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(AMMODRAMUS NELSONI) SPARROWS by Jennifer Walsh University of New Hampshire, September 2015

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HYBRID ZONE DYNAMICS BETWEEN SALTMARSH (AMMODRAMUS CAUDACUTUS) AND NELSON’S (AMMODRAMUS NELSONI) SPARROWS BY JENNIFER WALSH Baccalaureate Degree (BS), University of New Hampshire, 2007 Master’s Degree (MS), University of New Hampshire, 2009 DISSERTATION Submitted to the University of New Hampshire in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Natural Resources and Environmental Studies September, 2015 This dissertation has been examined and approved in partial fulfillment of the requirements for the degree of Natural Resources and Environmental Studies in the Department of Natural Resources and Earth Systems Science by: Dissertation Director, Adrienne I. Kovach Research Associate Professor of Natural Resources Brian J. Olsen, Assistant Professor, School of Biology and Ecology, University of Maine W. Gregory Shriver, Associate Professor of Wildlife Ecology, University of Delaware Rebecca J. Rowe, Assistant Professor of Natural Resources Kimberly J. Babbitt, Professor of Natural Resources On July 9, 2015 Original approval signatures are on file with the University of New Hampshire Graduate School. ACKNOWLEDGEMENTS While pursuing my doctorate, a number of people have helped me along the way, and to each of them I am exceedingly grateful. First and foremost, I am grateful for my advisor, Adrienne Kovach, for her guidance, support, and mentorship. Without her, I would not be where I am, and I will be forever grateful for the invaluable role she has played in my academic development. Her unwavering enthusiasm for the project and dedication to its success has been a source of inspiration and I will never forget our countless road trips and long days out on the marsh. I am also grateful for my committee members, Brian Olsen, Greg Shriver, Kimberly Babbitt, and Rebecca Rowe for their help and encouragement. Thanks to Brian Olsen and Greg Shriver for the many conversations about Saltmarsh Sparrows and evolution and for all of the pep talks. Thanks to Kim Babbitt for always being so enthusiastic and excited about the research. Thanks to Rebecca Rowe for the many lunches, words of wisdom, career and life advice, and for being such a strong role model: her guidance and mentorship has been invaluable over the past years. This work would not have been possible without the endless amount of sampling and logistical support in the field. U.S Fish and Wildlife Service, the Nature Conservancy, and the Great Bay National Estuarine Research Reserve System facilitated access to marshes. Thanks to Paul Stacy and Rachel Stevens for their support and for facilitating access to Great Bay marshes. Nancy Pau and Erin King provided invaluable help with field and sampling logistics. A special thanks to Kate O’Brien for her support, enthusiasm, and advise on the project: her expertise has ! iii! been invaluable in interpretation and dissemination of results. Thank you to Fletcher Smith and Oksana Lane for teaching me to capture, band, and handle sparrows and to Len Reitsma for teaching me how to collect blood samples. Thanks to Evan Erlich, Denyelle Surrell, Elizabeth Natola, and Ricky Regius for their help in the field. I am especially thankful for Ben Flemer, Katrina Papanastassiou, and Molly Hunt for always being reliable, enthusiastic, dedicated, and entertaining even on the hottest and buggiest of days. Chris Elphick and Tom Hodgman provided endless logistical advice, both in the field and with data analysis: I am grateful for their support and input. I am also grateful for the camaraderie of my fellow SHARP graduate students: Mo Correll, Alyssa Borrowske, Kate Ruskin, Whitney Weist, Becky Kern, and Chris Field. I received immense support from my lab community at UNH. A number of undergraduates contributed time to extracting DNA from blood samples, including Peter Goode, Tricia Gunther, Emily Johnston, Stephanie Royka, and Courtney Mills. I also thank Thea Kristensen, Stephanie Coster, and Lindsey Fenderson for listening to research ideas and for positive reinforcement. A special thanks to Charlotte Gabrielsen and Dan Hocking for always being there when I needed someone to talk to and for all of their comments, input, advice, and kind words. Thanks to Bri Benvenuti for fearlessly jumping into the Saltmarsh and for carrying on the torch in the demographic sites. Her commitment to the project and to the sparrows is an inspiration to me and I am incredibly grateful to have worked besides her on the marsh. Thanks to Jobriah Anderson for help with genotyping and sequencing and to Mike Routhier and Lucie Lepine for help with GIS and spatial analyses. A special thanks to David Berlinsky for introducing me to science, for providing our group with a lab space, for always believing in me, and for not asking any questions about photosynthesis during my defense. ! iv! I received financial support from the UNH Graduate School, Department of Natural Resources and the Environment, and the Department of Natural Resources and Earth System Sciences program. This project was supported by the Agricultural Experiment Station and by funding from the United States Fish and Wildlife Service. I was fortunate enough to receive grants from the American Ornithologists’ Union, the American Museum of Natural History, and the Maine Association of Wetland Scientists. Finally, I’d like to extend my appreciation to my family, Joanne, Randy, and Jordan Walsh for their endless support and encouragement. Thank you for teaching me the importance of hard work and dedication. Thanks to Toola and Marcel Emond for the words of encouragement and for humoring me when I send along bird-related articles. Thanks to Nico and Artemis for accompanying me on my many mind-clearing runs. To Marc Emond for always standing by me, for always supporting me, and for always baking cookies for my academic presentations. And lastly, I would like to express my gratitude to the sparrows, particularly my favorite bird – 2511-26151 – for her persistence and purposefulness, which I find very endearing. This has been an incredible system to work in and I am beyond thankful for the opportunity to conduct research in such a magical place. ! v! TABLE OF CONTENTS ACKNOWLEDGMENTS……………………………………………………….….. iii LIST OF TABLES………………………………………………………………....... x LIST OF FIGURES…………………………………………………………….….... xiii ABSTRACT………………………………………………………………………..... xix INTRODUCTION…………………………………………………………………... 1 RELATIONSHIP OF PHENOTYPIC VARIATION AND GENETIC ADMIXTURE IN THE SALTMARSH-NELSON’S SPARROW HYBRID ZONE…………………... 17 ABSTRACT………………………………………………………………………….. 17 INTRODUCTION………………………………………………………………….... 18 METHODS………………………………………………………………………..….. 21 Sample Collection and Morphological Data...……………………….…….... 21 Genotyping, Admixture Analysis, and Identification of Genotypic Classes.. 23 Correlating Phenotypic Variation with Genotype………………………….... 25 RESULTS…………………………………………………..………………………... 26 DISCUSSION………………………………………………………..……………… .29 DIFFERENTIAL INTROGRESSION AND THE MAINTENANCE OF SPECIES BOUNDARIES IN AN ADVANCED GENERATION AVIAN HYBRID ZONE……………………...................................................................................................... 45 ABSTRACT………………………………………………………………….…...… 45 INTRODUCTION………………………………………………….…………..…... 46 METHODS……………………………………………….………………….….….. 50 Geographic Transect and Sample Collection…………………………….... 50 Analysis of Molecular Markers…..……………..……………………...….. 51 Population Structure……………………………..……………………..….. 53 Patterns of Differential Introgression: Genomic Clines……………….…... 54 Patterns of Differential Introgression: Geographic Clines………………… 56 ! vi! Phenotypic Variance……………………………………………………….. 57 RESULTS…………………………………………..………………………………. 58 Genetic Structure of the Nelsoni-Caudacutus Hybrid Zone………..……… 58 Genomic and Geographic Analyses of Introgression………………………. 60 DISCUSSION……………………………………………….……………………… 62 Patterns of Differential Introgression and Mechanisms for Isolation…..….. 64 Asymmetrical Introgression……………..……………….………………… 67 Conclusions………………………………………….……………………... 69 EXOGENOUS SELECTION SHAPES ENVIRONMENT-GENOTYPE ASSOCIATIONS IN A HYBRID ZONE BETWEEN TWO TIDAL MARSH BIRDS…………...... 89 ABSTRACT………………………………………………………………….…..… 89 INTRODUCTION………………………………………………….…………..…... 90 METHODS……………………………………………….………………….….….. 95 Sample Collection………………………………………………………….. 95 Quantifying Environmental Variation…………..…………………………. 95 DNA Extraction and Microsatellite Genotyping.………………………….. 98 Admixture Analysis……………………………………………………….. 99 Genotype-Habitat Associations………………………..………………….. 100 Ecological Niche Models………………………………………………….. 101 RESULTS…………………………………………..……………………………….. 102 Genetic Variation and Hybrid Zone Analysis…………….………..………. 102 Habitat Variation………………………………….……………………….. 103 Genotype-Habitat Associations and Ecological Niche Models…………… 104 DISCUSSION……………………………………………….……………………… 106 Relationship between genotype and marsh habitat……………………..….. 107 Exogenous Selection as a Mechanism for Hybrid Zone Maintenance….…. 110 ! vii! INTRINSIC AND EXTRINSIC FACTORS INFLUENCE FITNESS ACROSS AN AVIAN HYBRID ZONE………………………………………….………………………...... 133 ABSTRACT………………………………………………………………….…..…133 INTRODUCTION………………………………………………….…………..…...134 METHODS……………………………………………….………………….….…..138 Field Methods and Sample Collection.…………………………… 138 Genetic Analyses and Hybrid Identification……..……….………. 140 Daily Rates of Nest Survival and Reproductive Success...……….. 142 Differential Fitness in Pure and Hybrid Females……….……..….. 143 Testing Predictions of Haldane’s Rule……………………..……………….
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