Systematics, Evolution, and Ecology of Melastomataceae 9783030997410, 9783030997427

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Renato Goldenberg Fabián A. Michelangeli Frank Almeda   Editors

Systematics, Evolution, and Ecology of Melastomataceae

Systematics, Evolution, and Ecology of Melastomataceae

Renato Goldenberg Fabián A. Michelangeli  •  Frank Almeda Editors

Systematics, Evolution, and Ecology of Melastomataceae

Editors Renato Goldenberg Departamento de Botânica Centro Politécnico Universidade Federal do Paraná Curitiba, Paraná, Brazil

Fabián A. Michelangeli Institute of Systematic Botany The New York Botanical Garden Bronx, NY, USA

Frank Almeda Department of Botany Institute for Biodiversity Science and Sustainability California Academy of Sciences San Francisco, CA, USA

ISBN 978-3-030-99741-0    ISBN 978-3-030-99742-7 (eBook) https://doi.org/10.1007/978-3-030-99742-7 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 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

Foreword

I first came across Melastomataceae 42 years ago, in 1980, when Klaus Kubitzki, who had just come back from Brazil, suggested I should work on ant/plant interactions or bee/flower interactions for my doctoral dissertation. I decided on the latter topic, but soon realized that melastomes would afford me an opportunity to also study the former. The systematics of the family began to interest me only during my postdoc with John Wurdack (1921–1998) at the Smithsonian in Washington in the mid-1980s. It was there that Frank Almeda and I first got to know each other, during one of his regular visits to the US National Herbarium. Besides doing monographic and floristic work, Frank moved forward the study of the chromosomes and seed morphology of Melastomataceae with broad taxon sampling and state-of-the-art microscopy, the hope being that these traits would turn out taxonomically useful. In 1997, I met Fabián Michelangeli, who was then doing his doctoral research on Tococa, one of the ant-plant clades in the Melastomataceae. This topic immediately brought us together since I had also worked on Tococa and done ant-exclusion experiments on one of its species (Renner 1997; Renner and Ricklefs 1998). Fabián and I were both interested in the application of computer-based phylogenetics, but at the time we were still relying on morphological data. Renato Goldenberg and I began corresponding in the early 1990s, initially about apomixis, which he had studied in southern Brazilian species, but later mostly about Renato’s efforts with Frank, Fabián, and others on the Nomenclator for Miconia (Goldenberg et al. 2013). From our first personal meeting—in Munich, Germany—I mostly recall being struck by Renato’s ambition and decisiveness. It is an immense pleasure therefore to have been asked by this team—Renato Goldenberg, Fabián Michelangeli, and Frank Almeda—to provide a foreword for this book, a milestone achievement in our understanding of the systematics, evolution, biogeography, and ecology of the Melastomataceae. The editors have brought together 72 authors from 17 countries to accomplish this first modern synthesis of research focusing on this family; they provide background on their aims, and the book’s content, in their preface. I can therefore use this foreword to reminisce on the progress that we have made in our understanding over the past 30–40 years. Given that the World’s population has increased from v

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5.4 in 1991 to 7.8 billion today, and that there are now more systematists than ever before, it is expected that the number of people working on Melastomataceae has increased. An argument can be made, however, that the scope and quality of work on this family has increased disproportionally. One measure of this is provided by a symposium on the systematics and evolution of the Melastomataceae that I organized at the Smithsonian Institution in Washington in 1991. Among the six or seven speakers were Thomas Morley (1917–2002), James Maxwell (1945–2015), John Wurdack, and Frank Almeda. Henri Jacques-Félix (1907–2008) could not attend for health reasons, meaning that there was no presentation at all on African Melastomataceae. Seen from today, we had almost no understanding of the age of the family, its biogeography, the relationships between Olisbeoideae and Melastomoideae, the role of hybridization, the function of the dimorphic stamens, or the true taxon diversity and endemicity. On all these topics, there has been tremendous progress over the past 30 years as documented in this volume. The year 1991 had been chosen for the Melastomataceae symposium at the Smithsonian to commemorate the publication of Celestin Alfred Cogniaux’s (1891) Monographiae Melastomacearum, the last book to deal with the systematics of entire family. In a way, it is this work that is being replaced by this volume, which presents a new classification for the subfamilies, tribes, and allocation of genera (Penneys et  al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”; Stone, Chapter “Phylogeny and Circumscription of the Subfamily Olisbeoideae”; and other chapters in Part II). Systematists today work in teams, rather than alone as we did well into the early 1990s. The internet, which officially began on 1 January 1983, with the full impact felt in herbaria from 1985 onwards, has made it easier to find, share, and discuss data and insights. The worldwide data accessibility and teamwork leads to consensus classifications, with more people buying into particular arrangements of higher taxa. The classification in this volume by Penneys and colleagues (Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) is based on nuclear and plastid DNA sequences from 2435 species (2973 terminals) representing 158 of 175 currently accepted genera. This means that the deeper relationships in the Melastomataceae are now clear. With solid phylogenies in hand, we can apply molecular-clock approaches to infer the dispersal and radiation of particular clades. Twenty years ago, with my then-students Gudrun Clausing (now Kadereit) and Karsten Meyer, I was involved in the “switch” from morphology-based to DNA-based attempts at discerning relationships and geographic histories (e.g., Renner and Meyer 2001; Clausing and Renner 2001; Renner 2004). However, when it comes to melastomes, my first love remained their pollination and function of their stamens (Luo et al. 2008), and their capacity for asexual reproduction (apomixis). On these and other ecological, physiological, and cytological aspects, too, there has been great progress over the past 30 years as documented by dedicated chapters in this volume. A third measure of progress is the increase in number of species and our understanding of species ecology. For the “Monographiae,” Cogniaux revised 2731 species (and 555 varieties, not always easy to interpret today), 793 of them new to

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science. The work involved is unimaginable today, for example, Cogniaux wrote to Asa Gray that it had taken him “much longer than I thought at first” to prepare the alphabetical index to the c. 8000 names treated in the “Monographiae” (Renner 1990). According to data in this volume, the family now comprises 5858 species, over twice as many than in 1891. I suspect that collecting of herbarium specimens between 1991 and 2021 has not matched that during 1971–1990. Nevertheless, we are reaping the fruits of the earlier collecting in novel ways: Firstly, by obtaining DNA sequences from herbarium collections and secondly, but applying computer-­ based approaches to the analysis of georeferenced museum collections. For example, Michelangeli et  al. (Chapter “Historical Biogeography of the Neotropical Miconieae (Melastomataceae) Reveals a Pattern of Progressive Colonization Out of Lowland South America”) have investigated the biogeographic patterns of Miconieae based on 90,000 distribution records for over 1000 species. This type of analysis allows an understanding of niche occupation and radiation into new niches that was not possible 30 years ago, but that depends on, and is limited by, herbarium collections. A final argument supporting the need for this single-volume compilation dedicated to the Melastomataceae is that a book with numerous authors collaborating in dynamically changing teams will give the new classification of the family the proper outing and weight. The current knowledge and still-open questions are here for all to find, accept, and improve. Of my own classification (Renner 1993) nothing remains except the subfamily Kibessioideae, which I resurrected following Charles Naudin (1849–1853). Naudin was a pioneer of experimental research on hybridization, and his thinking is known to have influenced Darwin (Marza and Cerchez 1967). Thinking about this, the greatest success for this volume will be if it encourages, and facilitates, the interconnectedness of research not only among those interested in Melastomataceae today, but also others who may know little about this tropical group, but who are seeking to address evolutionary or ecological questions for which melastomes would make great study objects. As Renato Goldenberg, Frank Almeda, and Fabián Michelangeli write in their preface, this book should spur a new generation of research topics to be addressed in the family. Department of Biology Washington University St. Louis, MO, USA

Susanne S. Renner

References Clausing G, Renner SS (2001) Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution. Am J Bot 88(3):486–498 Cogniaux CA (1891) Mélastomacées. In: de Candolle ALPP, de Candolle C (eds) Monographieae phanerogamarum vol 7, pp 1–1256. G. Masson, Paris Goldenberg R, Almeda F, Caddah MK, Martins AB, Meirelles J, Michelangeli FA, Weiss M (2013) Nomenclator botanicus for the neotropical genus Miconia (Melastomataceae: Miconieae). Phytotaxa 106:1–171

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Luo Z, Zhang D-X, Renner SS (2008) Why two kinds of stamens in buzz-pollinated flowers? Experimental support for Darwin’s division-of-labor hypothesis. Funct Ecol 22:794–800 Marza VD, Cerchez N (1967) Charles Naudin, a pioneer of contemporary biology. J Agric Trop Bot Appl 14:369–401 Renner SS (1990) C. A. Cogniaux (1841–1916). Blumea 35:1–3 Renner SS (1993) Phylogeny and classification of the Melastomataceae and Memecylaceae. Nord J Bot 13:519–540 Renner SS (1997) Tococa caryophyllaea (DC.) Renner (Melastomataceae): a climbing Tococa. BioLlania Ed Esp 6:497–500 Renner SS (2004) Bayesian analysis of combined data partitions, using multiple calibrations, supports recent arrival of Melastomataceae in Africa and Madagascar. Am J Bot 91(9):1427–1435 Renner SS, Meyer K (2001) Melastomeae come full circle: biogeographic reconstruction and molecular clock dating. Evolution 55(7):1315–1324 Renner SS, Ricklefs RE (1998) Herbicidal activity of domatia-inhabiting ants in patches of Tococa guianensis and Clidemia heterophylla. Biotropica 30(2):324–327

Preface

This volume summarizes much of what is currently known about the systematics, phylogeny, classification, biogeography, and ecology of Melastomataceae, one of the ten largest families of flowering plants. The family is largely a tropical one that is mostly unknown to people who have spent their lives in temperate latitudes. A few northern-hemisphere garden-lovers will recognize the glory bushes (Pleroma) or a few species of Medinilla that are cultivated in greenhouses, while some North Americans might be familiar with the several species of meadow beauties (Rhexia) that are distributed across a good part of the eastern United States. On the other hand, anyone with some experience in tropical and subtropical floras around the world has surely encountered the extraordinary diversity of species presented by this family. Although it is one of the easiest to recognize at the family level, the task of identifying genera and species has typically been an onerous one for the generalist. Despite its size and diversity, we suspect that the primarily tropical distribution of Melastomataceae has contributed to its almost forgotten and largely unknown status in terms of systematics, evolution, and ecology. Redressing this shortcoming by bringing together the many recent research advances focused on Melastomataceae into one volume is a major objective of this book. Unlike the Asteraceae, Fabaceae, Orchidaceae, and Poaceae—larger widespread flowering plant families that have attracted an army of specialists—relatively few botanists have gravitated to the Melastomataceae. Until the end of the twentieth century, few systematists dedicated all or a portion of their careers to botanical research on the Melastomataceae in a global or regional context. These included A.  P. de Candolle (1778–1841) in Geneva, D.  Don (1799–1841) in London, C. V. Naudin (1815–1899) in Paris, J. J. Triana (1828–1890 ), a Colombian and the first Latin American specialist who conducted field work and study visits to European herbaria, C.  A. Cogniaux (1841–1916) in Brussels, H.  A. Gleason (1882–1975) in New  York, R.  C. Bakhuizen van den Brink, Jr. (1911–1987) in Leiden, H. Jacques-Félix (1907–2008) in Paris, and J. J. Wurdack (1921–1998) in Washington, D.C. In the last two and a half decades, the number of researchers working on various aspects of melastome systematics, ecology, and evolution has grown exponentially. ix

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This has involved everything from herbarium-based alpha-level taxonomic studies and phylogenetic reconstructions using DNA sequence data to studies focused on biogeography and reproductive biology. Most importantly, many new students of the family based in melastome-rich countries, especially in the neotropics, have made field-based studies a critical centerpiece of their research efforts. We find ourselves at a historically unique crossroad with respect to melastome research since we now have a sizeable cadre of researchers asking significant evolutionary questions and generating a wealth of new data that are ripe for a first-ever modern synthesis. It is hoped that this book fills that need. We have brought together a diverse community of 72 authors from 17 countries to accomplish this synthesis. This volume consists of 34 chapters grouped into four sections. The first section introduces the Melastomataceae with chapters on overall diversity and distribution, classification history prior to the molecular era, morphological variability, and historical biogeography in a global context. The second section provides a new phylogenetically based classification of the family and summarizes what we now know about each of the subfamilies and tribes based on comparative morphological and molecular data sets. We used this opportunity to assemble a third section that addresses advances in a diverse set of subjects ranging from floral ontogeny, seed morphological features, chromosome number evolution, pollination biology, aspects of reproductive biology, and patterns of diversification and biogeography of Miconieae, the largest tribe in the family. The fourth and final section deals with some broad ecological topics including species distributions along soil gradients, seed germination ecology, seed dispersal, and the ecology of naturalized species of Melastomataceae around the world. We conclude the volume with a statement of future prospects emphasizing avenues of research in need of sustained attention. In putting this volume together, each author was given free rein to gather a team of collaborators and to develop text appropriate to each chapter topic. We avoided establishing strict content guidelines to accommodate available information for each chapter and to encourage individual creativity. Some chapters are literature reviews while others incorporate previously unpublished data. Because of space limitations, authors were encouraged to provide relevant supplemental data pertinent to their chapters that will be available online at Springer Nature. We recognize that some important topics have not been treated here such as gall morphology and biology, the meager fossil record, and ethnomedicinal uses and pharmacological properties. These are topics for a future volume or book-length volumes of their own. For the sake of brevity and uniformity, we have adopted some conventions that depart from standard practices. Authorities for scientific names are given only in Chapters “Melastomataceae: Global Diversity, Distribution, and Endemism” and “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology” instead of the first time they are used in each chapter, since these are now generally available in a number of online venues. Types for names are also generally not provided except for newly proposed taxa such as tribes in Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology” or where tribal names with priority have been newly adopted.

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Books of this type put a spotlight on a group of organisms by integrating information from a variety of disciplines, whether they are descriptive, experimental, or historical in nature. It is our hope that this volume will bring the Melastomataceae to the attention of a much broader audience. Beyond being a summary of our current knowledge on the systematics, ecology, and evolution of Melastomataceae, we hope this book highlights the gaps in knowledge that need to be filled and spurs a new generation of research topics in the family. Curitiba, Paraná, Brazil Bronx, NY, USA  San Francisco, CA, USA 

Renato Goldenberg Fabián A. Michelangeli Frank Almeda

Acknowledgments

We are grateful to all of our melastome colleagues who agreed to contribute to this project. They took precious time from their busy schedules to write chapters for this book and unflinchingly responded to our requests for changes, both big and small, to their manuscripts. We also thank the many reviewers who have given freely of their time and expertise to evaluate the scientific content and presentation of book chapters. Their constructive comments and suggestions have increased the accuracy and improved the quality of every chapter. All chapters have been reviewed by two or more specialists, all of whom are named and thanked in each chapter if they chose not to remain anonymous. For the chapters that involved all three book editors as co-authors, we invited guest editors to handle the review process; for this, we give special thanks to Lucas Bacci, Agnes Dellinger, Peter Fritsch, Walter Judd, Ricardo Pacifico, and Carmen Ulloa. We also take this opportunity to pay tribute to the important early work and achievements of our predecessors who are mentioned in the Preface and in Chapter “Classification History of the Melastomataceae: Early Beginnings Through the Pre-­ molecular Era”. These individuals produced seminal studies of the Melastomataceae, all based on fewer collections and none of the sophisticated technology available to us today. Their collective work provides the critical foundation that has allowed the growing community of melastome researchers to identify knowledge gaps, test relationships, and advance our overall understanding of the family. We will also want to thank João Pildervasser, scientific editor at Springer Nature, who believed we had an important subject to present from the start. We are also grateful to Sowmya Thodur, production editor of books at Springer Nature for all of her guidance through the publication process, and the staff at Springer Nature for assistance during book format design, production, and all the attendant details required to bring a book of this kind to completion. Finally, we owe much gratitude to our home institutions—the California Academy of Sciences, the New  York Botanical Garden, and the Universidade Federal do Paraná. They have provided us with ongoing financial and logistical support and a stable home base to pursue our research passions focused on the megadiverse Melastomataceae over many years. xiii

Contents

Part I An Introduction to Melastomataceae  Melastomataceae: Global Diversity, Distribution, and Endemism ������������    3 Carmen Ulloa Ulloa, Frank Almeda, Renato Goldenberg, Gudrun Kadereit, Fabián A. Michelangeli, Darin S. Penneys, R. Douglas Stone, and Marie Claire Veranso-Libalah  Classification History of the Melastomataceae: Early Beginnings Through the Pre-molecular Era ��������������������������������������������������������������������   29 Frank Almeda  Morphological Variability Within the Melastomataceae (Myrtales), Including a Discussion of the Associated Terminology��������������������������������   45 Walter S. Judd, Lucas C. Majure, Fabián A. Michelangeli, Renato Goldenberg, Frank Almeda, Darin S. Penneys, and R. Douglas Stone  Historical Biogeography of the Melastomataceae����������������������������������������   87 Marcelo Reginato, Frank Almeda, Fabián A. Michelangeli, Renato Goldenberg, Peter W. Fritsch, R. Douglas Stone, and Darin S. Penneys Part II Systematics  New Melastomataceae Classification Informed by Molecular A Phylogenetics and Morphology����������������������������������������������������������������������  109 Darin S. Penneys, Frank Almeda, Marcelo Reginato, Fabián A. Michelangeli, Renato Goldenberg, Peter W. Fritsch, and R. Douglas Stone  Phylogeny and Circumscription of the Subfamily Olisbeoideae ����������������  167 R. Douglas Stone

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 The Subfamily Kibessioideae, its Tribe Pternandreae, and its Sole Genus, Pternandra��������������������������������������������������������������������������������������������������������  193 Susanne S. Renner  Systematics of the Tribe Astronieae Based on Morphology: Prospects for Resurrecting Bamlera and Incorporating Tessmannianthus������������������������  197 Jeffrey P. Mancera, Frank Almeda, and Darin S. Penneys  Systematics of Tribe Henrietteeae (Melastomataceae) ��������������������������������  219 Walter S. Judd and Darin S. Penneys Why Recognize Miconia as the Only Genus in Tribe Miconieae (Melastomataceae)? ����������������������������������������������������������������������������������������  235 Fabián A. Michelangeli, Antoine N. Nicolas, Gilberto Ocampo, Renato Goldenberg, Frank Almeda, Walter S. Judd, Eldis R. Bécquer, J. Dan Skean Jr, Mayara K. Caddah, Gretchen M. Ionta, Darin S. Penneys, Marcela Alvear, and Lucas C. Majure  Phylogenetics and Taxonomy of the Tribe Merianieae ��������������������������������  255 Fabián A. Michelangeli, Agnes S. Dellinger, Renato Goldenberg, Frank Almeda, Humberto Mendoza-Cifuentes, Diana Fernández-Fernández, Carmen Ulloa Ulloa, and Darin S. Penneys  Systematics and Climatic Preferences of Bertolonieae and Trioleneae������  275 Lucas F. Bacci, Thuane Bochorny, Géssica C. A. Bisewski, Luan S. Passos, Renato Goldenberg, and Fabián A. Michelangeli  Overview of Pyxidantheae (Melastomataceae) ��������������������������������������  291 An Darin S. Penneys and Frank Almeda  The Cyphostyleae, a Small Tribe Rich in Rare Characters in the Family ����������������������������������������������������������������������������������������������������  307 Fabián A. Michelangeli, Jhon Steven Murillo-Serna, and Humberto Mendoza-Cifuentes  Systematics of the Tribe Sonerileae����������������������������������������������������������������  321 Ying Liu, Marie Claire Veranso-Libalah, Gudrun Kadereit, Ren-Chao Zhou, J. Peter Quakenbush, Che-Wei Lin, and Jarearnsak Sae Wai  Systematics and Phylogeny of Dissochaeteae������������������������������������������������  345 Abdulrokhman Kartonegoro, Gudrun Kadereit, and Marie Claire Veranso-Libalah  Systematics and Evolution of Tribe Pyramieae��������������������������������������������  359 Thuane Bochorny, Lucas F. Bacci, Fabián A. Michelangeli, Frank Almeda, and Renato Goldenberg Systematics of Tribe Rhexieae������������������������������������������������������������������������  373 Walter S. Judd and Gretchen M. Ionta

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 Lavoisiereae: A Neotropical Tribe with Remarkable Endemism on Eastern Brazilian Mountaintops����������������������������������������������������������������������������������  385 Ricardo Pacifico and Frank Almeda  Systematic Studies in the Neotropical Tribe Marcetieae������������������������������  409 Maria José Reis da Rocha, Diego Nunes da Silva, and Paulo José Fernandes Guimarães  Systematics and Taxonomy of the Tribe Melastomateae������������������������������  429 Marie Claire Veranso-Libalah, R. Douglas Stone, Gudrun Kadereit, and Paulo José Fernandes Guimarães Part III Evolution: Morphology, Biology, Reproduction and Biogeography  Comparative Approach to Floral Ontogeny in Melastomataceae ����������  467 A João Paulo Basso-Alves and Simone Pádua Teixeira  New Perspective on Seed Morphological Features in Melastomataceae  491 A Gilberto Ocampo, Fabián A. Michelangeli, Darin S. Penneys, Vanessa Handley, Rocío González-Moreno, Edgar Herrera-Dimas, and Frank Almeda  Patterns of Chromosome Number Diversity and Evolution in the Melastomataceae����������������������������������������������������������������������������������������������  533 Frank Almeda and Darin S. Penneys Apomixis in Melastomataceae������������������������������������������������������������������������  563 Ana Paula Souza Caetano and Paulo Eugênio Oliveira  Pollination in Melastomataceae: A Family-­Wide Update on the Little We Know and the Much That Remains to Be Discovered����������������������������  585 Agnes S. Dellinger, Constantin Kopper, Katharina Kagerl, and Jürg Schönenberger  Stamen Diversity in Melastomataceae: Morphology, Color, and Function 609 Lílian R. F. Melo, Thais N. C. Vasconcelos, Ana Paula Souza Caetano, and Vinícius L. G. de Brito  Historical Biogeography of the Neotropical Miconieae (Melastomataceae) Reveals a Pattern of Progressive Colonization Out of Lowland South America������������������������������������������������������������������������������������������������������������  629 Fabián A. Michelangeli, Antoine N. Nicolas, Gilberto Ocampo, Renato Goldenberg, Frank Almeda, Walter S. Judd, Eldis R. Bécquer, J. Dan Skean Jr, Ricardo Kriebel, Karla Sosa, Mayara K. Caddah, Gretchen M. Ionta, Jesus R. de Santiago, Darin S. Penneys, Marcela Alvear, Maria Gavrutenko, Janelle M. Burke, Lucas C. Majure, and Marcelo Reginato

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 Patterns of Diversification of Miconia (Miconieae) in the Greater and Lesser Antilles ������������������������������������������������������������������������������������������  645 Lucas C. Majure, Eldis R. Bécquer, J. Dan Skean Jr, Gretchen M. Ionta, and Walter S. Judd  Colonization and Diversification of Melastomataceae in the Atlantic Forest of South America����������������������������������������������������������������������������������  673 Lucas F. Bacci, Thuane Bochorny, Renato Goldenberg, Mayara K. Caddah, Fabrício S. Meyer, Marcelo Reginato, and Fabián A. Michelangeli Part IV Ecology  Distributions of Amazonian Melastomataceae Species Along a Soil Gradient������������������������������������������������������������������������������������������������������������  689 Kalle Ruokolainen, Lassi Suominen, and Hanna Tuomisto  Seed Germination Ecology in Neotropical Melastomataceae: Past, Present, and Future������������������������������������������������������������������������������������������  707 Carlos A. Ordóñez-Parra, João Vitor S. Messeder, Carolina Mancipe-­ Murillo, Manuela Calderón-Hernández, and Fernando A. O. Silveira  Seed Dispersal Ecology in Neotropical Melastomataceae����������������������������  735 João Vitor S. Messeder, Tadeu J. Guerra, Marco A. Pizo, Pedro G. Blendinger, and Fernando A. O. Silveira  Ecology and Control of Naturalized Melastomataceae��������������������������������  761 Saara J. DeWalt, Julie S. Denslow, and M. Tracy Johnson Conclusion and Future Prospects������������������������������������������������������������������  791

Editors and Contributors

About the Editors Renato Goldenberg  is a full professor (Professor Titular) at the Botany Department in the Universidade Federal do Paraná, in Curitiba, Brazil. He studied Agronomy at the Universidade de São Paulo, then got both his masters and PhD in Plant Biology at the Universidade Estadual de Campinas, with a short internship at the National Museum of Natural History, in Washington, DC. He spent two sabbatical periods in the USA, working at the New York Botanical Garden and, again, at the National Museum of Natural History. Nowadays, he teaches mostly plant systematics and field botany for undergrads, and also in the botany/vegetal biology graduate programs at his home institution and also at UNICAMP. His research focuses on taxonomy, systematics, and any other topic related to Melastomataceae. He is currently section editor for Phytotaxa and the Brazilian Journal of Botany and receives a productivity research grant from CNPq (Brazil). Fabián A. Michelangeli  is the Abess Curator of Tropical Botany in the Institute of Systematic Botany of the New York Botanical Garden. He studied Biology in his native Caracas at the Universidad Central de Venezuela and obtained a PhD in Plant Sciences from Cornell University. His research focuses on the systematics, taxonomy, and evolution of tropical plants, especially on the family Melastomataceae. He also teaches in the graduate program in Biology at the City University of New York and Forestry and Environmental Sciences at Yale University. He has been an Associate Editor of Brittonia since 2004. Frank  Almeda  is Curator Emeritus of Botany in the Institute for Biodiversity Science and Sustainability at the California Academy of Sciences (CAS) where he also served two terms as Director of Research. He did his undergraduate work in Botany and Bacteriology at the University of South Florida (Tampa) and then earned a PhD in Plant Sciences at Duke University. His research focuses on the Systematics and evolution of tropical vascular plants with a special emphasis on Melastomataceae xix

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and Symplocaceae. Before official retirement, he was also Research Professor of Biology at San Francisco State University (SFSU) where he served as major professor to numerous graduate students in the SFSU/CAS joint training program, an activity that he continues. He currently serves on the Editorial Board of Harvard Papers in Botany.

Contributors Frank  Almeda  Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA Marcela  Alvear  Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA Lucas  F.  Bacci  Florida Museum of Natural History, University of Florida, Gainesville, FL, USA João Paulo Basso-Alves  Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Eldis R. Bécquer  Jardín Botánico Nacional, Universidad de la Habana, La Habana, CP, Cuba Géssica C. A. Bisewski  Programa de Pós-graduação em Botânica, Universidade Federal do Paraná, Curitiba, PR, Brazil Pedro  G.  Blendinger  Instituto de Ecología Regional, CONICET  - Universidad Nacional de Tucumán, San Miguel de Tucumán, Argentina Thuane  Bochorny  Departamento de Botânica, Universidade Federal do Paraná, Centro Politécnico, Curitiba, PR, Brazil Vinícius  L.  G.  de  Brito  Instituto de Biologia, Universidade de Uberlândia, Uberlândia, Brazil Janelle  M.  Burke  Department of Biology, Howard University, Washington, DC, USA Mayara  K.  Caddah  Departamento de Botânica, Campus Reitor João David Ferreira Lima, Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil Ana Paula Souza Caetano  Laboratôrio de Estudos Integrados de Plantas, Instituto de Biociências,, Universidade Federal de Mato Grosso, Cuiabá, MT, Brazil Manuela  Calderón-Hernández  Laboratorio Nacional de Semillas, Instituto Colombiano Agropecuario, Antioquia, Colombia Agnes S. Dellinger  Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria

Editors and Contributors

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Julie  S.  Denslow  Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA, USA Saara  J.  DeWalt  Department of Biological Sciences, Clemson University, Clemson, SC, USA Diana Fernández-Fernández  Herbario Nacional del Ecuador QCNE, Unidad de Investigación, Instituto Nacional de Biodiversidad, Quito, Ecuador Peter W. Fritsch  Botanical Research Institute of Texas, Fort Worth, TX, USA Maria  Gavrutenko  Department of Biology, City University of New  York, New York, NY, USA Renato Goldenberg  Departamento de Botânica, Universidade Federal do Paraná, Centro Politécnico, Curitiba, PR, Brazil Rocío González-Moreno  Departamento de Biología, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes, Mexico Tadeu J. Guerra  Departamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil Paulo José Fernandes Guimarães  Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Vanessa  Handley  Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA Edgar Herrera-Dimas  Aguascalientes, Mexico Gretchen M. Ionta  Department of Biological & Environmental Sciences, Georgia College, Milledgeville, GA, USA M.  Tracy  Johnson  USDA Forest Service, Institute of Pacific Islands Forestry, Hilo, HI, USA Walter S. Judd  Department of Biology and Florida Museum of Natural History, University of Florida, Gainesville, FL, USA Gudrun  Kadereit  Systematik, Biodiversität & Evolution der Pflanzen, Ludwig-­ Maximilians Universität München and Botanische Staatssammlung München, Staatliche Naturwissenschaftlichen Sammlungen Bayerns (SNSB), München, Germany Katharina Kagerl  Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria Abdulrokhman  Kartonegoro  Research Center for Biodiversity and Biosystematics, National Research and Innovation Agency (BNIN), Bogor, Indonesia

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Constantin Kopper  Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria Ricardo  Kriebel  Department of Botany, California Academy of Sciences, San Francisco, CA, USA Che-Wei Lin  Herbarium of Taiwan Forestry Research Institute, Taipei, Taiwan Ying Liu  State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China Lucas C. Majure  Department of Biology and Florida Museum of Natural History, University of Florida, Gainesville, FL, USA Jeffrey P. Mancera  Department of Biology, University of the Philippines Manila, Manila, Philippines Carolina Mancipe-Murillo  Bogotá, DC, Colombia Lílian R. F. Melo  Programa de Pós-Graduação em Ecologia e Conservação dos Recursos Naturais, Universidade de Uberlândia, Uberlândia, MG, Brazil Humberto  Mendoza-Cifuentes  Jardín Botánico de Bogotá, Bogotá, DC, Colombia João Vitor S. Messeder  Biology Department & Ecology Program, Pennsylvania State University, State College, PA, USA Fabrício S. Meyer  Departamento de Botânica, Universidade Federal do Paraná, Centro Politécnico, Curitiba, PR, Brazil Fabián A. Michelangeli  New York Botanical Garden, Bronx, NY, USA Jhon Steven Murillo-Serna  Instituto de Biología, Herbario HUA, Universidad de Antioquia, Medellín, Colombia Antoine N. Nicolas  Department of Biology, Manhattan College, School of Science, Bronx, NY, USA Gilberto  Ocampo  Departamento de Biología, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes, Mexico Paulo Eugênio Oliveira  Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, MG, Brazil Carlos  A.  Ordóñez-Parra  Centro de Síntese Ecológica e Conservação, Departamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil Ricardo Pacifico  Universidade Federal do Espírito Santo - Campus São Mateus, São Mateus, ES, Brazil Luan S. Passos  Programa de Pós-graduação em Botânica, Universidade Federal do Paraná, Curitiba, PR, Brazil

Editors and Contributors

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Darin S. Penneys  Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA Marco A. Pizo  Departamento de Biodiversidade, Universidade Estadual Paulista, Instituto de Biociências, São Paulo, SP, Brazil J.  Peter  Quakenbush  Department of Biological Sciences, Western Michigan University, Kalamazoo, MI, USA Marcelo  Reginato  Departamento de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Susanne  S.  Renner  Department of Biology, Washington University, St. Louis, MO, USA Maria José Reis da Rocha  Departamento de Ciências Biológicas, Universidade do Estado de Minas Gerais, Ibirité, MG, Brazil Kalle Ruokolainen  Department of Biology, University of Turku (Turun Yliopisto), Turku, Finland Jesus R. de Santiago  Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico Jürg Schönenberger  Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria Diego Nunes da Silva  Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Fernando A. O. Silveira  Centro de Síntese Ecológica e Conservação, Departamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil J. Dan Skean Jr  Department of Biology, Albion College, Albion, MI, USA Karla Sosa  Department of Biology, Duke University, Durham, NC, USA R.  Douglas  Stone  School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa Lassi Suominen  Department of Biology, University of Turku (Turun Yliopisto), Turku, Finland Simone Pádua Teixeira  Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil Hanna Tuomisto  Department of Biology, University of Turku (Turun Yliopisto), Turku, Finland Carmen Ulloa Ulloa  Missouri Botanical Garden, St. Louis, MO, USA

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Thais  N.  C.  Vasconcelos  Department of Biological Sciences, University of Arkansas, Fayetteville, AR, USA Marie  Claire  Veranso-Libalah  Systematik, Biodiversität und Evolution der Pflanzen, Ludwig-Maximilians-Universität München, München, Germany Jarearnsak Sae Wai  Division of Biological Science, Faculty of Science, Prince of Songkla University Hat Yai, Songkhla, Thailand Ren-Chao  Zhou  State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China

Part I

An Introduction to Melastomataceae

Melastomataceae: Global Diversity, Distribution, and Endemism Carmen Ulloa Ulloa, Frank Almeda, Renato Goldenberg, Gudrun Kadereit, Fabián A. Michelangeli, Darin S. Penneys, R. Douglas Stone, and Marie Claire Veranso-Libalah

Introduction The Melastomataceae are among the 10 largest families of flowering plants with an estimated 173 genera and some 5858 species. The family has a long history of classification (Almeda, chapter “Classification History of the Melastomataceae: Early Beginnings Through the Pre-molecular Era”) and is divided into three major clades, the Kibessioideae (Renner, chapter “The Subfamily Kibessioideae, its Tribe Pternandreae, and its Sole Genus, Pternandra”), the Melastomatoideae (see individual tribe chapters) and the Olisbeoideae (Stone, chapter “Phylogeny and Circumscription of the Subfamily Olisbeoideae”). The majority of genera have a tribal placement confirmed by molecular analysis and supported by morphological characters (Michelangeli et al. 2020; Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”), including C. Ulloa Ulloa (*) Missouri Botanical Garden, St. Louis, MO, USA e-mail: [email protected] F. Almeda Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA e-mail: [email protected] R. Goldenberg Departamento de Botânica, Centro Politécnico, Universidade Federal do Paraná, Curitiba, PR, Brazil e-mail: [email protected] G. Kadereit Systematik, Biodiversität & Evolution der Pflanzen, Ludwig-Maximilians Universität München, München, Germany Botanische Staatssammlung München, Staatliche Naturwissenschaftlichen Sammlungen Bayerns (SNSB), Botanischer Garten München-Nymphenburg, München, Germany e-mail: [email protected]

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 R. Goldenberg et al. (eds.), Systematics, Evolution, and Ecology of Melastomataceae, https://doi.org/10.1007/978-3-030-99742-7_1

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six genera placed in three newly described tribes (Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). While the Kibessioideae are paleotropical, the Melastomatoideae and Olisbeoideae are pantropical, as are three tribes (the Astronieae, Melastomateae, and Sonerileae) within the Melastomatoideae. About 64% (3741) of the species of the Melastomataceae occur in the Americas, 25% (1472) in Asia and Oceania, 5.5% (349) in Madagascar, and 5.5% in continental Africa (326). The family is subcosmopolitan, mainly distributed in tropical and subtropical regions, but some species reach temperate latitudes. Melastomes range in elevation from sea level to about 4500 m in the tropical Andes of South America. Although some species occur in seasonally dry habitats in Africa, Madagascar, Sri Lanka, Thailand, and Brazil, there are no Melastomataceae in true desert environments. No genera are native to both the New and Old Worlds, but a few genera are disjunctly distributed between Africa, Madagascar, and Asia, e.g., Lijndenia, Medinilla, and Memecylon. Studies have heavily focused on the New World Melastomataceae with recent treatments, revisions, or monographs (see Michelangeli et al. 2020). Africa, with fewer species, mostly in the Melastomateae and Olisbeoideae, has also been the subject of recent phylogenetic and monographic publications (Stone 2012, 2014; Veranso-Libalah et al. 2017a, 2021). In contrast, the Asian tropics are poorly studied, with large genera like Astronia, Astronidium, Medinilla, Melastoma, Oxyspora, Phyllagathis, and Sonerila in need of modern revisions. Since 2000, 674 new species of Melastomataceae have been published: 446 for the Americas, 166 for Asia, 31 for continental Africa, and 31 for Madagascar and the Mascarenes. In the following, we present a summary of the number of species and distribution of all genera of the Melastomataceae following the recent tribal classification by Michelangeli et  al. (2020) and Penneys et  al. (chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”).

F. A. Michelangeli Institute of Systematic Botany, The New York Botanical Garden, Bronx, NY, USA e-mail: [email protected] D. S. Penneys Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA e-mail: [email protected] R. D. Stone School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa e-mail: [email protected] M. C. Veranso-Libalah Systematik, Biodiversität und Evolution der Pflanzen, Ludwig-Maximilians-Universität München, München, Germany e-mail: [email protected]

Melastomataceae: Global Diversity, Distribution, and Endemism

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Results This section provides separate accounts of melastome diversity and distribution in the Americas, Africa and Madagascar, and Asia and Oceania (Fig. 1), followed by a detailed summary (see Annotated Checklist) of species numbers and distributions of all genera sorted by taxonomic rank (subfamily, tribe) and geography (Fig. 2). For the Americas, the current distributions are found in the Vascular Plants of the Americas’ website (Ulloa Ulloa et  al. 2018): www.tropicos.org/project/VPA). Information on the nomenclature of the family is available at www.melastomataceae.net.

Fig. 1  Melastomataceae from various continents. Clockwise from top left: Blakea maurofernandeziana, Central America (photograph by F. Almeda, Costa Rica); Meriania aurata, South America (photograph by L.  Jost, Ecuador); Tristemma mauritianum, Africa (photograph by F.  Almeda, Madagascar); Melastoma malabathricum, South Pacific Islands (photograph by D.S.  Penneys); Osbeckia octandra, Southeast Asia (photograph by F. Almeda, Sri Lanka); Melastomastrum capitatum, continental Africa (Photograph by R. E. Gereau, Democratic Republic of Congo)

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Fig. 2  Melastomataceae species density by country or areas. For the Americas, the geographical areas include North America (Canada and the United States), Central America, West Indies, Guianas, and the Southern Cone, following the arrangement of Ulloa Ulloa et al. (2017)

Currently, there are 3 recognized subfamilies, the largest (the Melastomatoideae) with 21 tribes. All genera are now placed in tribes, but some have not been sampled in a molecular phylogenetic context (see Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). The Dinophoreae, Dissochaeteae, Feliciadamieae, and Kibessioideae are exclusively distributed in the Old World; the Melastomateae, Olisbeoideae, and Sonerileae are pantropical; the Astronieae are amphi-Pacific; and the remaining 15 tribes are New World endemics (i.e., the Bertolonieae, Cyphostyleae, Eriocnemeae, Henrietteeae, Lavoisiereae, Lithobieae, Marcetieae, Merianieae, Miconieae, Pyramieae, Pyxidantheae, Rhexieae, Rupestreeae, Stanmarkieae, and Trioleneae) (Fig. 3). The total number of Melastomataceae genera is 173 with ca. 5858 species (see Annotated Checklist). There are 84 genera currently recognized in the New World with ca. 3742 accepted species. In the Old World, there are ca. 89 genera comprising ca. 2117 species (see Annotated Checklist). Generic delimitation problems, especially within the Sonerileae, prevent us from having a clear picture of the number of genera and species, and the lack of monographs, large regional floras, and phylogenetic analyses hinders our estimates of species numbers in Asia.

Melastomataceae: Global Diversity, Distribution, and Endemism

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Fig. 3  Number of species of Melastomataceae by tribe/subfamily and geographical area

Americas The New World harbors 3741 species of Melastomataceae in 84 genera and in two subfamilies: the Olisbeoideae (2 gen./99 spp.) and the Melastomatoideae with 18 tribes: Astronieae (1 gen./7 spp.), Bertolonieae (1/35), Cyphostyleae (4/25), Eriocnemeae (3/7), Henrietteeae (3/95), Lavoisiereae (3/~269), Lithobieae (1/1), Marcetieae (20/~149), Melastomateae (17/~496), Merianieae (8/~301), Miconieae (1/1901), Pyramieae (4/70), Pyxidantheae (2/204); Rhexieae (3/21), Rupestreeae (1/2), Sonerileae (6/12), Stanmarkieae (2/4), and Trioleneae (2/43). They occur across North and South America, but most of the species (3689) are found in the tropics from western and southern Mexico throughout Central America to Bolivia and Brazil and the Caribbean. The most diverse genus by far is Miconia with 1901 currently known species, followed by five  genera with more than 100 species, Microlicia (258), Blakea (192), Pleroma (161), Meriania (120), and Chaetogastra (117); 48 genera are represented by less than 10 species and, of these, 17 are monospecific (Bisglaziovia, Brasilianthus, Dicrananthera, Eriocnema, Leiostegia, Lithobium, Maguireanthus, Mallophyton, Neblinanthera, Nepsera, Ochthephilus, Opisthocentra, Quipuanthus, Rostranthera, Sandemania, Schwackaea, and Tateanthus). The majority of species (2632) are restricted to a single country or area (following the Vascular Plant of the Americas arrangement), and fewer than 100 species are

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widespread. A few species have escaped cultivation to become noxious weeds elsewhere (e.g., Miconia calvescens DC., with beautiful purple-colored abaxial leaf surfaces is called the Purple Plague in Hawaii). The most invasive species is Koster’s Curse ((Clidemia hirta (L.) D.  Don, now Miconia crenata (Vahl) Michelang.), which is naturalized in tropical Africa, Indian Ocean islands, Asia, Oceania, Australia, and Hawaii (see DeWalt et  al., chapter “Ecology and Control of Naturalized Melastomataceae”). With some 1453 species, Brazil is by far the country with the highest melastome diversity in the Americas and globally (Fig. 2). Nearly two-thirds (929) of the species are endemic (Baumgratz et al. 2010; Goldenberg et al. 2020a). These species are centered in the Cerrado and the campo rupestre, the Atlantic Forest (see Bacci et al., chapter “Colonization and Diversification of Melastomataceae in the Atlantic Forest of South America”), and also in and around the Amazon basin, mostly near the wetter areas closer to the Andes to the west, the Guiana Shield to the north, and the transition to the Cerrado to the south. In all, 11 genera are endemic to Brazil: Bertolonia (near-endemic), Bisglaziovia, Brasilianthus, Cambessedesia, Eriocnema, Fritzschia, Lithobium, Merianthera, Microlicia (nearly endemic), Physeterostemon, and Rupestrea. Another six genera are largely centered in or have their greatest diversity in Brazil: Huberia, Marcetia, Pleroma, Pterolepis, Rhynchanthera, and Siphanthera. The uniquely Brazilian vegetation known as campo rupestre at higher elevations (mostly from about 800 to 2000 m), on the Cadeia do Espinhaço in Minas Gerais and Bahia states, is noted for its high incidence of generic and species-level endemism in a number of angiosperm families. In virtually all campo rupestre areas that have been studied to date, the Melastomataceae are typically one of the 10 or 12 families represented by the greatest number of species (Harley 1995; Giulietti and Pirani 1997; Pacifico and Almeda, chapter “Lavoisiereae, a Neotropical Tribe with Remarkable Endemism on Eastern Brazilian Mountaintops”). The tropical Andes with 1964 species is another hotspot on the South American continent with most species in the montane cloud forests. Colombia has 991 spp., Peru 663 spp., Venezuela 636 spp., Ecuador 602 spp., and Bolivia 331  spp. The endemic and near-endemic genera of the tropical Andes are Allomaieta, Alloneuron, Andesanthus (nearly endemic), Brachyotum, Bucquetia, Castratella, Centradeniastrum, Chaetolepis (nearly endemic), Chalybea, Kirkbridea, Quipuanthus, and Wurdastom. Amazonia (as defined by Cardoso et al. 2017, i.e., land below 1000 m elevation) harbors around 690 species, many of them widely distributed or found in more than one country. The most species-rich areas in western and northern Amazonia are near the foothills of the Andes or the Guiana Highlands. Amazonian-centered genera are Acanthella, Bellucia, Henriettea, Opisthocentra, and Pachyloma. Among the tropical Andean countries, Colombia is a notable center of diversity. It has 991 species in 54 genera, 326 (ca. 33%) of which are endemic to the country. The distribution of melastome species among the 10 biogeographic regions of Colombia recognized by Bernal et al. (2016) is heavily concentrated in the Andes with 650 species (ca. 65%); some 261 (40%) species are endemic. Miconia, with 543 species, constitutes nearly 55% of melastome species in the country (Almeda

Melastomataceae: Global Diversity, Distribution, and Endemism

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et al. 2016b; Michelangeli et al. 2020). The Sierra Nevada de Santa Marta (SNSM) in northern Colombia, the world’s highest coastal mountain, is a displaced fault-­ bounded block that is isolated from the continuous ranges of the Andes by wide alluvial plains. This massif has long been recognized for its biological diversity and endemism, but much of the area remains insufficiently explored (Rangel and Garzón 1997). To date, some 17 genera and 86 species of Melastomataceae have been reported for the SNSM. In all, one genus, Kirkbridea, and 15 species are endemic to the SNSM (Alvear et al. 2015). Because of its large size (12,000 sq. km), elevation (5775 m), habitat diversity, and geographic position in northernmost Colombia, the SNSM could have played a stepping stone role in the migration of the Melastomataceae from the Andes to Central America, which is reflected in species distributions and affinities of these two regions (Alvear et al. 2015). At about 10.5° N, the range is actually farther from the equator than Panama and most of Costa Rica, which are to its southwest and west, respectively. The Guiana Shield (Guyana, Suriname, French Guiana, Venezuelan Guayana, and neighboring Brazil) has a unique flora with some 450 species (Berry et  al. 2002). Endemic genera to this region are Appendicularia, Comoliopsis, Leiostegia, Maguireanthus, Mallophyton, Neblinanthera, Ochthephilus, Rostranthera, Tateanthus, and Tryssophyton. Two genera disjunct between the Andes and the Guiana Shield are Boyania, with one species in Caquetá (Colombia) and one in Guyana, and Phainantha, with one species on the sandstone table tops of the Cordillera del Cóndor in southeastern Ecuador and four in southeastern Venezuela and western Guyana. Macrocentrum is also mostly centered in the Guiana Shield with 25 species, but one species is endemic to the Coastal Cordillera of Venezuela and 2 to the Andes of Ecuador and Peru. The Mexican and Central American region represents the northern center of diversity for the family in the western hemisphere. It has 546 species in 29 native genera (plus Heterotis and Pleroma, introduced adventives) representing 11 tribes of the Melastomatoideae plus the Olisbeoideae (Almeda 2009). Many species in several genera are shared with the tropical Andes and the adjacent areas of South America, but an impressive 317 species (58%) are endemic to the region. A heavy concentration of this diversity is centered in Costa Rica and Panama where 166 species (ca. 30%) are endemic. Species numbers decrease as one moves northward to Mexico where some 204 species occur (Villaseñor 2016; Zabalgoitia et al. 2020). Much of the diversity in Mexico is centered in the southern states of Oaxaca, Chiapas, and Veracruz with the 48 endemic Mexican species scattered throughout the southern and western states of the country. Two genera, Heterocentron and Stanmarkia, are restricted to the Mexican/Central American region and two others, Centradenia and Pilocosta, have all but one of their species restricted to the region, which makes them near-endemics. In the Greater Antilles, some 452 species are found. There are no genera endemic to this region, although several radiations in the Miconieae and Merianieae have occurred. However, 392 species (87%) are endemic to the region, with most of them being single island endemics. In the Lesser Antilles, there are 66 species, and 13 of

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them endemic (see Majure et al., chapter “Patterns of Diversification of Miconia (Miconieae) in the Greater and Lesser Antilles”). The Melastomataceae are not particularly diverse in temperate regions. Two genera occur in continental United States. The West Indian species Miconia bicolor L. reaches southern Florida. Rhexia, with 13 species, is largely centered in the southeastern United States, with one species, Rhexia virginica L., reaching Lake Huron in southern Ontario and Nova Scotia in Canada, and one other, Rhexia cubensis Griseb., reaching the Greater Antilles (Cuba, Dominican Republic, and Puerto Rico). In the Southern Cone (Argentina, Paraguay, and Uruguay), there are 67 species. Chile, with its large Atacama Desert, is the only country in the Americas without records of native Melastomataceae.

Africa and Madagascar Tropical Africa harbors 675 species of Melastomataceae in 41 genera and two subfamilies: the Melastomatoideae (37 gen./440 spp.) and the Olisbeoideae (4 gen./235 spp.). The African/Malagasy Melastomatoideae species belong to four tribes (the Dinophoreae (2 gen./3 spp.), Feliciadamieae (1/1), Melastomateae (25/199), and Sonerileae (87/237)). The most species-rich genera are Memecylon (172), Gravesia (116), Medinilla (76), Warneckea (49), Dichaetanthera (36), and Rosettea (21). Dichaetanthera, with 28 species, and Gravesia with 116 stand out as the two African/ Malagasy genera with the major centers of diversity in Madagascar (Almeda et al. in press). In all, 11 genera are monospecific (Anaheterotis, Almedanthus, Benna, Cailliella, Derosiphia, Dionychastrum, Dinophora, Feliciadamia, Pseudosbeckia, Pyrotis, and Spathandra). The remaining 24 genera comprise fewer than 20 species each. Only three genera, Lijndenia, Medinilla, and Memecylon, are also found in Asia with Memecylon extending to Oceania. There are no genera shared between tropical Africa and the Americas. Although mainland tropical Africa is about 32 times larger than Madagascar, the latter is the fourth largest island in the world (587,041 km2) and is home to more than half of the melastome species in the two  regions (51%; 346 spp.). One-quarter of Madagascar’s genera are endemic to the island, and, at the species level, 99% are endemic (Almeda et al. in press). For the melastomes, as for most flowering plant families, Madagascar harbors a higher incidence of species-level endemism than any area of comparable size in the world. Approximately 80% of the Malagasy species belong to just three of the 12 native genera—Gravesia, Medinilla, and Memecylon. After Madagascar, the Guinean-Congolian region follows in terms of species richness and endemism with the following countries leading: Cameroon (7 gen./104 spp.), The Democratic Republic of Congo (DR Congo) (15/99), Gabon (14/89), Guinea (9/59), Equatorial Guinea (3/51), The Republic of Congo (Congo) (2/47), Liberia (2/45), and Nigeria (2/43). Several countries of the Zambezian region are also species-rich in several endemic species (Tanzania (29/73), Angola (17/62), Zambia (2/37), Mozambique (7/27), South Africa (5/11), Kenya (4/15), and Malawi

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(1/15)). The southern part of Africa is not species-rich, but of the 11 species occurring there, five are endemic. The small islands Comoros (3/13), Mauritius (3/7), São Tomé and Príncipe (1/11), Réunion (1/2), and Seychelles (1/3) also harbor few species, some of which are endemic. Three genera (Amphorocalyx, Dionycha, and Rousseauxia) are endemic to Madagascar, and nine genera (Antherotoma, Dichaetanthera, Gravesia, Lijndenia, Medinilla, Memecylon, Nerophila, Tristemma, and Warneckea) are disjunct between Africa and Madagascar but with only three disjunct species (Antherotoma naudinii Hook.f., Tristemma mauritianum J.F.  Gmel., and Warneckea sansibarica (Taub.) Jacq.-Fél.). The remaining 27 genera are endemic to Africa. One species, Memecylon cordatum Lam., is disjunct between Mauritius and Réunion. The Guinean-Congolian and Zambezian regions are not just species-rich; each of them tends to show strong patterns of endemism. Almedanthus, Dissotidendron, Eleotis, Pseudosbeckia, and Pyrotis are all restricted to the Zambezian region; Dionychastrum is endemic to Tanzania. Three genera (Benna, Cailliella, and Feliciadamia) are endemic to Guinea. Anaheterotis is narrowly distributed and restricted to Guinea and Sierra Leone. Eight other genera, Amphiblemma, Derosiphia, Dicellandra, Dinophora, Dissotis, Ochthocharis, Preussiella, and Spathandra, are restricted to the Guinean-Congolian regions, whereas Nothodissotis is endemic to the Congolian region with a narrow distribution in Cameroon, Equatorial Guinea, Gabon, and São Tomé and Príncipe. There are only a few widespread species and genera, e.g., Heterotis is widespread in tropical Africa and extends to Mauritius and Seychelles. Heterotis prostrata Benth is not only known in Africa but is also naturalized outside of the continent in India, Singapore, Australia, the West Indies, Costa Rica, and the islands in the Pacific Ocean.

Asia and Oceania The Asia and Oceania region, as concerns the Melastomataceae, is inclusive of India to the west, Nepal, Bhutan, China, and Japan to the north, the island nations and territories of the South Pacific to the east, Australia to the south, and all of the Malesian floristic area. In this discussion, five bioregions are recognized: Mainland Asia and Sundaland, Wallacea, Sahul, the Philippines, and Oceania. Because generic monophyly is unconfirmed in most cases, and modern monographs and floras are generally lacking, the tallies cited here are likely to change as our understanding improves. The Melastomataceae are represented here by 50 genera and ca. 1462 species belonging to the three subfamilies: the Kibessioideae, a monogeneric subfamily (Pternandra, 15 species), is exclusive to Asia; the Olisbeoideae with 2 genera/204 species; and the Melastomatoideae with  five tribes (the Astronieae, Dinophoreae, Dissochaeteae, Melastomateae, and Sonerileae) with 47/1240. Of these tribes, only the Dissochaeteae is endemic to the region. The most diverse genus by far is Medinilla (379), followed by Memecylon (202), Sonerila (184),

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Melastoma (80), Phyllagathis (74), Astronidium (67), Astronia (59), and Osbeckia (51). Eight genera are monospecific. Indonesia (457 species) and Malaysia (365) are the most diverse countries, followed by India (199), the Philippines (183), Vietnam (135), China (113), and Brunei (109). The northernmost temperate species, Osbeckia chinensis L., reaches the main Japanese island of Honshu and the southern islands of Shikoku and Kyushu. Six introduced species of the Miconieae have been recorded in the region, with Miconia crenata being particularly noxious and widespread. Some other aliens include Arthrostemma (1 species), Bellucia (1), Heterocentron (2), Heterotis (1), Pleroma (6), and Tristemma (1). For the purposes of this discussion on Melastomataceae diversity and distribution, Mainland Asia and Sundaland are inclusive of India, the southern flanks of the Himalayas, China, Japan, Taiwan, Borneo, Bali, Java, Sumatra, Sri Lanka, and all other lands within this delimitation. These areas have been connected by land bridges during glacial maxima, likely explaining their biological similarity. Except for Lijndenia, Medinilla, and Memecylon, which are shared with the African region, all genera are endemic and several range beyond the mainland and Sundaland; no genus is native to both the Asian and American realms. The Olisbeoideae in Mainland Asia and Sundaland include Lijndenia with three species, all endemic, and Memecylon (at all ranks) has 167 taxa in the region, all but 10 of which are endemic. Within the Melastomatoideae, the Astronieae are represented by Astronia (7 species/2 endemic) and Beccarianthus (1/1). The five species of Ochthocharis (Dinophoreae) are restricted to this region, three of which are also found in Wallacea and/or the Sahul. The Dissochaeteae have Creochiton (6/6), Dalenia (1/1), Diplectria (8/8), Dissochaeta (49/41), Macrolenes (18/18), and Pseudodissochaeta (4/4). The Melastomateae in this region include Melastoma (51/40) and Osbeckia (50/49), the former with 41 species in Borneo and the latter with 30 species in India alone. Situated on the Sunda Shelf, Borneo is the world’s third largest island (748,168 sq. km.) and has a greater diversity of melastome genera and species (32 genera and 388 species) than any other. Boerlagea (1 species), Brittenia (1), Cyanandrium (5), and Neodriessenia (6) are all restricted to Borneo. Borneo is the center of diversity for Anerincleistus with 22 of its 39 species occurring there, Catanthera (9 of 17), Dissochaeta (26 of 54), Driessenia (14 of 14), and Heteroblemma (12 of 14). Pternandra has 12 of its 15 species in Borneo; seven are found on Mainland Asia, two of which are absent from Borneo, and only one species is extralimital. The Sonerileae have diversified extensively in Mainland Asia and Sundaland, with members occupying a wide range of habitats and adopting life forms from small, understory herbs to shrubs, trees, climbers, and epiphytes. Only Medinilla and seven other genera have ranges that extend beyond this region, i.e., Anerincleistus (1  in the Philippines), Catanthera (1  in Maluku Islands, 10  in New Guinea), Driessenia (1 in Sulawesi), Heteroblemma (1 in New Guinea), Pachycentria (1 in Maluku Islands, 2  in New Guinea and the Philippines), Sarcopyramis (1  in the Philippines), and Sonerila (3 in Maluku Islands, 2 in Sulawesi and the Philippines, 1 in New Guinea). The 22 genera in the Sonerileae that are restricted to this region

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are Aschistanthera, Barthea, Blastus, Boerlagea, Bredia, Cyanandrium, Fordiophyton, Kendrickia, Kerriothyrsus, Neodriessenia, Oxyspora, Phyllagathis, Plagiopetalum, Plethiandra, Poilannammia, Scorpiothyrsus, Sporoxeia, Stussenia, Styrophyton, Tashiroea, Tigridiopalma, and Vietsenia. Compared to Mainland Asia and Sundaland, the melastome flora east of Wallace’s Line is generally depauperate. Herbaceous taxa are nearly absent. Consistent with typical patterns of island biogeography, smaller, more isolated islands have fewer species and larger ones with more varied niches have richer melastome floras. Wallacea is the biogeographical region that lies in between the Sunda Shelf to the west and the Sahul Shelf to the east. This is a series of mostly Indonesian islands including the Lesser Sunda Islands (from Lombok eastward), Maluku Islands, and Sulawesi. There are 81 species of melastomes native to Wallacea. Of those, 41 are endemic, seven are shared with the Sahul region, 17 are shared with Sundaland, and 16 are found in all three areas. The Olisbeoideae are represented by Memecylon (12 species, 6 endemic) and the Kibessioideae by Pternandra (3/1). Other groups represented in this region are Astronia (Astronieae; 7/4), Ochthocharis (Dinophoreae; 1/0), Dissochaeta (Dissochaeteae; 8/0), Melastoma (15/10), and Osbeckia (1/1) in the Melastomateae and, in the Sonerileae, Catanthera (1/1), Driessenia (1/1), Medinilla (26/12), Pachycentria (1/0), and Sonerila (5/5). Situated on the Sahul Shelf, a region that also includes Australia, New Guinea (785,753 sq. km) is the second largest island on Earth and has 228 native melastome species (188 endemic, 82%) (Cámara-Leret et al. 2020). In all, 16 genera from all seven major groups (subfamilies and tribes) of melastomes that occur in the Asia-­ Oceania region are found here. Members of the Astronieae have radiated on the island with Astronia (30 species/29 endemic), Astronidium (23/21), and Beccarianthus (4/4). The Sonerileae are the largest tribe on the island, totaling 130 species. Medinilla comprises 91 species (82 endemic), followed by Poikilogyne (25/23), Catanthera (10/9), Pachycentria (2/1), Heteroblemma (1/1), and Sonerila (1/0). Memecylon (16/10) is the only member of the Olisbeoideae in New Guinea. The remaining taxa are for the Dissochaeteae: Creochiton (4/4) and Dissochaeta (8/3); for the Melastomateae: Melastoma (30/15) and Osbeckia (1/0); for the Dinophoreae: Ochthocharis (3/1); and for the Kibessioideae: Pternandra (4/0). The 15 melastome species native to Australia are closely allied to those in nearby New Guinea and include Medinilla (1/1), Melastoma (7/0), Memecylon (3/2), Osbeckia (2/1), Poikilogyne (1/0), and Pternandra (1/0). The Philippines has a complex and varied geological history that is reflected in its floristic affinities with Sundaland, Wallacea, and the Sahul. Considering the melastome genera found in this country, it is more similar to the latter two biogeographic regions than it is to Mainland Asia and Sundaland. The Philippines has 180 native melastome species. Heterotis prostrata and Miconia crenata are aliens. In the Astronieae, Astrocalyx calycina is an endemic, monospecific, endangered genus. Astronia has 20 species, 19 of which are endemic. Here, the four species of Beccarianthus are all endemic. In addition, Ochthocharis javanica (Dinophoreae); Creochiton (3 species/3 endemic) and Dissochaeta (8/2) in the Dissochaeteae; Melastoma (11/3) and Osbeckia chinensis in the Melastomateae; Lijndenia (1/0)

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and Memecylon (38/32) in the Olisbeoideae; and Anerincleistus (1/1), Medinilla (88/78), Pachycentria (2/0), Sarcopyramis (1/0), and Sonerila (2/1) in the Sonerileae are also reported here. Here, Oceania is limited to the region encompassing the South Pacific island nations and territories within Melanesia, Micronesia, and Polynesia. Within this immense expanse of oceanic islands, there are a total of four genera and 77 native melastome species. Fiji has the greatest diversity with four genera and 31 native species, followed by the Solomon Islands (2/21), Samoa (3/10), Vanuatu (4/7), Caroline Islands (3/6), Society Islands (2/6), Wallis-Futuna Islands (2/2), and the Marianas (2/2). Of the 46 species of Astronidium here, only four are distributed between two areas, the rest are single-area endemics. There are 25 species of Medinilla, each restricted to a single area. Melastoma denticulatum Labill. is widespread in this region and can even be found in Australia; two other species of this genus are found in Samoa, and one variety of Melastoma malabathricum L. is in two areas. One Memecylon species is distributed in two areas, and a second is a single-area endemic.

Annotated Checklist. The Melastomataceae are arranged by subfamily, tribe, and genus. For each genus, the current number of accepted species in parenthesis, a brief geographic range, and the recent literature are presented. Tribes and their genera are arranged alphabetically. Groups that contain both New World and Old World genera are presented first by geography I. Subfamily Olisbeoideae (see Stone, chapter “Phylogeny and Circumscription of the Subfamily Olisbeoideae”) Americas, Africa, Asia, Oceania, six genera; Stone (2006). Tropical America Mouriri Aubl. (89), Tropical America, especially Brazil (53); Morley (1976). Votomita Aubl. (10), Panama, Cuba, Amazonia: Colombia, Venezuela, Guianas, Brazil; Morley (1963, 1976, 1989, 1999), Morley and Almeda (1995). Africa, Asia, Oceania Lijndenia Zoll. & Moritzi (16), Tropical Africa, Madagascar, Sri Lanka, Malesia; Bremer (1982). Jacques-Félix (1985a, b), Stone and Luke (2015), Stone (2017). Memecylon L. (391), Africa (76), Madagascar (96), Indian Ocean islands (14), South and Southeast Asia (98), Malesia (97), Oceania (13); Jacques-Félix (1985a, b), Stone (2012, 2014), Amarasinghe et al. (2021). Spathandra Guill & Perr. (1), West and Central Africa; Jacques-Félix (1978). Warneckea Gilg (49), Africa, Madagascar, Mauritius; Stone and Andreasen (2010). II. Subfamily Kibessioideae (see Renner, chapter “The Subfamily Kibessioideae, Its Tribe Pternandreae, and Its Sole Genus, Pternandra”) Tropical Asia, one genus. Pternandra W. Jack (15), Australia, Southeast Asia to India; Maxwell (1981).

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III. Subfamily Melastomatoideae Pantropical, 21 tribes. 1. Astronieae (see Mancera et al., chapter “Systematics of Tribe Astronieae Based on Morphology: Prospects for Resurrecting Bamlera and Incorporating Tessmannianthus”) Amphi-Pacific tribe in America, Asia, and Oceania. Tropical America. Tessmannianthus Markgr. (7), Panama, Colombia to Peru; Almeda (2009). Tropical Asia, Oceania. Astrocalyx Merrill (1), Philippines; Maxwell and Veldkamp (1990a), Penneys (2013), Mancera 2017. Astronia Blume (59), China, Malaysia, Philippines, Pacific Islands; Maxwell and Veldkamp (1990a), Mancera (2017). Astronidium A. Gray (67), Malay Archipelago; Maxwell and Veldkamp (1990b), Mancera (2017). Beccarianthus Cogn. (9), Malay Archipelago; Maxwell and Veldkamp (1990b), Mancera (2017). 2. Bertolonieae (see Bacci et al., chapter “Systematics and Climatic Preferences of Tribes Bertolonieae and Trioleneae”) Tropical America, one genus. Bertolonia Raddi (35), Brazil (Atlantic Forest); Baumgratz (1989), Bacci et al. (2018, 2020). Unplaced species: Bertolonia venezuelensis Wurdack, Venezuela. 3. Cyphostyleae (see Michelangeli et al., chapter “The Cyphostyleae, a Small Tribe Rich in Rare Characters in the Family”) Western South America, four genera; Michelangeli et al. (2011). Allomaieta Gleason (10), Colombia; Lozano and Becerra de Lozano (1999), Michelangeli et al. (2011). Alloneuron Pilg. (6), Colombia and Peru; Wallnöfer (1996, 1999), Michelangeli and Ulloa Ulloa (2016). Quipuanthus Michelang. & C. Ulloa (1), Eastern Ecuador and northeastern Peru; Michelangeli et al. (2014). Wurdastom B. Walln. (8), Colombia to Peru; Wallnöfer (1996), Mendoza-Cifuentes (2020). 4. Dinophoreae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) Tropical Africa and Asia; Veranso-Libalah et al. (2018). Dinophora Benth. (1), West-Central Africa; Jacques-Félix (1983). Ochthocharis Blume (5), Tropical Asia; Hansen and Wickens (1981). Phaeoneuron Gilg (2), West Tropical Africa; Hansen and Wickens (1981). 5. Dissochaeteae (see Kartonegoro et al., chapter “Systematics and Phylogeny of Dissochaeteae”) Tropical Asia, six genera (Kartonegoro et al. 2021). Creochiton Blume (12), New Guinea, Java, Philippines; Kartonegoro and Veldkamp (2013), Kartonegoro et al. (2020). Dalenia Korth. (7), India, Malaysian region; Kartonegoro et al. (2021). Diplectria (Blume) Rchb. (7), Burma, Malay Peninsula; Kartonegoro et al. (2021). Dissochaeta Blume (30), China, India, Indonesia, Malaysia, Myanmar, New Guinea, Philippines, Vietnam; Kartonegoro et al. (2018, 2021). Macrolenes Naudin (27), Peninsular Thailand, the Malay Peninsula, Sumatra, Java and Borneo; Kartonegoro et al. (2019, 2021). Pseudodissochaeta Nayar (5), Southeast Bhutan, northeastern India, northern Myanmar, southern China, northern Thailand, Cambodia, Laos, Vietnam; Kartonegoro et al. (2020). 6. Eriocnemeae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) Tropical America, three genera. Eriocnema Naudin (1), Brazil; Penneys et al. (2020). Ochthephilus Wurdack (1), Guyana; Penneys et al. (2020). Physeterostemon R. Goldenb. & Amorim (5), Brazil; Goldenberg and Amorim (2006), Amorim et al. (2009).

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7. Feliciadamieae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) Africa, one monospecific genus. Feliciadamia Bullock (1), Guinea; Jacques-Félix (1994). 8. Henrietteeae (see Judd & Penneys, chapter “Systematics of Tribe Henrietteeae”) Tropical America, three genera. Bellucia Neck. ex Raf. (22), Tropical America; Renner (1989), Penneys et al. (2010). Henriettea DC. (71), Tropical America; Penneys et al. (2010). Kirkbridea Wurdack (2), Colombia; Wurdack (1976). 9. Lavoisiereae (see Pacifico & Almeda, chapter “Lavoisiereae, a Neotropical Tribe with Remarkable Endemism on Eastern Brazilian Mountaintops”) Tropical America, three genera, mostly in Brazil; Fritsch et al. (2004); Versiane et al. (2021). Microlicia D. Don (249), Mostly Brazil, a few species elsewhere in tropical South America; Koschnitzke and Martins (2006), Martins (1997), Martins and Almeda (2017). Poteranthera Bong. (5), Colombia, Bolivia, Venezuela, Brazil; Kriebel (2012), Rocha et al. (2016), Almeda and Pacifico (2018). Rhynchanthera DC. (15), Mexico to Brazil and Paraguay, but most in southeastern Brazil; Renner (1990). 10. Lithobieae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) Tropical America, one genus. Lithobium Bong. (1), Brazil (Minas Gerais), campos rupestres; Penneys et al. (2020). 11. Marcetieae (see Rocha et al., chapter “Systematic Studies in the Neotropical Tribe Marcetieae”) Tropical America, 20 genera. Acanthella Hook.f. (2), Colombia, Venezuela, Brazil. Aciotis D. Don (13), Southern Mexico, Central America, Colombia and Venezuela to the Guianas, Brazil, Trinidad; Freire-Fierro (2002). Acisanthera P. Browne (8), Southern Mexico to Argentina, Paraguay, Caribbean; Kriebel (2008), Guimarães et al. (2017), Rocha et al. (2018 [2017]). Appendicularia DC. (3), Venezuela, Guianas, northeastern Brazil; Rocha et al. (2018 [2017]), Silva et al. (2020). Brasilianthus Almeda & Michelang. (1), Brazil (Pará); Almeda et al. (2016a), Rocha et al. (2018 [2017]). Comolia DC. (12), Brazil, Colombia, Guianas, Trinidad, Venezuela; Seco (2006). Comoliopsis Wurdack (3), Venezuela (Cerro de la Neblina). Dicrananthera C. Presl. (1), Colombia, Venezuela, Brazil; Rocha et al. (2018 [2017]). Ernestia DC. (14), Colombia, Peru, Venezuela, Guianas, Brazil; Rocha et al. (2018 [2017]). Fritzschia Cham. (12), South-Central Brazil; Rocha et al. (2018 [2017]). Leiostegia Benth. (1), Venezuela, Guianas, Brazil; Rocha et al. (2018 [2017]). Macairea DC. (22), Tropical South America; Renner (1989). Mallophyton Wurdack (1), Venezuela; Berry et al. (2002). Marcetia DC. (30), Most diverse in Brazil, also Colombia, Guianas, Venezuela; Martins (1989). Nepsera Naudin (1), Central America, Colombia, Ecuador, Venezuela, Guianas, Brazil, Cuba to Trinidad. Noterophila Mart. (6), Tropical America; Rocha et al. (2018 [2017]). Pseudoernestia (Cogn.) Krasser (2), Brazil, Colombia, Guianas, Venezuela; Rocha et al. (2018 [2017]). Rostranthera M.J.R. Rocha & P.J.F. Guim. (1), Brazil, Guianas; Rocha et al. (2018 [2017]). Sandemania Gleason (1), Venezuela, Peru, Bolivia, Brazil; Renner (1987). Siphanthera Pohl ex DC. (15), Colombia, Peru, Bolivia, Guianas, Brazil; Almeda and Robinson (2011).

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12. Melastomateae (see Veranso-Libalah et al., chapter “Systematics and Taxonomy of the Tribe Melastomateae”) Worldwide, tropical and subtropical, 44 genera. Tropical America, 17 genera. Andesanthus P.J.F. Guim. & Michelang. (9), Costa Rica, Panama, Venezuela to Ecuador; Todzia and Almeda (1991), Guimarães et al. (2019). Brachyotum (DC.) Triana (55), Andes, Colombia to northern Argentina; Wurdack (1953), Meyer et al. (2021). Bucquetia DC. (3), Andes, Venezuela to Ecuador; Guimarães et al. (2019). Castratrella Naudin (2), Venezuela and Colombia; Guimarães et al. (2019). Centradenia G. Don (4), Southern Mexico to Colombia; Almeda (1977). Chaetogastra D. Don (117), Southern Mexico to Argentina, Uruguay, southern Brazil; Guimarães et al. (2019), Meyer et al. (2021). Chaetolepis (DC.) Miq. (10), Costa Rica, Colombia, Venezuela, Guianas; Grimm and Almeda (2013). Desmoscelis Naudin (2), Colombia to Paraguay and eastern Brazil, Guianas; Wurdack et al. (1993). Heterocentron Hook. & Arn. (14), Mexico, Central America; Whiffin (1972). Loricalepis Brade (2), Colombia, Brazil; Goldenberg et al. (2020b). Monochaetum (DC.) Naudin (54), Mexico and Central America through Andes to Peru, Venezuela, Guianas, Brazil; Alvear and Almeda (2019). Pilocosta Almeda & Whiffin (5), Costa Rica to Ecuador; Almeda and Whiffin (1980), Almeda (1993a). Pleroma D. Don (161), Northwestern South America, mostly eastern Brazil; Da Silva et al. (2014), Guimarães et al. (2019). Pterogastra Naudin (3), Venezuela to Peru, Guianas; Renner (1994b). Pterolepis (DC.) Miq. (16), Mexico and Central America to Argentina and Paraguay, Greater and Lesser Antilles; Renner (1994a), Almeda and Martins (2015). Schwackaea Cogn. (1), Mexico (Oaxaca and Chiapas) to Colombia; Renner (1994b). Tibouchina Aubl. (38), Central America to Guianas, Brazil; Guimarães et al. (2019). Africa, Asia, Oceania, 27 genera: Almedanthus Ver.-Lib. & R.D. Stone (1), East Africa: Burundi, DR Congo, Tanzania; Veranso-Libalah et al. (2020). Amphorocalyx Baker (5), Madagascar; Perrier de la Bâthie (1951). Anaheterotis Ver.-Lib. & G. Kadereit (1), West Africa: Guinea and Sierra-Leone, Veranso-Libalah et al. (2017a). Antherotoma Hook.f. (11), Widespread in Africa (12), Madagascar (1); Veranso-Libalah et al. (2020). Argyrella Naudin (7), Tropical Africa; Veranso-Libalah et al. (2017a, 2017b). Cailliella Jacq.-Fél. (1), Guinea; Veranso-Libalah et al. (2021). Derosiphia Raf. (1), West Africa; Veranso-Libalah et al. (2020). Dichaetanthera Endl. (36), Tropical Africa (8), Madagascar (28); Perrier de la Bâthie (1951), Ranarivelo and Almeda (2019). Dionycha Naudin (3), Madagascar; Perrier de la Bâthie (1951). Dionychastrum A. Fern. & R. Fern. (1), Tanzania; Fernandes and Fernandes (1956), Veranso-Libalah et al. (2017a). Dissotidendron (A. Fern. & R. Fern.) Ver.-Lib. & G. Kadereit (11), East Africa; Veranso-Libalah et al. (2017a). Dissotis Benth. (6), West Africa; Veranso-Libalah et al. (2020). Dupineta (Sm.) Raf. (5), Tropical Africa; Veranso-Libalah et al. (2017a). Eleotis Ver.-Lib. & R.D. Stone (4), Angola, Congo, DR Congo, Zambia; Veranso-Libalah et al. (2020). Feliciotis Ver.-Lib. & G. Kadereit (12), Tropical Africa; Veranso-Libalah et al. (2020). Guyonia Naudin (14), Tropical Africa; Veranso-Libalah et al. (2020). Heterotis Benth. (6), Tropical Africa, but naturalized in India, Singapore, Australia, West Indies Costa Rica, Brazil, and islands in the Pacific Ocean; Veranso-Libalah et al. (2017a). Melastoma L. (80), India, Malesia, Japan, China, Borneo, Australia, Pacific Islands; Meyer (2001), Wong (2016), Neo et al. (2017). Melastomastrum Naudin (6), Tropical Africa; Veranso-Libalah et al. (2017a). Nerophila Naudin (8), Tropical Africa; Veranso-Libalah et al. (2020). Nothodissotis Ver.-Lib. & G. Kadereit (2), Cameroon, Equatorial Guinea, Gabon, São Tomé & Príncipe; Veranso-Libalah et al. (2019). Osbeckia L. (51), India, Sri Lanka and Nepal to Vietnam, southern China, Taiwan, Japan, Philippines, Peninsular Malaysia, Indonesia, New Guinea, and northern Australia; Hansen (1977), Prashob and Thomas (2019). Pseudosbeckia A. Fern. & R. Fern. (1), East Africa: Mozambique, Zimbabwe; Veranso-Libalah et al. (2017a). Pyrotis Ver.-Lib. & R.D. Stone (1), DR Congo, Zambia; Veranso-Libalah et al. (2020). Rosettea Ver.-Lib. & G. Kadereit (21), Tropical Africa; Veranso-Libalah et al. (2020). Rousseauxia DC. (13), Madagascar; Jacques-Félix (1973a). Tristemma Juss. (16), Tropical Africa (16), Madagascar (1); Veranso-Libalah et al. (2017a). Unplaced species: Dissotis leonensis Hutch. & Dalziel, Guinea, Sierra Leone. Dissotis splendens A. Chev. & Jacq.-Fél., Guinea.

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13. Merianieae (see Michelangeli et al., chapter “Phylogenetics and Taxonomy of the Tribe Merianieae”) Tropical America, eight genera. Adelobotrys DC. (31), Southern Mexico and Central America to Peru and Bolivia, Amazon basin; Schulman and Hyvönen (2003). Axinaea Ruiz & Pav. (41), Costa Rica through Andes to Bolivia; Cotton et al. (2014). Centronia D. Don (5), Northern South America; Mendoza-Cifuentes and Fernández-Alonso (2011). Graffenrieda DC. (68), Southern Mexico, Central America, West Indies to Guyana, tropical Andes to Bolivia, southeastern Brazil. Macrocentrum Hook. f. (25), Northern South America, mainly Guianas; Bacci et al. (2019). Maguireanthus Wurdack (1), Guyana. Meriania Sw. (120), Southern Mexico and Guatemala, southern Central America, Greater Antilles to tropical Andes, Guayana Highlands, southeastern Brazil; Mendoza-Cifuentes (2021). Salpinga Mart. ex DC. (10), Colombia to Peru, Guyana, Brazil. 14. Miconieae (see Michelangeli et al., chapter “Why Recognize Miconia as the only Genus in Tribe Miconieae?”) Tropical America, one genus. Miconia Ruiz & Pav. (1901), Tropical America; Goldenberg et al. (2013), Michelangeli et al. (2019). 15. Pyramieae (see Bochorny et al., chapter “Systematics and Evolution of Tribe Pyramieae”) Tropical America, four genera. Bisglaziovia Cogn. (1), South-Central Brazil; Baumgratz et al. (2004). Cambessedesia DC. (25), South-Central Brazil; Martins (1984), Fidanza (2009). Huberia DC. (37), Southeastern Brazil, one in Ecuador, two in Peru; Baumgratz (2004), Tavares (2005), Bochorny et al. (2019). Merianthera Kuhlm. (7), Southeastern Brazil; Bochorny et al. (2019), Goldenberg et al. (2012). 16. Pyxidantheae (see Penneys & Almeda, chapter “An Overview of the Tribe Pyxidantheae”) Tropical America, two genera. Blakea P. Browne (192), Tropical America, mainly Costa Rica to Ecuador; Penneys and Judd (2013a, b). Chalybea Naudin (12), Andes of Colombia to Bolivia; Morales (2010), Bernal et al. (2015), Penneys et al. (2015). 17. Rhexieae (see Judd & Ionta, chapter “Systematics of Tribe Rhexieae”) North America to South America, three genera. Arthrostemma Pav. ex D. Don (4), Mexico to Bolivia and Brazil, Greater Antilles and Trinidad; Almeda (2009). Pachyloma DC. (4), Northern South America. Rhexia Gronov. (13), United States (10 in Florida) reaching Canada, Greater Antilles; Kral and Bostick (1969), Nesom (2012). 18. Rupestreeae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) South America, one genus. Rupestrea R. Goldenb., Almeda & Michelang. (2), Eastern Brazil (Bahia); Goldenberg et al. (2015).

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19. Sonerileae (see Liu et al., chapter “Systematics of the Tribe Sonerileae”) Tropical, Old World with 43 genera, and Neotropics with 6 genera. Tropical America Boyania Wurdack (2), Colombia, Guyana; Bacci et al. (2019), Wurdack and Michelangeli (2019). Neblinanthera Wurdack (1), Venezuela and Brazil (Cerro Neblina); Wurdack (1964). Opisthocentra Hook. f. (1), Amazonian Colombia, Venezuela, Brazil; Berry et al. (2002). Phainantha Gleason (5), Southeastern Venezuela, Guyana, Ecuador; Berry et al. (2002), Ulloa Ulloa and Neill (2006). Tateanthus Gleason (1), Venezuela and Brazil; Berry et al. (2002). Tryssophyton Wurdack (2), Guyana; Wurdack and Michelangeli (2019). Tropical Africa and Asia Amphiblemma Naudin (15), West-Central Africa; Jacques-Félix (1973b), Bánki et al. (2021). Anerincleistus Korth. (39), India and Peninsular Malaysia; Maxwell (1989). Aschistanthera C. Hansen (1), Vietnam; Hansen (1987a). Barthea J.D. Hooker (1), China (Fujian, Guangdong, Guangxi, Hunan), Taiwan; Hansen (1980). Benna Burgt & Ver.-Lib. (1), Guinea, West Africa; van der Burgt et al. (2022). Blastus Loureiro (12), Cambodia, China, eastern India, Indonesia, Japan (Ryukyu Islands), Laos, Myanmar, Thailand, Vietnam; Hansen (1982). Boerlagea Cogn. (1), Borneo; Cogniaux (1891). Bredia Blume (23), China, Taiwan, Japan; Zhou et al. (2019). Brittenia Cogn. (1), Borneo; Hansen (1985a). Calvoa Hook.f. (19), Tropical Africa; Jacques-Félix (1981), Figueiredo (2001). Campimia C. Hansen (3), Borneo; Hansen (1988a). Catanthera F.V. Muller (19), Borneo, New Guinea, Sumatra; Nayar (1982), Bánki et al. (2021). Cincinnobotrys Gilg (8), Tropical Africa; Jacques-Félix (1981), Jacques-Félix (1994). Cyanandrium Stapf (5), Borneo; Nayar (1969). Cyphotheca Diels (1), China (Yunnan); Hansen (1990a). Dicellandra Hook.f. (3), West-Central Africa and Uganda; Jacques-Félix (1974). Driessenia Korth. (19), Vietnam, Borneo, Sumatra, Java; Hansen (1985b), Bánki et al. (2021). Enaulophyton Steenis (2), Malaysia; Nayar (1965). Fordiophyton Bullock (15), China, Vietnam; Zeng et al. (2016). Gravesia Naudin (116), Tropical Africa (DR Congo, Gabon, Tanzania; 5), Madagascar (111); Fernandes and Fernandes (1956), Jacques-Félix (1994), Perrier de la Bâthie (1951). Heteroblemma (Blume) Cámara-Leret, Ridd.-Num. & Veldk. (15), Peninsular Malaysia, Sumatra, Borneo, Sulawesi, New Guinea, and Vietnam; Cámara-Leret et al. (2013), Okada et al. (2017). Kendrickia J.D. Hooker (1), Sri Lanka; Cámara-Leret et al. (2013). Kerriothyrsus C. Hansen (1), Laos; Hansen (1988b). Medinilla Gaudich. (379), Tropical Africa (3), Madagascar (73), Southeast Asia (303), Australia (1); Perrier de la Bâthie (1951), Wickens (1975), Jacques-Félix (1983), Regalado (1990, 1995), Whiffin (1990), Bánki et al. (2021). Neodriessenia Nayar (6), Borneo; Hansen (1985c). Oxyspora DC. (37), Bhutan, India, Cambodia, China, Laos, Myanmar, Nepal, Thailand, Vietnam Melanesia; Bakhuizen f. (1943), Bánki et al. (2021). Pachycentria Blume (8), Myanmar, Thailand, Peninsular Malaysia, Sumatra, Java, Borneo, Philippines Sulawesi, New Guinea; Clausing (2000). Phyllagathis Blume (74), Brunei, China, Indonesia, Malaysia, Myanmar, Thailand; Hansen (1992), Cellinese (2002, 2003). Plagiopetalum Rehd. (3), China, Myanmar, Vietnam; Hansen (1988c), Chen and Renner (2007). Plethiandra J.D. Hooker (8), Borneo, Sumatra, Malay Peninsula; Nayar (1974), Kadereit (2005). Poikilogyne E.G. Baker (28), Melanesia, mainly New Guinea; Cellinese (2007), Bánki et al. (2021). Poilannammia C. Hansen (4), Vietnam; Hansen (1987b). Preussiella Gilg (2), West-Central Africa; Jacques-Félix (1977). Sarcopyramis Wallich (2), Southeast Asia; Hansen (1979), Chen and Renner (2007), Bánki et al. (2021). Scorpiothyrsus Hui-Lin Li (3), China (Guangxi, Hainan); Li (1944). Sonerila Roxburgh (184), India and Sri Lanka to southern China and through Malesia to New Guinea; Cellinese (1997), Bánki et al. (2021). Sporoxeia W.W. Sm. (7), China, Myanmar; Hansen (1990b). Stussenia C. Hansen (1), Vietnam; Hansen (1985d). Styrophyton S.Y. Hu (1), Southern China (Guangxi, Yunnan); Hu (1952). Tashiroea Matsum. (12), China, Japan; Kokubugata et al. (2019), Zhou et al. (2019), Bánki et al. (2021). Tigridiopalma C. Chen (2), China (Guangdong); Zeng et al. (2021). Tylanthera C. Hansen (2), Thailand; Hansen (1990c). Vietsenia C. Hansen (4), Vietnam; Hansen (1984).

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20. Stanmarkieae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) Tropical America, two genera. Centradeniastrum Cogn. (2), Andes, Colombia to Peru; Almeda (1997). Stanmarkia Almeda (2), Mexico (Chiapas), Guatemala; Almeda (1993b). 21. Trioleneae (see Bacci et al., chapter “Systematics and Climatic Preferences of Tribes Bertolonieae and Trioleneae”) Tropical America, two genera; Bacci et al. (2019). Monolena Triana ex Benth. & Hook.f. (16), Guatemala to Brazil; Warner (2002). Triolena Naudin (27), Southern Mexico to Brazil.

Acknowledgments  Liz Gjieli (NY) prepared the maps. Marcelo Reginato assisted with the species checklist. We thank W. Judd, L. Majure, and an anonymous reviewer for their comments. We also thank Roy E. Gereau and Lou Jost for permission to use their photographs.

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Classification History of the Melastomataceae: Early Beginnings Through the Pre-molecular Era Frank Almeda

Introduction Unlike the classification history of other large and diverse families of flowering plants, that of the Melastomataceae is long but uncomplicated. Working with the technology of the time and limited collections from far-flung tropical lands, early students of the family made incremental advances in our understanding of tribal and generic delimitations and the morphological and anatomical characters upon which these categories were based. This chapter draws on scattered information about the individuals who made significant contributions to an understanding and classification of the family and expands upon the historical synopsis by Renner (1993). This survey traces early beginnings and provides a historical survey of classification systems ending with the scheme proposed by Renner just prior to the routine use of DNA sequencing in the last couple of decades (Table 1).

Early Beginnings: Pre-Triana Era The family Melastomataceae was established by the French botanist, Antoine-­ Laurent de Jussieu (1748–1836). He belonged to a distinguished dynasty of three generations of botanists at the Jardin du Roi, which became the Muséum national d’Histoire naturelle de Paris in 1793 (Lamy 2019). Jussieu was the first botanist to attempt a natural classification of plants and the originator of the family concept in botany. In Jussieu’s Genera Plantarum (1789), angiosperm families were divided F. Almeda (*) Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 R. Goldenberg et al. (eds.), Systematics, Evolution, and Ecology of Melastomataceae, https://doi.org/10.1007/978-3-030-99742-7_2

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Triana (1866, 1871) Melastomatoideae  Microlicieae  Pleromeae  Osbeckieae  Rhexieae  Merianieae  Oxysporeae  Sonerileae  Bertolonieae  Dissochaeteae  Miconieae  Pyxidantheae  Astronioideae  Astronieae Memecyloideae  Mouririeae  Memecyleae

Hooker (1867) Melastomatoideae  Microlicieae  Osbeckieae  Rhexieae  Merianieae  Oxysporeae  Sonerileae  Medinilleae  Miconieae  Blakeeae  Astronioideae  Astronieae Memecyloideae  Memecyleae

Cogniaux (1891) Melastomatoideae  Microlicieae  Tibouchineae  Osbeckieae  Rhexieae  Merianieae  Oxysporeae  Sonerileae  Bertolonieae  Dissochaeteae  Miconieae  Blakeeae  Astronioideae  Astronieae Memecyloideae  Memecyleae  Axinandreae

Table 1  Major classifications of the Melastomataceae Krasser (1893) Melastomatoideae  Tibouchineae  Osbeckieae  Rhexieae  Microlicieae  Merianieae  Oxysporeae  Bertolonieae  Cassebeerieae  Dissochaeteae  Tamoneae  Blakeeae  Astronioideae  Astronieae  Kibessieae Memecyloideae  Memecyleae  Axinandreae

van Vliet et al. (1981) Melastomatoideae  Tibouchineae  Sonerileae  Rhexieae  Osbeckieae  Microlicieae  Miconieae  Merianieae  Dissochaeteae  Blakeeae  Astronieae Memecyloideae  Pternandreae  Memecyleae Crypteronioideae  Crypteronieae

Renner (1993) Melastomatoideae  Astronieae  Sonerileae  Merianieae  Rhexieae  Melastomeae  Microlicieae  Miconieae  Blakeeae Kibessioideae  Kibessieae Memecylaceae Crypteroniaceae

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into 14 classes based on perianth details and position of ovaries (Davis and Heywood 1973); these classes were further divided into 100 ordines naturales (which were equivalent to families). Each of these families was named and provided with concise diagnostic descriptions of vegetative and reproductive characters. In all, 76 of Jussieu’s plant family names have remained in use since the publication of Genera Plantarum (Stevens 1994). One of these families is the Melastomataceae to which Jussieu attributed nine genera—Blakea, Mayeta (= Miconia), Melastoma, Osbeckia, Rhexia, Tibouchina, Tococa, Topobea, and Tristemma. Aside from grouping the melastome genera based on whether they had superior or inferior ovaries, he provided no formal groupings that reflected a sense of relationship. He included both Memecylon and Mouriri, now of the subfamily Olisbeoideae (the Melastomataceae), in the Onagraceae for reasons that are not obvious based on the descriptions he provided. He was evidently impressed by the foliar venation and staminal details of the species known to him at the time. One of the earliest seminal papers on the Melastomataceae was published by David Don (1799–1841) in 1823. Don, a Scottish botanist, was best known for his work on conifers and the flora of Nepal. He was trained in horticulture and botany under his father, George, before he was offered a position at the Royal Botanic Garden Edinburgh. In 1819, he moved to London where he became a librarian to Aylmer Bourke Lambert who had amassed an important herbarium that at the time housed one of the finest herbarium collections of Melastomataceae in Europe. Don recognized melastomes as one of the most natural but least studied families of flowering plants. He lamented the difficulty of studying the family because of its predominantly tropical distribution and, except for a few species in cultivation, there was little opportunity to study the species in a living state. It was Don (1823) who first noted a number of important taxonomic features in the family such as flower merosity and aestivation, posture and declination of the stamens of buds and at anthesis, details of the poricidal anthers, the presence or absence of appendages on the staminal connectives, and the structural differences between baccate and capsular fruits. He stressed ovary locule number, placentation details, and seed morphology. Don provided detailed descriptions of some 19 genera and nearly 120 species. In all, 12 of these genera are still recognized today, four of which he proposed as new—Aciotis, Centronia, Microlicia, and Pleroma. Like Jussieu, Don also excluded the Linnean genera Memecylon and Mouriri from the Melastomataceae because of differences in their fruit and seed characters. During the nineteenth century, the Candolle family stood out as major contributors to the field of systematic botany. The patriarch and most celebrated member of the family was Augustin Pyramus de Candolle (1778–1841) who was born in Geneva, Switzerland, and trained in Paris under the tutelage of René Louiche Desfontaines (Lawrence 1951). Candolle was a professor of botany at Montpellier for less than a decade (1808–1816), but he spent the last 25 years of his life back in Geneva where he continued work on his Prodromus Systematis Naturalis Regni Vegetabilis. In this monumental undertaking, which had never been attempted before, he proposed to describe and classify every known species of seed plant. This Prodromus, as it was commonly referred to, encompassed 17 volumes, the last 10

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of which were written by a cadre of specialists after Candolle’s death and edited by his son, Alphonse L.  P. P. de Candolle (1806–1893). Augustin P. de Candolle’s industriousness was unmatched by his contemporaries. In addition to his tireless work on the Prodromus, he produced nearly 100 monographs on selected flowering plant families. One of these was his memoir on the Melastomataceae that was published in June of 1828, about three months after the appearance of the treatment for the family in the Prodromus. In his accounts of the family for both of these publications, de Candolle (1828a, b) recognized 68 genera, about 36 of which are recognized today. The Melastomataceae were organized into four tribes—the Lavoisiereae, Rhexieae, Osbeckieae, and Miconieae. He assigned genera to these tribes based on characters such as ovary position (superior to inferior), fruit type (dry capsules or fleshy berries), seed morphology (cochleate or rounded vs. straight), and whether the ovary apex was glabrous or adorned with bristles or scales. This led to some broadly defined tribes and genera. His Lavoisiereae, for example, included genera that are currently assigned to the Bertolonieae, Marcetieae, Melastomateae, Merianieae, and Pyramieae. Although the tribal name Microlicieae has been used by all subsequent students of the family, Candolle’s Lavoisiereae predates the Microlicieae as a validly proposed name at the tribal rank by 21 years, so it must be adopted for this clade because it has priority according to Article 11.3 of the Shenzhen Code (Turland et al. 2018). His circumscription of the Miconieae included Neotropical and paleotropical genera with both capsular and baccate fruits. The genera Candolle placed in this tribe have subsequently been reassigned to five other tribes. His tribe Rhexieae was also a heterogeneous assemblage of capsular-fruited genera, some of which included a disparate assemblage of species. His treatment of the genus Arthrostemma, for example, included several sections, at least seven of which were elevated to generic status by subsequent students of the family. Like his predecessor, Jussieu, Candolle excluded Mouriri and Memecylon from the Melastomataceae but he created a family, the Memecylaceae, to accommodate them (de Candolle 1828c). During the several decades that followed, botanical exploration around the world helped enrich the holdings of herbaria, especially those in Europe. Many important collections from the New World, Africa, and Southeast Asia made their way to the herbarium in Paris (P), making it one of the most important herbaria for Melastomataceae in the world. This collection would prove to be a treasure trove for the next notable student of the Melastomataceae, Charles Victor Naudin (1815–1899). Naudin published voluminously and widely in horticulture and experimental botany, but his most celebrated work was done on problems of plant hybridization (Marza and Cerchez 1967). He was born in Autun, France, and earned a baccalaureate in science from Montpellier in 1837; following some health challenges that resulted in total deafness, he was recommended for a volunteer position at the herbarium of the Muséum national d’Histoire naturelle in 1846 by his longtime friend and supporter, Joseph Decaisne. It was during that time that Naudin produced an important set of publications describing many new genera and species that had accumulated in the vast melastome collection of the Paris herbarium (Naudin 1849–1853). Naudin’s cumulative publications amounted to a detailed descriptive

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catalog of the collections of the Melastomataceae at P. He described hundreds of new species and genera, many of which were superbly illustrated with line drawings of habit, flowers, hypanthia, petals, stamens, placentation, and seeds. For the New World alone, he described 41 new genera, 582 species, and 50 varieties (Martin and Cremers 2007). Only about a dozen of his newly described Neotropical genera are accepted today, and dozens of his new species have been synonymized. Yet, many of the species he proposed have stood the test of time and the scrutiny of subsequent specialists. He was working at a time when, globally, the melastome flora was little-­ known and woefully understudied. Naudin grouped the genera and species of the Melastomataceae known to him into five subfamilies—the Melastomatoideae,  Astronioideae, Kibessioideae, Memecyloideae, and Mouririoideae. He further divided the Melastomatoideae into four tribes: the Microlicieae (most closely matching present-day circumscription, except for Centradenia and Siphanthera), the Lasiandreae (containing mostly genera currently assigned to the Melastomateae and Marcetieae), the “Pyramidales” (this included Cambessedesia and Pyramia (now a section of Cambessedesia) and Rhexia), and the Miconieae. He further divided the latter into six subtribes, nearly all of which contained distantly related genera as we understand them today; many of the genera he recognized in these groupings have either been merged with other genera or redistributed to other tribes. Naudin’s subtribe “Clidemia” is especially noteworthy. It contained many genera that are now included in the monogeneric tribe Miconieae, but it also included genera that have since been reassigned to the Pyxidantheae (Chalybea), the Pyramieae (Huberia), a long-overlooked tribal name that has priority (Naudin 1851) over the recently proposed, superfluous Cambessedesieae (Bochorny et al. 2019), the Henrietteeae (Bellucia, Henriettea), and the Melastomateae (Bucquetia and Pleroma (as Svitramia)). His Sonerilinae was also a heterogeneous assemblage with genera now assigned to the Bertolonieae (Bertolonia), Eriocnemeae (Eriocnema), Lithobieae (Lithobium), and Trioleneae (Triolena). Although Naudin’s infrafamilial classification and circumscription of genera left much to be desired, his descriptions and illustrations of critical diagnostic features provided a step forward and an important working framework for future students of the family. Unlike his predecessors, Naudin included the paleotropical Memecylon (together with Lijndenia and Spathandra in his subfamily Memecyloideae) and the Neotropical Mouriri (in the subfamily Mouririoideae) in his more broadly defined concept of the family.

Chronological Survey of the Major Classification Systems A little over a decade after Naudin completed his final published papers on the melastome collections housed in Paris, José Jerónimo Triana (1828–1890) created a new and original classification of his own (1866, 1871; Table 1). Triana was born in

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Zipaquirá, Colombia. Because the botanical sciences in Colombia were not an established tradition until the 1930s, Triana began his botanical studies in Bogotá under the private tutelage of Francisco Javier Matis, one of the last survivors of the famous José Celestino Mutis botanical expeditions to Colombia (Arbeláez 2021). Unlike his predecessors, Triana was the first serious student of the Melastomataceae to have extensive field experience with the rich and diverse representation of the family in his native Colombia. Beginning in 1850, Triana was appointed by the government as a botanist on the commission charged with preparing a new geographical map of Colombia. This allowed Triana to travel and collect plants throughout the Andes where he made well-documented collections that amounted to some 3800 species (Arbeláez 2021). In the early 1850s, Triana benefitted from the visits of European botanical explorers who were sent for training as field botanists. About this time, he was already corresponding with several European explorers (Schlim, Linden, Planchon, Warszewicz, Karsten, and others) who had field experience and/ or research interests in the flora of Colombia. In 1856, the Colombian government sent Triana to Europe for a period of two years to publicize Colombian plants of economic importance. He used his time in Paris, Brussels, London, and Madrid productively to study the important herbarium collections for the Colombian flora generally and to access bibliographical resources needed for his work (Diaz-­ Piedrahita 1991). Triana had already gained the respect and admiration of the European botanical community for his dedication and quality of work by the time he proposed the synoptic outline for his new classification of the Melastomataceae at the International Botanical and Horticultural Congress in Amsterdam in 1865. With some minor modifications, the expanded account of Triana’s classification appeared in 1872 and was followed for over a century by his successors (see Table 1) and other students of flowering plant classification (Hooker 1867; Cogniaux 1891; Krasser 1893; Hutchinson 1973; Cronquist 1981; Thorne 1992). Triana’s system (1866, 1871) departed from Naudin’s in recognizing 14 tribes that he divided into three informal groupings—the Astronieae (one tribe), Memecyleae + Mouririeae (second group), and a greatly expanded Melastomatoideae that embraced 11 tribes instead of four (Table 1). His recognition of new tribes took into account the fruit type, placentation, and general seed morphology (cochleate vs. straight). He also paid special attention to flower merosity, stamen morphology, the number of anther pores, the presence or absence of pedoconnectives, and the nature and position of staminal appendages when present. Geographic distribution (Old World vs. New World) also figured into his taxonomic groupings. Triana also merged Naudin’s Astronieae and Kibessieae into one group. Triana correctly adopted the name Pyxidantheae (see Table 1), which, according to pagination notes in Stearn (1965), was published by Grisebach (1860) for what all of his successors treated as the Blakeeae, a later name proposed by Hooker (1867). Triana’s access to the rich holdings in European herbaria allowed him to describe hundreds of new taxa. His new classification scheme included some 134 genera, about 86 of which are accepted today; of the five genera proposed by Triana, only Brachyotum appears to be presently recognized.

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The generic composition of most of Triana’s tribes nevertheless continued to be heterogeneous. His Merianieae and Miconieae provided the closest matches to present-­day tribal concepts. As noted by Renner (1993), there were also some disparities between Triana’s tribes and wood anatomical features that were first raised by van Tieghem (1891). Wood anatomy, for example, did not support Triana’s merger of the Asteroideae and Kibessioideae, and the tribes that he based heavily on staminal connective details were also in conflict with wood anatomical features. His tribal groupings that relied heavily on seed morphology, however, were upheld by wood anatomy. About the time that Triana presented his new classification of the Melastomataceae at the Congress in Amsterdam, Joseph Dalton Hooker (1817–1911) was already at work on the three-volume Genera Plantarum with George Bentham. Hooker, who was the son of Sir William Jackson Hooker, studied medicine at Glasgow University where he received an MD in 1839, but his leisure time was spent studying botany and entomology. He was appointed as the assistant director of the Royal Botanic Gardens, Kew, in 1855 and succeeded his father as the director a decade later. It was at Kew that the younger Hooker met George Bentham, a frequent visitor to the herbarium. Their joint collaboration to produce Genera Plantarum began in 1857. Despite his demanding administrative duties, Hooker (1867), who was not a melastome specialist, completed a commendable generic conspectus of the family largely following the overall structure of Triana’s (1866, 1871) classification. In keeping with the format of Genera Plantarum generally, which has been touted as a model of thoroughness and accuracy, Hooker produced a concise treatment of the tribes and genera. He formalized the recognition of three subfamilies to which Triana had alluded—the Astronioideae, Memecyloideae, and Melastomatoideae (Table 1). He also recognized the same 134 genera that Triana treated, together with full synonymy and distributional information based on the rich herbarium and bibliographic resources at Kew. For the Melastomatoideae, Hooker treated only nine tribes as opposed to the 11 recognized by Triana. Hooker’s account of the family differed from that of Triana’s in a few notable ways (Table 1). He erroneously replaced the tribal name Pyxidantheae with Blakeeae. Triana’s Pleromeae was merged with the Osbeckieae; the genera were organized into informal Old World and New World series under the latter to accommodate the Neotropical genera that Triana had assigned to the Pleromeae. The Sonerileae was divided into three series—Asian, African, and American. The latter included Triana’s Bertolonieae. Finally, Hooker merged Triana’s Dissochaeteae with a tribe he called Medinilleae. This compounded the long-standing challenges of adequately characterizing and properly assigning genera to the Dissochaeteae and Sonerileae (including the Oxysporeae) based on morphological characters (see Penneys et  al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). The next notable student of the Melastomataceae was Célestin Alfred Cogniaux (1841–1916), a Belgian botanist who received a teacher’s diploma from the École Normale de Nivelles in Belgium at the age of 22 (Renner 1990). Cogniaux taught at several schools in Belgium before accepting a position at the Jardin Botanique in Brussels in 1872. It was at that time that he signed on to prepare the treatment of the

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Melastomataceae for Flora Brasiliensis. For unknown reasons, Cogniaux resigned his position at the Jardin in 1880 and returned to teaching school. He evidently taught school full-time until his retirement in 1901. His discipline and sustained capacity for work and study allowed him to complete the comprehensive treatment of the Melastomataceae for Brazil (1883–1888), his monumental worldwide monograph of the family (1891), and other comprehensive treatments of the Cucurbitaceae and Orchidaceae. His familial monograph treated 138 genera (as had Triana and Hooker). The treatment of the family down to the species level was unparalleled at the time, and no student of the family has attempted anything like it since. Of the 2731 species (and 555 varieties) that he treated in the monograph, some 793 species were new to science (Renner 1990). Cogniaux’s monograph treated just less than 50% of the species known today. In both of these extraordinary and widely praised publications, Cogniaux largely followed Triana’s family classification. Like Triana, he also recognized 11 tribes in the Melastomatoideae but replaced the name Pleromeae with Tibouchineae. He followed Hooker (1867) in using the name Blakeeae for what Triana correctly called the Pyxidantheae, reintroduced the tribe Bertolonieae, and created the tribe Axinandreae to accommodate the small Southeast Asian genus Axinandra under the subfamily Memecyloideae (Table 1). Axinandra, currently included in the Crypteroniaceae, a related family in the Myrtales (Stevens 2001), is superficially similar to Mouriri and Memecylon of Cogniaux’s Memecyleae (Table  1). The three genera share opposite leaves, similar brochidodromous leaf venation, and an inferior ovary. Axinandra, however, has large prominently veined caducous stipules (vs. the absence of true stipules), petals that are apically connate and shed together like an umbrella (vs. petals that fall away individually), anther connectives lacking glands (vs. connectives with an elliptic terpene-producing gland), corky or woody capsular fruits (vs. fleshy fruits), and ovules that are anatropous (vs. campylotropous) (Dahlgren and Thorne 1984; Heywood et al. 2007). In addition, the inflorescence of elongate racemes or racemules, typical of the Crypteroniaceae, is unknown in members of the Memecyloideae. All of these characters provide a convincing rationale for excluding Axinandra even in the broadly defined Memecyloideae. Cogniaux (1891) described many of the above-mentioned features in his descriptions of these genera, but, for some reason, the taxonomic significance of these differences did not register with him at the time. Cogniaux’s familial monograph had considerable subsequent influence on tribal and generic concepts. Fridolin Krasser (1863–1922), the Austrian botanist and paleontologist, who prepared a substantive illustrated generic conspectus for Engler and Prantl’s Die Natürlichen Pflanzenfamilien (Krasser 1893), followed the general outline of Cogniaux’s tribal classification. He also recognized three subfamilies, but increased the number of tribes from 14 to 15 (Table 1) and the number of genera from 138 to 148. Krasser used the name Cassebeerieae for the Sonerileae and Tamoneae for the Miconieae, but these superfluous names were abandoned by subsequent students of the family. Under the Astronioideae, he continued to recognize the Astronieae but parted with Cogniaux in describing the new tribe Kibessieae to include Pternandra (including Kibessia) and Plethiandra. The latter had been placed next to Kibessia in

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the Astronieae by J. D. Hooker when he proposed it as a genus, and it was included by Cogniaux (1891) in the more broadly circumscribed Astronieae. Krasser continued to group Plethiandra with Pternandra perhaps because they share a fleshy fruit. This is otherwise puzzling because Plethiandra is prevailingly epiphytic, has 6-­merous polystemonous flowers with linear, oblong unappendaged anthers that are poricidal (vs. longitudinal slits), and axile placentation (vs. parietal placentation). Its affinities are clearly with Medinilla and related segregate genera in the Sonerileae (Nayar 1974; Penneys et  al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Of the 10 additional genera that Krasser recognized, three were described as new, Naudiniella (=Astronidium), Naxiandra (=Axinandra), and Pseudoernestia, but only the latter is currently recognized. Krasser also recognized Antherotoma, Fordiophyton, and Lijndenia (genera that had not yet been published prior to 1891 or were lumped by Cogniaux with other genera). The four other genera included in Krasser’s treatment that were not recognized by Cogniaux were synonyms of names that already had nomenclatural priority (Gymnagathis (= Fordiophyton); Olisbea (=Mouriri); Purpurella (= Chaetogastra); and Pyxidanthus (= Blakea)). Krasser’s circumscription of the Sonerileae, Dissochaeteae, and Oxysporeae continued the practice of grouping some genera together, which were not closely related; identifying monophyletic genera in the Sonerileae (including the Oxysporeae) alliance continues to be a challenge in need of satisfactory resolution (see Liu et al., Chapter “Systematics of the Tribe Sonerileae”). Some nine decades would pass before another classification system was proposed by Gerardus J. C. M. van Vliet (b. 1948 -) and associates (van Vliet et al. 1981). This emanated from a Dutch team of plant anatomists working on the wood anatomy of the Myrtales (van Vliet 1981; ter Welle and Koek-Noorman 1981; van Vliet and Baas 1984). During the twentieth century, there was a surge of interest in the use of wood anatomical data in classification and phylogeny, and the treatises by Metcalfe and Chalk (1950) and Carlquist (1961) served as guides for the use of anatomical data in taxonomic and evolutionary studies of angiosperms. Wood characters are believed to be a conservative feature in plant evolution and thus might have value in determining relationships and evolutionary trends. Wood anatomy, however, is just one kind of anatomical data and its value can only be realized when correlated with other characters. van Vliet et al. (1981) were mindful of the fact that wood anatomical evidence alone could not form the basis of a robust classification. They offered their preliminary classification and phylogeny as a tentative framework that could be refined with data sets from other disciplines. Their classification based on wood anatomical evidence (Table  1) recognized three subfamilies—the Crypteronioideae (including Axinandreae of other classifications), the Memecyloideae (including Pternandreae and Memecyleae), and the Melastomatoideae. These groupings were recognized in the classifications of both Cogniaux (1891) and Krasser (1893) but at different taxonomic levels. van Vliet et al. (1981) abolished the classifications of the Astronioideae dating back to Triana (1866, 1871) (Table  1), as was earlier suggested by Janssonius (1950) and van Tieghem (1891), and reassigned the Astronieae s. s. and Kibessieae to the

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Melastomatoideae and Memecyloideae, respectively. These proposed changes were based on the production of fiber tracheids and axially included phloem in the Memecyloideae vs. the production of libriform fibers and lack of included phloem in the Melastomatoideae. The Crypteronioideae, unlike the Memecyloideae, have dry capsular fruits, numerous small seeds, and lack included phloem. The sum of these characters along with some distinctive floral differences have been used to argue for the idea that family status should be accorded to these two subfamilies, along with the Melastomataceae (Dahlgren and Thorne 1984). The tribal classification of the Melastomatoideae by van Vliet et  al. (1981) largely followed the schemes proposed by Cogniaux and Krasser. This decision was attributed to the “lack of sufficiently great and patterned wood anatomical diversity in the subfamily.” The only notable departure from the classifications of Cogniaux and Krasser was the combination of the Sonerileae and Oxysporeae into one tribe with two subtribes. This modest and not unexpected lumping was evidently based on whether the intervessel pits were scalariform (Sonerilinae) or alternate (Oxysporinae). van Vliet et al. (1981) appear to have overlooked the Bertolonieae altogether (Table  1). They believed Alloneuron, which had been placed in the Cyphostyleae by Gleason (1929), to be close to the Miconieae based on wood anatomical features. That assessment is at odds with its current phylogenetic position and resurrected status as a tribe based on molecular and morphological data sets (Michelangeli et  al. 2011; Penneys et  al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). The last and most recent major classification that has to be considered is that of Renner (1993). Susanne S. Renner (b. 1954 -), a German botanist, earned a doctoral degree from the University of Hamburg in Germany, following two years of fieldwork in Amazonian Brazil. She then went back to Brazil and from there proceeded to postdoctoral work at the US National Herbarium. She subsequently held faculty positions in Denmark, Germany, and in the USA. In 2003, she moved to a professorial position at Ludwig Maximilian University in Munich where she was also the director of the Munich Botanical Garden and Herbarium. She retired from these posts in 2020. When Renner’s classification first appeared, it was welcomed for its cladistic approach and its critical assessment of the morphological and anatomical characters that had figured prominently in higher-level groupings of the Melastomataceae. Her phylogenetic analyses resulted in the removal and reassignment of the Crypteronioideae (including Axinandreae) to a family of its own and the recognition of three other major groupings for what had been assigned to the Melastomataceae by her immediate predecessors. She argued for elevation of the Memecyloideae to familial status in line with what had been proposed by de Candolle (1828c). Her rationale for the recognition of the Memecylaceae was that it and the Melastomataceae s. s. share no apomorphic character states aside from common myrtalean features like included phloem in the wood, diplostemonous flowers, and the presence of a well-developed hypanthium. She provided a list of morphological and anatomical differences between the two groups and summarized the history of efforts to separate or merge them. In subsequent analyses using DNA sequence data, the

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Memecyloideae (= Olisbeoideae), an early-diverging clade, has been recovered as sister to the Kibessioideae, which would render the Melastomataceae paraphyletic if the memecyloid genera are not included in a broadly circumscribed concept of the family (see Stone, Chapter “Phylogeny and Circumscription of the Subfamily Olisbeoideae”). In Renner’s circumscription of the Melastomataceae s. s., she recognized two subfamilies—the Melastomatoideae and Kibessioideae. The latter was resurrected for the sole genus Pternandra following Naudin (1849–1853) who first proposed this subfamily. Because the Kibessioideae shares some characters with both the Memecyloideae (fiber tracheids, radially included phloem, and antepetalous ovary locules) and the Melastomatoideae (acrodromous foliar venation, lack of terminal foliar sclereids, lack of terpene-producing gland on the connective, and small seeds), it has been regarded as an intermediate, thus supporting the argument that the Memecyloideae should be included as a subfamily of the Melastomataceae (Thorne in Dahlgren and Thorne 1984). The Kibessioideae is also an early-diverging clade in all phylogenetic analyses based on both morphological and molecular data sets (see Renner 1993; Penneys et al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”; Stone, Chapter “Phylogeny and Circumscription of the Subfamily Olisbeoideae”). Renner’s Melastomatoideae consisted of eight tribes (Table 1). Like van Vliet et al. (1981), she included the Astronieae in this subfamily with identical delimitation, abolishing the Astronioideae. With a few exceptions involving the inclusion or exclusion of one or a few genera, her circumscriptions of the Blakeeae (now Pyxidantheae), Merianieae, and Microlicieae (now Lavoisiereae) were a close match to the systems of Krasser and van Vliet et al.. She reduced the Rhexieae to include only the genus Rhexia because of its several autapomorphies such as atropous ovules, capsules developing from inferior ovaries, and unilocular anthers. Her concepts of the remaining tribes (the Sonerileae, Melastomateae, and Miconieae) were major departures from the classifications of her predecessors. Her Sonerileae, which she admitted was diverse and provisional, consisted of an Oxyspora alliance and a Sonerila-Bertolonia-Gravesia alliance. All of the genera assigned to the former alliance are native to the Old World and had previously been placed mostly in the Oxysporeae; the Sonerila et al. alliance was an amalgamation of genera from both the Neotropics and paleotropics that had been placed in the Bertolonieae, Dissochaeteae, and Sonerileae in past classifications. The enigmatic monospecific genus Feliciadamia of West tropical Africa (present-day Guinea), to which Jacques-­ Félix (1994) accorded a tribal status, was also assigned to the broadly defined Sonerileae. This genus is still known only from its type, and the lack of material for molecular analyses has hampered a critical appraisal of its phylogenetic affinities and taxonomic status. Renner concluded that the Sonerileae was a poorly defined heterogeneous grouping irrespective of whether it was interpreted in a strict or broad sense. Identifying monophyletic genera in this entire tribe is an ongoing challenge and remains a work in progress (Penneys et  al., Chapter “A New Melastomataceae Classification

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Informed by Molecular Phylogenetics and Morphology”; Liu et  al., Chapter “Systematics of the Tribe Sonerileae”). Renner resurrected the name Melastomeae (=Melastomateae) to collectively accommodate all the genera that had been assigned to the Old World Osbeckieae and the New World Tibouchineae. The merger of these two tribes was realistic and defensible based on their macromorphological characters. Some recent realignments among the Neotropical genera in this complex have resulted in a partial dismemberment of the Neotropical Melastomateae (Tibouchineae) and recognition of the new tribe Marcetieae with 20 genera (some resurrected) based on molecular data sets (see Rocha et  al. 2018; Penneys et  al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). A similar reevaluation of the African Melastomateae has also resulted in a new classification with the description of several genera for that geographical element of the tribe (see Veranso-Libalah et  al. 2020; Veranso-Libalah et  al., Chapter “Systematics and Taxonomy of the Tribe Melastomateae”). The tribe that received the greatest modification in Renner’s system was the Miconieae. The traditional circumscription of this berry-fruited assemblage included some 25 genera and nearly 1900 species with a distribution restricted to the Neotropics (Michelangeli et al. 2020). Renner’s delimitation of the tribe included berry-fruited and capsular-fruited genera (30 Neotropical and 12 Paleotropical genera with a collective 2000+ species). Most of the Paleotropical genera that she assigned to the broadened Miconieae had been placed in the Dissochaeteae by Cogniaux (1891) and Krasser (1893); the current delimitations, however, would assign fewer than half of the genera to the Dissochaeteae (Creochiton, Diplectria, Dissochaeta, Macrolenes, and Pseudodissochaeta) and all of the others to the Sonerileae (Boerlagea, Catanthera, Kendrickia, Medinilla, Pachycentria, Plethiandra, and Pogonanthera). A majority of the Neotropical genera assigned to the tribe had long been placed there. Renner placed Alloneuron, Allomaieta, and Cyphostyla (= Allomaieta), all capsular-fruited genera of the Cyphostyleae, in the Miconieae, which as noted above is not in agreement with the current phylogenetic analyses (see Michelangeli et al., Chapter “The Cyphostyleae, a Small Tribe Rich in Rare Characters in the Family”). Based on molecular data sets, other genera long associated with the Miconieae and retained there by Renner such as Chalybea and Huilaea (=Chalybea) have since been transferred to the Pyxidantheae (as Blakeeae) by Penneys and Judd (2013). A few other genera (Bellucia, Loreya (=Bellucia), Henriettea, Henriettella (=Henriettea), Kirkbridea, and Myriaspora (=Bellucia)) have also been removed from the tribe and assigned to the recently described Henrietteeae (Penneys et al. 2010). Renner noted that many of the changes she proposed had been suggested piecemeal by other workers or were in agreement with pre-Triana classification schemes, so, in many respects, she was providing a welcome synthesis and interpretative rationale for a good deal of what had been proposed by a long line of classificatory efforts. Renner (1993) recognized two subfamilies, nine tribes, and 166 genera of the Melastomataceae and six genera in the Memecylaceae. Like all proposed classifications, her system is being revised as more taxa are analyzed, especially using

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molecular data sets. Today, the number of recognized tribes have more than doubled from those recognized by Renner (Penneys et al., Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”), and the generic composition of each continues to change. Nevertheless, Renner’s system has provided a useful framework and springboard for ongoing studies of the second largest family in the order Myrtales and one of the 10 largest among flowering plants (Christenhusz and Byng 2016; Christenhusz et al. 2017).

End of the Pre-molecular Era Renner’s classification marked the end of an era that relied on morphological and anatomical data to assess infrafamilial relationships. In the last two decades, the development of robust molecular phylogenies with high confidence levels has modified and greatly improved the efforts to identify monophyletic genera and tribes. Molecular studies have provided a sound basis for elevating nine lineages (eight Neotropical and one Paleotropical) to a tribal status. This has been fueled by a dramatic increase in the number of researchers focused on the Melastomataceae and the acceleration of international collaborations. The benefits of these collaborative efforts are evidenced by the many multiauthored chapters in this volume. For a summary of the research generated during this new ongoing molecular era and the most current delimitation of tribal relationships, see the new classification by Penneys et  al. (Chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Acknowledgments  I thank Susanne Renner, Mayara Caddah, and an anonymous reviewer for their helpful comments on an earlier version of this chapter. I am also grateful to Rebekah Kim who helped me locate some literature references.

References Arbeláez EP (2021) Triana, José Gerónimo (or Jerónimo). https://www.encyclopedia.com/science/ dictionaries-­thesauruses-­pictures-­and-­press-­releases/triana-­jose-­geronimo-­or-­jeronimo Bochorny T, Michelangeli FA, Almeda F, Goldenberg R (2019) Phylogenetics, morphology and circumscription of Cambessedesieae: a new Neotropical tribe of Melastomataceae. Bot J Linn Soc 190:281–302 Carlquist S (1961) Comparative plant anatomy. Holt, Rinehart & Winston, New York Christenhusz MJM, Byng JW (2016) The number of known plant species in the world and its annual increase. Phytotaxa 261:201–217. https://doi.org/10.11646/phytotaxa.261.3.1 Christenhusz MJM, Fay MF, Chase MW (2017) Plants of the world: an illustrated encyclopedia of vascular plants. Royal Botanic Gardens, Kew & University of Chicago Press Cogniaux CA (1883–1888) Melastomaceae In: Martius CFP, Eichler AG (eds) Flora brasiliensis 14(3):1–510; 14(4):1–655

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Cogniaux CA (1891) Mélastomacées. In: de Candolle ALPP, de Candolle C (eds) Monographieae phanerogamarum, vol 7. G. Masson, Paris, pp 1–1256 Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, New York Dahlgren R, Thorne RF (1984) The order Myrtales: circumscription, variation, and relationships. Ann Missouri Bot Gard 71:633–699 Davis PH, Heywood VH (1973) Principles of angiosperm taxonomy. Robert E. Krieger Publishing Co., Huntington, New York de Candolle AP (1828a) Melastomaceae. In: Prodromus systematis naturalis regni vegetabilis, vol 3. Treuttel et Würtz, Paris, pp 99–202 de Candolle AP (1828b) Memoire sur la famille des Mélastomacées. Treuttel et Würtz, Paris de Candolle AP (1828c) Memecylaceae. In: Prodromus systematis naturalis regni vegetabilis, vol 3. Treuttel et Würtz, Paris, pp 5–8 de Jussieu AL (1789) Genera plantarum, secundum ordines naturales disposita, juxta methodum in horto regio Parisiensi exaratam, anno M.DCC.LXXIV. Herissant & Barrois, Paris Diaz-Piedrahita S (1991) José Triana, su vida y su obra In: Diaz-Piedrahita, S (ed) José Triana, su vida, su obra y su epoca. Academia Colombiana de Ciencias Exactas, Físicas y Naturales. Santa Fe de Bogotá, D. C., Colombia Don D (1823) An illustration of the natural family of plants called Melastomaceae. Mem Wernerian Nat Hist Soc 4:276–329 Gleason HA (1929) Studies on the flora of northern South America. XII. Cyphostyleae―a new tribe of Melastomataceae. Bull Torrey Bot Club 56:97–100 Grisebach AHR (1860) Melastomaceae. In: Flora of the British West Indian Islands (published in six parts). Lovell Reeve & Co., London, part 3, pp 243–269 Heywood VH, Brummitt RK, Culham A, Seberg O (2007) Flowering plant families of the world. Firefly Books Ltd., Buffalo, New York Hooker JD (1867) Melastomaceae In: Bentham G, Hooker JD (eds) Genera Plantarum 1:725–773. Reeve & Co., London Hutchinson J (1973) The families of flowering plants, 3rd edn. Clarendon Press, Oxford Jacques-Félix H (1994 [“1995”]) Histoire des Melastomataceae d’Afrique. Bulletin du Muséum National d’Histoire Naturelle, série 16, sect. B, Adansonia, 2–4:235–311 Janssonius HH (1950) Wood anatomy and relationship. Blumea 6:407–461 Krasser F (1893) Melastomataceae In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien III(7):130–199. Wilhelm Engelmann, Leipzig Lamy D (2019) Antoine-Laurent de Jussieu, a new method of plant classification. In: Huxley R (ed) The great naturalists. Thames & Hudson Ltd., London, pp 171–175 Lawrence GHM (1951) Taxonomy of vascular plants. The MacMillan Co., New York Martin CV, Cremers G (2007) Les Melastomataceae américaines décrites par C. Naudin. J Bot Soc Bot France 37:3–111 Marza VD, Cerchez N (1967) Charles Naudin, a pioneer of contemporary biology (1815-1899). J Agric Trop Bot Appl 14(10–11):369–401 Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons. 2 vols. Clarendon Press, Oxford Michelangeli FA, Nicolas A, Morales-P ME, David H (2011) Phylogenetic relationships of Allomaieta, Alloneuron, Cyphostyla, and Wurdastom (Melastomataceae) and the resurrection of the tribe Cyphostyleae. Int J Plant Sci 172:1165–1178 Michelangeli FA, Almeda F, Goldenberg R, Penneys DS (2020) A guide to curating New World Melastomataceae collections with a linear generic sequence to world-wide Melastomataceae. Preprints 2020:2020100203. https://doi.org/10.20944/preprints202010.0203.v1 Naudin CV (1849–1853) Melastomacearum quae in Musaeo Parisiensi continentur monographicae descriptionis. Annales des Sciences Naturelles, Botanique, série III. tom. xii-xviii, Victor Masson, Paris, (consolidated reprint) Naudin CV (1851) Melastomacearum quae in Musaeo Parisiensi continentur monographicae descriptionis. Ann Sci Nat Bot III 15:43–79

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Nayar MP (1974) A revision of Plethiandra (Melastomataceae). Reinwardtia 9:143–151 Penneys DS, Judd WS (2013) Combined molecular and morphological phylogenetic analyses of the Blakeeae (Melastomataceae). Int J Plant Sci 174:802–817 Penneys DS, Michelangeli FA, Judd WS, Almeda F (2010) Henrietteeae: a new neotropical tribe of berry-fruited Melastomataceae. Syst Bot 35:783–800 Renner SS (1990) C. A. Cogniaux (1841-1911). Blumea 35:1–3 Renner SS (1993) Phylogeny and classification of the Melastomataceae and Memecylaceae. Nord J Bot 13:519–540 Rocha MJR, Guimarães PJ, Michelangeli FA, Nogueira Batista JA (2018) Taxonomy of Marcetieae: a new neotropical tribe of Melastomataceae. Int J Plant Sci 179:50–74 Stearn WT (1965) Grisebach’s Flora of the British West Indian Islands: a biographical and bibliographical introduction. J Arnold Arbor 46:243–285 Stevens PF (1994) The development of biological systematics: Antoine-Laurent de Jussieu, nature, and the natural system. Columbia University Press, New York Stevens PF (2001 onwards) Angiosperm phylogeny website. Version 14, July 2017 [and more or less continuously updated since]. http://www.mobot.org/MOBOT/research/APweb/ ter Welle BJH, Koek-Noorman J (1981) Wood anatomy of the neotropical Melastomataceae. Blumea 27:335–394 Thorne RF (1992) Classification and geography of the flowering plants. Bot Rev 58:225–348 Triana J (1866) Dispositio Melastomacearum. Bull Congr Int Bot Hort Amsterdam 1865:457–461 Triana J (1871 [“1872”]) Les Mélastomacées. Trans Linn Soc London 28:1–188 Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Kusber W-H, Li D-Z, Marhold K, May TW, McNeill J, Monro AM, Prado J, Price MJ, Smith GF (eds) (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress, Shenzhen, China, July 2017. Regnum Vegetabile 159. Koeltz Botanical Books, Glashütten. https://doi.org/10.12705/ Code.2018 van Tieghem PEL (1891) Classification anatomique des Mélastomacées. Bull Soc Bot France 38:114–124 van Vliet GJCM (1981) Wood anatomy of the paleotropical Melastomataceae. Blumea 27:395–462 van Vliet GJCM, Baas P (1984) Wood anatomy and classification of the Myrtales. Ann Missouri Bot Gard 71:783–800 van Vliet GJCM, Koek-Noorman J, ter Welle BJH (1981) Wood anatomy, classification and phylogeny of the Melastomataceae. Blumea 27:463–473 Veranso-Libalah MC, Stone RD, Kadereit G (2020) Towards a complete phylogeny of African Melastomateae: systematics of Dissotis and allies (Melastomataceae). Taxon 69:946–991

Morphological Variability Within the Melastomataceae (Myrtales), Including a Discussion of the Associated Terminology Walter S. Judd, Lucas C. Majure, Fabián A. Michelangeli, Renato Goldenberg, Frank Almeda, Darin S. Penneys, and R. Douglas Stone

Introduction With more than 5800 species (Michelangeli et al. 2020; see Ulloa Ulloa, chapter “Melastomataceae: Global Diversity, Distribution, and Endemism”), the Melastomataceae are the ninth most species-rich family of angiosperms W. S. Judd (*) ∙ L. C. Majure Department of Biology, University of Florida, Gainesville, FL, USA University of Florida Herbarium, Florida Museum of Natural History, University of Florida, Gainesville, FL, USA e-mail: [email protected]; [email protected] F. A. Michelangeli Institute of Systematic Botany, The New York Botanical Garden, Bronx, NY, USA e-mail: [email protected] R. Goldenberg Departamento de Botânica, Centro Politécnico, Universidade Federal do Paraná, Curitiba, PR, Brazil e-mail: [email protected] F. Almeda Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA e-mail: [email protected] D. S. Penneys Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA e-mail: [email protected] R. D. Stone School of life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 R. Goldenberg et al. (eds.), Systematics, Evolution, and Ecology of Melastomataceae, https://doi.org/10.1007/978-3-030-99742-7_3

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(Christenhusz et al. 2017), and they are the second largest family of the Myrtales (following the Myrtaceae, with 5950 species). The group is exceptionally diverse morphologically, but most morphological characters are highly homoplasious. We present an overview of the exceptional morphological (including vegetative anatomical) variation within the Melastomataceae and also deal with the related issue of morphological terms, following the general outline proposed by Leenhouts (1968). Examples illustrating the patterns of variation are provided, especially those of systematic significance at the subfamilial and tribal levels. Additionally, examples of the taxonomic value of such character variation from specific to generic levels are provided, although in a family of such size and variability, such examples, out of necessity, are very far from being complete.

Habit Most Melastomataceae are trees, shrubs, or herbs, although lianas and vines also occur, and the mechanism of climbing is by adventitious roots (Fig.  1a; as in Adelobotrys, Blakea, Catanthera, some Graffenrieda, some Gravesia, Macrolenes, Miconia, and Phainantha) or more-or-less horizontal, lateral branches (e.g., most Dissochaeteae, some Pleroma, Arthrostemma ciliatum, Miconia sarmentosa; see also Kartonegoro et al. 2018). Some are epiphytic or hemiepiphytic (e.g., Monolena, Triolena, some species of Blakea, Medinilla, Miconia—the Pleiochiton clade, other species such as Miconia confertiflora, Miconia grandidentata, Miconia neoepiphytica, and Miconia trichocalyx; see Wurdack 1980; Renner 1986a; Almeda 2009; Reginato et al. 2010, 2013; Reginato and Michelangeli 2016a; Judd et al. 2018b). The tree habit (Fig. 1b–e) is concentrated in phylogenetically early-diverging clades, i.e., the Olisbeoideae, Kibessioideae as well as the Astronieae, Henrietteeae, Merianieae, and Miconieae of the Melastomatoideae, although the feature is highly homoplasious, also occurring in many other infrafamilial clades. Many herbaceous species occur in the Bertolonieae, Trioleneae, Sonerileae, Rhexieae, Marcetieae, and Melastomateae (see also Bacci et  al. 2019). Such species may be perennials (most herbaceous species) or annuals (Fig.  1f; e.g., Aciotis, some Acisanthera, Antherotoma, Brasilianthus, Derosiphia, some Nerophila, some Osbeckia, Poteranthera, Pterolepis, many Siphanthera). The bark of the woody species is usually gray or gray-brown and is smooth to shallowly and longitudinally furrowed or

Fig. 1  (continued) growth with terminal inflorescences deflexed and pseudolateral (Judd 3057). (e) Miconia crossosepala, shrub with Rauh’s model, axillary inflorescences (Ionta 2001). (f) Marcetia canescens, annual herb (Almeda 8287). (g) Miconia alainii, opposite, acrodromous leaves (Judd 8105). (h) Miconia vulcanidomatia, domatia (Skean 5000). (i) Miconia polyflora, domatia (Skean 5063). (j) Miconia lima, leaves with bulla-based hairs (Majure 6020). (k) Henriettea ramiflora, cauliflorous, berries (Judd 8346). (l) Medinilla myriantha, corolla contorted, androecium zygomorphic (no voucher). (m) Rhexia mariana, flowers 4-merous, buzz pollination (no voucher). (n) Monochaetum bonplandii, flowers 4-merous, buzz pollination (Michelangeli 1239). Photographs: a–e, g, h, k–m by Judd; f by Almeda, n by Michelangeli, i by J. D. Skean Jr., and j by Majure

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Fig. 1  Morphological variation in the Melastomataceae, I. (a) Blakea trinervia, liana with adventitious roots (Judd 8305). (b) Miconia macrocarpa subsp. tuerckheimii, shrub with Leeuwenberg’s model, terminal inflorescences (Judd 5102). (c) Miconia subcompressa subsp. beverlyana, terminal, pleiothyrsoid inflorescences, berries pale blue (Judd 6561). (d) Miconia crenata, sympodial

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flaking. The architectural growth model is usually associated with inflorescence position (more below). Plants with terminal inflorescences usually exhibit Leeuwenberg’s model (Fig. 1b), although others occur, e.g., Miconia tococa with Scarrone’s model or Miconia solenifera with Stone’s model; Hallé et al. 1978), and those with exclusively axillary inflorescences correspond to Rauh’s architectural model (Fig. 1e; Hallé et al. 1978; Judd 1986a, b). Cremers (1986) also reports species with Mangenot’s model (species of Mouriri, Votomita of the Olisbeoideae), Aubreville’s model (Blakea, Bellucia), Chamberlain’s model (Macrocentrum), Koriba’s model (Miconia), Fagerlind’s model (Miconia), and Petit’s model (Miconia). Herbaceous species usually have obvious stems, although more-or-less acaulescent herbs with basal rosettes occur in some clades, e.g., Lithobium and some Sonerileae and Trioleneae.

Underground Parts The root system has been poorly studied, but it may spread or form a taproot; plants may or may not be rhizomatous or adventitious shoots may develop on more-or-less horizontal roots (as in Rhexia; Holm 1907; Nesom 2012). The rhizomes of the Lithobieae and some Eriocnemeae are tuberous (Penneys et al. 2020), as are a few species of Phyllagathis (Cellinese 2002) and Sonerila (Navayanan et  al. 2017). Tubers are also found in Rhexia (Holm 1907; James 1956; Kral and Bostick 1969; Wurdack and Kral 1982; Nesom 2012), Chaetogastra (Meyer et al. 2021), and some Bertolonia, and a fleshy rhizome is characteristic of many Trioleneae. In the epiphytic Pleiochiton clade (within Miconia), the roots are succulent (Reginato et al. 2010, 2013). Several species of seasonally dry environments in the cerrado biome of Brazil and other savanna ecosystems produce subterranean woody lignotubers (xylopodia) that buffer plants against water loss, temporal nutritional deficiency, and also provide protection against fires (Gottsberger and Silberbauer-Gottsberger 2006; Martins and Almeda 2017; Veranso-Libalah et al. 2020).

Vegetative Buds There is usually only a single bud in each leaf axil, but, sometimes, superposed buds occur (especially in inflorescences, leading to multiple inflorescence axes per node; Weberling 1988). Bud scales are absent, but each bud is associated with two lateral prophylls. There is usually no dormant period, and growth is thus sylleptic, with the first internode of the new shoots being longer than the subsequently produced internodes. The young leaves (in the bud) show conduplicate, supervolute, revolute, or flat ptyxis (Cullen 1978, 2006).

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Stems Stems are often terete-to-ellipsoidal, but quadrangular stems are also common with the adjacent faces similar or divergent in form, i.e., varying in the presence or absence of a longitudinal groove, convex vs. concave in form, narrow vs. broad, with the stem itself having a square vs. diamond shape in cross section. Short shoots are present in some Pyramieae. Stems are rarely basally swollen (e.g., Noterophila; Rocha et al. 2018); however, they are markedly swollen with water storage adaptations in some species of Merianthera (Ziemmer et al. 2017) and Cailliella (VeransoLibalah et al. 2021). Swollen stems that form ant domatia occur in some cases, e.g., Blakea inflata and Pachycentria (Michelangeli 2010; Michelangeli and Goldenberg 2021). Stems are sometimes winged; see, for example, Miconia alatissima, of the Octopleura clade (Gamba and Almeda 2014), Miconia quadrialata (Renner and Beck 2003), Pleroma kollmanniana (Meyer et al. 2016), Rhexia virginica (Kral and Bostick 1969), Medinilla magnifica, and some species of Memecylon (Stone 2015). Stem shape is frequently useful taxonomically, especially at the level of species or species groups, e.g., within the Miconia subcompressa complex (Judd and Beaman 1988; Judd 2007), in Miconia sect. Sagraea (Ionta et  al. 2012), in Pleroma (Goldenberg, pers. comm.), in Rhexia (Kral and Bostick 1969), and in Memecylon of the Olisbeoideae (Amarasinghe et al. 2021). However, stem shape is sometimes quite variable, even within a species, as in Miconia stenobotrys (Judd and Karpook 1993). Shape can also change with the age of the stem. The nodes may or may not be differentiated, and, often, an interpetiolar nodal line extends across the node. The nodal line is rarely extended, forming a conspicuous outgrowth or flange or even stipuliform flaps, e.g., in Miconia crassinervis of Miconia sect. Sagraeoides (Skean Jr 1993; Skean Jr et al. 2018); in Miconia bractiflora, Miconia solearis, and relatives of the Octopleura clade (Gamba and Almeda 2014, 2015); in Miconia cinnamomifolia of Miconia sect. Glossocentrum and in Miconia elvirae and Miconia punctibullata of Miconia sect. Cremanium (Morales-­ Puentes et  al. 2008, see also species listed therein); or in some Dissochaeta (Kartonegoro et al. 2018) and some Blakea (Penneys and Judd 2011). Some species have conspicuous lenticels associated with the nodes (Judd 2007; Judd and Ionta 2013; Kriebel 2016a). Some species of Warneckea, of the Olisbeoideae, have a tuft of bristles in the leaf axils (Gilg 1904).

Stem and Wood Anatomy The distribution of wood anatomical characters in the Melastomataceae is taxonomically useful (Tieghem 1891a, b; Metcalfe and Chalk 1950; Koek-Noorman et  al. 1979; ter Welle and Koek-Noorman 1981; van Vliet 1981; van Vliet et  al. 1981; van Vliet and Baas 1984). Vessel elements have simple perforation plates and vestured pits. The typical Melastomataceae have libriform fibers, often large and

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simple vessel-ray pits, fiber dimorphism, libriform septate and nonseptate fibers, and grouped vessels. However, Pternandra (i.e., Kibessioideae) has fiber tracheids and intraxylary phloem, as in the Olisbeoideae (ter Welle and Koek-Noorman 1981; van Vliet 1981; van Vliet et  al. 1981; van Vliet and Baas 1984; see also Renner 1993). Wood rays are uniseriate, and some of them are two- to five-seriate, heterocellular, or less often homocellular; the wood parenchyma is commonly paratracheal and rather scanty but sometimes also occurs in apotracheal ribbons, including some vertical crystalliferous strands. Crystals of calcium oxalate form crystal sand, druses (widespread within the family), or styloids/megastyloids (Henrietteeae, Astronieae), although rarely are both druses and styloids absent (e.g., the Charianthus clade within Miconia) (see also ter Welle and Mennega 1977; Baas 1981; Penneys and Judd 2005). Large styloids have been recorded from the wood of the Olisbeoideae (Memecylon, Mouriri) and Kibessioideae (Pternandra), although such crystals are lacking (or at least not obvious) in the leaf lamina, where they are largely replaced by druses (Baas 1981). In contrast, in the Astronieae and Henrietteeae of the Melastomatoideae, megastyloids are abundant and obvious in the leaves (see the section “Leaf Anatomy” below). Stems have internal phloem, as is typical of the Myrtales (Judd et al. 2016), and, sometimes, an interxylary phloem is present as well. Medullary vascular bundles are often present and are likely synapomorphic for a large subclade of the Melastomatoideae (excluding the Henrietteeae and Astronieae, which lack these bundles), although losses within this large clade do occur, e.g., in some Sonerileae. Cortical vascular bundles are sometimes present, e.g., in the Rhexieae. Lignified idioblasts may be densely scattered in the cortex to sparse or lacking. The cortices of species of the Olisbeoideae have elongated and/or branched sclereids. The cells of the pith may be lignified or unlignified. The nodes are unilacunar (Metcalfe and Chalk 1950), although the vascular bundle often quickly divides into several strands at the petiole base (see references under the section “Leaf Anatomy”). In the Olisbeoideae, however, the petiolar strand is not divided but, instead, is weakly to strongly arcuate or even cylindrical (Morley 1953).

 eaves (Including Arrangement, Structure, Petiole, Shape L of the Blade, Base of the Blade, Apex of the Blade, Margin of the Blade, and Venation) and Stipules The terminology relating to variation in leaf form has been inconsistently used in systematic botany, and we recommend the straightforward and consistent set of descriptive terms advocated by Hickey (1973, 1979), Dilcher (1974), Ellis et  al. (2009), and Judd et al. (2016). Leaves of the Melastomataceae are usually opposite and decussate (Figs. 1b, g and 2h; although sometimes appearing two-ranked), but whorled leaves occasionally occur (e.g., some Medinilla; Regalado 1995; some Miconia; Goldenberg and

Fig. 2 (a) Blakea trinervia, enlarged bracteoles, flowers 6-merous, androecium actinomorphic (Judd 5506). (b) Miconia umbellata, flowers 6-merous, androecium zygomorphic (Judd 8084). (c) Henriettea succosa, androecium zygomorphic, porose anthers (Goldenberg 1738). (d) Miconia dodecandra, flowers 5-merous, androecium zygomorphic, anthers porose, buzz pollination (Judd 5497). (e) Mouriri densifoliata, enlarged anther connective with gland (Goldenberg 2747). (f) Miconia albertobrenesii, ribbed hypanthium, berries expanding when fully mature (Almeda 10,257). (g) Miconia conorufescens, calyptrate calyx, notched petals (Judd 8324). (h) Meriania purpurea, note calyx teeth, contorted corolla, also acrodromous leaves (Judd 8319). (i) Miconia hispidula, calyx teeth elongated, flat (Judd 8153). (j) Cambessedesia fasciculata, petals bicolored (Almeda 9115). (k) Miconia albertobrenesii, note calyx teeth, petals with acute apex (Almeda 10,257). (l) Miconia purpurea, corolla forming a tube (Mori et  al. 26,862). (m) Microlicia cordata, note pedoconnective (Almeda 9188). (n) Melastoma candidum, note pedoconnective (no voucher). Photographs: a, b, d, g–i by Judd, c, n by Michelangeli, e by Goldenberg, f, j, k, m by Almeda, and l by C. Gracie

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Reginato 2007; Almeda 2009), and rarely are they strongly pseudoverticillate (e.g., Tryssophyton; K.  Wurdack and Michelangeli 2019). The plants are usually evergreen, but a few have deciduous leaves, e.g., among the Melastomatoideae, Amphorocalyx, Cailliella, Dionychastrum, some Dichaetanthera, Dissotidendron, Dionycha, Merianthera, Nothodissotis, a few Miconia, and Tibouchina papyrus and, among the Olisbeoideae, a few Mouriri species. Leaves may be equal in size and shape (Fig. 1d, j), or one member of the pair may be slightly to markedly smaller (Fig. 1e) and may also occasionally be different in form, i.e., anisophylly; for example, at least some species of Allomaieta, Bertolonia, Blakea, Centradenia, Macrocentrum, numerous Miconia (especially those formerly included in Maieta, Myrmidone, some Clidemia, e.g., Mauritia flexuosa, Mauritia farinasii, and Mauritia Longidentata) and also some members of the Octopleura clade, some Medinilla, some Phyllagathis, some Sonerila, and some Triolena (Cremers 1995; Muelbert et al. 2010; Michelangeli and Meier 2013; Gamba and Almeda 2014). The smaller leaf is developmentally suppressed or caducous in a few species, (e.g., Bertolonia alternifolia; some Centradenia, Macrocentrum, Miconia, Phainantha), leading to seemingly alternate leaves. Bertolonia michelangeliana seems to be truly alternate, but this needs anatomical study. Some species of Memecylon (Olisbeoideae) have branches with successive nodes with photosynthetic leaves alternating with reduced, often inflorescence-bearing, bract leaves (Jacques-Félix 1983; Stone 2014). The leaves are simple and petiolate-to-sessile, with the petiole that is terete to adaxially flattened or grooved. The blade may rarely be peltate, as in Blakea tuberculata, Miconia peltata (Kriebel 2016a), Miconia repens, some Meriania, Gravesia gunneroides, Gravesia ikongoensis, and Merianthera verrucosa. A variably developed basal pulvinus is present. The blade varies greatly in size (from minute, as in some species of Microlicia and Marcetia, to extremely large, as in Miconia calvescens and Miconia serrulata), texture (from membranous to quite coriaceous), and shape (from narrowly to broadly ovate, elliptical, obovate, or oblong). The leaf base varies from decurrent, narrowly acute or cuneate to broadly cordate, and the apex varies from acute, acuminate, or attenuate to rounded or emarginate. The lamina margin varies from entire or undulate to variously toothed (especially regularly or irregularly dentate-to-serrate) and may be plane-to-strongly revolute. The margin may be associated with hairs, and, if these are simple and elongated, it is frequently described as ciliate, e.g., some species of Rhexia (James 1956) and Miconia suberosa (Meirelles and Goldenberg 2014). The predominant venation pattern is acrodromous (Figs. 1b–e, g–j and 2h, i), and this character is a possible familial synapomorphy. Although most species of the Olisbeoideae lack obvious acrodromous venation (Fig. 3e), the character is cryptically present anatomically in many species (Stone 2006). In several Paleotropical genera (Lijndenia, Spathandra, and Warneckea), the conspicuously acrodromous state appears exclusively or at least predominantly, and it was inferred by Stone (2006) to be the ancestral condition in the Olisbeoideae. The leaves of most species of Memecylon or Mouriri are best described as apparently uninervate (with only the midvein clearly present) or obscurely acrodromous (see also Jacques-­ Félix et al. 1978).

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Fig. 3 (a) Fritzschia sertularia, note pedoconnective (no voucher). (b) Miconia selleana, androecium actinomorphic, same color as petals, opening by slits (Judd 8158). (c) Meriania leucantha, capsules (Judd 8303). (d) Triolena amazonica, angular capsules (Michelangeli 1366). (e) Memecylon gracillimum, berries, note also obscure leaf venation (Amarasinghe et  al. D9). (f) Melastoma malabathricum, fruit with fleshy placentas, intermediate between capsule and berry (no voucher). Photographs: a by Almeda, b, c, f by Judd, d by Michelangeli, and e by P. Amarasinghe

Even within the Melastomatoideae, sometimes the venation is only cryptically acrodromous (with the pair of converging secondary veins inconspicuous and near the lamina margin) or even obviously pinnately veined and brochidodromous (e.g., Alloneuron; see Michelangeli et al. 2011, many Heterocentron; see Almeda 2009). In some, e.g., the Trembleya clade within Microlicia (Versiane et  al. 2021), the venation is highly reduced and obscure. The terminology of acrodromous venation is inconsistent across the literature and even within the Melastomataceae. There is an obvious midvein (always called the primary vein) and then pairs of arched veins on either side of the midvein that go from or near the base of the leaf blade toward its apex (Fig. 1g–j). These veins are very often also called primaries, but, if they become progressively thinner on the outer pairs, then they may be termed “secondaries,” a terminology also supported by the fact that they arise from the primary vein. However, this nomenclature is confusing because these paired veins can be given different names in closely related species or even in the same individual, depending on leaf size and maturity. We prefer to call these arching veins secondary and those that run from the midvein perpendicularly (or nearly so) to the secondaries as tertiary veins. This terminology has been adopted in recent species descriptions and in the fossil literature (see Carvalho et  al. 2021). The tertiary veins are usually percurrent (scalariform) and oriented more-or-less perpendicular to the midvein (Figs.  1d, e, g and 2h, i). The tertiary veins may be connected by one-to-several quaternary veins or separated by the development of a composite intertertiary vein. Higher-order veins are more-or-­less reticulate (Fig. 2b). The various veins may be flat to strongly impressed adaxially,

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resulting in the areoles ranging from obscure to strongly bullate. The midvein is (or the primary veins are) usually raised abaxially, and the secondary to higher-­order veins may be raised and prominent (Fig. 1g) to obscure (Fig. 1h). All of these leaf characters, especially those of venation, are frequently of systematic value (see the floras and taxonomic revisions included in the literature cited), although there is much homoplasy, and closely related species may differ in these characters, especially the extent of abaxial prominence of the veins and their pattern of interconnection (Judd 1994, 2007; Judd and Beaman 1988). Stipules are usually absent, but rarely are they present and conspicuous, and developmentally arise from the lower, modified portion of the lamina. They are often called pseudostipules (Bodegom and Veldkamp 2001), but it is simpler to call them stipules, as such structures are not homologous across angiosperms (Judd et al. 2016). Large and showy stipules occur in Astronidium miraculum-dei (Maxwell and Veldkamp 1990) and in several species of Medinilla (Bodegom and Veldkamp 2001). They also occur on the petioles of Miconia vincentiana (Judd and Ionta 2017). At least superficially similar structures occur in Miconia spennerostachya, but, in this species, they may actually represent extrafloral nectar glands. A clade within Blakea, i.e., the Blakea jativae group, has large, overlapping papery stipules, a unique feature of the family. Another distinctive stipular condition occurs in some species of Memecylon and Mouriri of the Olisbeoideae, in which a row of finger-­ like structures occurs on the stem adjacent to the petiole base (Dahlgren and Thorne 1984).

Domatia Ant domatia (formicaria) have evolved several times in the Melastomataceae and may occur in a hollow stem (some Blakea, Diplectria, and Dissochaeta; Penneys and Judd 2011; Clausing 1998), swollen stem (Blakea, Miconia; Michelangeli 2010, 2014; Michelangeli and Goldenberg 2021), in paired ascidia at the petiole base or apex (Miconia, in a few species formerly included in Clidemia; Michelangeli 2010), or in the petiole or base of the lamina (Allomaieta, Blakea, Henriettea DC., and especially in Miconia, occurring in various species formerly included, for example, within Clidemia, Conostegia, Maieta, and Tococa; Gleason 1931; Michelangeli 2005, 2010). Ant domatia may be found even in roots (Pachycentria, some Medinilla). Mite domatia (acarodomatia) have evolved on the abaxial leaf surfaces of many Melastomataceae (especially the Miconieae, Pyxidantheae, and Sonerileae but also in some Melastomateae and Merianieae). Such structures are usually found at the inrolled lamina margin (Fig. 1i) or at the junctions of the major secondary veins and the midvein (Fig. 1h) (although they may occasionally occur at other vein junctions) and (following the terminology of Stace 1965, and Wilkinson 1979; see also Jacobs 1966, and Schnell et al. 1968) they may be marsupiform (pouch-like, in vein axils, with or without outgrowths of the adjacent veins), revolute (formed by a revolute

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leaf margin), or hair tuft (formed by a tuft of usually elongated hairs in vein axils). Typical hair tuft domatia occur in some species of Miconia sect. Calycodomatia, but several species, e.g., Miconia wrightiana, Miconia torbeciana, and Miconia vulcanidomatia, have unusual volcano-like domatia (Fig. 1h), in which the mite chamber is formed by a group of connate hairs with an apical opening. Acarodomatia are typically inhabited by predatory or fungus-eating mites and, as such, are beneficial to the host plant (Pemberton and Turner 1989; Walter 1996); however, the ecology of domatia has been poorly studied. Domatia are usually absent from species that have a dense abaxial leaf indumentum, probably because the indumentum itself provides shelter for mites. Mite domatia are frequently taxonomically informative, e.g., in Blakea (Penneys and Judd 2011), or distinguishing Miconia fadyenii from the species of the Charianthus clade (Fig.  2l), with which it has been confused (Penneys and Judd 2003).

Leaf Anatomy The petiolar and laminar anatomies of the Melastomataceae are relatively complex (Solereder 1908; Metcalfe and Chalk 1950; Morley 1953; Baas 1981; Mentink and Baas 1992; Skean Jr 1993; Sampaio de Souza and Marquete 2000; Reis et al. 2004; Judd 2007; Kriebel 2016a; Silva et al. 2018; Carmo et al. 2019, 2020; Romero et al. 2021). Generally, in the Melastomatoideae, several major collateral, bicollateral, or amphicribal vascular bundles are present, often along with several smaller accessory bundles, and these form an interrupted arc when viewed in cross section, with the accessory bundles (if present) positioned within the arc. As the vascular supply passes along the midvein (of the lamina), the bundles may remain distinct or coalesce into a shallow or deeply U-shaped structure, sometimes with smaller accessory bundles positioned in its center. However, in the Olisbeoideae, more variability is seen, with the petiolar strand not divided, forming a weakly to strongly arcuate, or even cylindrical bundle, in both the petiole and midvein (Morley 1953; Mentink and Baas 1992), or dividing into three to five bundles positioned in an arc (Lignier 1887; Jacques-Félix 1935; Jacques-Félix et al. 1978). The petiole and lamina of the Olisbeoideae have elongated-to-branched sclereids associated with the highest-order vein endings (Morley 1953, 1976; Ananda Rao and Jacques-­Félix 1978; Ananda Rao et  al. 1983; Mentink and Baas 1992; Renner 1993), whereas these are absent in the Kibessioideae and Melastomatoideae, although lignified idioblasts may be present (see initial citations), and elongated sclereids (easily seen in dried leaves) have been reported from Aciotis (Melastomateae; Freire-Fierro 2002); Ananda Rao and Nayak (1987) reported vein-terminating idioblasts in the leaves of Pternandra (Kibessioideae). Stomatal crypts are usually present in the lamina abaxially in the Neotropical Olisbeoideae (Morley 1953, 1976; Goldenberg et al. 2013), but these are usually considered absent in the remaining clades within the family. However, stomatal crypts are found in Chaetolepis cufodontisii and Chaetolepis lindeniana (Melastomateae; Kriebel 2015), and they have been

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observed in Comoliopsis (Marcetieae; Rocha et  al. 2018) and Trembleya (Lavoisiereae; Carmo et al. 2020). The lamina structure is usually dorsiventral (but, occasionally, as in Rhexia alifanus, or in some species of Microlicia, both surfaces are identical; see Kral and Bostick 1969; Carmo et al. 2020), with a thin to extremely thick cuticle. The cells of the epidermis may have straight-to-sinuous anticlinal walls. A hypodermis (of one-to-three cell layers) is often present, and, in the species of Miconia formerly included in Pleiochiton, it functions in water storage (Reginato et  al. 2009). The palisade mesophyll is composed of 1–3 layers, and the spongy mesophyll varies from 2 to 20 cell layers and is often quite dense. The lamina varies greatly in thickness. The laminas of the Henrietteeae have prominent megastyloids, and these may be positioned parallel or at right angles to the leaf surface (Baas 1981; Judd 1986b; Judd et al. 2008; Carmenate-Reyes et al. 2017), and large styloid crystals are also a characteristic of the Astronieae (Mentink and Baas 1992). Most melastomes have druse crystals in the lamina (Mentink and Baas 1992), and these are especially conspicuous when positioned in extremely large cells of the adaxial epidermis, sometimes creating papillae-like structures adaxially when the leaf is dried. Some groups, e.g., the Charianthus clade of Miconia, have lost druses (Penneys and Judd 2005). The stomatal form (Wilkinson 1979) is exceptionally diverse within the Melastomataceae, including anomocytic, anisocytic, cyclocytic, diacytic, desmocytic, paracytic, polocytic, and tetracytic conditions (Baas 1981; Mentink and Baas 1992; Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Epicuticular waxes in the form of platelets may be present (Wurdack 1986; Renner 1989a). Most of the species seem to be hypostomatic, but amphistomatic species occur across many members of the Melastomateae, Microliceae, and Rhexieae (Kral and Bostick 1969; Mentink and Baas 1992; Guimarães and Woodgyer 2016).

Indumentum The Melastomataceae exhibit an excellent diversity of hair types, ranging from unicellular to multicellular and then uniseriate to multiseriate, nonglandular to glandular (then with heads globose to elongated, with cells obscure to well-differentiated), short to elongated, smooth to roughened or with short outgrowths/enations, straight to curved or even bent-crisped, unbranched to variously branched (stellate to variously dendritic), and even forming elongated and flattened scales or rounded peltate scales (Wurdack 1986; Mentink and Baas 1992; see also the various taxonomic revisions cited herein). Such scales, for example, are diagnostic for Andesanthus, Tibouchina s.s., and Loricalepis (Todzia and Almeda 1991; Rocha et al. 2018; Guimarães et al. 2019) and are synapomorphic for the core members of the Miconia decorticans clade (Majure et al. 2014). The cells adjacent to the hairs may or may not be modified, and extremely bullate-based hairs, i.e., hairs with the basal region dramatically expanded, also occur (e.g., see Majure et al. 2015, 2016).

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Although several useful terminology schemes pertaining to hair morphology have been proposed, e.g., Dilcher (1974), Payne (1978), and Theobald et al. (1979), we recommend the system developed for Neotropical Melastomataceae by Wurdack (1986). Because, often, several different kinds of hairs co-occur on leaves, hypanthia, and/or stems (e.g., Miconia umbellata (Fig. 2b), which has globular, stellate, elongated, simple, eglandular, and gland-headed hairs intermixed on its abaxial leaf surfaces; Judd and Ionta 2013), we do not recommend the use of indumentum terms such as “hirsute,” “scabrous,” “sericeous,” etc., which purport to describe the overall surface texture (as proposed, for example, in Stearn 1992; Harris and Harris 2001; Beentje 2012) used in floras (see Kiger and Porter 2001). Instead, the individual hairs should be described and their density and position on the plant should be stated, as advocated by Dilcher (1974). As would be expected, hair morphology is useful at multiple taxonomic levels, and these characters have traditionally been stressed in practical identification and in the circumscription of specific-to-infrafamilial groups (Gleason 1930, 1931, 1932, 1958; Macbride 1941; Wurdack 1962, 1973, 1980; Todzia and Almeda 1991; Almeda 1978, 2009; Judd 2007; Judd et  al. 2014a, b; Michelangeli et  al. 2015; Kriebel 2016a; Alvear and Almeda 2019; Carmo et al. 2019; see also other taxonomic revisions cited herein). Many examples of the species-level usefulness of hair morphology or density could be cited, e.g., Miconia howardiana, which has long-­ stalked, gland-headed hairs on the stems and hypanthia, while these are lacking in the related Miconia campanensis (Judd 2007) or Miconia tentaculicapitata, which has bulla-based hairs completely covering the areoles on the adaxial leaf surface, whereas in Miconia pedunculata, these hairs do not completely cover the areoles (Majure et  al. 2016). In addition, hair morphology is often useful in diagnosing groups of related species, such as Miconia lanceolata and relatives (within Miconia sect. Chaenopleura) with globular-stellate hairs with crisped arms, M. howardiana and relatives with dendritic hairs (Judd 2007), the Miconia discolor clade, with its dense stellate-to-short dendritic hairs or peltate scales (Michelangeli, in prep.), or the Caribbean species of Henriettea with ferrugineous peltate scales (Judd 1986b; Judd et al. 2008; Carmenate-Reyes et al. 2017). Hairs are also useful in recognizing higher-level clades, e.g., Adelobotrys always has T-shaped trichomes (Schulman and Hyvönen 2003). Henriettea can be distinguished from Bellucia by its distinctive hairs (Judd 1989; Penneys et al. 2010). The presence or absence of bulla-based hairs (Fig. 1j) and globular-stellate hairs is useful in distinguishing subclades within the Sandpaper clade of Miconia (Majure et  al. 2015), and the characteristic small, gland-headed hairs in which the individual cells of the glandular head are separated by furrows, diagnose Miconia sect. Sagraea, when taken together with their axillary inflorescences (Ionta et al. 2012; Judd et al. 2018b). In contrast, the Olisbeoideae and Kibessioideae are notable in their usual absence of hairs (Maxwell 1981; Dahlgren and Thorne 1984), although they are present on a few (e.g., Memecylon pubescens, Pternandra hirtella). In addition to hairs, the epidermal surface may have minute papillae, as in some species of Bellucia (Renner 1989a); otherwise, it varies from smooth to striate (Mentink and Baas 1992).

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Inflorescences The terminology relating to the inflorescence form is especially problematic; we not only recommend the terminology of Troll (1964) and Weberling (1965, 1989), which has been carefully applied to the families of the Myrtales, including the Melastomataceae (Weberling 1988), but also see the treatment of inflorescence variation in Cremers (1986). The inflorescences of the Melastomataceae are always monotelic (determinate), exhibiting various forms of cymose branching, although they may be reduced to fascicles, umbellate clusters, or even solitary flowers. Among the excellent array of inflorescence branching patterns, scorpioid inflorescences are probably the most visually striking, occurring in various Bertolonieae, Cyphostyleae, Merianieae, Miconieae, Sonerileae, and Trioleneae. The inflorescences may be terminal (or terminal and axillary) (Fig. 1b–d) or exclusively axillary (Figs. 1e, k and 2e, l) (and then in leaf axils, Fig. 1e, or on older leafless nodes, or even cauliflorous, Fig. 1k). Sometimes, the inflorescences can even emerge from the base of the trunk (Cámara-Leret and Veldkamp 2011) or the roots (Regalado 1995). As noted by Weberling (1988), the most common condition is a pleiothyrsoid (usually called a cyme or paniculate cyme in the American taxonomic literature Fig. 1c) terminating a vegetative shoot, as is seen, for example, in all or most species of Aciotis, Graffenrieda, Macairea, Meriania, Miconia, Microlicia, Monochaetum, Pachyloma, and Tibouchina (and its segregates). Axillary inflorescences (in leaf axils, old twigs, or cauliflorous) characterize the Kibessioideae, most Olisbeoideae and Henrietteeae, and all fairly early-divergent lineages of the Melastomataceae; yet, the terminal condition predominates in most Melastomatoideae. However, many Miconieae do show axillary flowers, e.g., Miconia sect. Sagraeoides (Skean Jr 1993; Judd et al. 2015; Skean Jr et al. 2018), Miconia sect. Sagraea (Ionta et al. 2012), Miconia leblondii of the Charianthus clade (Penneys and Judd 2005), some members of Miconia sect. Calycopteris (Judd et al. 2014a; Bécquer et al. 2018), some species of Miconia sect. Echinatae (Majure et al. 2015; Judd et al., submitted), and some species of the Conostegia clade (Kriebel 2016a) or “Leandra” (Martin et al. 2008a), all representing independent acquisitions of the condition (see also Michelangeli et al. 2004, for other axillary clades). The terminal inflorescence is usually quite obvious (see Fig. 1c), but, in some groups, the growth is sympodial, with the terminal inflorescence quickly deflexed to a seemingly lateral position, e.g., Miconia crenata of the Miconia octona clade (Fig. 1d), Miconia strigillosa of the phenetically similar M. strigillosa clade, and the Octopleura clade of Miconia, (Judd 1986a; Judd et al. 2018a; Gamba and Almeda 2014). Axillary inflorescences also occur in a few species of Medinilla (Regalado 1990, 1995). The flowers may be pedicellate or sessile. The ultimate inflorescence branches, i.e., the pseudo-pedicels, may also be elongated (with the flowers therefore clearly separated from each other) or quite short (with the flowers glomerulate, especially if the pedicels are also short), and such variation is often taxonomically useful, especially at the level of species or species groups (see the cited taxonomic revisions). Flowers are associated with two opposite bracteoles, which may be

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small-to-­enlarged, and persistent to caducous. Blakea (Fig. 2a) is diagnosed by the flowers associated with usually two pairs of enlarged bracts (Penneys and Judd 2011, 2013). The bracts associated with the basal inflorescence branches sometimes intergrade with leaves (Weberling 1988) and may even be brightly colored (some Medinilla).

 lower Structure (Including Symmetry, Floral Rewards, F Sexual Condition, and Merosity) Flowers are the source of numerous systematically significant characters in the Melastomataceae (see, for example, Almeda 1978; Skean Jr 1993; Michelangeli 2005; Judd 2007; Gamba and Almeda 2014; Kriebel et al. 2015; Reginato 2016; Reginato and Michelangeli 2016a, b; Kriebel 2016a; Bochorny et al. 2019; Alvear and Almeda 2019, along with the floras and other revisions cited herein). Flowers are morphologically intricate and developmentally complex, and an elaborate array of descriptive terminology exists, in order to allow clear communication and full taxonomic use of their variable features. We recommend the floral terminology outlined in Weberling (1989) along with the simplifying terms presented in Judd et al. (2016). Flowers of the Melastomataceae are usually bilaterally symmetrical (zygomorphic) as a result of the bilateral arrangement of the stamens, i.e., with all or some shifted to one side of the flower (Figs. 1l–n and 2b–d, j, m, n), but flowers of the Olisbeoideae and Kibessioideae are usually radially symmetrical (actinomorphic; Figs. 2e and 3b). Within the Melastomatoideae, reversals to the actinomorphic condition have evolved several times (e.g., for patterns in the Miconieae, see Gavrutenko et al. 2020; also Fig. 2a). Most Melastomataceae lack nectar glands (and this absence is likely synapomorphic for the familial clade), and, therefore, in the Melastomatoideae and Kibessioideae, plants usually reward pollinators using pollen. Buzz pollination is frequent (Renner 1983, 1986b–87, 1989b; Larsen and Barrett 1999; Brito et  al. 2016; see also Dellinger et  al., chapter “Pollination in Melastomataceae: A Family-Wide Update on the Little We Know and the Much That Remains to Be Discovered”), and the stamens typically show features of this bee pollination syndrome, i.e., anthers opening by pores, the presence of various kinds of staminal appendages, and usually contrasting with the petals in color (often being intensely yellow or yellow-orange, although a wide variety of colors occur; see below; see Figs. 1l–n, 2b–d, j, m, n and 3a). However, most of the Olisbeoideae have an oil-producing gland on the anther connective (Morley 1953; Venkatesh 1955; Buchmann and Buchmann 1981; Buchmann 1987; Renner 1989b; Oliveira 2016; Fig. 2e), although Renner (1993) considered this to be a mainly terpenoid-­ producing gland. These oil glands are likely synapomorphic for the Olisbeoideae but have been lost in multiple lineages (Stone and Andreasen 2010; Stone 2014). Unusual nectaries, sometimes involving nectary stomata, have evolved in relatively

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few taxa of the Melastomatoideae (e.g., at least some species of Blakea, Brachyotum, Chaetogastra, Chalybea, Medinilla, and Miconia), which attract an array of pollinators (hummingbirds, bats, other mammals) (Renner 1983, 1989b; Varassin et  al. 2008; Dellinger et al. 2019; Dellinger et al., chapter “Pollination in Melastomataceae: A Family-Wide Update on the Little We Know and the Much That Remains to Be Discovered”). They may occur on the stamens (either near or on the connective, on connective appendages, at the filament joint, or near the point of filament’s attachment to the hypanthium), the petals, or ovary apex (Stein and Tobe 1989; Renner 1989b, 1993; Judd 2007; Varassin et al. 2008). The color of the petals and/or stamens may change as the flower ages (Renner 1989b; Pereira et al. 2011; Brito et al. 2015; personal observations). Flowers are usually scentless and only rarely aromatic (e.g., rose- or lemon-scented in numerous Blakea, with a vomit-like odor in a few species of Miconia; Wester et al. 2016). Flowers are usually perfect (bisexual), but unisexual flowers (and dioecy) have evolved in a few taxa (e.g., some species of Miconia sect. Cremanium; Almeda and Dorr 2006; Burke and Michelangeli 2013, 2018; de Santiago Gómez and Michelangeli 2016). Some Astronia species in the Philippines are androdioecious (Mancera 2017). In Lijndenia (Olisbeoideae), the flowers are perfect in some species but are androdioecious in Lijndenia laurina (Bremer 1982; Stone 2017). Numerous flowers of an inflorescence may be simultaneously at anthesis, as in Miconia laevigata, Miconia prasina, M. serrulata, or Miconia minutiflora, whereas others, e.g., species of M. sect. Chaenopleura, have only a few flowers open at any one time (see also Goldenberg et al. 2008; Brito et al. 2016). Flowers are quite variable in merosity, i.e., 3- to 10-merous, but 4-, 5-, or 6-­merous flowers are the most common conditions. Five-merous flowers are likely ancestral, both in the Myrtales and in Melastomataceae (Stone 2004). Floral merosity is assessed by the number of sepals and petals, and the stamens are typically twice the number of petals (diplostemonous; Figs. 1m, 2b, d, j, and 3b), although secondary increases occur (Fig. 2g; Wanntorp et al. 2011; Kriebel et al. 2015; Kriebel 2016a; Michelangeli and Goldenberg 2021). Haplostemony (stamens equaling the number of petals) is uncommon but has evolved independently in several tribes of the Melastomatoideae (Cyphostyleae, Dissochaeteae, Lavoisiereae, Lithobieae, Marcetieae, Melastomateae, Miconieae, Pyramieae, Pyxidantheae, and Sonerileae; Fidanza 2009; Almeda et al. 2016; Alvear and Almeda 2019) by the suppression of one of the staminal whorls (see below). The number of carpels frequently does not match the petal number and may vary even within a single species (see cited revisions). Although quite homoplasious, merosity is frequently of systematic significance at a lower taxonomic scale, e.g., 4-merous flowers with four-­loculate gynoecia are a likely synapomorphy of Miconia sect. Sagraeoides and the Miconia ulmarioides complex (Tiernan and Michelangeli 2018; Skean Jr et al. 2018). Floral merosity is also useful in sorting out relationships within the Pyramieae (= Cambessedesieae) (Bochorny et al. 2019). The 4-merous state shared by Pternandra, the Paleotropical Olisbeoideae, and the Neotropical Votomita appears to be a synapomorphy for the putative Olisbeoideae + Pternandra clade, with the predominant 5-merous condition seen in Mouriri interpreted as a reversal (Stone 2004).

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Hypanthium As is typical for members of the Myrtales, flowers of the Melastomataceae have a hypanthium. The hypanthium may be entirely free from the gynoecium, in which case the ovary is positioned completely superior (and the perianth and androecium are thus perigynous). On the other hand, the hypanthium may be completely adnate to the gynoecium, forming a completely inferior ovary (and the floral parts are thus epigynous). Partial adnation is common, and, frequently, the extent of adnation (and the amount of the ovary that is inferior) changes as the flower develops into a fruit. Thus, the ovary position, as is typical in clades that contain hypanthia (see Soltis and Hufford 2002; Soltis et  al. 2003), is variable and extremely homoplasious within the Melastomataceae, as a result of variable development of floral intercalary meristematic activity (Basso-Alves et al. 2017b). In the Dissochaeteae, the ovary is connected to the hypanthium by radial partitions, forming extraovarian chambers, in which the anthers are inserted into the bud; thus, the question of ovary position becomes ambiguous. Extraovarian chambers are also recorded for Chaetogastra clinopodifolia (Basso-Alves et al. 2017b), in many species of Phyllagathis (Cellinese 2002), and in some species of Pleroma. The hypanthial shape is variable within the Melastomataceae, ranging from campanulate or spreading conic to globose, cylindrical, quadrangular, trigonous, or urceolate, and the shape may change as development of the fruit occurs. It may be constricted above the ovary or fruit, as in Rhexia, in those species of Miconia traditionally treated as Tetrazygia, or in some Melastomateae and Pyramieae; however, this feature, as with hypanthial shape, is extremely homoplasious (Goldenberg et al. 2008; Michelangeli et al. 2008; Judd et al. 2014b; Bochorny et al. 2019). Although homoplasious, the hypanthium/calyx shape was stressed by Cogniaux (1891) in his infrageneric classification of Miconia. The hypanthium/calyx shape has been shown to be phylogenetically informative in the Pyramieae (Bochorny et  al. 2019). The inner surface of the hypanthium may be smooth or variously ridged, but this variation also shows homoplasy (Judd 2007). Finally, some hypanthia are strengthened with longitudinal ribs of lignified cells (Fig. 2f), i.e., the core clade within Miconia, as in M. laevigata and M. prasina, and the Octopleura clade, as in Miconia biolleyana and Miconia rubescens (a likely synapomorphy). External wings may be present on the outer hypanthial surface, e.g., in Miconia alatiflora (Whiffin 1971) or in Miconia inusitata and Miconia valenzuelana (of the Miconia florbella group; Michelangeli and Goldenberg 2021) and in Miconia mcvaughii and Miconia bailloniana (Wurdack 1968). Hypanthium wings are also found in Schwackaea and Pterogastra of the Melastomateae (Renner 1994; Kriebel 2016b). Pternandra (Kibessioideae) has hypanthia that are tessellate-to-echinate (Maxwell 1981). A specialized fringe of hairs on the hypanthial torus (i.e., a fringe of hairs along the hypanthial rim, visible adaxially) may be present or absent and sometimes is taxonomically useful (e.g., within the Leandra clade of Miconia, Reginato 2016). The elongated and fleshy torus hairs of M. sect. Sagraeoides are synapomorphic for the group (Skean Jr 1993). The indumentum of the outer surface of the hypanthium

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is frequently of taxonomic value (and may differ from that of the abaxial leaf surface); the hypanthial surface of Pterolepis and Heterotis (Melastomateae) possess vascularized projections, and similar structures are also found in some Melastoma and Osbeckia.

Calyx The sepals may be distinct, but, usually, they are connate to some extent, forming a tube with calyx lobes. Complete connation has evolved multiple times, leading to a calyptrate structure enclosing the flower bud (Fig. 2g). Such thick-to-­membranaceous, variously shaped calyx caps may open in various ways at anthesis, e.g., a circumscissile slit (as in the species of Miconia formerly included within Conostegia), by irregular rupturing (as in most species of Miconia sect. Sagraeoides, Miconia sect. Laceraria, Chalybea calyptrata, and in Kirkbridea) (Wurdack 1976; Skean Jr 1993; Morales-Puentes and Penneys 2010; Kriebel 2016a; see also Michelangeli and Goldenberg 2021). Calyptras occur in all subfamilies (Merianieae, Miconieae, Olisbeoideae, Kibessioideae, Astronieae, Henrietteeae, Pyxidantheae, Cyphostyleae, Sonerileae, and Dissochaeteae; Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) and have even evolved multiple times within a tribal clade, as in the Miconieae, where they occur in M. sect. Laceraria, scattered species of the Caribbean clade (Judd et al. 2014a, b; Bécquer et al. 2018; Judd and Majure 2019), M. sect. Sagraeoides (Skean Jr 1993; Skean Jr et al. 2018), and in M. florbella and relatives (Michelangeli and Goldenberg 2021), and also have evolved multiple times within the Conostegia complex (Kriebel et al. 2015; Kriebel 2016a). Furthermore, similar calyptrate calyces have evolved in the related tribe, Merianieae, e.g., Graffenrieda (Goldenberg and Meirelles 2011), as well as in the phenetically similar Henrietteeae, i.e., Kirkbridea and some Bellucia (Wurdack 1976; Renner 1989a). The calyx lobes are usually valvate in the bud but occasionally are open (see, for example, Miconia sect. Miconiastrum; Judd et  al. 2014b). Imbricate aestivation also occurs (e.g., in the Olisbeoideae). The calyx lobes vary greatly in size and are sometimes even reduced to a mere rim terminating the hypanthium. Calyx lobes are usually persistent, but deciduous lobes have evolved repeatedly, e.g., among the Melastomatoideae, Amphorocalyx, Brasilianthus, Dionycha, Pleroma, some species of Miconia, and Monochaetum, and in several species of Dissotis, and allied genera (see also Veranso-Libalah et al. 2020), as well as in the Olisbeoideae in Mouriri. Examples of taxonomically useful calyx characters are included in nearly all of the cited taxonomic revisions and floras. One of the distinctive characters of many Melastomatoideae is the presence of calyx teeth, i.e., variously elongated, flattened-to-terete structures arising from the dorsal surface of the hypanthium (Fig. 2h, i, k; see references cited by Basso-­Alves et al. 2017a). They arise by division from the sepal primordia and thus should be considered to be part of the calyx (Basso-Alves et al. 2017a). We recommend that

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the term “calyx teeth” be used for these structures, which sometimes have been called external calyx lobes or external teeth. They are frequently systematically useful, e.g., the calyx teeth are flattened parallel to the floral radii in Miconia sect. Calycopteris (Judd et al. 2014a; Bécquer et al. 2018; Fig. 2i), they are elongated and terete in Miconia octona and relatives as well as in M. strigillosa and relatives (Judd et al. 2018a), and they are common in the Caribbean clade (Judd and Ionta 2013; Majure et  al. 2016). Elongated calyx teeth are present in most species that once were included within the traditional (and highly polyphyletic) genera Clidemia or Leandra. However, they have been lost many times within the subfamily (e.g., Kriebel et  al. 2015), especially among the members of the pedoconnective clade (see phylogenetic discussion below and Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”).

Corolla The petals are usually distinct and are right-contorted in the bud (the latter is likely a familial synapomorphy; Stevens 2001 onward; Figs. 1l and 2h). They are quite variable in shape and size, ranging from minute to large and showy and from narrowly triangular to broadly ovate, elliptical, or obovate; they may be symmetrical or slightly to strongly asymmetrical (Figs. 1l–n and 2a, b, d, g, h, j, k, m, n). The petals may be broadly attached or basally constricted (even clawed, and then often sagittate, hastate, or auriculate basally). The apex varies from emarginate or rounded to acute or acuminate, and often an apical notch is present (interlocking the petals in the bud). The margin is usually entire or undulate but may also be irregularly lobed or ciliate. The petals may be white, cream, or greenish to brightly colored (yellow, orange, pink, red, purple, or blue) and often contrast in color with the stamens (Figs.  1 and 2). Occasionally, the petals are bicolored as in many species of Cambessedesia (Fig. 2j). Petals vary greatly in the indumentum, ranging from glabrous to densely pubescent. In some otherwise glabrous petals, a single (to few), multicellular, dorsal, apical-to-subapical hair(s) occur(s). The petals may be reflexed (Fig. 2d), held horizontally (Fig. 2b, c, g, m, n), or erect (Fig. 2l). In some groups, the petals are erect and tightly overlapping, exhibiting an appearance of being sympetalous, e.g., in the Charianthus clade of Miconia (Penneys and Judd 2005; Fig. 2l), the goblet clade of Miconia (Almeda 2003), or Miconia foveolata of M. sect. Chaenopleura (Judd 2007), and Miconia melanotricha. This arrangement has been associated with shifts to vertebrate pollination and also occurs in Beccarianthus, some Blakea, Brachyotum, some Chaetogastra, Chalybea, some Medinilla, and some Meriania (Wurdack 1953; Varassin et al. 2008; Almeda 2009; Penneys and Judd 2013). The petals usually fall soon after anthesis, but, in M. sect. Miconiastrum (Judd et al. 2014b), in several species of the Conostegia clade of Miconia, and in the M. floribunda complex, they persist long after the stamens have abscised. Persistent petals also occur in some Axinaea, Bertolonia, Meriania, and Pleroma. Petal

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characters are highly homoplasious (Majure et al. 2013; Gavrutenko et al. 2020), and often even closely related species have highly different petal forms (e.g., Skean Jr 1993; Gamba and Almeda 2014; Kriebel 2016a; Bochorny et al. 2019). Even in groups where petal characters traditionally were considered to be of generic value (e.g., within the Miconieae, in diagnosing Leandra or Ossaea from Clidemia or Miconia, using the acute vs. rounded petal apices), they result in polyphyletic assemblages (Skean Jr 1993; Goldenberg et  al. 2008; Michelangeli et  al. 2008). Some petal characters, however, are phylogenetically important, e.g., the Pachyanthus clade (sensu Bécquer 2012) is, in part, diagnosed by its asymmetrical and clawed petals, Cambessedesia by its bicolored petals (i.e., orange/red and yellow, see Fig.  2j; Bochorny et  al. 2019), or Huberia and Merianthera, with their usually asymmetrically thickened petals (Goldenberg et  al. 2012), diagnosis of blue- vs. white-petaled subclades within Memecylon (Olisbeoideae; Amarasinghe et al. 2021), and variation among the genera of the Melastomateae (Guimarães et al. 2019; Meyer et al. 2021). Notably, fleshy petals occur in some members of Axinaea, Beccarianthus, Bellucia, Blakea, Chalybea, Henriettea, and Meriania.

 ndroecium (See also Melo et al., Chapter “Stamen Diversity A in Melastomataceae: Morphology, Color and Function”) Staminal characters are exceptionally variable in the Melastomataceae and have traditionally been used for classification at various taxonomic levels (Naudin 1849–53; Triana 1871; Cogniaux 1891; Wilson 1950; Goldenberg et al. 2008; see also the numerous citations of floras and taxonomic revisions). Stamens are typically twice the number of petals and are arranged in two whorls (diplostemonous; Figs.  1l, m and 2c, d, m, n). The two whorls may be morphologically similar or divergent (i.e., heterantherous, and, in the latter case, may show differentiation of function; see Velloso et al. 2018; Telles et al. 2020). The extent of divergence in shape between the staminal whorls is highly homoplasious in the Melastomataceae as a whole (Veranso-Libalah et al. 2017, 2020; Melo et al. 2021) but may be informative at lower scales (e.g., within the Pyramieae; see Bochorny et al. 2019). One whorl is sometimes reduced to staminodia, as in Microlicia confertifolia (Martins and Almeda 2017; Versiane et al. 2021), some Monochaetum (Alvear and Almeda 2019), Noterophila (Rocha et al. 2018), Rhynchanthera (Renner 1990), Siphanthera (Almeda and Robinson 2011), and Poteranthera (Almeda and Pacifico 2018). The presence of a single staminal whorl (haplostemony) may be synapomorphic for the Cyphostyleae (Michelangeli et al. 2011); however, a single staminal whorl occurs scattered across the family, as in some Blakea, some Creochiton, some Dissochaeta, some Miconia (e.g., Miconia tetrandra), Monochaetum brachyurum, Pterolepis haplostemona, and most Sonerila (see also Kartonegoro et al. 2018). The stamens are almost always inflexed in the bud (as in most other Myrtales), and the filaments are often geniculate. However, erect anthers in the bud are known from Votomita

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and some Mouriri of the Olisbeoideae (Morley 1976) and some Merianieae (i.e., Adelobotrys, Axinaea, Graffenrieda, and Meriania; Mendoza-Cifuentes 2021). Filaments may be glabrous or variously pubescent. Anther shape was shown by Reginato and Michelangeli (2016a, b) to be correlated with phylogenetic pattern within Leandra s.s. (now the Leandra clade within Miconia). Extensive intraclade variation in staminal morphology was shown by Skean Jr. (1993; in M. sect. Sagraeoides), Kriebel (2016a; in the Conostegia clade of Miconia), Renner (1989a; in the Bellucia + Loreya clade), Penneys and Judd (2011, 2013, in Blakea), Rocha et  al. (2018; within the Marcetieae), and Bochorny et  al. (2019; within the Pyramieae); many other examples could be cited. The often rostrate anthers are usually tetrasporangiate and dithecous, but they are occasionally unithecal (Rhexia, Fig. 1m, due to the breakdown of the walls separating all four microsporangia at maturity; Eyde and Teeri 1967). However, the thecae become secondarily divided (and thus polysporangiate) in a few taxa (e.g., a few species of Meriania and Miconia and several species of Microlicia; Baumgratz et al. 1996; Lima et al. 2019; Caetano et al. 2020; Versiane et al. 2021). Bisporangiate anthers have been reported for Miconia latecrenata (Cortez et al. 2015). The anthers are extremely variable in size and shape (Figs.  1l–m, 2a–f, j, m, n, and 3a, b; Cogniaux 1891; Renner 1989a, 1993; Goldenberg et al. 2008; Penneys et al. 2010; Penneys and Judd 2011, 2013). They are straight to adaxially or abaxially curved and usually open by a single, terminal pore, which may be dorsally to ventrally inclined, much smaller than the width of the anther, or as large as the anther width, and frequently gaping and/or with an emergent septum. However, many open by two pores or even rarely by four pores (a few Miconia, e.g., M. tetrandra, some species of sect. Cremanium). The endothecium is usually poorly developed and more-­ or-­less nonfibrous in those groups with poricidal dehiscence, whereas the basal clades, the Kibessioideae and Olisbeoideae, have a well-developed and fibrous endothecium and open by short-to-elongated longitudinal slits (but these appear nearly porose in a few species of Mouriri; Morley 1976). The irregular shrinkage of the endothecium cells (occurring as the anther matures) leads to a rupture in the anther wall (Renner 1993). The Melastomatoideae are supported as monophyletic by the putative synapomorphy of a reduced endothecium and poricidal anther dehiscence. In this clade, anther dehiscence occurs as a result of dehydration in the pore regions, which lack a cuticle (Ziegler 1925; Eyde and Teeri 1967; Renner 1993; Cortez et  al. 2014). Interestingly, parallel evolutionary reversals to anther dehiscence by slits have occurred within the Melastomatoideae, i.e., either with two slits (as in Miconia sect. Chaenanthera, Goldenberg et al. 2003; Astronieae, Old World genera (Penneys 2013); Charianthus clade, see Fig. 2l; Penneys and Judd 2005) or four slits (as in Miconia sect. Chaenopleura, the Caribbean species, see Fig.  3b; Goldenberg et al. 2003; Judd 2007). The occurrence of anther slits in these groups likely correlates with shifts away from buzz pollination. To make matters more confusing, within sect. Chaenopleura, a secondary reversal from slits, back to a gaping terminal pore, has occasionally occurred (e.g., Miconia desportesii, Miconia sphagnicola, see Judd and Penneys 2004; Majure, unpublished analyses). Recent phylogenetic analyses have shown that anther pore number and shape, although

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emphasized by traditional systematists working on the Melastomataceae (e.g., Cogniaux 1891), and especially used in infrageneric classifications of Miconia, are extremely homoplasious (Goldenberg et al. 2008; Michelangeli et al. 2008; Penneys and Judd 2011, 2013). The traditional sections of Miconia are thus non-­monophyletic (Goldenberg et al. 2008). Additionally, the pore number varies infragenerically in Bellucia (Renner 1989a) and Blakea (Almeda 1990; Penneys and Judd 2011, 2013). The anthers may be the same color as the corolla (Fig. 3b), or slightly to strongly contrasting (Figs. 1l–n, 2a–d, g, m, n, and 3a), and they may be yellow-to-orange, white-to-red, blue, or purple. Anther color, although often variable within closely related species (e.g., the Leandra clade of Miconia, Reginato and Michelangeli 2016a, b), is of taxonomic value in some groups, e.g., anthers the same color as the corolla characterize the Antillean species of Miconia sect. Chaenopleura as well as most species of sect. Cremanium (Judd 2007) or the evolution of blue anthers in a subclade of Blakea (Penneys and Judd 2011, 2013). Finally, anther wall development may be either of the monocotyledonous or dicotyledonous type (Cortez et al. 2015). The variously thickened anther connective, sometimes considered a familial synapomorphy (Judd et  al. 2016), is more likely a synapomorphy uniting the Melastomataceae with the Crypteroniaceae + Alzateaceae + Penaeaceaae clade (Clausing and Renner 2001; Stevens 2001 and onward). The connective usually supports the presence of a branched staminal vascular bundle (Wilson 1950; Morley 1953; Stevens 2001 and onward; Judd et  al. 2016), an unusual condition that is probably synapomorphic for the Melastomataceae. The thickened connective is extremely variable in shape, and additional appendages of various shapes are often present. The variously shaped connectives and the appendages are likely functional in pollination biology (Bochorny et al. 2021). Variously developed dorsal appendages arise from the expanded connective in, e.g., Adelobotrys, Graffenrieda, Meriania, and relatives (Triana 1871; Wurdack 1973, 1980; Judd and Skean Jr 1987; Michelangeli et al. 2015). Axinaea and some Meriania have bulbous dorsal anther connective appendages modified into food bodies consumed by passerine birds (Dellinger et al. 2014). Merianthera and many Meriania and Adelobotrys have a double dorsal appendage (Goldenberg et al. 2012; Mendoza-Cifuentes 2010), yet, some, e.g., most species of Miconia, lack such appendages or have only a small dorsal bump (e.g., the Tococa clade; Michelangeli 2005). The Octopleura clade, within Miconia, has a prominent dorso-basal appendage (Gamba and Almeda 2014). In such anthers, the connective is not elongated. Other taxa, however, have a basal ventrally, more-or-less prolonged connective (i.e., a pedoconnective, Figs.  2m, n and 3a; see Jacques-Félix 1953, 1981), and, the appendages, if present, arise at the base of the pedoconnective, where they join the filament (Figs. 2m, n and 3a). The presence of pedoconnectives may be synapomorphic for a large clade within the Melastomatoideae (including the Dissochaeteae, Lavoisiereae, Marcetieae, Melastomateae, Pyramieae, Rhexieae, Sonerileae, Trioleneae, etc.), although frequent reversals (i.e., extreme shortening or loss of pedoconnectives) occur within this clade. Appendage forms, whether arising dorsally from the anther connective, or ventral-basally from the pedoconnectives, are of taxonomic significance (see

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Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology,” and the many taxonomic revisions cited herein). There are a few genera, however, with both dorsal and ventral appendages, e.g., Medinilla, Opisthocentra, and Pachyloma. Finally, the connective may be glabrous or possess multicellular hairs. The presence or absence of hairs on the filament may also be taxonomically useful, e.g., in the Melastomateae. Pollen grains are small, tricolporate, radially symmetrical, and isopolar, usually with poorly to well-developed pseudocolpi alternating with the true colpi (Patel et al. 1984; Renner 1989a; Skean Jr 1993). In Miconia stephanotricha and M. tococa, the colpi are short and the pseudocolpi are absent (Patel et al. 1984). The surface texture is smooth and striate or rugulate or rugulate-verrucate. Polyads are present in Miconia spadiciflora (Patel et al. 1984). The mature pollen contains two cells (Tobe and Raven 1984). Pollen morphology is fairly uniform and has not been shown to be taxonomically useful within the family.

Gynoecium The gynoecium is syncarpous, with 2–6 (rarely to 25) carpels. Usually, there are as many locules as carpels, and the placentation is then axile, or less commonly basal-­ axile or basal, as in the Olisbeoideae (Morley 1953), and in some Melastomatoideae, e.g., a few species of Miconia in the West Indies (Majure et  al. 2013; Judd & Bécquer, unpublished data). However, the ovary may also be unilocular (as in many Olisbeoideae) with either a parietal placentation (e.g., the Kibessioideae, a few Olisbeoideae, only certain species of Mouriri) or free central (e.g., some Olisbeoideae). The placenta is often expanded, extending into each locule, and may be unlobed or once-to-twice divided. The number of ovules per placenta is either usually numerous (Kibessioideae, Melastomatoideae) or few to several (rarely numerous; Olisbeoideae). These features are of some taxonomic value. Placentation was used by Morley (1953) in his infrageneric classification of Mouriri (Olisbeoideae). Locule number is sometimes useful, e.g., in the Marcetieae (Rocha et al. 2016, 2018), the Lavoisiereae (Versiane et al. 2021, Pacífico & Almeda, chapter “Lavoisiereae, a Neotropical Tribe with Remarkable Endemism on Eastern Brazilian Mountaintops”), and in Miconia sect. Chaenopleura (Judd 2007). The locules are usually without mucilage but are mucilage-filled in many species of the Conostegia clade of Miconia (Kriebel et al. 2015). The ovules are generally anatropous and crassinucellate and have two integuments (with both contributing to the micropyle, i.e., the zigzag condition; Tobe and Raven 1983). Only in a few Olisbeoideae are the ovules campylotropous (Morley 1953, 1976). The outer integument varies from two-layered (the likely ancestral condition) to multilayered and may be taxonomically useful in the Olisbeoideae and Melastomatoideae (Caetano et al. 2018). The megagametophyte is monosporic and is eight-celled (with development of the Polygonum type) but only five-celled at maturity due to the early breakdown of the antipodals (Tobe and Raven 1983;

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Renner 1993). The endosperm development is nuclear, but it is absent at seed maturity. Embryo development is usually of the onagrad type (Tobe and Raven 1983), although asexual (apomictic) embryos develop in several different ways (Caetano & Oliveira, chapter “Apomixis in Melastomataceae”). The ovary varies from superior to completely inferior, as a result of the extent of adnation with the hypanthium. The ovary shape is also variable, and, occasionally, the locules are positioned in the basal part of the free hypanthium (see Mouriri; Morley 1953, Fig. 42) or at least extended into the free hypanthium (see Miconia pseudopedicellata and Miconia blancheana of the Caribbean clade; Judd in prep.). The apex of the ovary may form a hemispheric-to-conic projection or it may be flat to apically concave. Although highly homoplasious, ovary position is sometimes phylogenetically informative, e.g., within the Pyramieae (Bochorny et al. 2019). The style is single, terminal, and may or may not be surrounded by a flange of tissue extending from the ovary apex, i.e., the collar, which may be short-to-­ elongated and lobed or unlobed. The ovary apex (or the collar) may also be provided with elongated, multicellular, glandular, or eglandular hairs or scales, which may form a crown. Ovary crowns are phylogenetically widespread and homoplasious within the Melastomataceae. A crown should not be confused with the mere presence of scattered hairs, of various types, on the ovary apex. The presence or absence of an ovary crown is occasionally useful, e.g., for distinguishing the Melastomateae from the Lavoisiereae, Marcetieae, and Rhexieae (see Michelangeli et al. 2013), or at finer scales, such as distinguishing Miconia pratensis and the related Miconia hirsuta, which lack ovary crowns, from most other species of Miconia sect. Echinatae, which have them (Judd et al., submitted). The style may be short-to-elongated, stout-to-slender, and straight-to-distally curved (Figs. 1n, 2c, e and 3b). The terminal stigma is truncate, punctate-to-variably capitate, or even expanded and in funnel form; it is usually unlobed but is occasionally distinctly lobed (e.g., see variation within the Conostegia clade of Miconia, which is especially impressive; Kriebel 2016a; see also Bellucia vs. Henriettea; Renner 1989a; Penneys et al. 2010). The style may be glabrous or variably pubescent (and its hairs either glandular or eglandular). The stigma is often spatially separated from the stamens (herkogamous) (Fig.  2b, c). Such characters are often taxonomically significant (e.g., Gamba and Almeda (2014), Kriebel et al. (2015), Kriebel (2016a), Reginato and Michelangeli (2016a, b), and the “Flora do Brasil” (http://reflora.jbrj.gov.br/rreflora/floradobrasil/FB161)).

Fruits Loculicidal capsules (Fig. 3c, d) and berries (Figs. 1c, k, 2f, and 3e) predominate in the Melastomataceae, although the fruits of Rupestrea are dry and indehiscent (Goldenberg et al. 2015), i.e., an indehiscent pod, in the terminology of Judd et al. (2016). A fruit form is often taxonomically informative (Baumgratz 1985; Clausing et al. 2000). Examples include the bertolonidium-type capsule of the Bertolonieae

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(Pizo and Morellato 2002; Bacci et  al. 2019), the extremely similar obconic and angled capsules of the Trioleneae (Bacci et al. 2019), and the urceolate capsules of Rhexia (Kral and Bostick 1969). Capsule morphology is also taxonomically significant among Schwackaea and relatives (Kriebel 2016b). Loculicidal capsules are likely ancestral in the Melastomataceae (given the outgroup families; see Clausing et al. 2000 and Reginato et al. 2020), but homoplasy and intermediate conditions, e.g., fleshy capsules or dry capsules with fleshy placentas (Fig.  3f; Meyer 2001; Michelangeli et al. 2011), make the pattern of variation difficult to interpret. Berries have evolved several times (Clausing et al. 2000; Reginato et al. 2020). The most distinctive are the berries of the Olisbeoideae (Fig. 3e) that are often unilocular and contain a single, large seed, though some species have several locules and are few-­ seeded (Morley 1976). Berries with small seeds (or fleshy capsules) characterize the Kibessioideae. The differences in fruit development between these two subfamilies perhaps suggest that their berries evolved in parallel. Berries also evolved independently in several clades within the Melastomatoideae (Reginato et al. 2020; Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Berries are a putative synapomorphy for the species of the Henrietteeae (Fig. 1k), distinguishing them from the related Astronieae, which have capsules. Berries also evolved in (and are a synapomorphy of) the species-­rich Miconieae (Figs.  1c and 2f), whereas the related Eriocnemeae and Merianieae are capsular (Fig. 3c). Again, berries are a likely synapomorphy of the Pyxidantheae. The berries of the Henrietteeae, Miconieae, and Pyxidantheae (with some exceptions in each group) have numerous, tiny seeds. Within the large pedoconnective clade (and related tribes), berries have also evolved, e.g., in the Sonerileae (Medinilla and relatives), Dissochaeteae (Dissochaeta and relatives), Dinophoreae (Dinophora), and Melastomateae (some Melastoma have berries, but most have rupturing capsules and fleshy placentas, Tristemma) (Clausing et  al. 2000; Kartonegoro et  al. 2018; Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Aciotis (Marcetieae) has fruits that are either capsular or fleshy and indehiscent (FreireFierro 2002). The shift from capsular to berry fruits is also seen in other families of the Myrtales, e.g., the Lythraceae, Onagraceae, and Myrtaceae (Judd et al. 2016). Capsular fruits are usually tan-to-brown at maturity, whereas berry fruits are variously colored (blue-black, purple, light blue, iridescent or intense blue, red, orange, yellow, white, or green). The berries are variable in size and shape (but mainly globose-to-ovoid), often expand to a greenish or reddish color and submature size, and then rapidly plump and change color at full maturity. Thus, determination of mature fruit size is difficult. The berries range from rather insipid to quite flavorful. The size, shape, and color of berries are occasionally taxonomically useful, e.g., Miconia sphagnicola, with bright red berries, is easily distinguished from the related M. desportesii and Miconia monciona that have blue-black fruits (Judd and Penneys 2004); fruit color is putatively synapomorphic for Antillean M. sect. Chaenopleura (Judd 2007; pale blue; Fig. 1c), a large subclade within the Brevicyma clade of M. sect. Sagraea (Ionta et al. 2012; Judd et al. 2018b; iridescent, sky blue; Fig.  1e), and pale blue to white fruits characterize the Pleiochiton clade within Miconia (Reginato et al. 2010, 2013). Many species of the M. discolor clade have

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orange fruits. Miconia laevigata and Miconia pyramidalis are close relatives but are consistently differentiated by fruit size (Judd and Kabat 2005), and the Caribbean species of M. sect. Chaenopleura have large fruits, contrasting with the smaller fruit characters of the related species in sect. Cremanium (Judd 2007). Dispersal of seeds of capsular species is mainly by wind or raindrops (Renner 1989b; Pizo and Morellato 2002; Bacci et al. 2019). River dispersal is suspected in some, e.g., Dichaetanthera africana, which has seeds provided with a row of elongated, inflated appendages. Seeds of berry-fruited species are dispersed biotically (mainly by birds but also by mammals, turtles, lizards, and fish; some are secondarily ant-dispersed) (see Renner 1989b; Messeder et al. 2020; Messeder et al., chapter “Seed Dispersal Ecology in Neotropical Melastomataceae”).

Seeds The number of seeds per fruit varies from one to numerous, and the seeds may be large (in the Olisbeoideae) to small or minute (in the Kibessioideae, Melastomatoideae). The testa of seeds in the Melastomatoideae is palisade-to-­ cuboidal and lignified (Stevens 2001 onward). A differentiated raphal region and hilar operculum are present in the Melastomatoideae but are lacking in the Olisbeoideae (Renner 1993; Stevens 2001 onward). They are quite variable in shape and surface texture of the testa, as discussed and illustrated in Ocampo et al. (chapter “A New Perspective on Seed Morphological Features in Melastomataceae”; see also Whiffin and Tomb 1972; Baumgratz 1985; Groenendijk et  al. 1996; Martin et al. 2008b; Martin and Michelangeli 2009; Ocampo and Almeda 2013; Bécquer et al. 2014; Rocha et al. 2018). An endosperm is lacking, and the small-to-large, straight-to-curved, white or green embryo has two cotyledons, often unequal, which may be folded, wrinkled, or rolled (Olisbeoideae) or merely flat-straight (Kibessioideae, Melastomatoideae); the radicle is often bent. Germination of the embryo is either cryptocotylar (Olisbeoideae) or phanerocotylar (remaining clades). Vivipary has also been reported (Thite et al. 2016; Bacci et al. 2021).

 orphological Characters of Potential Phylogenetic M Importance in Diagnosing Early-Branching Clades The putative morphological synapomorphies of the Melastomataceae include the loss of nectaries on the inner surface of the hypanthium, a right-contorted corolla in the bud, anther connectives with a branched vascular trace, and uninucleate anther tapetal cells (Wilson 1950; Dahlgren and Thorne 1984; Johnson and Briggs 1984; Renner 1993; Stevens 2001 onward; Varassin et al. 2008). Furthermore, acrodromous leaf venation may represent an additional synapomorphy, either if the

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acrodromous leaves of some Olisbeoideae are taken as ancestral (as suggested by Stone 2006) or if the Kibessioideae (Pternandra) are actually sister to the Olisbeoideae instead of the Melastomatoideae. As a member of the Myrtales, the Melastomataceae also have vestured pits, internal phloem, flowers with a hypanthium, stamens incurved in the bud, a single, undivided style, and pollen grains with well-developed poreless furrows, i.e., pseudocolpi (Judd et al. 2016). Moreover, as a member of a clade also containing the Crypteroniaceae, Alzateaceae, and Penaeaceae, they have dorsally expanded anther connectives (Clausing and Renner 2001; Stevens 2001 onward). The Olisbeoideae are morphologically quite divergent, showing the putative synapomorphies of branched and/or elongated sclereids in the stems and leaves, leaves with a thick cuticle, flowers with stamens that prevailingly have an oil-­producing gland on the dorsal anther connective, a gynoecium usually with only one or a few ovules developing, and a berry with usually only one or, more rarely, a few large seeds (see also Renner 1993). The Kibessioideae (only Pternandra) may either be sister to the Olisbeoideae or to the Melastomatoideae (Maurin et al. 2021; Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”; Majure, pers. comm.). Their monophyly is perhaps supported by their superficial cork cambium, tessellate-to-echinate hypanthia, and parietal placentation. Like the Olisbeoideae, they have actinomorphic androecia, ovary locules opposite the petals, and wood with an intraxylary phloem (perhaps synapomorphic similarities; see van Vliet and Baas 1984). The remaining species of the Melastomataceae comprise the extremely large subclade, treated here as the Melastomatoideae (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”), which is supported by the following putative synapomorphies: anthers with a poorly developed and more-or-less nonfibrous endothecium (usually associated with poricidal anther dehiscence), seeds with a hylar operculum, and wood (when present) with libriform fibers (see also Clausing and Renner 2001). Although homoplasious within this clade, the possession of calyx teeth, a zygomorphic androecium, and staminal appendages may be the additional synapomorphic characters of the Melastomatoideae. Anatomical details relating to the seed coat (i.e., exotesta that is palisade-to-cuboid and lignified and radicle in a testal pocket) may also be synapomorphic for this subfamily (Stevens 2001 onward). Within the Melastomatoideae, the Henrietteeae and Astronieae may represent the sister clade to the remaining tribes; both have leaves with abundant styloid or megastyloid crystals, whereas such crystals are lacking in the remaining members of the Melastomatoideae. The berry fruits of the Henrietteeae are likely synapomorphic for that tribe; the group has axillary inflorescences (perhaps a retained ancestral character, as both the Kibessioideae and Olisbeoideae have axillary inflorescences). In contrast, the Astronieae have terminal inflorescences (a possible apomorphy) and capsular fruits (probably plesiomorphic). The remaining tribes of the Melastomatoideae are characterized by the likely synapomorphy of stems with medullary vascular bundles, which are absent from the species of the Henrietteeae, Astronieae, Pternandra, and Olisbeoideae. Within the clade characterized by medullary vascular bundles, the Lithobieae (herbs with tuberous rhizomes) may be

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sister to the rest, which form two large subclades, i.e., the Merianieae + Miconieae + Eriocnemeae clade and the Bertolonieae + Pyxidantheae + a clade with frequent occurrences of stamens with pedoconnectives (see Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). The Merianieae usually have dorsally appendaged stamens, whereas stamen appendages are extremely reduced or absent in Miconieae + Eriocnemeae; the Miconieae are woody and berry-fruited (the latter is an apomorphy), and the Eriocnemeae are usually herbaceous or suffrutescent (an apomorphy) and capsular-­ fruited. The Eriocnemeae + Miconieae clade may be supported by the cryptic synapomorphy of ovules with a multilayered outer integument (Caetano et al. 2018). The Bertolonieae may be diagnosed by the herbaceous habit, scorpioid inflorescence, and bertolonidium capsules, although the first two characters show much homoplasy (Bacci et al. 2019). A majority of the species in the Pyxidantheae have each flower subtended by two pairs of usually enlarged bracts, berry fruits, and axillary inflorescences (Penneys and Judd 2011, 2013). The remaining tribes of the Melastomatoideae include the Stanmarkieae, Trioleneae, Cyphostyleae, Sonerileae, and the large clade in which pedoconnectives are common (but with many exceptions), i.e., the pedoconnective clade (sensu Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). This large clade is comprised of the Dissochaeteae, Pyramieae, Dinophoreae, Rhexieae, Lavoisiereae, Marcetieae, Rupestreae, and Melastomateae. Relationships are still rather poorly understood within this clade (and its putative relatives, such as the Sonerileae, Trioleneae, etc.), with many of the tribes being resurrected or recently recognized, recircumscribed, and/or poorly diagnosed morphologically. The Trioleneae stand apart in their capsule form—spreading and three-angled. Cyphostyleae flowers have only a single staminal whorl. The pedoconnective clade is variable in habit: trees to herbs, with terminal-to-axillary inflorescences; and calyx teeth have been lost in several groups. The Dissochaeteae are difficult to diagnose but have berries and often a liana or scrambling habit. The Lavoisiereae have subcochleate-to-reniform seeds (Fritsch et al. 2004), but cochleate seeds are also found in the Melastomateae (Freire-Fierro 2002) and Rhexieae (Whiffin and Tomb 1972). Rhexia (of the Rhexieae) is quite distinctive, with often strongly urceolate hypanthia, unisporangiate anthers (at maturity), and ovary locules opposite the petals (James 1956; Ionta et al. 2007). The Rhexieae are diagnosed by their cochleate seeds with the testa tuberculate-costate (and with the tuberculae multicellular), and these characters may be synapomorphic (Whiffin and Tomb 1972; Clausing and Renner 2001; Renner and Meyer 2001; Ionta et al. 2007). Within this group of tribes, the Marcetieae may be cryptically diagnosed by their ovules with a multilayered outer integument (Caetano et al. 2018). The Melastomataceae show an extremely high level of homoplasy in their morphological characters (Judd and Skean Jr 1991; Majure et  al. 2013; Gavrutenko et al. 2020), which has made the delimitation of tribes and genera especially difficult. The above-referenced character patterns should, therefore, be taken only as preliminary hypotheses. Explicit phylogenetic assessments of morphological variation, to this point, have been made for only particular subclades of the

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Melastomataceae, e.g., the axillary-flowered Miconieae (Judd 1989), Bellucia (Renner 1989a), Miconia sect. Sagraeoides (Skean Jr 1993; Skean Jr et al. 2018), the Tococa clade of Miconia (Michelangeli 2000, 2005), Adelobotrys (Schulman and Hyvönen 2003), the Lavoisiereae (Fritsch et al. 2004), the Charianthus clade of Miconia (Penneys and Judd 2005), Rhexia (Ionta et  al. 2007; Ionta 2018), the Pyxidantheae (Penneys and Judd 2011, 2013), Siphanthera (Marcetieae; Almeda and Robinson 2011), the Cyphostyleae (Michelangeli et al. 2011), the Sandpaper clade of Miconia (Majure et al. 2015), the Conostegia clade of Miconia (Kriebel et al. 2015; Kriebel 2016a), the Marcetieae (Rocha et al. 2016, 2018), the Leandra clade of Miconia (Reginato 2016), the Astronieae (Penneys 2013; Mancera 2017), the Pyramieae (Bochorny et al. 2019), the Bertolonieae (Bacci et al. 2020), Dissotis and relatives (Veranso-Libalah et al. 2020), the Lavoisiereae (Versiane et al. 2021), and Memecylon (of the Olisbeoideae; Amarasinghe et al. 2021), other than the preliminary, and now outdated, family-wide analysis of Renner (1993), and thus a comprehensive assessment of such variation is needed. Additionally, much more DNA-based phylogenetic work is required to elucidate evolutionary patterns within the family, which hopefully can then be integrated into morphology, leading to an explicit assessment of putative morphological synapomorphies for major clades. Acknowledgments  We thank the numerous collaborators with whom we have worked over the years on the systematics of the Melastomataceae. We also thank P. Amarasinghe, C. Gracie, and J. D. Skean for allowing the use of their photographs. We are grateful for the helpful comments and corrections of two anonymous reviewers. These morphological investigations were supported, in part, by the National Science Foundation grants DEB-SBS-2002270 (at the University of Florida) and DEB-SBS-2001357 (at the New York Botanical Garden).

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Historical Biogeography of the Melastomataceae Marcelo Reginato, Frank Almeda, Fabián A. Michelangeli, Renato Goldenberg, Peter W. Fritsch, R. Douglas Stone, and Darin S. Penneys

Introduction The Melastomataceae include some 5858 species predominantly distributed over tropical biomes across the planet (Ulloa Ulloa et  al., chapter “Melastomataceae: Global Diversity, Distribution, and Endemism”). Although the family shows a disjunct pantropical distribution, most of its major groups have a more restricted distribution. Of the 23 major clades currently recognized in the family, 22 are included in a phylogenetic hypothesis (Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). In all, 14 of these clades are restricted to the Neotropical region (NT) and two to eastern and southeastern Asia (EA). Six clades have disjunct distributions across major realms. The Rhexieae are found both in the Neotropical and Nearctic regions reaching temperate areas, and the others show disjunctions across tropical areas: the Astronieae (EA and NT), Dinophoreae (Africa and EA), and Melastomateae, Olisbeoideae, and Sonerileae across the NT, EA, and Africa + Madagascar regions. The pantropical distribution observed in the extant diversity of the family was initially hypothesized to have resulted from Gondwanan fragmentation (Raven and Axelrod 1974). In this scenario, the clades with disjunctions would date from the Supplementary Information The online version contains supplementary material available at [https://doi.org/10.1007/978-­3-­030-­99742-­7_4]. M. Reginato (*) Departamento de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil e-mail: [email protected] F. Almeda Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA e-mail: [email protected] F. A. Michelangeli Institute of Systematic Botany, The New York Botanical Garden, Bronx, NY, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 R. Goldenberg et al. (eds.), Systematics, Evolution, and Ecology of Melastomataceae, https://doi.org/10.1007/978-3-030-99742-7_4

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Upper Cretaceous and the fragmentation of Gondwana would have played a major role in establishing their current distribution. The fossil record of the Melastomataceae is scarce, and few fossils can be assigned to specific lineages within the family. Only with the emergence of molecular time-calibrated phylogenies have attempts been made to estimate the historical biogeography of the family. Early studies focused especially on determining whether Gondwanan fragmentation played some role in the current pantropical distribution (Renner et  al. 2001; Morley and Dick 2003; Renner 2004a, b). These studies, especially for the disjunct tribes Melastomateae and Sonerileae, have demonstrated that the Gondwanan hypothesis is incompatible with the ages of these clades (Renner et al. 2001; Renner 2004a, b). Accordingly, hypotheses of trans-oceanic long-distance dispersal were invoked to explain these shallow geographical disjunctions (Renner et al. 2001). The same two groups were later subjected to analyses with wider sampling (Veranso-Libalah et al. 2018; Zhou et al. 2019). Both studies corroborated the younger ages of the Melastomateae and Sonerileae and the incompatible Gondwanan scenario but found slightly older ages than previously inferred. More recently, the third major clade with a disjunct pantropical distribution (Olisbeoideae) has been subjected to biogeographical analyses (Amarasinghe et al. 2021), and the same conclusion of trans-oceanic dispersal versus Gondwanan fragmentation was reached. In addition to trans-oceanic long-­ distance dispersal, migration through the North Atlantic land bridge was also suggested as a possible scenario to explain such disjunctions (Renner et al. 2001; Veranso-Libalah et al. 2018; Zhou et al. 2019). The other major lineages showing disjunctions across major realms (Astronieae, Dinophoreae, and Rhexieae) have not been addressed in biogeographical analyses until now. Initial attempts to uncover the historical biogeography of the family were based on visual inspection of a dated phylogeny and known distribution of fossils and extant taxa (Renner et al. 2001; Morley and Dick 2003, Renner 2004a, b). Although age estimates for the Melastomataceae and its tribes played a central role in early debates, this topic has not been fully addressed in more recent phylogenetic papers R. Goldenberg Departamento de Botânica, Universidade Federal do Paraná, Centro Politécnico, Curitiba, PR, Brazil e-mail: [email protected] P. W. Fritsch Botanical Research Institute of Texas, Fort Worth, TX, USA e-mail: [email protected] R. D. Stone School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa e-mail: [email protected] D. S. Penneys Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA e-mail: [email protected]

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with wider sampling (Veranso-Libalah et al. 2018; Zhou et al. 2019; Reginato et al. 2020; Amarasinghe et al. 2021). Recent attempts to provide estimates of divergence times in the family have largely relied on the same few fossils, which have not been fully scrutinized. Two fossils have been widely used as time constraints in the Melastomataceae. The leaf fossil Acrovena laevis from the Early Eocene of North Dakota, USA (Hickey 1977), has been commonly used as the oldest known fossil for the family (Renner et al. 2001; Berger et al. 2016; Veranso-Libalah et al. 2018; Zhou et al. 2019; Amarasinghe et al. 2021). In addition, Miocene seeds from Central Europe (Collinson and Pingen 1992) have been used to constrain the age of the Rhexieae (Veranso-Libalah et  al. 2018; Reginato et  al. 2020) or a deeper node including the Rhexieae + Melastomateae (Renner et al. 2001; Berger et al. 2016; Zhou et al. 2019; Amarasinghe et al. 2021). Moreover, the leaf fossil Melastomites montanensis from the Paleocene of Montana, USA (Brown 1962), has been used as an alternative to A. laevis as the oldest known fossil of the Melastomataceae (Reginato et  al. 2020). The recently discovered leaf fossil Xystonia simonae has been described from the Paleocene of Colombia and attributed to the family (Carvalho et al. 2021). Whereas previous early records were all from the Nearctic region, this discovery has expanded the known distribution of the family during the Paleocene to the Neotropics. Other fossils with potential use as time constraints in the family include leaf fossils of two species in the genus Tibouchina s.l. from Minas Gerais, Brazil (Duarte 1956). The strata where these leaf fossils were found were first interpreted as Pliocene or Upper Miocene (Duarte 1956), but more recent analyses have placed them as Eocene/Oligocene (Maizatto et al. 2008). The latest Melastomataceae phylogeny now includes more than 2400 species (Penneys et  al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”), corresponding to about 42% of the known species diversity in the family and a 26-fold increase in species sampling from previous family-wide biogeographical studies (Renner et al. 2001). Despite consensus on particular aspects of the history of the family (e.g., Gondwanan fragmentation does not explain the current distribution of the Melastomateae and Sonerileae), other scenarios have emerged or have not been fully evaluated (e.g., the role of land bridges). Additionally, despite the heavy impact of molecular dating on the outcome of biogeographical scenarios, this step has been usually overlooked in the literature of the Melastomataceae. Therefore, a major objective of this chapter is to shed light on the historical biogeography of the family with special attention to the estimation of divergence times. Here, we compare the impact of various fossil calibrations across four different calibration schemes and estimate ancestral range distributions on a continental scale across the family phylogeny. We address three major questions: (1) Are there repeated patterns of dispersal among the various pantropical groups? (2) If so, are these restricted to specific time periods? (3) What are the main source and sink biogeographical realms for the Melastomataceae?

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Materials and Methods Divergence-Time Estimation Molecular sampling was based on the DNA sequence data set presented in Penneys et  al. (chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) with the following modifications. Duplicated terminals of the same species and terminals identified as “cf.”, “aff.”  or “sp.”  were removed. A reduced data set of molecular markers was used for all analyses, where only regions with at least 500 terminals were included. The filtered data set was concatenated and comprised two nuclear ribosomal spacers (nrETS and nrITS) and six plastid regions (accD-psaI, atpF-atpH, ndhF, psbK-psbI, rbcL, and trnS-trnG). Sequence alignment was performed as described in Penneys et al. (chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Bayesian molecular dating was performed in BEAST v.2.6.3 (Bouckaert et al. 2014). The maximum likelihood phylogenetic hypothesis recovered (full data set) in Penneys et  al. (chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”) was used to constrain the topology of our analyses. A log-normal, exponentially distributed clock prior was used, the model of substitution was set to GTR + G, the tree prior to the birth and death, and runs included 80 million generations, sampling every 10,000. Four different combinations of time prior constraints were analyzed independently, with the same parameters and genic regions mentioned above. Four different calibration constraints and calibration schemes were used (Tables 1 and 2; see the next paragraph for further details on time constraints). For each calibration scheme, the maximum clade credibility tree was summarized from the stable posterior distribution with the common heights option in TreeAnnotator v.2.6.0 (Bouckaert et al. 2014). The same four calibration schemes were also analyzed with sampling from the prior-only option in BEAST. Prior and posterior marginal distributions for nodes associated with time constraints across different schemes were compared visually. Density plots were generated in R (R Core Team 2018), with both distributions estimated from 1000 random trees sampled from the post-burn-in distributions.

Table 1  Calibration constraints used across the four different schemes, including the type (secondary/fossil), age interval, node, and reference Calibration Age (Ma) 1 Secondary 96.8 [171.1–65.4] 2 Fossil 60–58 3 Fossil 4 Fossil

23–20 40–33.9

Clade (crown) Melast. + CAP

Reference Stem age of Melastomataceae, Silvestro et al. (2021) Melastomataceae Xystonia simonae M. Carvalho, Carvalho et al. 2021 Rhexieae Seeds, Collinson and Pingen (1992) Melastomateae Tibouchina dolianitii Duarte, Duarte (1956)

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Table 2  Calibration schemes and the presence/absence (x) of constraints used in the four comparisons (All-fossils, No-Tibouchina, No-oldest, and No-seeds), including prior type and associated parameters describing the age intervals in Table 1 Prior 1 Normal 2 Log-­ normal 3 Log-­ normal 4 Log-­ normal

Parameters m = 96.8; sigma = 15 m = 2; s = 1; offset = 53 m = 2; s = 1; offset = 13 m = 2; s = 1; offset = 29

Clade (crown) Melast. + CAP

All-­ fossils x

No-Tibouchina No-oldest No-seeds x x x

Melastomataceae x

x

Rhexieae

x

x

Melastomateae

x

x x x

x

All calibration schemes included a soft secondary constraint on the root based on an age estimate of the Melastomataceae (stem) from Silvestro et al. (2021). As based on its more precise age estimate, the new Paleocene fossil from Colombia (Carvalho et al. 2021) constitutes a natural replacement as the oldest known fossil for the family in comparison to those used in previous divergence-time analyses. In the description of this fossil, the authors suggested that it could belong in the Melastomatoideae because of its acrodromous foliar venation (Carvalho et al. 2021). However, acrodromous venation is also observed in the Olisbeoideae and Kibessioideae. We thus placed this fossil at the Most Recent Common Ancestor (MRCA) of the entire family. The Miocene seeds from Central Europe (Collinson and Pingen 1992) have been commonly used to constrain either the crown node of the Rhexieae (Veranso-Libalah et  al. 2018; Reginato et  al. 2020) or a deeper node including the Rhexieae + Melastomateae (Renner et al. 2001; Berger et al. 2016; Zhou et al. 2019; Amarasinghe et al. 2021). Here, we opted to use the Rhexieae because these fossil seeds appear to have multicelled tuberculae, a feature found in the three extant genera of the Rhexieae but absent from all known seeds of the Melastomateae or Marcetieae, where tuberculae are formed by one cell. The Tibouchina leaves (Duarte 1956) have seldom been used for molecular calibrations in the family (Renner 2004b). This is likely due to the Pliocene or Upper Miocene age attributed to these fossils when described (Duarte 1956). The ages of the strata where these fossils were found have been recently revised as Eocene/Oligocene (Maizatto et al. 2008), making them useful fossils for molecular calibration. Here, we adopted a conservative approach and placed them at the crown node of the Melastomateae.

Current Distribution All species included in the chronogram (including the sister Crypteroniaceae + Alzateaceae + Penaeaceae—CAP clade) were scored as present or absent in the major realms of the world, as defined by the World Wildlife Fund (WWF)

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ecoregions shapefile (Olson et  al. 2001). Thus, the part of the world where the Melastomataceae is known to occur was divided into five areas: Afrotropics, Australasia, Indo-Malay, Nearctic, and Neotropics. The geographical distribution of all species was based on records available at GBIF.org (https://doi.org/10.15468/ dl.4ppbzv) and cleaned as described in Reginato et al. (2020). The presence/absence coding was complemented with geographical distribution information from POWO (2019; Supplementary Table S1). The richness distribution of the sampled species of each clade was performed with the cleaned distribution points, climatic layers from Bioclim2 (Fick and Hijmans 2017), and a random forest model (Breiman 2001). This was implemented in R with the packages randomForest v.4.6 (Liaw and Wiener 2002) and raster v.3.4 (Hijmans 2020).

Ancestral Range Estimation Ancestral range distribution was estimated with maximum likelihood as implemented in the R package BioGeoBEARS v.1.1 (Matzke 2013). The chronogram of the scheme “All-fossils” and the presence/absence matrix were used in these analyses. The maximum range size parameter was set to the maximum number of areas observed across all terminals (= 2). The best-fit range evolution model was estimated through Akaike’s information criterion (AIC) comparison in BioGeoBEARS.  Four models of range evolution were compared: DEC (AIC = 809.7), DEC + J (AIC = 803.0), DIVA-like (AIC = 822.8), and DIVA-like + J (AIC  =  816.1). The best-fit model (DEC  +  J) was used for the ancestral range estimation. Results were summarized, including information on the number of events, age of dispersals, and other descriptive results, with BioGeoBEARS and ape v.5.4 (Paradis and Schliep 2019).

Results Divergence-Time Estimation For each of the four different calibration schemes, we calculated the prior and posterior marginal densities of nodes associated with each time constraint (Fig. 1). The stem mean age of the Melastomataceae varied from 71.3  Ma [95% Highest Probability Density (HPD) 55–91] (No-Tibouchina) to 80.3 Ma [66–98] (No-seeds), whereas its crown mean age ranged from 68.5  Ma [53–83] (No-Tibouchina) to 75.2 Ma [62–89] (No-seeds). Despite this variation in mean ages, the posterior densities of these two nodes strongly overlapped across the four calibration schemes. In addition, regarding these two nodes, the calibration scheme with the highest sensitivity to the prior (i.e., the highest overlap between prior and posterior densities)

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Fig. 1  Prior (light gray) and posterior (dark gray) marginal densities of nodes associated with time constraints across four different schemes (All fossils, No-Tibouchina, No-seeds, No-oldest). M = posterior median age

was the No-Tibouchina scheme. The other two nodes with time constraints showed greater variation in divergence-time estimates, with older ages in the No-seeds or No-oldest schemes and the youngest ages in the No-Tibouchina scheme (Fig. 1). Melastomateae crown ages were highly sensitive to its priors in all schemes that included a time constraint for this node (All-fossils, No-seeds, and No-oldest), whereas Rhexieae crown ages only showed strong overlap of prior and posterior marginal densities in the No-Tibouchina scheme. The maximum clade credibility tree of each calibration scheme is available in Supplementary File S1. The ages of the major clades, including 95% HPD intervals, are presented in Table 3.

Current Distribution A summary of the geographical distribution of the species sampled in our analyses, including the number of sampled/total accepted species, is provided in Fig.  2. Although most of the major clades in our analysis are restricted to the Neotropics (Fig.  2), their respective distributions within this region are not uniform. Some clades are widespread throughout the region (Miconieae, Henrietteeae, Marcetieae, and Merianieae), whereas others show a more restricted range. The groups with relatively few species (up to 35 spp.) and limited geographical ranges are the Bertolonieae, Cyphostyleae, Eriocnemeae, Lithobieae, Rupestreeae, and Stanmarkieae. These smaller clades are either restricted to the Andes (sometimes reaching Central America) or to eastern Brazil. Moreover, some clades with

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Table 3  Summary of results by major clade, including stem and crown ages, HPD interval [brackets], ancestral range estimate, and associated probability. “|” indicates the range of areas Stem age Crown age (Ma, 95%HPD) (Ma, 95%HPD) Ancestral range 27.77 [19.7,37.64] 21.11 [15.5,28.06] Indo-Malay | Neotropic Bertolonieae 51.31 16.05 Neotropic [43.13,62.33] [10.56,21.56] Pyxidantheae 40.88 [34.65,49] 16.3 [8.29,26.81] Neotropic Pyramieae 38.19 29.92 Neotropic [24.27,48.29] [21.78,37.03] Cyphostyleae 37.12 [28,46.32] 17.39 [11.13,25.2] Neotropic Dinophoreae 41.38 7.4 [2.38,13.72] Afrotropic | [35.26,49.54] Indo-Malay Dissochaeteae 38.19 22.64 Indo-Malay [24.27,48.29] [14.96,30.66] Eriocnemeae 20.88 7.79 [4.08,10.78] Neotropic [15.39,28.64] Henrietteeae 27.77 [19.7,37.64] 16.86 Neotropic [12.23,21.66] Kibessioideae 48.74 12.48 [6.83,18.93] Indo-Malay [36.42,63.59] Lithobieae 39.63 – Neotropic [28.41,52.95] Marcetieae 40.31 29.47 Neotropic [34.16,48.49] [23.97,35.49] Melastomateae 40.31 32.97 Neotropic [34.16,48.49] [29.41,38.53] Merianieae 40.19 30 [23.5,37.94] Neotropic [30.13,51.28] Miconieae 20.88 16.71 [13.3,20.64] Neotropic [15.39,28.64] Lavoisiereae 38.75 22.39 Neotropic [29.39,47.85] [16.37,29.16] Olisbeoideae 48.74 31.4 [24.98,39.05] Neotropic [36.42,63.59] Rhexieae 37 [27.6,46.26] 30.03 [21.14,37.5] Neotropic Rupestreeae 37 [27.6,46.26] – Neotropic Sonerileae 40.88 [34.65,49] 36 [29.2,44.14] Neotropic Stanmarkieae 37.12 [28,46.32] 11.64 [3,20.38] Neotropic Trioleneae 47.8 [40.49,58.28] 28.02 [20.9,35.66] Neotropic Melastomataceae 76.22 68.51 Neotropic [62.02,94.09] [57.28,81.98] Clade Astronieae

Probability 0.57 1 1 1 1 0.89 1 1 1 0.99 – 1 0.9 1 1 1 0.69 0.89 – 0.98 1 1 0.52

intermediary richness and geographical breadth show some similar patterns, such as the Pyxidantheae and Trioleneae (Andes and Central America) and the Lavoisiereae and Pyramieae (centered mainly in eastern Brazil). Two clades (Kibessioideae and

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Fig. 2  Summary of the geographical distribution of the species sampled in our analyses across the 22 major clades. Smaller maps next to the phylogeny show the presence (red) or absence (white) across the major realms analyzed. The other maps show, for each major clade (numbers at the top-­ left corner follow the numbers indicated in the phylogeny), the estimated richness distribution with warmer colors indicating higher richness, the total number of accepted species (sampled species) in boldface, and the clade name at the bottom. The total accepted numbers of species are from Ulloa Ulloa et al. (chapter “Melastomataceae: Global Diversity, Distribution, and Endemism”)

Dissochaeteae) are restricted to southeastern Asia, where both are found in the Indo-­ Malay and Australasia regions. Among the other clades with disjunctions across the tropics, the Melastomateae and Olisbeoideae have a more similar pattern with wider distributions, whereas the Sonerileae, although found in the same major areas, have

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low species numbers and more restricted distributions in the Neotropics. Unique distributional patterns are found in the Astronieae, Dinophoreae, and Rhexieae.

Ancestral Range Estimation The maximum likelihood estimate of biogeographical range evolution yielded results in which most of the cladogenetic events in the family are sympatric (98.1% of all events) at the geographical scale analyzed. Other cladogenetic events estimated are founder events (ca. 0.2%), vicariance or subset (ca. 1%), and anagenetic dispersal events (0.7%). The analysis recovered 47 dispersal events (including jump dispersals; Table 4). A summary of the estimated direction of founder and dispersal events and their associated ages is depicted in Fig. 3 and the number of dispersals among areas in Table 4. The Neotropical and Indo-Malay regions are the source of most dispersals across the family (Table 4), whereas the events from the Neotropics are in general older (Fig. 3). Exchange of lineages between these two areas also followed this same pattern (Fig. 3). The Australasian and Nearctic realms were never recovered as source areas, whereas dispersals to the Indo-Malay region were only  recovered from the Afrotropical region (Table  4). In absolute numbers, the most common type of dispersal is from the Indo-Malay region toward neighboring Australasia (27), followed by dispersals from the Afrotropics to the Indo-Malay region; the other types are less frequent (Table 4). The biogeographical reconstruction over the All-fossils chronogram is presented in Fig. 4, and the annotated tree with ancestral range estimates is in Supplementary File S2. The ancestral range estimated for the family MRCA is ambiguous (Neotropic = 0.52 or Neotropic | Indo-Malay = 0.48); nonetheless, most of the backbone nodes are recovered in the Neotropics with high confidence (Fig.  4; Supplementary File S2). The ancestral range estimate of each major clade is presented in Table 3. A summary of dispersal events for the clades found in more than one area is presented in Table 5. The clade with the highest number of dispersal events among the analyzed areas is the Sonerileae (15 events of 5 distinct Table 4  Number of dispersal events among areas estimated with maximum likelihood under the DEC + J model of biogeographical range evolution To From

Afrotropic Afrotropic | Indo-Malay Australasia Indo-Malay Nearctic Neotropic

Afro. – 0 0 4 0 3 7

Afro. | Indo. 0 – 0 0 0 1 1

Austral. 0 0 – 27 0 0 27

Indo. 6 0 0 – 0 3 9

Nearc. 0 0 0 0 – 1 1

Neotr. 0 0 0 2 0 – 2

6 0 0 33 0 8 47

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Fig. 3  Ages of cladogenetic jump dispersals and anagenetic dispersals across the Melastomataceae. Barplot x-axes show the frequency of events and y-axes the age in Ma. Pie charts show the clades where the events occurred. (a) Neotropic to Indo-Malay. (b) Neotropic to Afrotropic. (c) Neotropic to Afrotropic and Indo-Malay. (d) Neotropic to Nearctic. (e) Indo-Malay to Afrotropic. (f) Indo-­ Malay to Neotropic. (g) Indo-Malay to Australasia. (h) Afrotropic to Indo-Malay

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Fig. 4  Maximum likelihood estimate of the historical biogeography of the Melastomataceae under the DEC + J model over the All-fossils chronogram. Pie charts at the nodes represent the probability of ancestral range estimates; colors and letters follow the map and legend. Pie charts are shown for all backbone and major clade nodes and are omitted within major clades when the estimate matches that of the immediate ancestor. Distribution coding (presence/absence) and the names of major clades corresponding to tribes are shown at the right. A time scale is shown at the bottom in Ma; P. = Pleistocene + Holocene

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Table 5  Summary of dispersal events in clades found in more than one major realm. “|” indicates the range of areas. The number of events is indicated by “n”. When more than one event was estimated, the mean age and the total range are provided Clade Melastomateae

Olisbeoideae

Sonerileae

Astronieae Dinophoreae Rhexieae Dissochaeteae Kibessioideae

Dispersal events Neotropic > Afrotropic (n = 1, age = 28.4); Afrotropic > Indo-Malay (n = 1, age = 20.2); Indo-Malay > Australasia (n = 7, mean age = 2.0 [0.2, 5.87]) Neotropic > Afrotropic (n = 1, age = 29.5); Afrotropic > Indo-Malay (n = 4, mean age = 12.4 [9.3, 15.8]); Indo-Malay > Afrotropic (n = 2, mean age = 5.4 [1.1, 9.7]); Indo-Malay > Australasia (n = 2, mean age = 2.9 [1.1, 4.8]) Neotropic > Afrotropic (n = 1, age = 28.0); Afrotropic > Indo-Malay (n = 1, age = 26.4); Indo-Malay > Afrotropic (n = 2, mean age = 6.7 [3.5, 9.8]); Indo-Malay > Neotropic (n = 2, mean age = 4.0 [2.6, 5.4]); Indo-Malay > Australasia (n = 9, mean age = 2.5 [1.2, 7.3]) Neotropic > Indo-Malay (n = 1, age = 24.4); Indo-Malay > Australasia (n = 1, age = 14.3) Neotropic > Afrotropic | Indo-Malay (n = 1, age = 24.4) Neotropic > Nearctic (n = 1, age = 27.2) Indo-Malay > Australasia (n = 6, mean age = 1.9 [1.1, 2.9]) Indo-Malay > Australasia (n = 2, mean age = 1.9 [1.9, 1.9])

combinations of source/sink areas), followed by the Olisbeoideae (9 of 4), and the Melastomateae (9 of 3) (Table  5). Although some dispersal events are unique to some clades (e.g., from the Neotropics to Nearctic in the Rhexieae and from Indo-­ Malay to the Neotropics in the Sonerileae), others are recurrent and sometimes overlap in time (Table 5, Fig. 3). For example, the dispersals from the Neotropics to the Afrotropics in the Melastomateae, Olisbeoideae, and Sonerileae have similar ages (ca. 27–29 Ma) as do most of the dispersals from Indo-Malay toward Australasia (Table 5, Fig. 3).

Discussion The Age of the Melastomataceae Age estimates for the origin of the Melastomataceae (stem ages) based on time-­ measured tree analysis, as well as early diversification of its extant taxa (crown ages), have varied greatly in the literature. Angiosperm-level analyses based on different data sets and methodology have stem age estimates varying from 73  Ma [53–86] (Magallón et al. 2015) to 134 Ma [100–143] (Janssens et al. 2020), among others. More restricted analyses focusing on the Myrtales or Melastomataceae recovered ages within these ranges, with stem ages of 91 Ma [82–99] (Berger et al. 2016) and 88  Ma [80–96] (Reginato et  al. 2020). Here, we recovered stem ages

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across the four calibration schemes comparable to some previous estimates, ranging from 71.3 Ma [55–91] (No-Tibouchina) to 80.3 Ma [66–98] (No-seeds). It is interesting to note that although we have included slightly older time constraints for the family MRCA than those in previous analyses (Berger et al. 2016; Reginato et al. 2020), the mean ages recovered here are slightly younger. This suggests that despite recent discoveries (Carvalho et al. 2021), the fossil record of the Melastomataceae useful for time constraints within the family is biased toward younger ages (at least under conservative assignments) because mean estimates, when including a broader sampling, are in general older (Berger et al. 2016; Janssens et al. 2020). A widely sampled time-measured tree analysis for the Myrtales is needed to improve dates within the Melastomataceae. Despite recurrent uncertainty associated with the estimates of divergence times and strong overlap across the four schemes, our constraint comparisons demonstrated that the widely used set of fossils in prior studies (i.e., Renner et al. 2001; Berger et al. 2016; Veranso-Libalah et al. 2018; Zhou et al. 2019; Reginato et al. 2020; Amarasinghe et al. 2021) was the most sensitive to its priors (No-Tibouchina, Fig. 1). This scheme also recovered the youngest mean ages, whereas divergence-­ time estimates tended to be older with the inclusion of the Tibouchina fossil (All-­ fossils, No-seeds, and No-oldest schemes). Thus, future studies should consider the inclusion of more time constraints in the Melastomataceae phylogeny than those usually employed.

 he Neotropics as the Historical Repository T of the Melastomataceae The maximum likelihood estimate of biogeographical range evolution yielded results in which most of the cladogenetic events in the family are sympatric (98.1% of all events) at the geographical scale analyzed, indicating that the geographical integrity observed in the phylogeny of shallower clades (Reginato and Michelangeli 2016) is also observed at a higher level. The crown nodes of most major clades were found to be placed in the Neotropics (Table 3, Fig. 3), where most of the species also occur (Fig.  2) and where there are also many “depauperons” (Bertolonieae, Cyphostyleae, Eriocnemeae, Lithobieae, Rupestreeae, and Stanmarkieae; Fig.  2). An equally common source area is the Indo-Malay region (Table 4), also with many species and one “depauperon” (Pternandra of the Kibessioideae), but dispersals from this area to other regions are younger than those from the Neotropics (Fig. 3). Our estimate of the geographical origin area of the family is ambiguous regarding these two areas, with a putative origin estimated either in the Neotropics or in the Neotropic + Indo-Malay region. Nonetheless, this whole scenario indicates that the Neotropical region may have played a major role in the early diversification of the family, as hypothesized by a pre-molecular study (Raven and Axelrod 1974).

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Moreover, these results contradict early interpretations of the historical biogeography of the Melastomataceae based on molecular data, where the tropical belt that bordered northern Tethys was suggested as the region of origin (Renner et al. 2001). This interpretation was mainly based on the earliest fossil record being restricted to Laurasia and occurrence in Southeast Asia of the oldest surviving lineages (Renner et al. 2001). As mentioned earlier, a recent fossil discovery has placed the family in the Neotropics early in its history (Carvalho et al. 2021), and the Kibessioideae and Astronieae no longer form an early divergent grade in the Melastomataceae phylogeny, although the relationship of the Kibessioideae with the rest of the family is still uncertain (Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Our results, moreover, do not support an African origin for the family as previously proposed (Morley and Dick 2003). Nonetheless, our stem age estimates for the family are in accord with a putative time for the onset of rainforest climates in equatorial South America (ca. 84 Ma, but possibly earlier; Morley 2000).

Repeated “Pantropicalization” Through the Same Route The pantropical clades in the family have been subjected to recent analyses, where estimates of origin were recovered as the Melastomateae and Sonerileae in the Neotropics (Veranso-Libalah et al. 2018; Zhou et al. 2019) and the Olisbeoideae in the Neotropics + Africa, albeit sampling in the latter was designed to investigate the biogeography of Memecylon (Amarasinghe et  al. 2021). Here, except for the Olisbeoideae, where a Neotropical origin was recovered, our results agree with those from previous studies (Veranso-Libalah et al. 2018; Zhou et al. 2019). In addition, here, we addressed whether or not the pantropical groups followed the same path and timing of dispersal. We found the same order of dispersals for these three clades: from the Neotropics to Africa, to the Indo-Malay region, and then reaching Australasia more recently (Fig.  3 and Table  5). Among these three clades, the Melastomateae were the only clade where no reverse dispersals were observed (Table 5), whereas dispersals from Indo-Malay back to Africa were estimated in the Olisbeoideae and Sonerileae. Regarding timing, we found coinciding dispersal ages from the Neotropics to Afrotropics across the three clades (Melastomateae, Olisbeoideae, and Sonerileae), whereas dispersal ages from the Afrotropics to Indo-­ Malay are more diffuse (Fig.  3 and Table  5). Dispersals from the Neotropics to Africa in these clades were interpreted as trans-oceanic dispersals by previous authors (Veranso-Libalah et al. 2018; Zhou et al. 2019), but the possibility of migration through the North Atlantic land bridge has been considered (Veranso-Libalah et al. 2018; Zhou et al. 2019). The coinciding dispersal timing across these groups may provide further support for the latter scenario.

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The Role of Land Bridges Beyond the pantropical clades, the oldest events recovered were dispersals from the Neotropics to the Indo-Malay region (in the backbone, Figs. 3 and 4), occurring at different times (ca. 60 Ma and ca. 40 Ma; Fig. 3). Around this time interval, the fossil record places the family both in South America and North America (Brown 1962; Hickey 1977; Carvalho et al. 2021). A putative origin of the Melastomataceae and allied families in South America with their associated dispersal routes has been considered previously (Morley and Dick 2003). This origin is corroborated by the current fossil record and finds support in our estimates of ancestral range distribution. In this scenario, the oldest dispersal events recovered here (ca. 60 Ma) from the Neotropics to Indo-Malay could have been via North America, facilitated by the Late Cretaceous/Paleocene South American-North American land bridge, in existence until ca. 55 Ma (Pindall et al. 1988; Hallam 1994), and globally warm climates during the Late Paleocene/Early Eocene thermal maximum (Morley 2000). In this scenario, ancestral lineages may have been able to invade the Paleocene/Eocene boreotropical flora reaching the Indo-Malay region. Whether dispersals took place through Beringia or Europe is still an open question. An Eocene wood fossil has been attributed to the Olisbeoideae (Memecyloxylon germanicum; Gottwald 1992), which would provide support for the latter scenario.

Trans-Oceanic Dispersals Despite the possibility of stepping-stone dispersals and/or migrations through land bridges, the prevalence of trans-oceanic dispersals has been hypothesized or inferred since early studies in the family (Renner et al. 2001). These estimates have been corroborated more recently (Veranso-Libalah et  al. 2018; Zhou et  al. 2019; Amarasinghe et al. 2021), and our results agree with them. Among the several trans-­ oceanic dispersals that probably have occurred in the family, here, we recovered two striking ones not previously reported in the Sonerileae. Our analyses recovered two dispersals from the Indo-Malay region back to the Neotropics in this clade around 4 Ma (Fig. 3, Table 5). The two species involved in these events are found in the highlands of the Guiana Shield (Tryssophyton and Neblinanthera). An early divergent clade in the Sonerileae (Boyania) is also found in the same region. The single event of dispersal to the Nearctic region inferred in the Rhexieae at ca. 27  Ma coming from the Neotropical region is too young to invoke the Late Cretaceous/Paleocene South American-North American land bridge (ca. 55  Ma) and is too old for the complete closure of the Panama Isthmus (3.5 Ma). Nonetheless, the exchange of lineages between North and South America is a highly debated topic in the literature, and pulses of dispersal of terrestrial organisms have been estimated during the last 30 Ma (Bacon et al. 2015).

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With a much higher frequency of events, dispersals from the Indo-Malay region to neighboring Australasia were the most frequent among those recovered in this analysis. Results also yielded a great asymmetry of dispersals between these two areas, with all events from Indo-Malay to Australasia, and none in the reverse direction. The results also indicated that the great majority of dispersal events are very recent (Fig.  3), with overlapping ages around 2  Ma (in the Dissochaeteae, Kibessioideae, Melastomateae, Olisbeoideae, and Sonerileae), except for an older event in the Astronieae (ca. 14 Ma). Such waves of dispersals to Australasia around the beginning of the Quaternary might have been facilitated by repeated fluctuations in sea levels and climate during the Pleistocene glacial cycles (Weigelt et al. 2016).

Future Directions Uncertainty in the backbone of the family phylogeny is still pervasive (Reginato et al. 2016; Maurin et al. 2021; Penneys et al., chapter “A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology”). Thus, a more widely sampled and less-uncertain phylogenetic hypothesis will be required to further improve our estimates of the biogeographical history for the family. In addition, finer-scale analyses of selected clades within each major realm, especially in the Neotropics (most studies have focused on the pantropical groups at a coarse scale), may provide insights into this important source area of diversity for the Melastomataceae. For instance, in-depth studies could provide further support for north-to-south versus south-to-north dispersals, supporting northern latitude land bridges versus trans-oceanic dispersal scenarios for pantropical groups. Added sampling and sequencing, as well as the availability of geographical distribution data, have all improved in recent years relative to fossil information, and the lack of fossils will likely continue to be the bottleneck for future studies. Despite the possibility of significant new findings, a more detailed and objective assessment of the available fossils would be needed to improve discussions on prior constraints, enabling less-conservative node assignments and, consequently, improving the utility of the available data. In this sense, a morphospace analysis of leaf venation and seed morphology would help. Estimates of ancestral distributions are biased by the current distributions, with undetected extinctions blurring estimates. Thus, improving our understanding of the historical biogeography of the Melastomataceae will also require that fossil distributions be incorporated into the models more directly (e.g., in the distribution information and not only in the time calibrations). Acknowledgments  We thank two anonymous reviewers and Ricardo Pacifico, guest editor, for helping improve our text. We thank the US National Science Foundation for support: NSF DEB-0508582, NSF DEB-0515665, NSF DEB-0818399, NSF DEB-1146409, NSF DEB-1343612, NSF DEB-1543721, NSF DEB-1754697, and NSF DEB-1754667. RG received support from the National Council for Scientific and Technological Development (CNPq)/Brazil-#308065/2017-4.

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Morley RJ (2000) Origin and evolution of tropical rain forests. Wiley, New York Morley RJ, Dick CW (2003) Missing fossils, molecular clocks, and the origin of the Melastomataceae. Am J Bot 90(11):1638–1644 Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51(11):933–938 Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528 Pindall JL, Cande SC, Pitman WC, Rowley DB, Dewey LF, Labrecque J, Haxby W (1988) A plate-kinematic framework for models of Caribbean evolution. Tectonophysics 155:121–138 POWO (2019) Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet. http://www.plantsoftheworldonline.org/. Accessed 1 Feb 2021 R Core Team (2018) R: a language and environment for statistical computing. R foundation for statistical computing. http://www.R-­project.org/. Accessed 1 Feb 2021 Raven PH, Axelrod DI (1974) Angiosperm biogeography and past continental movements. Ann Missouri Bot Gard 61(3):539–567 Reginato M, Michelangeli FA (2016) Untangling the phylogeny of Leandra s. str. (Melastomataceae, Miconieae). Mol Phylogenet Evol 96:17–32 Reginato M, Neubig KM, Majure LC, Michelangeli FA (2016) The first complete plastid genomes of Melastomataceae are highly structurally conserved. PeerJ 4:e2715 Reginato M, Vasconcelos TN, Kriebel R, Simões AO (2020) Is dispersal mode a driver of diversification and geographical distribution in the tropical plant family Melastomataceae? Mol Phylogenet Evol 148:106815 Renner SS, Clausing G, Meyer, K (2001) Historical biogeography of Melastomataceae: the roles of Tertiary migration and long‐distance dispersal. Am J Bot 88(7):1290–1300 Renner SS (2004a) Bayesian analysis of combined chloroplast loci, using multiple calibrations, supports the recent arrival of Melastomataceae in Africa and Madagascar. Am J Bot 91(9):1427–1435 Renner SS (2004b) Multiple Miocene Melastomataceae dispersal between Madagascar, Africa and India. Philos Trans R Soc Lond Ser B Biol Sci 359(1450):1485–1494 Silvestro D, Bacon CD, Ding W, Zhang Q, Donoghue PC, Antonelli A, Xing Y (2021) Fossil data support a pre-Cretaceous origin of flowering plants. Nat Ecol Evol 5(4):449–457 Weigelt P, Steinbauer MJ, Cabral JS, Kreft H (2016) Late quaternary climate change shapes island biodiversity. Nature 532(7597):99–102 Veranso-Libalah M, Kadereit G, Stone RD, Couvreur TL (2018) Multiple shifts to open habitats in Melastomateae (Melastomataceae) congruent with the increase of African Neogene climatic aridity. J Biogeogr 45(6):1420–1431 Zhou Q, Lin CW, Ng WL, Dai J, Denda T, Zhou R, Liu Y (2019) Analyses of plastome sequences improve phylogenetic resolution and provide new insight into the evolutionary history of Asian Sonerileae/Dissochaeteae. Front Plant Sci 10:1477. https://doi.org/10.3389/fpls.2019.01477

Part II

Systematics

A New Melastomataceae Classification Informed by Molecular Phylogenetics and Morphology Darin S. Penneys, Frank Almeda, Marcelo Reginato, Fabián A. Michelangeli, Renato Goldenberg, Peter W. Fritsch, and R. Douglas Stone

Introduction The Melastomataceae are a cosmopolitan family of herbs, shrubs, trees, epiphytes, and woody climbers primarily distributed in tropical and subtropical areas, from coastlines to about 4000 m above sea level. As treated here, with ca. 177 genera and 5858 species, the Melastomataceae are among the ten most species-rich angiosperm families (Christenhusz and Byng 2016). They are most common in wet, montane forests where they frequently represent one of the most abundant plant families. In some regions of tropical Africa and Brazil, they have diversified in open areas and grasslands, and in the Greater Antilles, in pinelands. The Melastomataceae have great ecological importance in their contributions to tropical forest biomass and nutrient cycling, nectar and pollen rewards to floral visitors, and berry fruits to avian and mammalian dispersers. Supplementary Information The online version contains supplementary material available at [https://doi.org/10.1007/978-­3-­030-­99742-­7_5]. D. S. Penneys (*) Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA e-mail: [email protected] F. Almeda Department of Botany, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA e-mail: [email protected] M. Reginato Departamento de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 R. Goldenberg et al. (eds.), Systematics, Evolution, and Ecology of Melastomataceae, https://doi.org/10.1007/978-3-030-99742-7_5

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In the last comprehensive monograph of the Melastomataceae, Cogniaux (1891) recognized 2730 species, representing ca. 47% of those recognized today. From 2004 through 2018, 532 new species were described in the family, at an average annual rate of 35.5 (IPNI 2021). Many more new species can be expected to be added, especially from relatively unexplored tropical areas in Africa, the Andes, Brazil, Borneo, Madagascar, and New Guinea. We are aware of scores of as-yet undescribed melastome species represented by specimens currently residing in herbaria. If recent trends continue, we estimate that the total number of Melastomataceae species will surpass 6000 by 2030. Assessments of the geographic range and conservation status of melastomes (Penneys and Cotton 2011; Bernal et  al. 2016; Cámara-Leret et  al. 2020; Flora do Brasil 2020) indicate that most species have limited distributions and are threatened with extinction from deforestation, climate change, and other anthropogenic impacts. Previous suprageneric classifications of the Melastomataceae (e.g., de Candolle 1828; Naudin 1849–1853; Triana 1866, 1871; Cogniaux 1891; Renner 1993) relied heavily on the morphology of the androecium, especially whether it is homoeandrous or heterandrous, whether the anthers are porose or rimose, the number of anther pores, the presence or absence of pedoconnectives, and the presence or absence and variation in dorsal and/or ventral anther connective appendages. Other characters that have been emphasized in the recognition of surprageneric taxa include: inflorescence position (terminal versus axillary), floral merosity, ovary position, ovary crown ornamentation, ovary placentation, fruit type, seed shape, testa texture, and Neotropical versus Paleotropical distribution (Triana 1866; Cogniaux 1891; Renner 1993). Except for some family classifications based on internal anatomy (van Tieghem 1891a, b; van Vliet et al. 1981), various combinations of these characters have formed the basis for all treatments of the Melastomataceae. However, the evidence from molecular phylogenetic analyses shows that most of these characters are homoplasious. The reliance on some seemingly arbitrarily emphasized characters for higher-level classification deserves critical reconsideration. Studies suggest that internal anatomical characters (van Tieghem 1891a, b, 1892; van Vliet 1981) and seeds (Whiffin and Tomb 1972) F. A. Michelangeli Institute of Systematic Botany, The New York Botanical Garden, Bronx, NY, USA e-mail: [email protected] R. Goldenberg Departamento de Botânica, Universidade Federal do Paraná, Centro Politécnico, Curitiba, PR, Brazil e-mail: [email protected] P. W. Fritsch Botanical Research Institute of Texas, Fort Worth, TX, USA e-mail: [email protected] R. D. Stone School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa e-mail: [email protected]

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harbor relatively low levels of homoplasy across the family, but comprehensive surveys of these characters have yet to be conducted. Renner (1993) and Almeda (chapter “Classification History of the Melastomataceae: Early Beginnings Through the Pre-molecular Era”) have provided historical overviews of the higher-level classification of the Melastomataceae. Cogniaux (1891) recognized 13 tribes in the family. Over the following century, only two additional tribes were added (Cyphostyleae, Gleason 1929; Feliciadamieae, Jacques-Félix 1995). Renner (1993) ascribed nine tribes to the Melastomataceae and considered the Memecylaceae as a separate family. With the advent of molecular phylogenetics, along with an influx of workers interested in the family, nearly all traditionally recognized tribes have been recircumscribed, and several new tribes have been added, i.e., Henrietteeae (Penneys et  al. 2010), Pyramieae (as Cambessedesieae, Bochorny et  al. 2019), Eriocnemeae (Penneys et  al. 2020), Lithobieae (Penneys et al. 2020), Marcetieae (Rocha et al. 2016a, b), and Trioleneae (Bacci et al. 2019). Here, we present the most comprehensive phylogenetic analysis of the Melastomataceae ever conducted at the tribal and generic levels. The analysis is based on DNA sequence data from the nuclear ribosomal external and internal transcribed spacers (ETS, ITS) and seven plastid regions (accD-psaI  +  atpF-­ atpH + ndhF + psbK-psbL + rbcL + rpl16 + trnS-trnG), with sampling encompassing 2973 terminals (of which 32 form the outgroup), 2435 melastome species, and 158 of the currently recognized 177 genera. We expect that this estimate will be useful for assessing morphological character evolution as well as better understanding the ecology, reproductive and pollination biology, biogeographical patterns, and adaptive radiations of melastomes worldwide. Moreover, this estimate can aid future investigations into the systematics and taxonomic revision of targeted groups within the family. With the inclusion of the three novel tribes established herein (i.e., Dinophoreae, Rupestreeae, and Stanmarkieae), our revised classification of the Melastomataceae comprises three subfamilies (i.e., Olisbeoideae, Kibessioideae, and Melastomatoideae) and 21 tribes. We also provide a description of the family and each subfamily and tribe together with brief notes on their distribution, diagnostic characters, and the taxonomy of their constituent genera.

Materials and Methods Taxon sampling—For all samples used in the molecular analysis, DNA was extracted from fresh leaf tissue dried in silica gel or from herbarium sheets. Voucher specimens are deposited in one or more of the following herbaria (acronyms as in Thiers 2021): BH, BRUN, CAS, CAY, CEPEC, COL, CR, F, FLAS, HAJB, K, L, M, MJG, MO, NY, RB, TAIE, UEC, UPCB, UPTC, US, VEN, WU, and Z. We sampled 158 of the 177 currently accepted genera (Michelangeli et al. 2020) in the Melastomataceae, with sample selection guided by tissue availabil-

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ity and previous hypotheses on phylogenetic relationships. The number of species sampled per genus was loosely proportional to the size of the genus to which they are assigned and the recognition of subgeneric and sectional groupings; however, testing monophyly at the generic level was largely beyond the scope of this study. All sequences of Melastomataceae and their sister “CAP clade” (Crypteroniaceae + Alzateaceae + Penaeaceae) available in GenBank were downloaded and divided into homologous regions based on their annotations and filtered as described in Reginato et al. (2020). The molecular phylogenetic analyses included 151 genera, 2290 species, and 2789 terminals of the Melastomatoideae, 1/9/16 of Kibessioideae, 6/136/136 of Olisbeoideae, and 13/32/32 from the CAP clade (the latter representing the outgroup used to root the cladograms; Supplementary Appendix 1). The data matrix containing concatenated sequences from all regions was analyzed simultaneously. No data were excluded, and indels were left unmodified. The matrix included ETS and ITS combined with seven plastid regions indicated above. For the 9-gene analysis, 2973 terminals were sequenced for ETS (2123 terminals)  +  ITS (2619)  +  accD-psaI (1542)  +  atpF-atpH (556)  +  ndhF (1171) + psbK-psbL (1925) + rbcL (922) + rpl16 (640) + trnS-trnG (713). The aligned matrix is 11,359 base pairs long, with 6934 variable sites, 5344 informative sites, and 55.4% missing data of which gaps comprise 22.1%. DNA extraction, amplification, and sequencing—For descriptions of DNA extraction, PCR amplification, and cycle sequencing methods, see Michelangeli et al. (2011), Rocha et al. (2016a), Penneys et al. (2020), and Maurin et al. (2021). Sequence editing and alignment—Contigs were assembled and edited with Geneious 10 (Biomatters Limited, Auckland, New Zealand). Sequence orientation and alignment were performed by using the R package DECIPHER 2.4.0 (Wright 2016) with the functions OrientNucleotides, AlignSeqs (iterations = 50, refinements  =  50) and AdjustAlignment. Poorly aligned regions of each individual region were removed by using aliscore.pl with the -r option (Misof and Misof 2009). Phylogenetic analysis—For each data set, maximum likelihood (ML) analyses were conducted in RAxML 8 (Stamatakis 2014) with the GTR + Γ model (partitioned by region). Branch support was calculated from 1000 bootstrap replicates and employed the thorough “-f” setting rather than the fast “-f a” setting in the configuration file. In this treatment, moderate bootstrap support is defined as 66%–85%, and strong support as 86%–100%. Morphology—Morphological descriptions and variation were assessed and summarized from the literature sources referenced under each subfamily and tribe. For some details, type specimens in JSTOR Global Plants were consulted, and online field photos were examined. Basis for classification—Subfamilies and tribes recognized in this classification are delimited through a combination of monophyly and statistical support in the 9-gene phylogenetic analysis (Fig. 1, Supplementary Fig. 1), precedent, morphological cohesion, and/or morphological uniqueness (the latter only in the case of the monospecific and unsampled Feliciadamieae).

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3/21 1/2 3/8 44/820 7/269 20/149 6/88 4/70 2/43 48/1099 4/25 2/4 2/204 1/35 1/1901 3/7 8/301 3/95 5/143 1/1 1/15 6/556

Fig. 1  Best phylogenetic tree of the Melastomataceae based on the partitioned maximum likelihood analysis of nine molecular regions (ETS, ITS, accD-psaI, atpF-atpH, ndhF, psbK-psbI, rbcL, rpl16, trnS-trnG) and 2973 terminals. The outgroup comprises Crypteroniaceae, Alzateaceae, Penaeaceae (= CAP clade). This tree summarizes subfamilies, tribes, and their inferred relationships; the full tree is shown in Supplementary Fig.  1. The monospecific tribe Feliciadamieae remains unsampled. Stars indicate new tribes described herein. Numbers above branches are ML bootstrap support values >50%. Codes following clade names denote New World (NW), Old World (OW), Pantropical (P), total number of genera and species

Results The ML analysis based on the combined 9-gene dataset (Supplementary Appendix 2) yielded a best tree (Supplementary Fig. 1) as summarized in Fig. 1. We consider only the subfamily and tribal-level relationships that have direct implications for the taxonomic treatment provided below (the internal relationships of individual tribes are treated separately in individual chapters within this volume). The Melastomataceae are monophyletic (bootstrap 100%), and Olisbeoideae form a clade (99%) that is sister to the remainder of the family (100%). Kibessioideae (100%) are the next-diverging clade (98%) along the backbone, sister to the Melastomatoideae (100%), which contains all the remaining taxa. Because the two subsequent clades along the backbone have low support (bootstrap