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From Microevolutionary Processes to Macroevolutionary Patterns: Investigating Diversification at Multiple Scales in Southeast Asian Lizards

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From Microevolutionary Processes to Macroevolutionary Patterns: Investigating Diversification at Multiple Scales in Southeast Asian Lizards By Anthony J. Barley Submitted to the graduate degree program in Ecology and Evolutionary Biology and the Graduate Faculty of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy. ________________________________ Chairperson Dr. Rafe M. Brown ________________________________ Dr. Mark Holder ________________________________ Dr. John Kelly ________________________________ Dr. Xingong Li ________________________________ Dr. A. Townsend Peterson ________________________________ Dr. Linda Trueb Date Defended: April 14, 2014 The dissertation committee for Anthony J. Barley certifies that this is the approved version of the following dissertation: From Microevolutionary Processes to Macroevolutionary Patterns: Investigating Diversification at Multiple Scales in Southeast Asian Lizards ________________________________ Chairperson Dr. Rafe M. Brown Date Approved: April 16, 2014 ii Abstract A comprehensive understanding of the evolutionary processes responsible for generating biodiversity is best obtained using integrative approaches at multiple scales. In doing so, these investigations can provide complex insights into how fine-scale microevolutionary processes operating at the population level, translate into the large-scale macroevolutionary biodiversity patterns we see in evolutionary radiations. Due to the complex geography, historical climatic fluctuations, and remarkably high concentrations of land vertebrate biodiversity, Southeast Asia is an ideal place to investigate these processes. Lizards of the genus Eutropis represent one of the more recognizable radiations of lizards in Southeast Asia, due to their high abundances, broad geographic distribution, and generalized external morphology. However, their evolutionary history has remained enigmatic due to their highly conserved morphology and a lack of dense population sampling of individuals and species across their range. In this dissertation, I first utilize a variety of approaches to delimit species in Philippine Eutropis and find that species diversity is vastly underestimated by current taxonomy, while more generally assessing how best to determine species limits in radiations where morphology is highly conserved. I then use a molecular phylogenetic framework to investigate biogeographic patterns and the timing of diversification within the genus across Southeast Asia. Lastly, I take a landscape genomic approach to determine the relative contributions of distance, and various geographic and environmental variables to population genetic differentiation and morphological diversity patterns in the common sun skink. This research contributes substantially to our understanding of species diversity in evolutionary radiations, as well as how historical and contemporary evolutionary processes shape the evolution of morphological and genetic diversity. iii Acknowledgements The research presented here, and my path to completing graduate school would not have been possible without the assistance and support of a large number people and institutions. Some chapters herein have been coauthored with Rafe Brown, Aniruddha Datta-Roy, Arvin Diesmos, Lee Grismer, Patrick Monnahan, K. Praveen Karanth, and Jordan White. I am grateful for the extensive financial support I have received during the course of my graduate career at KU from the Biodiversity Institute (Leonard Krishtalka), the Department of Ecology and Evolutionary Biology (Chris Haufler), the Office of Graduate Studies, and a number of professors (Andrew Short, Bill Duellman, and Linda Trueb) who provided me with research assistantship support that offered extra flexibility and valuable research time during my graduate career. I thank my major advisor Rafe Brown for the extensive support he has provided throughout my time at KU, from both an academic and personal standpoint. Rafe’s enthusiasm and mentorship has been instrumental in my success in research and my growth as a scientist. I also thank the other members of my dissertation committee Mark Holder, John Kelly, Xingong Li, Town Peterson, and Linda Trueb for being incredible academic resources and for challenging me intellectually. In particular I’d like to thank John for allowing me to work in his lab to collect genomic data for my dissertation research, and for answering a plethora of research questions over the years. Both of my undergraduate advisors Ronald Coleman and Brad Shaffer deserve thanks for providing me invaluable guidance, support, and opportunities, without which I likely would have never entered graduate school in the first place. During my graduate career I have been fortunate to collaborate with numerous field biologists who have loaned specimens and tissue samples they collected, as well as obtain loans from museum collections; without which none of this research would have been possible. This iv includes A. Resetar (FMNH), J. Vindum, D. Blackburn, R. Crombie (CAS), A. Wynn, K. de Queiroz (USNM), J. McGuire (MVZ), T. LaDuc (TNHC), J. Hanken, J. Losos, J. Rosado (MCZ), J. Barnes, V. Papal-latoc (PNM), A. Schmitz, W. Böhme (ZMFK). Fieldwork during the course of my dissertation would not have been possible without support from the Philippine government and the hardworking Philippine field team I was privileged to work with, particularly Arvin Diesmos and Jason Fernandez. I need to thank a large group of friends and colleagues that were important in making my graduate school experience at KU more enjoyable and successful, and providing intellectual input into my research, including: Mike Andersen, David Blackburn, Andrea Crowther, Matt Davis, Raul Diaz, Jake Esselstyn, Allison Fuiten, Rich Glor, Jesse Grismer, Boryana Koseva, Jacob Landis, Dean Leavitt, Andres Lira, Joe Manthey, Nick McCool, Julius Mojica, Rob Moyle, Jamie Oaks, Carl Oliveros, Karen Olson, Chan Kin Onn, Cameron Siler, Jeet Sukumaran, Scott Travers, Luke Welton, and Amber Wright. In particular, I thank Charles Linkem who was an important friend and mentor when I first moved to Lawrence, and provided me with much needed guidance during the early portion of my graduate school career. I would also like to thank members of the Tokyo Sandblasters including Michael Amick, Chris Coleman, Bob Jansen, Scott Cassaw, and Brian Finley; Monday night softball games were a much needed relaxation outlet from graduate school. I thank Levi Gray, a close personal friend who has been tremendously supportive in both personal and professional contexts over the years. Being able to count on him for advice and herping trips has been incredibly important to me during graduate school, and I wouldn’t be where I am today without his help. Phil Spinks is also a close friend who was a mentor to me as an undergraduate and was responsible for preparing me for graduate school in systematics; he v spent countless hours working with me above and beyond what was expected. Bob Thomson is a close friend, mentor, and fellow California Gila Monster enthusiast; he has helped me on a variety of important fronts during graduate school for which I am extremely grateful. Last, but not least, I would like to thank my entire family. My wife Laci has provided me with unlimited amounts of love, support, and encouragement, which has been integral to the completion of my dissertation. She has also provided countless insights during conversations that have helped me grow as both a person and a scientist while at KU. My parents Dave and Winnie Barley have always been role models for me, as well as provided encouragement and much needed financial support throughout my academic career. My brothers David, Dominic, and Michael have been there for me during my highest and lowest points, and the fishing trips and barbecues we’ve had during graduate school have been essential to my happiness. Additionally, Dave and Mike deserve credit for first teaching me how to noose lizards and find salamanders when I was a kid. vi Table of contents Title Page i Acceptance Page ii Abstract iii Acknowledgements iv Chapter 1: The challenge of species delimitation at the extremes: diversification without morphological change in Philippine Sun Skinks 1 Chapter 2: Sun Skink diversification across the Indian-Southeast Asian biogeographical interface 39 Chapter 3: Landscape genomics across Southeast Asia: the evolution of genetic and morphological diversity in the common sun skink 63 Chapter 4: Reconciling morphological conservatism, taxonomic chaos, and evolutionary history: a partial taxonomic revision of Philippine sun skinks of the genus Eutropis (Reptilia: Squamata: Scincidae) 94 Literature Cited 136 Appendices 170 vii Chapter 1 The challenge of species delimitation at the extremes: diversification without morphological change in Philippine sun skinks Barley AJ, White J, Diesmos AC, Brown RM. 2013. The challenge of species delimitation at the extremes: diversification without morphological change in Philippine sun skinks. Evolution 67:3556–3572. Abstract An accurate understanding of species diversity is essential to studies across a wide range of biological subdisciplines. However, delimiting species remains challenging in evolutionary radiations where morphological diversification is rapid and accompanied by little genetic differentiation or when genetic lineage divergence is not accompanied by morphological change. We investigate the utility of a variety of recently developed
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  • Philippine Crocodile Crocodylus Mindorensis Merlijn Van Weerd

    Philippine Crocodile Crocodylus Mindorensis Merlijn Van Weerd

    Philippine Crocodile Crocodylus mindorensis Merlijn van Weerd Centre of Environmental Science, Leiden University, Abel Tasmanstraat 5bis, Utrecht 3531 GR, Netherlands ([email protected]) Common Names: Philippine crocodile (English), buwaya 2009 IUCN Red List: CR (Critically Endangered. Criteria (general Philippines), bukarot (northern Luzon) A1c. Observed decline in extent of occurrence >80% in 3 generations. C2a. Less than 250 adults in the wild, populations highly fragmented and declining; IUCN 2009) (last assessed Range: Philippines in 1996). Taxonomic Status The Philippine crocodile was described in 1935 by Karl Schmidt on the basis of a type specimen and three paratypes from the island of Mindoro (Schmidt 1935, 1938). Schmidt also described the closely related New Guinea freshwater crocodile (Crocodylus novaeguineae) in 1928 and later made a comparison of morphological differences between C. mindorensis, C. novaeguineae and C. porosus, maintaining C. mindorensis as a separate species (1956). However the Philippine crocodile has long been treated as C. novaeguineae mindorensis, a sub-species of the New Guinea crocodile, by other authorities. Hall (1989) provided new evidence of the distinctness of the Philippine crocodile and nowadays C. mindorensis is generally treated as a full species endemic to the Philippines. Figure 1. Distribution of Crocodylus mindorensis. Figure 2. Juvenile C. mindorensis in Dunoy Lake, in Northern Sierra Madre National Park, northern Luzon. Photograph: Merlijn van Weerd. Conservation Overview CITES: Appendix I Ecology and Natural History CSG Action Plan: The Philippine crocodile is a relatively small freshwater Availability of recent survey data: Adequate crocodile. Although much is still unknown, studies at two Need for wild population recovery: Highest captive breeding facilities [Palawan Wildlife Rescue and Potential for sustainable management: Low Conservation Centre (PWRCC), Palawan Island (Ortega Van Weerd, M.