TRACING THE DAWN OF THE ELAPIDAE THROUGH THE MOLECULAR SYSTEMATICS AND HISTORICAL BIOGEOGRAPHY OF OLD WORLD CORALSNAKES by UTPAL SMART Presented to the Faculty of the Graduate School of Biology The University of Texas at Arlington in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY THE UNIVERSITY OF TEXAS AT ARLINGTON November 2016 Copyright © by Utpal Smart 2016 All Rights Reserved ii Acknowledgements Having spent over six long years as a (often helpless and bungling) graduate student in the Biology Department at UTA, I owe my gratitude to countless colleagues, faculty and staff. I would like to start by thanking my adviser Eric Smith who saw potential in me despite of my atypical academic background and gave me the opportunity to pursue my PhD under his guidance in the U.S. He has been a supportive adviser in the lab and a fun companion in the field. In the same breath, I would also like to thank all my doctoral committee members for guiding me through my dissertation research, starting with Jonathan Campbell, Esther Betran, Matt Fujita, Paul Chippindale and Todd Castoe. I would especially like to thank Matt Fujita and Todd Castoe for opening up their labs and introducing me to modern genomic techniques. Another group of people that have been vital in my student life at UTA are the office ladies, Linda Taylor, Sherri Echols, Paulette Batten and Gloria Burlingham. Without these superwomen I would not have made it past the first semester at UTA. I would also like to thank Zaida Alsina and Derik Austin for so generously providing their time to help me deal with incompetent or misbehaving computers. Moreover, I am grateful to Jill Castoe, Melissa Muenzler and recently Kimberly Bowles for their excellent service at the Genomic Core Facility. Carl Franklin was helpful with work in the museum and very lavish with his rather unique sense of humour. I would additionally like to thank my funding sources namely, The Beta Phi Chapter of Phi Sigma Society for their travel and research grants and the National Science Foundation for their grant (DEB-1146324) awarded to E. N. Smith which funded my field work in Indonesia. Outside of UTA, I have several researchers and colleagues who offered me some form of assistance or support during the last six years. In this context, I thank Dr. Karthikeyan Vasudevan of LaConES and Dr. Praveen Karanth and iii his lab at the Indian Institute of Science, for sequencing Indian coralsnakes, which would have otherwise never been incorporated in my research. I would also like to extend my thanks to my colleagues and friends from Indonesia, namely Pak Amir Hamidy, Pak Irvan Siddik, Pak Nia Kuriawan, Ibu Mirza Kusrini, Mbak Evy Arida, Mas Wayhoo Triloksono and Masbro Adool who made my work and stay in Indonesia fruitful and enjoyable. I am grateful to Indraneil Das, David Bickford, Lee Grismer and other researchers working in Southeast Asia for sharing their samples of rare coralsnakes with me. The following people have played the dual role of friends and mentors in the past six years and I owe a lot to them: Jyotiska Chaudhuri, Jeff Streicher, Coleman Sheehy, Walter Schargle, Christian Cox, Heath Blackmon, Jesse Meik, Claudia Marquez amongst several other that I am sure I am forgetting. I would like to thank the Castoe and Fujita labs and also the people of my own lab namely, Panupong Arm Thammachoti, Kyle Shaney, Goutam Sarker and Elijah Wostl. I am especially indebted to close friendships that kept me going through rough times, including the corrupting influence of Jacobo Reyes Velasco and David Sanchez; the goofy and pleasurable company of Kyle Shaney, James Titus McQuillan, Corey Roelke, Debanjana Roy and Malini Kotak; the help and support of Ruben Tovar and Paul and Karen Pasichnyk; last but not the least, the love and warmth of Coridon Laws, Amrita Pai and Umilaela Arifin. I would like to end with a profound thankyou to my family and especially my parents who are the force behind everything that I am today, all that I have achieved thus far and all that I will accomplish in the future. Nov 3, 2016 iv Abstract TRACING THE DAWN OF THE ELAPIDAE THROUGH THE MOLECULAR SYSTEMATICS AND HISTORICAL BIOGEOGRAPHY OF OLD WORLD CORALSNAKES Utpal Smart, PhD The University of Texas at Arlington, 2016 Supervising Professor: Eric Nelson Smith Much debated since the early 20th century, the evolutionary history and origin of the clinically important family Elapidae is of enormous interest. A persistent lack of higher-level phylogenetic resolution however, has impeded a clear understanding of the biogeography of this charismatic group of snakes. The traditional limiting factor in studies on higher-level elapid relationships has been the availability of samples from Old World coralsnakes (genera Sinomicrurus and Calliophis). Usually small, shy and fossorial, these animals are amongst the rarest Oriental snakes and their sampling in molecular studies has been sparse. Herein, primarily using molecular data, I work out the systematic relationships and biogeography of these two elusive genera of Asian coralsnakes. I leverage multilocus datasets, employing parametric phylogenetics and multispecies coalescent methods to provide a first insight into the systematic relationships and species boundaries of Calliophis species from South and Southeast Asia. I further use a phylogenetic framework to investigate biogeographic drivers of diversification in the Taiwan-Ryukyu Archipelago, using the genus Sinomicrurus. Finally, I estimate the most v comprehensive phylogenetic relationships to-date among Old World coralsnakes and evaluate their position among the Elapidae. In doing so I make available one of the best resolved tree of higher-level elapid relationships to date. My phylogenetic analyses refute the monophyly of Old World coralsnakes and lead to a major revision of the known subfamilial relationships within Elapidae. Additionally, a fossil calibrated time-tree reveals that the genus Calliophis forms a distinct basal group in relation to all other elapids. My biogegoraphical analyses suggest that the Elapidae originated in Asia and the collision between the Indian and Laurasian plates may have acted as a driver of diversification in ancestral lineages. Overall, my dissertation work provides seminal information on the taxonomy, systematics and biogeography of one of the rarest and most enigmatic groups of venomous snakes in Asia. My research thus elucidates the role of major biogeographic breaks and also highlights novel patterns of evolutionary divergence across the Oriental biogeographic realm. This improved framework of phylogenetic relationships is expected to significantly benefit all future efforts of conservation and studies of toxin evolution in the Elapidae. vi Table of Contents Acknowledgements .............................................................................................................iii Abstract ............................................................................................................................... v List of Illustrations .............................................................................................................. xi List of Tables ..................................................................................................................... xv Chapter 1 A brief introduction to Old World coralsnakes .................................................... 1 Chapter 2 A preliminary molecular phylogeny of Indian Calliophis species ....................... 6 Introduction ..................................................................................................................... 6 Materials and Methods ................................................................................................... 8 Taxon sampling .......................................................................................................... 8 Molecular methods ................................................................................................... 10 Model selection and phylogenetic analyses ............................................................. 11 Species tree analysis ................................................................................................ 12 Results .......................................................................................................................... 13 Phylogenetic analyses .............................................................................................. 13 Species tree analysis ................................................................................................ 15 Discussion .................................................................................................................... 16 Chapter 3 Molecular phylogeny and species delimitation of the long-glanded Sundaland Calliophis ........................................................................................................ 18 Introduction ................................................................................................................... 18 Materials and Methods ................................................................................................. 21 Taxon sampling ........................................................................................................ 21 Molecular Methods ................................................................................................... 21 Phylogenetic analyses .............................................................................................