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The Wide Distribution of the Same Species, and of Closely Allied Species of Freshwater Shells Must Have Surprised Every One Who Has Attended to the Subject.”

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The Wide Distribution of the Same Species, and of Closely Allied Species of Freshwater Shells Must Have Surprised Every One Who Has Attended to the Subject.” “The wide distribution of the same species, and of closely allied species of freshwater shells must have surprised every one who has attended to the subject.” - C. Darwin, 1882. Nature. 26: 529-530. Exploring Levels of Genetic Variation in the Freshwater Mussel Genus Villosa (Bivalvia Unionidae) at Different Spatial and Systematic Scales: Implications for Biogeography, Taxonomy, and Conservation Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Kody F. Kuehnl, B.S., M.S. ***** The Ohio State University 2009 Dissertation Committee: Approved by Professor Marymegan Daly, Co-Advisor Professor G. Thomas Watters, Co-Advisor _________________________________ Professor H. Lisle Gibbs Advisor Graduate Program in Evolution, Professor Elizabeth A. Marschall Ecology, and Organismal Biology Copyright by Kody F. Kuehnl 2009 Abstract Freshwater mussels (Family Unionidae) are one of the most imperiled groups of animals in North America with approximately 75% of the currently recognized species listed by federal or states as endangered, threatened or species of concern. Despite this designation, conservation of freshwater mussels has been extremely difficult being limited by an inadequate knowledge of even the most basic principles of biology (e.g. life history, reproductive biology, ecology, habitat requirements, etc). Two of these that continue to pose challenges to the conservation of this important group of animals include; identification of 1) taxonomic units appropriate for conservation, and 2) criteria useful for the establishment or re-establishment of populations of freshwater mussels that are endangered, threatened, or species of concern. To address issues associated with the identification of freshwater mussels we employed a modern phylogenetic approach using an enigmatic and important group of unionids (Villosa) in order to assess ambiguities in taxonomic position and delineate species boundaries. We used nucleotide sequences of the cytochrome oxidase I subunit (COI) and NADH dehydrogenase I (NDI) subunit of the mitochondrial DNA (mtDNA) genome to infer taxonomic boundaries and to provide a more relevant phylogenetic framework within the Unionidae. We also used a nearly panmictic species, Villosa iris, to address patterns of speciation associated with observed ii morphological variation in a small river taxon which also allowed us to evaluate existing hypotheses regarding the evolution of drainage basins of the eastern U.S. Lastly, we provide a set of criteria that should be addressed for conservation activities associated with the relocation, translocation, and reintroduction of freshwater mussels. Our assessment of Villosa iris revealed multiple cryptic species across the range of this taxon that correlate with vicariant events associated with the evolution of major drainages throughout the eastern U.S. (Chapter 2). Our phylogenetic studies also revealed a polyphyletic Villosa comprised of at least 9 clades that include species from five different genera (Chapter 3). These studies indicate 1) that current systematics for Villosa is largely inadequate, 2) morphological (conchological) characters used to diagnose taxonomic boundaries within the Villosa in most instances are not useful, 3) a modern phylogenetic approach is necessary for accurate identification of evolutionary lineages within unionids, 4) modern phylogenetic methods will aid in implementing appropriate conservation strategies. Finally, using two federally endangered freshwater mussels, Pleurobema clava and Epioblasma torulosa rangiana; we provide a framework for evaluating potential sites for relocation, translocation, and reintroduction in two Ohio watersheds. This framework includes a discussion of past and current threats, conservation activities, and identifies biological and physical criteria that can be used to evaluate potential sites for conservation activities. iii Dedicated to Amy Dawn, Emily Lynn, Ella Ann, Claire Elizabeth, and Gabriel David Kuehnl iv Acknowledgements I believe it is accurate to say that the process of obtaining a doctorate is unattainable without the generosity of others. Indeed, this process requires numerous sacrifices from a plethora of individuals; I am grateful now to have the opportunity to acknowledge them here. My sincerest gratitude goes out to the many friends, colleagues, and faculty members that have helped me throughout this lengthy and often times difficult process. I am especially grateful and appreciative to Dr. Tom Watters who not only provided me with the opportunity to pursue my doctorate, but who also expanded my intellectual horizons by introducing me to a unique and very charismatic group of animals that I knew nothing about, and which I still claim to know very little about. Without his support, kindness, and willingness to indulge me in doing a molecular based work (something I am sure still causes him great consternation), little of this work would have been possible. I am also deeply indebted to Dr. Meg Daly whose support, guidance, and dedication to mentoring provided me with the strength and optimism I needed in order to navigate this very unique and often times precarious journey. Her encouragement was constant, her guidance always on target, and her advice always came at a timely manner. v One could not ask nor expect more dedication than I have had from my dissertation committee. Drs. Lisle Gibbs and Libby Marschall were fantastic committee members; supportive, patient, and understanding, especially during the early formulation of my dissertation when it seemed to take a new direction weekly. Both offered their labs, their encouragement, and their wisdom at critical points during my dissertation. I greatly appreciate the significant contributions they have invested in me during this process. I would like to thank Jose Diaz, whose laboratory assistance and skill at troubleshooting problems while keeping every critical piece of equipment operating was both uncanny and unnerving at the same time. I would also like to thank Drs. Laura Salter-Kubatko and Alexandros Stamatakis for taking the time out of their incredibly busy schedules to help me troubleshoot various molecular analysis programs. There have, of course, been numerous others whose professionalism, advice (scientific and not), and friendship have made a significant difference in the pursuit of my doctorate and also in my life while at Ohio State. Of these I would like to thank the members of the Daly Lab; especially Fani Rodriguez, Annie Lindgren, Luciana Gusmao, Esprit Heestand, Abby Reft; the Fuerst Lab, especially Mike Sovic, and Jen Carmichael; the Gibbs lab, especially Katy Greenwald, Jimmy Chiucchi, Tony Fries, Christine Anderson, Angelika Poesel, and Kristin Mylecraine; the Aquatic Ecology Lab, especially Jason Van Tassell, Joe Beuchel, Janelle Bigrigg, Samantha Fedor, Paris Collingsworth, Melissa Marburger, Barbara Fate, and Dr. Roy Stein, and the Columbus Zoo and Aquarium’s Freshwater Mollusc Conservation and Research Facility, especially Brooke Smith, Trisha Gibson, Mike Brittsan, Doug Warmolts, Marc Kibbey, Kristi Harraman, vi Hope Valentine, and Dr. Barb Wolfe. I would also like to thank Drs. John Freudenstein and John Wenzel for their help and encouragement. Looking back on this endeavor, it really is quite amazing the people that come into your life precisely at the moment you are in need; each one of these individuals fulfilled this role for me at different times throughout my dissertation, and for that I am deeply thankful. I appreciate the contributions of several undergraduates I have had the opportunity to mentor on several aspects of this work, especially Roxana Capper and MiLinda Nimmo. They each helped me to think more clearly about various problems associated with this research and provided substantial laboratory assistance. I owe many thanks to the efforts of numerous clam diggers, noodlers, and all around fantastic malacologists who procured tissue samples for my molecular work, especially Chris Barnhart, Art Bogen, Jen Buhay, David Campbell, Alan Christian, Jacob Culp, Kevin Cummings, Mike Eackles, Nathan Eckert, Ryan Evans, Brant Fisher, Neil Ford, Steve Fraley, Wendell Haag, Randy Hoeh, Paul Johnson, Jess Jones, Tim L. King, Stuart McGregor, Monte McGregor, Jim Layzer, Mike Patterson, Tim Pearce, Bernard Sietman, Jamie Smith, Dan Spooner, Robert Szafoni, Sara Thomas, Caryn Vaughn, and Greg Zimmerman. Project funding came primarily from the Ohio Division of Wildlife, Department of Natural Resources as a Research Associate through a Section 6 (Endangered Species Program, Cooperative Endangered Species Conservation Fund) grant to Dr. Tom Watters and the Columbus Zoo and Aquarium’s Freshwater Mollusc Conservation Research Facility. The Ohio State University supported me with a Helen M. and Milton O. Lee vii Fellowship and the Department of Evolution, Ecology, and Organismal Biology supported me as a Teaching Associate and with travel grants. Ultimately, the opportunity and completion of such a large undertaking comes down to family, of which I have been blessed beyond measure. My parents provided me with countless opportunities to advance my education and were always supportive in every endeavor I undertook. I am especially thankful to my father, David Kuehnl, for instilling in me his love of nature and all living things which gave me the desire to pursue knowledge of all critters large and small, whether charismatic
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