of their children relative to adults in the caudate nucleus, the dorsal anterior cingulate cortex (dACC), and visual cortex (Li et al. 2017) (Fig. 3.2). The caudate nucleus is part of the nigrostriatal DA system, which is also involved in reward and motivation (Ikemoto et  al. 2015) and commonly activated in neuroimaging studies of parental brain function

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Fig. 3.1  INOT effects on father and infant behavior during father–infant interactions. *p