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JOHNSON N.Pdf GENETIC INVESTIGATIONS REVEAL NEW INSIGHTS INTO THE DIVERSITY, DISTRIBUTION, AND LIFE HISTORY OF FRESHWATER MUSSELS (BIVALVIA: UNIONIDAE) INHABITING THE NORTH AMERICAN COASTAL PLAIN By NATHAN ALLEN JOHNSON 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 2017 © 2017 Nathan Allen Johnson To all my collaborators, colleagues, family, and friends who helped make this endeavor a success ACKNOWLEDGMENTS This work would not have been completed without the guidance, friendship, support and assistance of my advisors, committee members, colleagues, and loved ones. My advisor, Dr. Jim Austin, provided continuous guidance and stimulus throughout my graduate career and above all, gave me total freedom to pursue a research project that piqued my interests. I also express my gratitude to Dr. Jim Williams for sharing his wealth of knowledge on aquatic fauna and for all his time and effort traveling around the “southeast corner” of the US making collections for this project and connecting me to a network of aquatic biologists around the world. Many thanks to the rest of my graduate committee, Dr. Mark Brenner, Dr. Tom Frazer, and Dr. Gustav Paulay who were always available for important discussions regarding my research and extremely helpful through all the steps of my graduate career. I give special thanks to Dr. Ken Rice, Howard Jelks, and Gary Mahon who provided continued support for my dissertation research, publications, and development of my freshwater mussel research program at the U.S. Geological Survey Wetland and Aquatic Research Center in Gainesville, Florida. I also give special thanks to my fellow graduate students and laboratory mates (Andrew Barbour, Jason Butler, John Hargrove, Aria Johnson, Matt Lauretta, James Nifong, Wade Ross, Emily Saarinen, Matt Shirley, and Joe Townsend), and dozens of mussel biologists, laboratory technicians, USGS colleagues, and museum staff who provided logistical support or helped with specimen collection, laboratory data collection, and curation for my projects (Caitlin Beaver, Mandy Bemis, Amy Benson, Tim Boozer, Ben Bosman, Sherry Bostick, Mike Buntin, Lyuba Burlakova, Bob Butler, Patricia Caccavale, Celine Carneiro, Janet Clayton, Mike Cordova, Kevin Cummings, Gerry Dinkins, Drew Dutterer, Scott Faiman, 4 Todd Fobian, Paul Freeman, Mike Gangloff, Jeff Garner, John Harris, Mike Hart, Paul Hartfield, Libby Hartfield, Karen Herrington, Jordan Holcomb, Bob Howells, Maggie Hunter, Ben Hutchins, Jaclyn Irwin, John Johansen, Matt Johnson, Paul Johnson, Bob Jones, Jess Jones, Ben Lundeen, Steve McMurray, John Moran, Bruce Moring, Cheryl Morrison, Particia Morrison, Eric Nagid, Susan Oetker, Michael Perkins, Heather Perry, John Pfeiffer, Emma Pistole, Tracey Popejoy, Jeff Powell, Sandy Pursifull, Morgan Raley, Charles Randklev, Clint Robertson, Kevin Roe, Matt Rowe, Shane Ruessler, Sara Seagraves, Colin Shea, Shawna Simpson, Joe Skorupski, Todd Slack, John Slapcinsky, Chase Smith, Charrish Stevens, Carson Stringfellow, Jeremy Tieman, Eric Tsakris, Travis Tuten, Brian Watson, Carla Wieser, Jason Wisniewski, and Craig Zievis). Funding for this project was provided by Florida Fish and Wildlife Conservation Commission, U.S. Fish and Wildlife Service, and U.S. Geological Survey. Ultimately, support from my loved ones provided me the strength and motivation to complete such a large, selfish undertaking. My parents, John Johnson and Karen True, nurtured my hunger for knowledge from birth and continue to this day. I also give special thanks to my siblings for always pushing me to achieve my dreams. Last, and most importantly, to my amazing wife, Antonia, who provided unwavering love, support, and inspiration during the purist of my professional aspirations. 5 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 8 LIST OF FIGURES .......................................................................................................... 9 LIST OF ABBREVIATIONS ........................................................................................... 11 ABSTRACT ................................................................................................................... 12 CHAPTER 1 INTRODUCTION .................................................................................................... 14 2 USING DNA BARCODES TO RECALIBRATE TAXONOMY, TEST MISIDENTIFICATION RATES, AND UNCOVER PATTERNS OF GENETIC DIVERSITY IN FRESHWATER MUSSELS (BIVALVIA: UNIONIDAE) ................... 23 Methods .................................................................................................................. 27 Taxon Sampling and Data Collection ............................................................... 27 Data Analyses .................................................................................................. 30 Results .................................................................................................................... 32 Misidentifications .............................................................................................. 33 Barcode Gap Analyses ..................................................................................... 34 Shallow Interspecific Divergence and Non-monophyletic Species ................... 35 Cases of Deep Intraspecific Divergence and Putative Cryptic Diversity ........... 37 Anodontini .................................................................................................. 37 Lampsilini ................................................................................................... 39 Pleurobemini .............................................................................................. 41 Quadrulini................................................................................................... 41 Discussion .............................................................................................................. 42 3 APPLYING DNA BARCODES TO INVESTIGATE ECOLOGICAL HOST ASSOCIATIONS AND SPECIES BOUNDARIES FOR FRESHWATER MUSSELS ............................................................................................................... 82 Methods .................................................................................................................. 85 Specimen Collection ......................................................................................... 85 DNA Sequencing and Data Analyses ............................................................... 86 Results .................................................................................................................... 88 Reference DNA Barcode Library ...................................................................... 88 Juvenile Mussel Identification and Host Fish Characterization ......................... 90 Discussion .............................................................................................................. 93 DNA Barcode Reference Library ...................................................................... 93 6 Importance of DNA Reference Libraries ........................................................... 94 Shallow Interspecific Divergence ...................................................................... 94 Deep Intraspecific Divergence .......................................................................... 95 Misidentifications .............................................................................................. 95 Fish Hosts ........................................................................................................ 96 4 INTEGRATIVE TAXONOMY RESOLVES GENERIC PLACEMENT AND SPECIES BOUNDARIES FOR IMPERILED FRESHWATER MUSSELS ............. 114 Methods ................................................................................................................ 117 Taxon Sampling and Molecular Data ............................................................. 117 Phylogenetic and Phylogeographic Analyses ................................................. 118 Morphometric Analyses .................................................................................. 120 Results .................................................................................................................. 121 Taxon Sampling and Molecular Analyses....................................................... 121 Morphometric Analyses .................................................................................. 123 Discussion ............................................................................................................ 124 Implications for Taxonomy and Conservation ................................................. 126 Discussion of Generic-level Relationships...................................................... 127 5 CONCLUSIONS ................................................................................................... 138 LIST OF REFERENCES ............................................................................................. 142 BIOGRAPHICAL SKETCH .......................................................................................... 159 7 LIST OF TABLES Table page 2-1 The number and percentage of freshwater mussel misidentifications revealed
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