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Systematic Revision of the Neotropical Fruit Bats of the Genus Sturnira : A

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Systematic Revision of the Neotropical Fruit Bats of the Genus Sturnira : A SYSTEMATIC REVISION OF THE NEOTROPICAL FRUIT BATS OF THE GENUS Sturnira: A MOLECULAR AND MORPHOLOGICAL APPROACH By CARLOS ALBERTO IUDICA A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2000 Copyright 2000 by Carlos A. ludica This work is dedicated to Maria Eugenia Fullana Jornet, the most important person in my life and to John Frederick Eisenberg, an eminent scientist whose influential company will be missed after his retirement. ACKNOWLEDGMENTS This project would not have been possible without the help, support, and encouragement of many people. Most significantly, I thank John F. Eisenberg for suggesting the phylogeny of the entire genus Sturnira as a dissertation subject. W. Mark Whitten and Norris H. Williams guided me through all the lab work involved in this project. I thank them also for their willingness to maintain endless conversations on varied subjects, from science to history, from politics to life. For their suggestions during the planning stage, for assisting on every aspect of my work, and for helping me to process and interpret the data, I thank the members of my committee: Brian Bowen, Colin Chapman, John F. Eisenberg (Chairperson), Walter Judd, and Norris H. Williams. Although W. Mark Whitten was not a formal member of my committee, his daily contributions were essential to the development of this work and he deserves an honorary seat on my committee. I thank Wesley E. Higgins, Juan Manuel Alvarez, Savita Shankar, Ana "Sam" Bass, and Ginger A. M. Clark for their guidance on statistical and computer analyses, and for their valuable help in the lab. I am grateful to W. Mark Whitten and Norris H. Williams for allowing me to have unrestricted access to their computers and to the molecular systematic laboratory at the Florida Museum of Natural History. Funding for this project was provided by several agencies, institutions, and people. I thank The Lincoln Park Zoological Society for their "Scott Neotropical IV Fund," the National Museum of Natural History and the American Museum of Natural History for their "Collection Study Grants." Funding also was available through travel awards from the Department of Zoology, the Graduate Student Council, and the College of Liberal Arts and Sciences of the University of Florida. The McLaughlin Dissertation Fellowship from the University of Florida partially supported the last stages of this work. Special thanks are extended to the following institutions and people who kindly provided access to comparative specimens and tissue collections in their care: American Museum of Natural History, New York (Nancy B. Simmons, Karl F. Koopman, Brian Kraatz); Angelo State Natural History Collections, Angelo State University, San Angelo (Robert Dowler); Carnegie Museum of Natural History-Edward O'Neil Research Center, Pittsburgh (Timothy McCarthy, Sue McLaren, Duane Schlichter, John Wible); Centra de Ecologia, Universidad Nacional Autonoma de Mexico, Distrito Federal (Rodrigo Medellin, Ricardo Lopez-Wilches); Florida Museum of Natural History, University of Florida, Gainesville (Charles A. Woods, Laurie Wilkins, Candace McCaffery); The Field Museum, Chicago (Bruce D. Patterson, John Phelps); Museum of Natural Science, Louisiana State University, Baton Rouge (Mark S. Hafner, Shannon K. Allen, David Reed); Museum of Comparative Zoology, Harvard University, Cambridge (Maria E. Rutzmoser, Terri McFadden, Gail Pinderhughes); Museum d'histoire naturelle de la Ville de Geneve, Geneve; Museum of Southwestern Biology, University of New Mexico, Albuquerque (Terri Yates, William Gannon); Michigan State University, East Lansing; Museo de Historia Natural de la Universidad Mayor de San Marcos, Lima (Irma Franke, Elena Vivar, Sergio Solari); Museum of Vertebrate Zoology, University of California, Berkeley (James L. Patton, Carta Cicero); Museum of Zoology, University of Michigan, Ann Arbor (Phil Myers); United States National Museum of Natural History, Smithsonian Institution, Washington (Linda Gordon, Alfred L. Gardner, Charles O. Handley, Jr., Jeffrey F. Jacobs, Don E. Wilson); Oklahoma Museum of Natural History, University of Oklahoma, Norman (Michael Mares, Janet Braun); Royal Ontario Museum, Centre for Biodiversity and Conservation Biology, Toronto (Mark Engstrom, Lim Burton); Texas Cooperative Wildlife Collection, Department of Wildlife & Fisheries Sciences.Texas A&M University, College Station (Duane Schlitter, John W. Bickham); The Museum, Texas Tech University, Lubbock (Nicky Ladkin, Robert Baker, Ricardo Monk); University of Nebraska State Museum, Lincoln (Patricia Freeman, Thomas Labedz). Many of my fellow students and colleagues opened their intellects and invited me to fruitful discussions, creating the best academic environment at school. Their friendship and support were a constant source of advice. I am specially indebted to my friends for their comments and encouragement. My deepest gratitude goes to my wife Maria, whose love, understanding, patience, and support have been pivotal during these five years. She helped me out in periods of great stress and encouraged me to pursue and continue my work through her example of integrity and determination. I am truly grateful to her. vi PREFACE During the course of my masters research (ludica 1994) I observed the important ecological role that bats of the genus Sturnira have as seed dispersers fruit in northwestern Argentina. I became intrigued by the fact that among those bats there were three allied species with almost the same body size and (from what was known) probably the same dietary requirements. This overview of the ecological role of those bats in that particular rain forest provided the basic I for information that I used as a preamble for the problem that wanted to work on a Ph.D. dissertation. Together with Sturnira lilium, two other putative species of Sturnira were supposed to occur sympatrically in the mountain rainforest of northwestern Argentina. Tschudi (1844) described those two allied species as S. erythromos and S. oporaphilum. Not much was known about their ecology, other than what was assumed from studies of other related fruit bats and what was known from S. lilium, a much more common, widespread, and better studied species. S. erythromos is a well defined species with a restricted distribution on the eastern slopes of the Andes from northwestern Argentina to Ecuador. The other, S. oporaphilum represents a rather controversial taxon assignment (see below on current status of Sturnira), and little was known about its ecology. I decided to analyze the status of these three co-occurring species in northwestern Argentina in an effort to resolve their taxonomic status. My Ph.D. advisor, Dr John F. Eisenberg, suggested that I embrace the entire problematic VII genus instead of just doing a partial overview of three species of Sturnira. Without realizing the challenge, I naively embarked in what was a new journey for me. I then resolved to change my PhD project from being an ecological description of resource partitioning among three sympatric fruit bat species into a systematic review of the phylogeny of the entire genus Sturnira. In 1996 the molecular systematics of bats was already an accepted taxonomic tool. I decided to explore the evolutionary history of Sturnira by combining at that time the most up-to-date techniques in molecular systematics with the traditional, low- budget (and most "trustworthy" for many), morphological approach. The ultimate goal was to obtain hard evidence to explain and describe the systematic status and phylogenetic relationships among species of the genus Sturnira. viii . TABLE OF CONTENTS Page ACKNOWLEDGMENTS iv PREFACE vii ABSTRACT xii 1 INTRODUCTION 1 Systematic Background and Current Status of Sturnira 1 The Importance of a Phylogeny Based on DNA: Why Use the Cytochrome b Gene? 6 2. MATERIALS AND METHODS 16 Morphological Data 16 Molecular Data 18 DNA Extraction, Polymerase Chain Reaction (PCR), and Sequencing 18 DNA isolation and extraction 18 Gene amplification, PCR, and sequencing 22 Search Strategies 24 3. RESULTS 35 All Available DNA Sequences and Selected Specimens 35 The Large Data Set: 133 Specimens (4 Outgroup Species and 129 Sturnira Specimens) 35 The Small Data Set: 37 Specimens (4 Outgroup Species and 33 Sturnira Specimens) 40 The DNA data set 40 The morphological data set 42 Combined data--DNA and morphological data sets 43 Pairwise Distances 45 Patterns of Character Evolution: Selected Cases 46 ix DISCUSSION 185 The Corvira Complex 1 89 The Ludovici Complex 1 90 The Luisi Complex 1 94 Lilium The Complex 1 97 The Entire "Well Defined Lingual Cusps" Group 198 The Remaining Species 199 Pairwise Distances 201 The Whole Picture: The Genus Sturnira 201 Final Remarks 203 APPENDIX 1 INSTITUTIONAL NAMES 219 APPENDIX 2 MORPHOLOGICAL CHARACTERS 221 APPENDIX 3 SPECIMENS MEASURED 223 APPENDIX 4 QUALITATIVE CHARACTERS 243 APPENDIX 5 CHARACTER MATRIX 247 APPENDIX 6 TISSUE SAMPLES 248 APPENDIX 7 LIST AND FORMULAE OF STOCK SOLUTIONS USED IN THE DNA EXTRACTION OF TISSUE SAMPLES 261 APPENDIX 8 FINAL SEQUENCES 262 REFERENCES 272 BIOGRAPHICAL SKETCH 284 Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy SYSTEMATIC REVISION OF THE NEOTROPICAL FRUIT BATS OF THE GENUS Sturnira: A MOLECULAR AND MORPHOLOGICAL APPROACH By Carlos Alberto ludica December
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