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Ecological and Evolutionary Drivers of Biodiversity and Extinction Risks in Amphibians and Squamates

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Ecological and Evolutionary Drivers of Biodiversity and Extinction Risks in Amphibians and Squamates Ecological and Evolutionary Drivers of Biodiversity and Extinction Risks in Amphibians and Squamates by João Filipe Riva Tonini Licentiate in Biological Sciences, October 2008, Universidade Federal do Espírito Santo B.S. in Biological Sciences, October 2009, Universidade Federal do Espírito Santo M.S. in Biological Sciences, February 2011, Universidade Federal do Espírito Santo A Dissertation submitted to The Faculty of The Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy August 31, 2017 Dissertation directed by R. Alexander Pyron Robert F. Griggs Assistant Professor of Biology The Columbian College of Arts and Sciences of The George Washington University certifies that João Filipe Riva Tonini has passed the Final Examination for the degree of Doctor of Philosophy as of July 18, 2017. This is the final and approved form of the dissertation. Ecological and Evolutionary Drivers of Biodiversity and Extinction Risks in Amphibians and Squamates João Filipe Riva Tonini Dissertation Research Committee: R. Alexander Pyron, Robert F. Griggs Assistant Professor of Biology, Dissertation Director Amy Zanne, Associate Professor of Biology, Committee Member Rayna C. Bell, Curator of Amphibians and Reptiles, Committee Member © Copyright 2017 by João Filipe Riva Tonini All rights reserved Dedication To Lari and Caú. Acknowledgements I am immensely grateful to the Brazilian Government for the financial support of my studies and research through undergraduate, masters, and doctorate degrees (since 2004 to 2017). Additional support during the doctoral program was provided by The George Washington University through a graduate teaching assistantship and Harlan fellowships. My special thanks to my dearest mentor Dr. Alex Pyron, for sharing his lab, resources, and vast areas of expertise. Alex have been always supportive and keen to help me thinking on meaningful research questions. He motivated and pushed to pursue my own research interest and supported my choices. Thank you for the friendship and great lunch times in fancy places! I am thankful to current and past members of the Pyron Lab, in special to Cat Hendry. Cat helped in every single thing that I ever had to do in the graduate program, we had great times over beers, and she is the greatest! Thanks as well to Sara Green, Sara Rhodig, and Tim Colston. Thanks to all members of my graduate (g) and dissertation (d) committee: Amy Zanne (g), Guillermo Orti (g), Kelly Zamudio (g), and Rayna Bell (d). Their guidance and wiliness to help improved the quality of the dissertation and manuscripts. My special thanks to Amy and Guillermo for encouraging on my research interests, sharing their lab infrastructure, and for great moments hiking and enjoying a good meal with caipirinhas. Thank you to Hartmut Doebel, Robert Donaldson, and Tara Scully for guidance during the teaching assistantships. I am indebted to colleagues, and their institutions, for sharing resources and expertise: Roy McDiarmid, Kevin de Queiroz, Addison Winn, and Jeremy Jacobs (Smithisonian National Museum of Natural History); Felipe Toledo and Sandra Goutte (Universidade de Campinas); Frank Burbrink and David Kizirian (American Museum of Natural History); Karen Beard (Utah State University); Walter Jetz (Yale University). I am also grateful to Adam Wong and Glenn MacLachlan in the high-performance computer cluster of GWU (Colonial One) for helping to troubleshoot the analyses of my doctorate research. I wish to thank Rafael de Sá (University of Richmond) for opening the doors of his lab and support me to be able to compete for a position in a doctoral program in the United States. Thanks Rafael for sharing the excitement about frogs, supporting my research interests, for the friendship, and great trips to amazing places! I was fortunate to enjoy the time during the graduate program with many great friends whom Lari and I shared great moments, laughs, and delicious food: Rodrigo Ferreira and Cecília Weichert, David Santana and Janine Ziermann, Pedro Peloso and Silvia Pavan, Dan Mulcahy and Bonnie Blaimer, Chuy and Belén Chávez, Thiago Moreira and Sandra Lara, Drew and Jackie Thompson, Nick and Thayna Joice, Lenice and Oscar Shibatta, Ligia Benavides, Maddison Anderson, Lily Hughes, Joe Stiegler, Bob and Laura Kallal, Drew Moore, David Stern, Amy Millo, Ricardo Betancur and Diana Arcila, Karen Poole, Dominic White, Aidan, Jimmy Munoz, Joana Mooney, Carol Perez, Tiffini Smith, Amulya Yarpala. My special thanks to Rodrigo for the friendship and collaboration of many years, it has been reinvigorating enjoy times with you dear friend. At last, I thank to my parents (Eduardo and Neide), my brother (Luiz Guillerme), and my beloved Lari whom is my greatest motivation to pursue my dreams. Thank you for our beautiful son, Caú. Abstract of Dissertation Ecological and Evolutionary Drivers of Biodiversity and Extinction Risks in Amphibians and Squamates Amphibians and squamates are together the most diverse clade of terrestrial vertebrates, and their biodiversity is thought to reflect many of the most important biogeographic and ecological forces that have generated species richness through time. To understand patterns of relatedness and the drivers of diversification, phylogenetic trees are instrumental to estimate the relative contribution of evolutionary and ecological processes. My dissertation comprises four chapters related to phylogenetic patterns of biodiversity in amphibians and squamates. First, I tested across the frog Tree of Life whether species could escape the constraint imposed by body size on sound frequency and evolve new types of calls. The results show that frogs have multiple shifts in body-size allometry for calls. These shifts comprise species endemic to hyper-diverse regions such as Africa, Australia, New Guinea, Southeast Asia, and the Neotropics. Those shifts seem to reflect biogeographic invasions and instances of ecomorphological escape. Second, I asked what drives species co-occurrence and community assembly in Neotropical frogs? I find that the composition of most communities has been generated by stochastic variation of speciation, local extinction, and colonization rates. Thus, Neotropical ecoregions comprise distinct assemblages of frogs, as demonstrated by several regionalization studies, but community assemblages are a random sample of the regional pool. Third, I asked how many times has phytotelm-breeding evolved across Neotropical frogs, and do these lineages ever revert to pond- or stream-breeding? If not, is phytotelm-breeding an evolutionary dead end, preventing diversification and raising extinction rates? I find that the history of phytotelm- breeding is labile, with support for at least 68 potential origins and 107 reversals. There is some support for state-dependent extinction (higher for phytotelm-breeding lineages), but I cannot uniformly reject state-independent models. Fourth, I asked whether extinction risk in squamates is clustered evolutionarily and whether high-risk species represent a disproportionate amount of total evolutionary history. I found currently assessed threat status to be phylogenetically clustered at broad level in Squamata, suggesting it is critical to assess extinction risks for close relatives of threatened lineages. There is no association between threat and distinctiveness, suggesting that extinctions may not result in a disproportionate loss of evolutionary history. The results show that immediate efforts should focus on geckos, iguanas, and chameleons, in Amazon, Southeast Asia, and New Guinea. Table of Contents Dedication iv Acknowledgments v Abstract of Dissertation vii List of Figures xii List of Tables xvi Chapter 1: Evolutionary variation in allometric constraints on call evolution in frogs suggests ecomorphological escape 1 Abstract ............................................................................................................................... 1 Introduction ......................................................................................................................... 2 Material and Methods .......................................................................................................... 6 Phylogenetic and comparative data ......................................................................... 6 Statistical modeling ................................................................................................. 9 Results ............................................................................................................................... 11 Diversity and sound frequency and body size across frogs ................................... 11 Regime shifts in acoustic allometric scaling ......................................................... 12 Discussion ......................................................................................................................... 19 Future directions .................................................................................................... 22 Chapter 2: Transitions to phytotelm-breeding in Neotropical frogs are common, but may increase extinction 25 Abstract ............................................................................................................................. 25 Introduction ....................................................................................................................... 26 Material and Methods .......................................................................................................
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