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Systematics of Collared Snakes and Burrowing Asps (Aparallactinae

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Systematics of Collared Snakes and Burrowing Asps (Aparallactinae University of Texas at El Paso DigitalCommons@UTEP Open Access Theses & Dissertations 2017-01-01 Systematics Of Collared Snakes And Burrowing Asps (aparallactinae And Atractaspidinae) (squamata: Lamprophiidae) Francisco Portillo University of Texas at El Paso, [email protected] Follow this and additional works at: https://digitalcommons.utep.edu/open_etd Part of the Zoology Commons Recommended Citation Portillo, Francisco, "Systematics Of Collared Snakes And Burrowing Asps (aparallactinae And Atractaspidinae) (squamata: Lamprophiidae)" (2017). Open Access Theses & Dissertations. 731. https://digitalcommons.utep.edu/open_etd/731 This is brought to you for free and open access by DigitalCommons@UTEP. It has been accepted for inclusion in Open Access Theses & Dissertations by an authorized administrator of DigitalCommons@UTEP. For more information, please contact [email protected]. SYSTEMATICS OF COLLARED SNAKES AND BURROWING ASPS (APARALLACTINAE AND ATRACTASPIDINAE) (SQUAMATA: LAMPROPHIIDAE) FRANCISCO PORTILLO, BS, MS Doctoral Program in Ecology and Evolutionary Biology APPROVED: Eli Greenbaum, Ph.D., Chair Carl Lieb, Ph.D. Michael Moody, Ph.D. Richard Langford, Ph.D. Charles H. Ambler, Ph.D. Dean of the Graduate School Copyright © by Francisco Portillo 2017 SYSTEMATICS OF COLLARED SNAKES AND BURROWING ASPS (APARALLACTINAE AND ATRACTASPIDINAE) (SQUAMATA: LAMPROPHIIDAE) by FRANCISCO PORTILLO, BS, MS DISSERTATION Presented to the Faculty of the Graduate School of The University of Texas at El Paso in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Department of Biological Sciences THE UNIVERSITY OF TEXAS AT EL PASO May 2017 ACKNOWLEDGMENTS First, I would like to thank my family for their love and support throughout my life. I am very grateful to my lovely wife, who has been extremely supportive, motivational, and patient, as I have progressed through graduate school. My parents, who taught me how to appreciate wildlife and natural ecosystems, always encouraged me to learn and explore the outdoors without causing any disturbances to nature. I also thank my siblings, who have been great partners on many of my outdoor excursions and have always been a great support. My family continues to be a big inspiration to this day. I would like to thank my graduate committee, Dr. Eli Greenbaum, Dr. Carl Lieb, Dr. Michael Moody, and Dr. Richard Langford. I would like to give a special thanks to my Ph.D. advisor Dr. Eli Greenbaum who took me on as an undergraduate when I had very limited lab experience, and who provided superb guidance throughout my research as a graduate student. I would also like to thank all other faculty members that have helped along the way, including Dr. Jerry Johnson, Dr. Elizabeth Walsh, Dr. Craig Tweedie, and Dr. Vanessa Lougheed, all of whom provided help whenever I sought it. I thank the Louis Stokes Alliance for Minority Participation (LSAMP) fellowish that funded my dissertation research for two years. I would also like to thank the graduate school and the Dodson family for awarding me the Dodson Research Grant on three separate occasions. The Dodson Research Grants enabled me to travel to London (UK), Berlin (Germany), and Tervuren (Belgium) in order to examine crucial type specimens for my study. iv I thank the California Academy of Sciences, San Francisco (CAS), The Natural History Museum, London (BMNH), Muséum National d’Histoire Naturelle, Paris (MNHN), Museum of Comparative Zoology, Cambridge (MCZ), Museum of Vertebrate Zoology, Berkeley (MVZ), Royal Museum for Central Africa, Tervuren (RMCA), South African National Biodiversity Institue (SANBI), Florida Museum of Natural History, Gainesville (UF), United States National Museum (now National Museum of Natural History), Washington D.C. (USNM), and Museum für Naturkunde, Berlin (ZMB) for access to specimens. DNA samples were sequenced by Ana Betancourt at the UTEP DNA Analysis Core Facility (funded by a UTEP Dodson Research Grant). I thank William R. Branch (Bayworld and Nelson Mandela Metropolitan University), Werner Conradie (Bayworld and South African Institute for Aquatic Biodiversity), Mark-Oliver Rödel, Johannes Penner (Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity), Aaron M. Bauer (Department of Biology, Villanova University), Jean- François Trape (Laboratoire de paludologie et zoologie médicale, Institut de Recherche pour le Développement, UMR MIVEGEC), Zoltán T. Nagy (Royal Belgian Institute of Natural Sciences), Piero Carlino (Museo di Storia naturale del Salento, via Europa), Olivier S. G. Pauwels (Département des Vertébrés Récents, Institut Royal des Sciences naturelles de Belgique), Michele Menegon (Tropical Biodiversity Section, MUSE, The Science Museum of Trento), Tomáš Mazuch (Dříteč), Kate Jackson (Department of Biology, Whitman College), Wolfgang Wüster (Molecular Ecology and Evolution Group, School of Biological Sciences, Bangor University), Chifundera Kusamba (Laboratoire d’Herpétologie, Département de Biologie, Centre de Recherche en Sciences Naturelles), Shai Meiri, Erez Maza (Steinhardt Museum), Daniel F. Hughes (UTEP), Marius Burger, Jiri Smid, Luke Verbugt, and Mathias Behangana (Department of Environmental Sciences, Makerere University) for providing tissue v samples. I also thank William R. Branch and Johan Marais for providing excellent photos of live snakes. Lastly, I would like to thank my fellow Greenbaum lab members for their advice and help throughout this project. vi ABSTRACT The Subfamilies Aparallactinae (collared snakes) and Atractaspidinae (burrowing asps) occur in multiple habitats throughout sub-Saharan Africa, and they include multiple poorly studied genera. The monophyly of these groups are well established, but relationships within the subfamilies are poorly known. My study contains samples from six of eight aparallactine genera, and both atractaspidine genera in the Middle East and sub-Saharan Africa. I employed concatenated gene-tree analyses, divergence dating approaches, ancestral- area reconstructions, ancestral-state reconstructions, morphological analyses, and taxonomic assessments to infer phylogenies, biogeographic patterns, and evolutionary histories with a multi-locus data set consisting of three mitochondrial (16S, cyt b, and ND4) and two nuclear genes (c-mos and RAG1). Diversification occurred predominantly during the Miocene, with a few speciation events occurring during the Pliocene and Pleistocene. Biogeographic analyses suggested that the Zambezian biogeographic region composed of grasslands and woodlands, facilitated radiations, vicariance, and dispersal for many aparallactines. Moreover, the ranges of many forest species were fragmented during xeric and cooler conditions, thus aiding in diversification events. Biogeographic patterns of aparallactine and atractaspidine snakes were consistent with previous studies on other sub-Saharan herpetofauna. Ancestral-state reconstructions suggested the ancestor to collared snakes and burrowing asps was rear- fanged with a broad diet. Multiple fang types have rapidly evolved within burrowing asps, allowing these snakes to exploit specific prey items. Additionally, current classification of collared snakes and burrowing asps is insufficient; herein a taxonomic revision was conducted including the description of two new species, the first collared snakes to be described in over 40 years. vii TABLE OF CONTENTS ACKNOWLEDGMENTS...................................................................................................................... iv ABSTRACT ..................................................................................................................................... vii TABLE OF CONTENTS .................................................................................................................... viii LIST OF TABLES ................................................................................................................................x LIST OF FIGURES ............................................................................................................................ xii CHAPTER 1: GENERAL INTRODUCTION .............................................................................................1 RESEARCH QUESTIONS AND OBJECTIVES ......................................................................15 REFERENCES .................................................................................................................18 CHAPTER 2: PHYLOGENY AND BIOGEOGRAPHY OF THE AFRICAN BURROWING SNAKE SUBFAMILY APARALLACTINAE (SQUAMATA: LAMPROPHIIDAE) ...............................................................27 2.1 INTRODUCTION .............................................................................................................27 2.2 MATERIALS AND METHODS ..........................................................................................29 2.3 RESULTS .......................................................................................................................44 2.4 DISCUSSION ..................................................................................................................54 REFERENCES .................................................................................................................64 CHAPTER 3: MOLECULAR PHYLOGENY OF ATRACTASPIDINAE (SQUAMATA: LAMPROPHIIDAE)......78 3.1 INTRODUCTION .............................................................................................................78
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