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Origins of Genetic Variation and Population Structure Of ORIGINS OF GENETIC VARIATION AND POPULATION STRUCTURE OF FOXSNAKES ACROSS SPATIAL AND TEMPORAL SCALES By Jeffrey Ryan Row A thesis submitted to the Department of Biology in conformity with the requirements for the degree of Doctor of Philosophy Queen’s University Kingston, Ontario Canada January 2011 Copyright © Jeffrey Ryan Row, 2011 Library and Archives Bibliothèque et Canada Archives Canada Published Heritage Direction du Branch Patrimoine de l'édition 395 Wellington Street 395, rue Wellington Ottawa ON K1A 0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre référence ISBN: 978-0-494-78442-6 Our file Notre référence ISBN: 978-0-494-78442-6 NOTICE: AVIS: The author has granted a non- L'auteur a accordé une licence non exclusive exclusive license allowing Library and permettant à la Bibliothèque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par télécommunication ou par l'Internet, prêter, telecommunication or on the Internet, distribuer et vendre des thèses partout dans le loan, distrbute and sell theses monde, à des fins commerciales ou autres, sur worldwide, for commercial or non- support microforme, papier, électronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriété du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette thèse. Ni thesis. Neither the thesis nor la thèse ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent être imprimés ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission. In compliance with the Canadian Conformément à la loi canadienne sur la Privacy Act some supporting forms protection de la vie privée, quelques may have been removed from this formulaires secondaires ont été enlevés de thesis. cette thèse. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n'y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. Abstract Understanding the events and processes responsible for patterns of within species diversity, provides insight into major evolutionary themes like adaptation, species distributions, and ultimately speciation itself. Here, I combine ecological, genetic and spatial perspectives to evaluate the roles that both historical and contemporary factors have played in shaping the population structure and genetic variation of foxsnakes (Pantherophis gloydi). First, I determine the likely impact of habitat loss on population distribution, through radio-telemetry (32 individuals) at two locations varying in habitat patch size. As predicted, individuals had similar habitat use patterns, but restricted movements to patches of suitable habitat at the more disturbed site. Also, occurrence records spread across a fragmented region were non-randomly distributed and located close to patches of usable habitat, suggesting habitat distribution limits population distribution. Next, I combined habitat suitability modeling with population genetics (589 individuals, 12 microsatellite loci) to infer how foxsnakes disperse through a mosaic of natural and altered landscape features. Boundary regions between genetic clusters were comprised of low suitability habitat (e.g. agricultural fields). Island populations were grouped into a single genetic cluster suggesting open water presents less of a barrier than non-suitable terrestrial habitat. Isolation by distance models had a stronger correlation with genetic data when including resistance values derived from habitat suitability maps, suggesting habitat degradation limits dispersal for foxsnakes. At larger temporal and spatial scales I quantified patterns of genetic diversity and population structure using mitochondrial (101 cytochrome b sequences) and ii microsatellite (816 individuals, 12 loci) DNA and used Approximate Bayesian computation to test competing models of demographic history. Supporting my predictions, I found models with populations which have undergone population size drops and splitting events continually had more support than models with small founding populations expanding to stable populations. Based on timing, the most likely cause was the cooling of temperatures and infilling of deciduous forest since the Hypisthermal. On a smaller scale, evidence suggested anthropogenic habitat loss has caused further decline and fragmentation. Mitochondrial DNA structure did not correspond to fragmented populations and the majority of foxsnakes had an identical haplotype, suggesting a past bottleneck or selective sweep. iii Co-Authorship This thesis was formatted in the manuscript format as outlined in the guidelines provided by The Department of Biology. All chapters are co-authored by Stephen Lougheed, who contributed financially and intellectually to the design and development and editing of the thesis. The first and second chapters were also co-authored by Gabriel Blouin-Demers, who contributed intellectually and logistically for both of those chapters. Publications arising from and included in this thesis: Row JR, Blouin-Demers G, Lougheed SC (2010) Habitat distribution influences dispersal and fine-scale genetic population structure of eastern foxsnakes (Mintonius gloydi) across a fragmented landscape. Molecular Ecology, 19, 5157-5171. Row JR, Blouin-Demers G, Lougheed SC (in review) Movement and habitat use of the Eastern Foxsnake (Pantherophis gloydi) in a fragmented landscape. Journal of Herpetology. Row JR, Lougheed SC. Approximate Bayesian computation reveals the origins of genetic diversity and population structure of foxsnakes. Will be submitted to Journal of Evolutionary Biology. Publications arising from, but not included in this thesis: Row JR, Sun Z, Cliffe C, Lougheed SC (2008) Isolation and characterization of microsatellite loci for eastern foxsnakes (Elaphe gloydi). Molecular Ecology Resources, 8, 965–967. iv DiLeo M, Row JR, Lougheed SC (2010) Discordant patterns of population structure for two co-distributed snake species across a fragmented Ontario landscape. Diversity and Distributions, 16, 571–581. Xuereb A, Row JR, Lougheed SC (in review) Relation between parasitism, stress, and fitness correlates of the Eastern Foxsnake (Pantherophis gloydi) in Ontario. Journal of Herpetology. v Acknowledgements Without help from many people this thesis would not have been possible. First, I want to thank my supervisor, Stephen Lougheed, who is a well deserving co-author on all the chapters presented here. He provided assistance with every aspect of this thesis and was a large factor in shaping all the studies presented here. I would also like to thank Gabriel Blouin-Demers for his help both intellectually and logistically on the first two chapters. Thanks to Vicki Friesen and Dongmei Chen for the time and effort they have put in to serve on my committee and to Ryan Danby and Richard King for graciously agreeing to attend my defense as examiners. One of the greatest and worst traits of foxsnakes is their ability to stay calm in the face of danger (us catching them), making them very difficult to find. As evidenced from my acknowledgements at the end of each chapter, I had a huge amount of help in amassing the datasets presented throughout this thesis. For their hard work, in sometimes unfavourable weather conditions, I would like to thank Robyn Sharma, Cameron Hudson, Michelle DiLeo, Katie Geale, Rosamond Lougheed, Kayne Vincent, Kevin Donmoyer, Natalie Morrill, Christopher Monk and Amanda Xuereb. For generously collecting and/or providing blood and tissue samples I would also like to thank Kristen Stanford, Kent Bekker and Brian Putman, Gerry Nelson, Kyle Kucher, Brett Groves, Deb Jacobs, Ron Gould, Don Hector, Vicki McKay, the Chicago Field Museum, the staff at the Ojibway Nature Center and at Point Pelee National Park. I would also like to the thank the many members of the Lougheed Lab who made the long hours spent in the lab and office much more enjoyable. A special thanks to Dr. Anthony Braithwaite for dedicating huge amounts of his own time and resources to assist with transmitter implantation. vi This thesis would not have been possible without the financial support provided by the World Wildlife Fund (through the Endangered Species Recovery Fund), Environment Canada, Ontario Ministry of Natural Resources, Parks Canada, the Essex County Stewardship Network, Natural Sciences and Engineering Research Council of Canada (NSERC) and Queen’s University through the Summer Work Experience Program (SWEP). I would particularly like to thanks Kent Prior from Parks Canada for originally approaching me with this project and his help in acquiring the required funding. Last, but certainly not least, I would like to thank my family and friends. Being a student into your thirties can be trying at times, but was made much easier through their support. To my wife Heather, I am most in debt for the unwavering love and support that she provided throughout all of my graduate studies. Finally, I am grateful to the newest member of our family, whom I have not met yet, but I’m sure will graciously contribute a good night’s sleep before my defense. vii Table of Contents Abstract .......................................................................................................................................ii
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