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Copyright by Gregory Blair Pauly 2008 Copyright by Gregory Blair Pauly 2008 The Dissertation Committee for Gregory Blair Pauly Certifies that this is the approved version of the following dissertation: Phylogenetic Systematics, Historical Biogeography, and the Evolution of Vocalizations in Nearctic Toads (Bufo) Committee: David C. Cannatella, Co-Supervisor David M. Hillis, Co-Supervisor James J. Bull Michael J. Ryan Robin R. Gutell Phylogenetic Systematics, Historical Biogeography, and the Evolution of Vocalizations in Nearctic Toads (Bufo) by Gregory Blair Pauly, B.S. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin August 2008 Dedication To my parents, Matthew and Georgia, for many years of support and encouragement. Acknowledgements Many people have contributed to my dissertation research and to the earlier path that brought me to this point. First, I thank my parents, Matthew and Georgia, for their lifelong support and constant encouragement of my interests in science, the outdoors, and all things herpetological. I also thank my sister, Sara, and extended family for their encouragement. My family's appreciation of education, hard work, and the natural world has strongly influenced my career choices and contributed to my love of biology. I am truly grateful to the research opportunities provided to me by Brad Shaffer and Arthur Shapiro during my undergraduate career. Their mentorship was critical to my development as an academic biologist. In particular, in my first month as an undergraduate researcher in Brad Shaffer's lab, I went from a stressed out senior with no idea of what I would do after graduating to knowing what I would do for the rest of my life. This is a gift for which I will always be grateful. And to Art Shapiro, who threatened to stop paying me until I talked with Brad, thanks for recognizing what I should be doing when I had not yet figured it out for myself. My advisors and committee members (David Cannatella, David Hillis, Mike Ryan, Jim Bull, and Robin Gutell) have been excellent teachers, mentors, and friends. As my advisors, David Cannatella and David Hillis, have been extremely supportive of my work, spent countless hours critiquing drafts of manuscripts and grants, and also v introduced me to the culinary treats of Christmas Gumbo and venison. Though not formally my advisor, Mike Ryan kindly welcomed me into his lab and has served as an unofficial and very active advisor throughout my time in Austin. My work on sexual selection and mating signals has greatly benefited from interactions with Mike and his students. Over the course of my undergraduate and graduate career, I have met many friends who have contributed to my research and scientific growth. For setting excellent examples of how to succeed in graduate school and academia, and for friendships that extended well beyond Storer Hall and Patterson Labs, I am tremendously thankful to Rafe Brown, Cat Darst, Tracy Heath, Jeff Oliver, Katy Prudic, and the Baja Boys—Mike Benard, Darrin Hulsey, and Tom Near. My great aunt, Elizabeth H. Swope, my good friend and early mentor, Warren Brown, and my friend, mentor, and collaborator, A. Stanley Rand, each passed while I was in graduate school. These individuals are from different parts of my life, but each has been a great source of inspiration and encouragement. I am fortunate to have been able to call them friends and grateful for their years of support. As an official or unofficial member of the Cannatella, Hillis, Bull, and Ryan labs, I have had the chance to interact with many great people and talented graduate students. I thank the members of these labs for their contributions to my work and their friendships. There are too many names to list them all here, but they have helped make Texas a great place to be a graduate student. Below, I acknowledge some of these individuals for their contributions to specific chapters. vi For Chapter 1, I thank my collaborators on this research, David Cannatella and David Hillis. We thank Rafe Brown, Cat Darst, Ben Evans, Alisha Holloway, and especially Derrick Zwickl for assistance in the lab and/or with analysis; Chris Bell, Gabe Bever, Susan Masta, Dan Mulcahy, and Jenny Pramuk for insightful conversations about Bufo; Ulrich Mueller and Rachelle Adams for access to an automated sequencer; Nestor Basso, Rafe Brown, Jonathan Campbell, Carla Cicero and David Wake (Museum of Vertebrate Zoology, University of California, Berkeley), Joe Collins, Anna Graybeal, Ron Heyer and Roy McDiarmid (United States National Museum), Randy Jennings, Travis LaDuc, Dan Mulcahy, Andy Price, Michelle VanVleet (US Fish and Wildlife Service), and Jens Vindum (California Academy of Sciences) for providing tissue samples; and Carla Cicero, Meredith Mahoney, and David Wake (Museum of Vertebrate Zoology, University of California, Berkeley) for providing access to voucher specimens. The curatorial assistance provided by Travis LaDuc and Jessica Rosales (Texas Memorial Museum) is gratefully acknowledged. Previous versions of the manuscript were improved by comments from the Cannatella lab group, Rafe Brown, Joe Mendelson, Anne Yoder, Derrick Zwickl, and an anonymous reviewer. The use of Phylocluster for computational analyses was made possible by a NSF IGERT grant in Computational Phylogenetics and Applications to Biology (DGE-0114387). We also acknowledge the National Science Foundation for funding from NSF grant DEB-9981631. For Chapters 2 and 3, I thank Mike Ryan, David Cannatella, and David Hillis for helpful advice on this research and for providing comments that greatly improved these chapters. I am grateful to Mike Ryan and Thomas Keller for developing programs used for call analyses. Tracy Heath and Jeremy Brown provided assistance with the vii phylogenetic analyses. Santiago Ron, Emily Moriarty Lemmon, Ximena Bernal, and Rachel Page are fellow frog voyeurs who were always up for talking about frogs, sexual selection, phonotaxis, and mating signal evolution. Access to preserved specimens was provided by Jim McGuire and David Wake (MVZ), Jens Vindum (CAS), Brad Hollingsworth and Angelo Soto-Centeno (SDSNH), Roy McDiarmid and Steve Gotte (USNM), David E. Green and Stephanie Steinfeldt (USGS-NWHC), Wayne Roberts (UAMZ), Brad Shaffer (UCDMZ), Gavin Hanke (RBCM), Rafe Brown (KU), Steve Rogers (CM), John Friel (CU), and David Cannatella and Travis LaDuc (TNHC). Access to critical localities and/or logistical support was provided by Blake Hossack and Steve Corn (Aldo Leopold Institute, USGS), Lynn Verlanic and Ray Washtak (Lost Trail National Wildlife Refuge, Montana), Rebecca Wahl (University of Montana), Gale Bustillos (USFS), Ross Chapman (Elk Island National Park, Alberta), the kind staff of Meanook Biological Research Station (University of Alberta), and Cynthia Paszkowski, Connie Browne, Brian Eaton, and Cameron Stevens (University of Alberta). I especially thank the Spence and Miller families of Meanook, Alberta and Ron and Genevieve Bowman of Descanso, California who kindly provided access to their property; without their generosity this research would not have been possible. Bob Armstrong, Rod Brown, Richard Carstensen, Charlie Crisafulli, Joe Cook, Gary Fellers, Paul Hamby, Blake Hossack, Lance Lerum, Stephen MacDonald, John McDermott, Sam Sweet, and Sandra Talbot provided field assistance and/or tissue samples. This work was supported by a NSF Doctoral Dissertation Improvement Grant (No. 0508542) under IACUC protocol 02112201 and an NSF IGERT Fellowship in Computational Phylogenetics and Applications to Biology (DGE-0114387). Additional support was provided by the viii Society for the Study of Amphibians and Reptiles, the American Society of Ichthyologists and Herpetologists, The Explorer’s Club, and fellowships from the University of Texas, Austin. For Chapter 4, I thank my collaborators on this research, Robin Gutell and Jamie Cannone, who provided much insight into RNA secondary structure and methods for its analysis. David Cannatella and David Hillis provided helpful insights and discussions on this research and have encouraged all aspects of my research on bufonids. Funding was provided by a NSF IGERT fellowship in Computational Phylogenetics and Applications to Biology (DGE-0114387). ix Phylogenetic Systematics, Historical Biogeography, and the Evolution of Vocalizations in Nearctic Toads (Bufo) Publication No._____________ Gregory Blair Pauly, Ph.D. The University of Texas at Austin, 2008 Supervisors: David C. Cannatella and David M. Hillis The evolution of mating signals has long interested biologists because changes in mating signal production and/or reception can lead to reproductive isolation and speciation. Here, I examine the evolution of the male mating signal (the advertisement call) and the female preference for this call in the Western Toad, Bufo boreas. Call surveys and a morphological study for the occurrence of vocal sacs, which are necessary for producing these calls, reveal that only populations in the northeastern corner of this species’ range produce long, high-amplitude advertisement calls. This is the first study to report among-population variation in the presence of the major mating signal in any animal. Although populations vary in whether or not males call, phonotaxis tests demonstrate that female B. boreas in calling and non-calling populations have the preference for this call. Phylogenetic analyses indicate that the call
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