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Genetic Diversity and Distribution of the Ringed Salamander

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Genetic Diversity and Distribution of the Ringed Salamander GENETIC DIVERSITY AND DISTRIBUTION OF THE RINGED SALAMANDER (AMBYSTOMA ANNULATUM) ACROSS MULTIPLE SPATIAL SCALES A Dissertation presented to the Faculty of the Graduate School at the University of Missouri In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy by JACOB JONATHON BURKHART Dr. Lori S. Eggert, Dissertation Co-Advisor Dr. Raymond D. Semlitsch, Dissertation Co-Advisor JULY 2018 The undersigned, appointed by the dean of the Graduate School, have examined the dissertation entitled GENETIC DIVERSITY AND DISTRIBUTION OF THE RINGED SALAMANDER (AMBYSTOMA ANNULATUM) ACROSS MULTIPLE SPATIAL SCALES Presented by Jacob J. Burkhart, a candidate for the degree of Doctor of Philosophy, and hereby certify that, in their opinion, it is worthy of acceptance. ____________________________________ Professor Raymond D. Semlitsch ____________________________________ Professor Lori S. Eggert ____________________________________ Professor Reginald B. Cocroft ____________________________________ Professor Ricardo M. Holdo ____________________________________ Professor Matthew E. Gompper ACKNOWLEDGEMENTS I have had the good fortune of being surrounded by many supportive individuals throughout my academic career. First and foremost, I will be forever grateful to my dissertation advisors, Ray Semlitsch and Lori Eggert, for taking the chance on the wide- eyed and overly eager student who showed to interview for graduate school. With their encouragement and guidance, I am better able to focus on the bigger picture concepts and questions rather than on esoteric observations and harebrained schemes. I will always draw upon the advice and insight that Ray imparted during our conversations about research and life in our limited time working together. Similarly, I am grateful to Lori for her constant support and encouragement while allowing me the freedom to mentor undergraduate researchers and pursue research questions ancillary to my dissertation. Finally, I will be forever grateful to Brad Swanson for introducing me to ecological research. Words cannot express how thankful I am to have had all of you as mentors. I owe many thanks to my committee members – Matt Gompper, Rex Cocroft, and Rico Holdo – and faculty in the Division of Biological Sciences for playing a more active role in my graduate education than all of us anticipated. Rex’s insight and expertise were invaluable for many of my research projects whereas Matt and Rico provided vital assistance for analyzing and interpreting my data. Lastly, Manuel Leal served as an informal mentor who provided feedback for manuscripts and research questions. I am ever grateful to Manuel for letting me participate in lab his meetings and challenging me to think critically about ecological and evolutionary theory ancillary to my research foci. While at Mizzou, I have been surrounded by many amiable, generous, intelligent, and hard-working graduate students and lab mates. I am particularly grateful to members ii of the Semlitsch and Eggert labs, past and present, as well as other members of Tucker 2. I will be forever grateful for the encouragement, informal teaching, laughs, and sage wisdom that I received throughout my graduate career from Arianne Messerman, Bill Peterman, Britt Ousterhout, Dana Drake, Emily Puckett, Freya Rowland, Grant Connette, Holly Puglis, Joe Gunn, Katie O’Donnell, Kris Budd, and Rachelle Riegerix. Further, I had the pleasure of working with many fantastic undergraduate researchers: Adam Koenig, Chelsey Kroese, Christine Sholy, Emily Brocato, Kim Romine, Maddie Willis, Piper Stretz, and Stephanie Ruck. Thank you for your hard work, excitement, and patience while conducting research together. Good luck with your future endeavors. I have received support from the tremendous DBS staff members – Alan Marshall, Barb Sonderman, Josh Hartley, Melody Kroll, Nila Emerich, Rebecca Ballew, Saadiya Aswad, and Steve Heinrich – that has not gone unnoticed. Further, Richard Daniel was a critical resource for me as a teaching assistant and a researcher. Without his assistance, much of my dissertation research would not have been feasible. Finally, I would like to thank my family and friends. My parents, Arne and Kay, for encouraging me to pursue my passions and to never stop learning. My siblings and in- laws – Heidi, Heather and Chad, Joe, Nikolas and Theresa, Holly and David – for being role models, compatriots, and sounding boards over the years. Gretta for helping me stay sane and fed during the stressful times. Alice, Austin, Chelsea, Daniel, Ellee, Katie, Keala, Levi, Marco, and Ronnie for the game nights, potlucks, and discussions. Lastly, Grandma Mary for instilling a curiosity for the natural world through her love of bird- watching, and for sharing her honey wheat bread recipe that I used for many a PB&J. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS.……………………………………………..……………...ii LIST OF TABLES……...……………………………………………………………….vi LIST OF FIGURES...……………………...…………………………………………..viii ABSTRACT………………………………………………………………………………x CHAPTER 1 • INTRODUCTION INTRODUCTION..………….………………………………………………………..1 LITERATURE CITED…...……………………………………………………………4 CHAPTER 2 • POST-PLEISTOCENE DIFFERENTIATION IN A CENTRAL INTERIOR HIGHLANDS ENDEMIC SALAMANDER ABSTRACT…………………………………………………………………………6 INTRODUCTION………………………………………………………………...…..7 MATERIALS AND METHODS………………………………………………………12 RESULTS..………………………………………………………………………...17 DISCUSSION..……………………………………………………………………..21 ACKNOWLEDGEMENTS..…………………………………………………………..25 LITERATURE CITED……………………………………………………………….27 CHAPTER 3 • THE INFLUENCE OF BREEDING PHENOLOGY ON THE GENETIC STRUCTURE OF FOUR POND-BREEDING SALAMANDERS ABSTRACT………………………………………………………………………..42 INTRODUCTION…………………………………………………………………...43 MATERIALS AND METHODS………………………………………………………48 RESULTS..………………………………………………………………………...53 DISCUSSION..……………………………………………………………………..56 iv ACKNOWLEDGEMENTS..…………………………………………………………..62 LITERATURE CITED……………………………………………………………… 64 CHAPTER 4 • TESTING THE EFFICACY OF TERRESTRIAL ‘LIFE ZONES’ FOR THE ENDEMIC RINGED SALAMANADER ABSTRACT………………………………………………………………………..80 INTRODUCTION…………………………………………………………………...81 MATERIALS AND METHODS………………………………………………………84 RESULTS..………………………………………………………………………...90 DISCUSSION..……………………………………………………………………..92 ACKNOWLEDGEMENTS..…………………………………………………………..95 LITERATURE CITED……………………………………………………………….97 CHAPTER 5 • CONCLUSIONS CONCLUSIONS……………...……………………………………………………109 LITERATURE CITED…………………………………………………………..….113 APPENDIX A • ADDITIONAL RANGE WIDE GENETIC DIVERSITY ESTIMATES AND SUMMARIES.………………………………..115 APPENDIX B • DETAILED SUMMARIES OF GENETIC DIVERSITY AND LANDSCAPE RESISTANCE FOR FOUR CO-OCCURRING SALAMANDER SPECIES…………………………..…………….119 APPENDIX C • ADDITIONAL MOVEMENT SUMMARIES FOR AMBYSTOMA ANNULATUM……………………….…………….134 VITA...…………………………………………………………………………………135 v LIST OF TABLES Chapter 2. Table 1. Genetic diversity statistics for microsatellite DNA………………….....35 Table 2. Microsatellite DNA pairwise genetic and geographic distance matrix...36 Table 3. Mitochondrial DNA genetic diversity summary statistics……………...37 Table 4. Demographic parameter estimates……………………………………...38 Chapter 3. Table 1. Summary of samples collected by species.….….………………………72 Table 2. Genetic diversity summaries by species….….…………………………73 Table 3. Landscape resistance model rankings by species….….…………..........74 Chapter 4. Table 1. Summary of landscape characteristics…...……………………………102 Table 2. Summary of demographic and movement data by individuals………..104 Appendix A. Table A1. Estimates of contemporary migration rates between sampling sites..115 Table A2. Mitochondrial DNA pairwise genetic and geographic distance matrix……………………………………………………....……..…116 Appendix B. Table B1. Genetic diversity metrics for A. annulatum……………………........119 Table B2. Genetic diversity metrics for A. opacum...........…………....………..121 Table B3. Genetic diversity metrics for A. maculatum……………………........122 Table B4. Genetic diversity metrics for N. v. louisianensis...………....………..123 Table B5. Pairwise genetic and geographic distance matrix for A. vi annulatum……………………...........................................................124 Table B6. Pairwise genetic and geographic distance matrix for A. opacum...........…………....…………………………………….……126 Table B7. Pairwise genetic and geographic distance matrix for A. maculatum…………………………………...…………………........127 Table B8. Pairwise genetic and geographic distance matrix for N. v. louisianensis........…………....………………………………………128 Appendix C. Table C1. Movement summaries by sex and pond……………………………..134 vii LIST OF FIGURES Chapter 2. Figure 1. Geographic distribution, historic localities, and sampling locations for Ambystoma annulatum populations…...………………..….………39 Figure 2. Spatial distribution of genetic clustering assignments………………...40 Figure 3. Median joining haplotype network.….….….….………………………41 Chapter 3. Figure 1. Photographs of study organisms ……………………………………...76 Figure 2. Map of sampling locations overlaid on land use-land cover data……..77 Figure 3. Spatial distribution of genetic clustering assignments by species….….78 Figure 4. Isolation by distance summary plot by species……….……………….79 Chapter 4. Figure 1. Map of study area and individual movements……………...………...106 Figure 2. Summary of net displacement and total distance moved by sex…..…107 Figure 3. Summary of movement and precipitation data.…..…………………..108 Appendix A. Figure A1. Isolation by distance plot for microsatellite data……………...……117 Figure A2. Spatial arrangement of mitochondrial DNA haplotypes...…………118
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