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Downloaded from Genbank (Table 2.1) UNTANGLING A PHYLOGENETIC KNOT OF SERPENTS: INTEGRATIVE SYSTEMATICS ON NEOTROPICAL SNAKES by ROBERT C. JADIN B.Sc. – Northeastern State University, Tahlequah, OK, 2005 M.Sc. – University of Texas at Tyler, Tyler, TX, 2007 A dissertation submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2013 This thesis entitled: UNTANGLING A PHYLOGENETIC KNOT OF SERPENTS: INTEGRATIVE SYSTEMATICS ON NEOTROPICAL SNAKES Written by Robert Curtis Jadin has been approved for the Department of Ecology and Evolutionary Biology ____________________________________________________ Robert P. Guralnick _____________________________________________________ Jeffry B. Mitton _______________________________________________________ Andrew P. Martin _______________________________________________________ Patrick Kociolek _______________________________________________________ Herbert H. Covert Date: 6 May 2013 The final copy of this thesis has been examined by the signatories and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. Jadin, Robert C. (Ph.D., Ecology and Evolutionary Biology) UNTANGLING A PHYLOGENETIC KNOT OF SERPENTS: INTEGRATIVE SYSTEMATICS ON NEOTROPICAL SNAKES Dissertation directed by Robert P. Guralnick ABSTRACT Taxonomy based on evolutionary relationships plays a critical role in science and society, as properly named units of biological diversity allows for immediate recognition of the general appearance and basic natural history of a particular lineage. Consequently, it could be argued that systematics, a field that investigates not only the classification of organisms but also their diversity and origins, is among the most important with relevance to all other disciplines within biology. The challenge is documenting species in nature; these units are there to find but doing so requires compiling a variety of different sources of data and methods to test hypotheses about diversity. Through this dissertation, I combine my background in classical taxonomy, natural history, and descriptive morphology with modern molecular phylogenetics, implementing Bayesian, Likelihood, and Parsimony optimality criteria, to stabilize taxonomy, detect cryptic diversity, and understand snake phylogeny. In particular, I incorporate important guidelines recently defined for integrative taxonomy, that assure accurate classification of biodiversity; these guidelines should become the new standard for all systematic revisions. To assess these guidelines, I have focused on a group and region where taxonomic and systematic knowledge is still very limited. Central and South American snakes are not only a point of continued iii systematic confusion but also understanding the evolutionary histories of venomous species may provide applications to medical treatment and human health. Using these methods of modern systematics I investigate two lineages of Neotropical snakes whose systematic history begins with classical Linnean taxonomy and progresses over the centuries with the advancement of systematic techniques. Cryptic lineages, in combination with inadequate sampling, obscure the complete diversity of this group. This dissertation incorporates several important sub-sections of systematics including an integrative systematic revision (chapter 2), detection of cryptic species (chapter 3), and placement of an enigmatic lineage within the tree of life (chapter 4). Overall, this research highlights how these guidelines for integrative taxonomy are paramount to achieving an informative and stable classification system. Systematic studies like this are becoming increasingly important in our current age of rapid biodiversity loss. iv ACKNOWLEDGMENTS I thank my advisor, Robert P. Guralnick, for his positive attitude and guidance during my time in Boulder. Additionally, I thank Jeffry B. Mitton, Andy P. Martin, Patrick Kociolek, and Herbert H. Covert for serving on my dissertation committee and assisting in my development. Other faculty in the department of ecology and evolutionary biology who were influential include John Basey, Alexander Cruz, Samuel M. Flaxman, Pieter T.J. Johnson, Nolan C. Kane, and David W. Stock. I greatly appreciate all of their guidance, wisdom, and advice. By far, the most important person during my dissertation work has been my wife, Sarah A. Orlofske. Her guidance, positive influence, and inspiration have greatly enhanced my development as a scientist. Two people who have been motivating and shaped my view of evolution and science are Patrik Nosil and Dan Brooks. Patrik taught me a lot about evolutionary biology and how it should be taught. I enjoyed and learned so much in his speciation course as well as being his T.A. for evolutionary biology. Dan always challenges and improves my perspectives and I greatly appreciate our long conversations philosophically discussing academia, science, and life. Throughout my time at CU I have learned a lot from my fellow classmates. In particular, I would like to thank the following for their support through this time: S. Beals, I. Buller, E. Cheng, A. Comeault, K. Dosch Richgels, L.P. Erb, P. Erb, A. Faist, T. Farkas, S.M. Ferrenberg, M.B. Joseph, J.R. Mihaljevic, S. Hellmuth Paull, E.L. Paulson, A.C. Peterson, D.L. Preston, J. Prevey, M.S. Robeson III, L. Sackett, S.L. Stowell, M.R. Wilkins, A.C. Williams, and the post- doc B.A. Goodman. I thank the numerous collaborators that I have worked with over the years for their tremendous help in making me a better writer, biologist, and collaborator. At the top of this list v are Eric N. Smith, Gilson A. Rivas, Josiah H. Townsend, Jonathan A. Campbell, and Todd A. Castoe. During my time at CU Boulder, parts of my research and travel were funded through several institutions and societies. I sincerely thank the following for the funding they provided: American Museum of Natural History, American Society of Ichthyologists and Herpetologists, American Society of Parasitologists, California Academy of Sciences, CU EBIO Department, CU Graduate School, CU Museum of Natural History, East Texas Herpetological Society, Ecology and Evolution of Infectious Diseases conference, Society for the Study of Amphibians and Reptiles, and Society of Systematic Biologists. For the last year of my dissertation I was supported through an NSF GK-12 teaching fellowship. The faculty and staff of this program were very supportive and I thank W.D. Bowman, J.A. Feld, B. Graham, G. Ross, and L. Smith for such a great opportunity that has enhanced my ability to teach and conduct scientific outreach. vi CONTENTS Abstract …………………………………………………………………………………………iii Acknowledgments ……………………………………………………………………………….v List of tables……………………………………………………………………………………..ix List of figures……………………………………………………………………………………..x Chapter 1 SLITHERING INTO NEOTROPICAL EVOLUTION: INTEGRATIVE SYSTEMATICS OF NEW WORLD SNAKES Introduction to systematics………………………………………..………………………………1 Integrative systematics……………………………………………………………...………..……2 Detecting cryptic diversity………………………………………………………………………...4 Placing taxa in the tree of life……………………………………………......................................5 2 UNRAVELLING A TANGLE OF MEXICAN SERPENTS: A SYSTEMATIC REVISION OF HIGHLAND PITVIPERS Abstract….…………….……………………………………………..……………………………7 Introduction….………………………………….…………………....……………………………8 Materials and methods……………………………….…………………….………..…………….9 Results.….……………………………….…………………….………..………………………..17 Discussion….……………………………….…………………….………..…………………….26 Appendix 2.1...…………………………………………………………………………………...39 vii 3 CRYPTIC DIVERSITY IN DISJUNCT POPULATIONS OF MIDDLE AMERICAN MONTANE PITVIPERS: A SYSTEMATIC REASSESSMENT OF CERROPHIDION GODMANI Abstract….…………….…………………....……………………………………………………40 Introduction……………………………….…………………….………..………………………41 Methods….……………………………….…………………….………..……………………….42 Results….……………………………….…………………….………..………………………...46 Discussion….…………….…………………....…………………………………………………65 Appendix 3.1…….……………………………………………………………………………….71 4 FINDING ARBOREAL SNAKES IN AN EVOLUTIONARY TREE: PHYLOGENETIC PLACEMENT AND SYSTEMATIC REVISION OF THE NEOTROPICAL BIRDSNAKES Abstract….…………….…………………....……………………………………………………74 Introduction….…………….…………………....………….…………………………………….75 Methods….……………………………….……………….…….………..………………………76 Results….……………………………….…………………….………..………………………...82 Discussion.……………………………….…………………….………..……………………….85 5 CONCLUSIONS Introduction……………………………………………………………………………………….89 Future directions….…………….…………………....…………………………………………..90 Integrative taxonomy in modern biology….…………………....………………………………..92 References.…………………….…………………….………..…………………………………94 viii LIST OF TABLES Table 2.1 Taxa, vouchers, locality data, and GenBank accession numbers for sequences used in this study. Sequences newly added specifically for this study are in bold…………………………………………………………………13 2.2 Morphological comparisons between Cerrophidion barbouri and Agkistrodon browni………………………………………………………………………18 2.3 Measurements and counts of the type series of Cerrophidion barbouri and Agkistrodon browni………………………………………………………..19 2.4 Pairwise sequence divergences among (below diagonal) and within (diagonal) all New World genera as defined in this study using only cyt b gene………………………………………………………………………………...25 3.1 Taxa, vouchers, locality data, and GenBank accession numbers for sequences used in this study. Sequences newly added specifically for this study are in bold…………………………………………………………………44
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