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Evolution of Rattlesnake Venom Involves Geographically Structured Coevolution and Local Adaptation to Prey DISSERTATION Presente

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Evolution of Rattlesnake Venom involves Geographically Structured Coevolution and Local Adaptation to Prey DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Matthew Landon Holding Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2017 Dissertation Committee: H. Lisle Gibbs, Advisor Bryan Carstens Marymegan Daly Stuart Ludsin Copyrighted by Matthew Landon Holding 2017 Abstract Predators and prey coevolve to produce some of the most fascinating phenotypic characteristics of animals. However, coevolution is not a simple race toward the most extreme traits. The occurrence, strength, and outcomes of coevolution are hypothesized to be determined by multiple factors; some are environmental and others are intrinsic to the species involved. Although this complexity has been recognized and studied in fast- evolving hosts-parasite systems, testing the key predictions of coevolutionary theory in natural populations of predators and prey has remained a difficult task. I evaluated the effects of two key factors that impact coevolving rattlesnake venom and ground squirrel venom resistance–mechanisms of interaction and population demography–and I provide evidence that the broader composition of the small mammal prey community exerts selection on the venom phenotype as well. Toward this end, I collected Northern Pacific rattlesnake (Crotalus oreganus) venom and California ground squirrel (Otospermophilus beecheyi) blood serum (which contains venom inhibitors) from multiple populations in California where California ground squirrels have evolved resistance to the venom. I developed an experiment to test for population-level adaptation of venom metalloproteinases in their interaction with ground squirrel venom inhibitors. I demonstrated local adaptation in a snake-prey relationship for the first time, where venom metalloproteinase enzymes have evolved to overcome ground squirrel resistance. ii Furthermore, the existence of local adaptation in these biochemical traits suggests that the mechanism of coevolution involving venom is not an escalating arms race as previously thought, but rather a phenotype matching-based interaction involving a molecular lock- and-key mechanism between multiple snake venom proteins and prey inhibitor molecules. The high levels of medically-significant intraspecific venom variation seen in snakes must now be also viewed in terms of a geographic mosaic of molecular coevolution with resistant prey species, and not merely in terms of broad scale variation in the prey species consumed. Yet, the extent that each population of snakes is adapted to local squirrels varied, and two demographic factors, population size and the relative amount of gene flow in each species, are predicted to explain this variation. I generated thousands of DNA-based SNP loci for both rattlesnakes and squirrels using RAD-seq to test the prediction that rattlesnakes, as the locally adapted interacting species, will have higher effective population sizes and less gene flow than ground squirrels, facilitating the adaption of the snakes over squirrels. Using coalescent-based population genetic analysis, I supported the prediction that the difference in effective population sizes between rattlesnakes and ground squirrels is positively associated with the population-specific signals of local adaptation. This work represents the first analysis of theoretically- predicted impacts of demography on coevolution outside of a host-parasite system, and the first quantitative demonstration of a relationship between effective population size and local adaptation in any coevolving system in nature. Finally, ground squirrels are present at every site I sampled, while the broader mammalian prey community differs substantially. To understand the potential importance of prey community variation in iii venom divergence among populations, I measured quantitative differences in the venom protein expression profiles of each population. Both population genetic differentiation based on RADseq loci and differences in the prey community combine to predict over 70% of the between-population variation in venom, thus supporting a role for the prey community in driving divergence and suggests that isolation by environment in the heterogeneous landscape of California may drive correlated levels of population genetic differentiation and adaptive divergence in venom composition. Overall, my work will help in understanding how diverse evolutionary and ecological factors influence the coevolutionary process to produce the planet’s diversity of species and their traits. iv Dedication To my parents, Linda and Harold Holding, for supporting my dreams and never stifling my curiosity. And to my wife, Sloane Henningsen, for unwavering love despite the distances. v Acknowledgments This work would not have been possible without the assistance of many people to whom I owe a serious debt of gratitude. First, I would like to thank my advisor, Lisle Gibbs. Lisle supported by efforts to find success in a new study system at every step, taught me to think critically while still thinking big, and has been a model for both professionalism and enthusiasm for discovery in science. I also thank my dissertation committee, Bryan Carstens, Meg Daly, and Stu Ludsin, who have offered valuable advice while challenging me to improve my science and myself. I thank the members of my lab, Rob Denton, David Salazar, Tony Fries, Sarah Smiley-Walters, and Mike Sovic for being the first filter for my bad ideas and for helping build the good ones. Several other Ohio State colleagues deserve recognition for their invaluable support and assistance, including Isaac Ligocki, Eric McCluskey, Jason Macrander, Erin Lindstedt, Jordan Satler, Paul Blischak, Megan Smith, and Destiny Palik, Andreas Chavez, and Ian Hamilton, and Amy Kulesza, and Judy Ridgway. My field collection efforts were greatly assisted by Margaret Earthman, Kayla Hammer, Josh Zajdel, Tony Frazier, Amber Branske, Emily Taylor, Steve Van Middlesworth, Bree Putman, and Rulon Clark. I am grateful to Jose Diaz, Jim Biardi, Mark Margres, Margaret Seavy, and Darin Rokyta, who provided assistance for several of the laboratory analyses included herein. Discussions with Scott Nuismer provided key insights about how to test predictions from coevolutionary theory with empirical data. I would like to thank the University of California (UC) Sedgwick vi Reserve, UC McLaughlin Reserve, Hopland Research Extension Center, San Joaquin Experimental Range, Wind Wolves Preserve, Big Chico Creek Ecological Reserve, and Vandenberg Air Force Base for both allowing me to conduct research at their facilities and to do so on a tight budget. Key persons made access to my field sites easy and enjoyable, including Mike Westphal, Howard Hamman, Kate McCurdy, Cathy Koehler, Kathryn Purcell, Rhys Evans, Ryan Bourque, and Bob Stafford. This work was made possible by a National Science Foundation Graduate Research Fellowship, Ohio State University Presidential Fellowship, a Theodore Roosevelt Memorial Grant from the American Museum of Natural History, a Student Research Award from The American Society of Naturalists, a Grant-in-Aid from the American Society of Mammalogists, an American Society of Ichthylogists and Herpetologists’ Gaige Award, a Grant-in-aid of research from Sigma Xi, the Herpetologists’ League Jones-Lovich Grant, an Alumni Grant from Ohio State University, a Graduate Student Research Grant from the Chicago Herpetological Society, and funding from the California Bureau of Land Management and the Ohio State University. vii Vita 2005................................................................Yorktown High School, Yorktown, IN 2005-2009 ......................................................B.S. Biology, Ball State University 2009-2011 ......................................................M.S. Biological Sciences ............................................................California Polytechnic State University 2010-2014 .....................................................National Science Foundation Graduate Research Fellow, California Polytechnic State University and Ohio State University 2011, 2014-2015 ............................................Graduate Teaching Associate, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University 2016-2017 ......................................................Presidential Fellow, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University Publications Hudson, P., Denton, R.D., Holding, M.L., and Gibbs, H.L. 2016. Repeatability of locomotor endurance in the Smallmouth Salamander (Ambystoma texanum). Herpetological Review 47:583-586 viii Holding, M.L., Drabeck, D.H., Jansa, S.A., and Gibbs, H.L. 2016. Venom resistance as a model for understanding the molecular basis of coevolutionary adaptations. Integrative and Comparative Biology 56: 1032-1043. Holding, M.L., Biardi, J.E., Gibbs, H.L. 2016. Coevolution of venom function and prey resistance in a rattlesnake predator and its squirrel prey. Proceedings of the Royal Society B: Biological Sciences 283:28-41. Saccucci, M., Denton, R.D., Holding, M.L., Gibbs, H.L. 2016. Polyploid unisexual salamanders have higher tissue regeneration rates than diploid sexual relatives. Journal of Zoology 300: 77-81. Pomento, A.M., Perry, B.W., Denton, R.D., Gibbs, H.L., Holding, M.L. 2016. No safety in the trees:
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