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Genetic, Physiological, and Ecological Consequences of Sexual and Kleptogenetic Reproduction in Salamanders

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Genetic, Physiological, and Ecological Consequences of Sexual and Kleptogenetic Reproduction in Salamanders Genetic, physiological, and ecological consequences of sexual and kleptogenetic reproduction in salamanders DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Robert Daniel Denton Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2017 Dissertation Committee: H. Lisle Gibbs, Advisor Bryan Carstens William Peterman Copyrighted by Robert Daniel Denton 2017 Abstract Every year, there is at least one widespread news story documenting a “virgin birth” in a variety of animals as diverse as snakes and sharks. These events capture our attention because they represent departures from an assumed necessity of vertebrate life: having sex. Yet, vertebrates do not always reproduce via sex, and biologists have long studied the evolutionary costs and benefits of this type of reproduction. One of the main costs of sex are males, who cannot directly generate offspring and use up resources from reproductive females that cannot be put towards additional offspring. Eastern North America is home to one of the strangest vertebrates that lack males and appear to be sexual and asexual at the same time: an all-female group of salamanders that appear to “steal” sperm from males of other species. These all-female salamanders can potentially retain the advantage of gaining new genetic diversity from other species without males of their own. However, the extent and flexibility of this mating systems is still not understood, and the factors that promote the coexistence of all-female salamander lineages and the sexual species from which they use reproductive material are mysterious. I have investigated three primary questions concerning these unusual animals. First, how do we identify an all-female salamander in Ohio? Because of their cryptic morphology compared to similar sexual species, all-female Ambystoma salamanders are only reliably identified by sequencing their mitochondrial DNA, which is independently transferred maternally. However, mitochondrial sequences that closely ii resembled those of all-female salamanders were previously found in salamander individuals across Ohio that were identified morphologically as either the smallmouthed or streamside salamander. I gathered microsatellite data from these potentially misidentified animals and evaluated three hypotheses for why the mitochondrial data does not match the nuclear DNA or morphological species identity. The best supported hypothesis was one of mitochondrial introgression, where the mitochondrial haplotypes of one species (streamside salamanders) were introgressed into populations of another species (smallmouth salamanders). This chapter describes the evolutionary basis for the discordance between mitochondrial and nuclear DNA markers and provides necessary diagnostic information to correctly identify all-female salamander lineages in Ohio. Second, can differences in dispersal between breeding environments dictate the coexistence between all-female salamanders and other salamander species, preventing mutual extinction? I inferred salamander movements across a fragmented agricultural landscape in Ohio with genetic data and treadmill endurance trials, and I found that sexual species traveled significantly greater distances between breeding sites and fatigue much more slowly than unisexuals, contrary to a hypothesis that would explain the ecological coexistence between these groups. Third, what environmental factors determine the coexistence of all-female salamanders and their sexual relatives at broad scales? I gathered rangewide occurrence data for blue-spotted, Jefferson’s salamanders, and all-female salamanders that vary by the number of nuclear genomes possessed from either sexual species. By comparing the niche overlap from ecological niche models representing all-female salamander groups and each sexual species, I found that neither the total number of genomes or the composition of all-female salamander genomes iii explained the amount of niche overlap. Instead, niche overlap was significantly greater than expected for all comparisons between sexual species and the all-female lineage. I additionally used joint species modeling techniques to suggest that species interactions, in this case the all-female salamanders’ reproductive requirement for sperm, are the most powerful predictor of ecological niche in all-female salamanders and limit their ability to differentiate from their sexual relatives. Taken together, these chapters have expanded our understanding of how all-female salamanders have evolved to navigate the tradeoffs of intermediacy between sexual and asexual reproduction while providing new avenues of research for the future, including physiological limitations in members of the all- female lineage and molecular discordance between their separate mitochondrial and nuclear genomes. iv Dedication For my Grandfather and Mother, my most relentless supporters. You told me to chase a dream while generously shielding me from the consequences of doing so. For Ashley and Wallace, who both believe I can do anything. But without them, anything feels like nothing. v Acknowledgments Scientific work cannot happen in isolation, and I have been fortunate to benefit from a truly outstanding collection of colleagues and friends who have devoted their time, perspective, and effort to helping me succeed. Lisle Gibbs brought me to his lab and gave me the chance to become the scientist I wanted to be. His carefully crafted advice and commitment to professionalism has influenced me greatly, and I will likely repeat his words to myself and others many times during the course of my career. I thank the members of my dissertation and defense committees, Bryan Carstens, Steve Matthews, Bill Peterman, and Joe Williams. Whether when initially forming my thoughts for PhD research or looking back on these projects after completion, my committee members have struck a perfect balance of providing both challenge and support. I am grateful for my cohort of colleagues in the Department of EEOB. Some of these individuals have provided relief with empathetic ears, some have given me perspective across discipline and culture, and some have inspired me with their own incredible work. Some of these individuals do all three on a daily basis. In alphabetical order, I thank Mike Broe, Paul Blischak, Tony Fries, Jenn Hellman, Laura Kenyon, Isaac vi Ligocki, Erin Lindstedt, Jason Macrander, Eric McCluskey, Tara Pelletier, David Salazar, Jordan Satler, Sarah Smiley-Walters, Mike Sovic, Ben Titus, and Jamin Wieringa. I especially thank Matt Holding, my closest collaborator and steadfast companion, who has responded to years of sarcasm with only laughter and unrelenting assistance. Finally, I am grateful for all of the undergraduates who have worked with me in the lab and field. They have likely never realized the extent that their enthusiasm, dedication, and spirit has affirmed my desire to help others do exciting science. I especially thank Collin Ries, Meghan Parsley, Paul Hudson, Mónica Saccucci, Abby Pomento, Katherine Costello, and Blair Perry. I also acknowledge Bobby Arnold for providing quiet support for many years. Other individuals have played crucial roles in generating the following thesis chapters and more: Jose Diaz and Josh Dyer. Jose’s assistance in the lab has provided me additional freedom that is rare for a graduate student, and his personality is the core of what makes working in our lab special. Josh’s dedication to amphibian conservation has made my fieldwork in Crawford County possible, and his talent as an educator has been a yearly source of inspiration. Finally, I truly appreciate the work by Chanelle Kinney, Corey Ross, and Sue Meier for making the most offending scheduling, administrative, or financial issue disappear without a single complaint. I am especially grateful towards Katy Greenwald, who told me about weird salamanders over a beer in Providence, Rhode Island. Without having that conversation, the last seven years would have looked much different and likely not been as fun. My work has been generously supported by the many landowners of Crawford County and their desire to learn more about the animals with which they share their vii fertile land. I have received financial support from the Ohio Biodiversity Conservation Partnership between Ohio State University and the Ohio Division of Wildlife, the National Science Foundation, the Ohio State University Graduate School, the American Society of Ichthyologists and Herpetologists, those who participated in the SciFund Challenge, the Society for the Study of Amphibians and Reptiles, and the Ohio State Council of Graduate Students. viii Vita 2005.............................................................Eastbrook High School, Marion IN 2005-2009 ...................................................B.S. Biology, Ball State University 2009-2011 ...................................................M.S. Biological Sciences .........................................................Eastern Kentucky University 2011-2012 ..................................................University Fellow, The Ohio State University 2012-2015 ...................................................Graduate Teaching Assistant, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University 2012-2016 ...................................................Graduate Research Assistant, Department of Evolution, Ecology, and
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