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In Western North America Amanda Marie MAKING CONTACT: A POPULATION GENETIC ANALYSIS OF WARBLING VIREOS (VIREO GILVUS) IN WESTERN NORTH AMERICA AMANDA MARIE CARPENTER Bachelor of Science, University of Wisconsin-Platteville (USA), 2016 A Thesis Submitted to the School of Graduate Studies of the University of Lethbridge in partial fulfillment of the requirements for the degree MASTER OF SCIENCE in BIOLOGY Department of Biological Sciences University of Lethbridge Lethbridge, Alberta, Canada © Amanda M. Carpenter, 2019 MAKING CONTACT: A POPULATION GENETIC ANALYSIS OF WARBLING VIREOS (VIREO GILVUS) IN WESTERN NORTH AMERICA AMANDA MARIE CARPENTER Date of Defense: December 10, 2019 Dr. T. Burg Professor Ph.D. Thesis Supervisor Dr. A. Iwaniuk Associate Professor Ph.D. Thesis Examination Committee Member Dr. R. Laird Associate Professor Ph.D. Thesis Examination Committee Member Dr. T. Russell Associate Professor Ph.D. Chair, Thesis Examination Committee Abstract This thesis examined range wide population genetic structure, morphological differences, and hybridization among three morphologically cryptic subspecies of warbling vireo (Vireo gilvus). MtDNA and microsatellite markers show genetic differences between the eastern, gilvus, and two western, swainsonii and brewsteri, subspecies, while genetic differences between the two western subspecies were detected only with microsatellite markers suggesting their separation is recent. Microsatellite genetic groups do not correspond to current taxonomic range distributions of the two morphologically similar western subspecies. A low frequency of hybridization between gilvus and swainsonii in Alberta suggest strong reproductive isolating barriers. A wide, unreported contact zone between swainsonii and brewsteri in southern British Columbia through western Montana had a high frequency of hybridization, where genetic composition of hybrids appears related to habitat and elevation. Molecular markers are a crucial tool in recognizing cryptic biodiversity for taxonomic and conservation implications. iii Acknowledgments Little did I know growing up that my frequent exposure to backyard bird watching with my grandmother would come full circle and have me eventually go down the path of studying the genetics of a songbird. During my undergraduate degree, it was not until my final semester that I finally knew a narrower field I wanted to involve myself in. I took an ornithology class with Dr. Jeff Huebschman, who opened my eyes to this fascinating field and the excitedness of bird watching – which, I thought was an old person hobby. When I saw my first bird in the field and positively IDed it based on our class (a white-breasted nuthatch), I was hooked. I explored other avenues of ornithology and came across bird banding, which greatly intrigued me. I took my first solo road trip across the United States, from Wisconsin to Idaho, to participate in a beginner’s bird banding workshop. The first bird I held, unbeknown to me as the bird I would soon spend two years of my life studying, was a warbling vireo. I took away a lot of skills from the workshop and a sense of self growth from driving across the United States alone. My mom would tell you, however, that she didn’t really want me to travel alone again. Well, I found myself doing grassland breeding bird surveys for the USGS in Saco, Montana, which required me to leave the home roost once more on my own. Forward another year, I am once again traveling solo (unless you count my dog) to Lethbridge, Alberta to begin my MSc in Biology. I’d like to thank Theresa first and foremost for “taking me under her wing” in her lab with my little genetic background. Your patience with me over the last two years has been appreciated, and for all of the work she has put into teaching me to prepare me for defending this thesis. I would also like to thank my committee members, Dr. Andrew Iwaniuk and Dr. Rob Laird, for their iv input at meetings, their patience in my preparation of this thesis, and their thoroughness of examining my thesis. I am very grateful for other faculty members at the University of Lethbridge. Jennifer Burke and Katrina Mendez have been supportive of my time here, always welcoming me to pop by for a bit of chit chat. Many thanks to the rest of the lab, Kanishka Sevenvirathna, Dilini Abeyrama, and Ian Gazeley, for making it feel more than just lab, but a little unit of good friends helping each other to succeed. A huge thank you to Brendan Graham, who accompanied me on both summer field seasons. Not only did you put up with me for a couple of months each summer, you have always been a person I can discuss and bounce ideas off of. I greatly appreciate your help and support throughout this process. Finally, I couldn’t have finished this degree without the support from my family and friends. Thanks to my parents, my brother, and my sister in-law for the constant check-ins and pep talks, and the occasional care package. To the number of friends I have made here during my time at the U of L, I am grateful for your help in ways big and small. I’d also like to thank each, and every bird caught in our mist nets. Without you, my genetic data would have not been as complete. I would also like to extend a thank you to my two collaborators, Garth Spellman of the Denver Museum of Nature and Science and John Klicka of the Burke Museum of Natural History and Culture, for their support. We gratefully acknowledge samples provided from other museum collections (Natural History Museum University of Oslo, University of Michigan Museum, Field Museum of Natural History, Cleveland Museum of Natural History, and Royal Alberta Museum) for this research. v Table of Contents Abstract iii Acknowledgments iv List of Tables viii List of Figures ix List of Abbreviations x Chapter 1: General Introduction 1 1.1 Background 1 1.1.1 Contact zones and population genetics 1 1.1.2 Pleistocene epoch 2 1.1.3 Hybridization 3 1.2 Study species 5 1.3 Molecular markers 7 1.4 Thesis goals 8 1.4.1 Subspecies differences and overall population genetic structure 9 1.4.2 Contact zones 10 1.5 Thesis organization 10 1.6 Literature cited 15 Chapter 2: Range-wide microsatellite and mtDNA population 20 genetic structure in a cryptic species complex, the warbling vireo (Vireo gilvus) 2.1 Introduction 21 2.2 Methods 24 2.2.1 Sample collection and DNA extraction 24 2.2.2 MtDNA sequencing 25 2.2.3 Microsatellites 26 2.2.3.1 Genotyping 26 2.2.3.2 Bayesian clustering 27 2.2.3.3 FST 28 2.2.3.4 Morphology 29 2.2.3.5 Ecological niche modeling 29 2.3 Results 30 2.3.1 Sequencing and mtDNA lineages 30 2.3.2 Microsatellites 31 2.3.2.1 Bayesian clustering 31 2.3.2.2 FST 32 2.3.2.3 Morphology 33 2.3.2.4 Ecological niche modeling 33 2.4 Discussion 34 2.4.1 Historic population genetic structure 34 2.4.2 Contemporary population genetic structure 36 2.4.3 Delineation of subspecies range 39 2.5 Conclusions 42 2.6 Literature cited 51 vi Chapter 3: Making contact: examining hybridization in populations 59 of warbling vireo (Vireo gilvus) in a previously reported contact zone in Alberta and an unreported contact zone in western North America 3.1 Introduction 60 3.2 Methods 62 3.2.1 Sample collection and acquisition 62 3.2.2 MtDNA screening 64 3.2.3 Microsatellites 65 3.2.3.1 Genotyping 65 3.2.3.2 Bayesian clustering 66 3.3 Results 67 3.3.1 MtDNA screening 67 3.3.2 Microsatellites 67 3.4 Discussion 69 3.4.1 West contact zone 69 3.4.1.1 Western United States and British Columbia 69 3.4.1.2 Montana 71 3.4.2 Alberta contact zone 72 3.4.3 General conclusions 75 3.5 Conclusions 76 3.6 Literature cited 83 Chapter 4: General Discussion 87 4.1 Subspecies distributions 87 4.2 Contact zones 89 4.3 Future considerations 91 4.4 Closing statement 92 4.5 Literature cited 93 Appendices Appendix 1: Supplementary information for Chapter 2 96 1.1 Individual details of warbling vireo samples 97 1.2 Pairwise FST values and p-values 106 1.3 Mixed model ANOVA statistical results 107 1.4 Ecological niche model BioClim layers 108 1.5 Eastern warbling vireo (V. g. gilvus) plumage variation 109 Appendix 2: Supplementary information for Chapter 3 110 2.1 Individual details of warbling vireo samples 111 vii List of Tables Table 2.1 Populations used in cyt b, ATPase 6 and 8, microsatellite 43 and morphological analyses Table 2.2 Microsatellite primers 44 Table 2.3 Heat table of pairwise FST comparisons for microsatellites 45 Table 3.1 Populations used in cyt b and microsatellite analyses 78 viii List of Figures Figure 1.1 Map of the North American continent with the two main ice 12 Sheets during the Pleistocene Figure 1.2 Breeding ranges of all five subspecies of warbling vireo 13 Figure 1.3 Plumage comparisons of the western subspecies, V. g. 14 swainsonii and eastern subspecies, V. g. gilvus Figure 2.1 Results from cyt b and ATPase 6 and 8 analyses 46 Figure 2.2 Hierarchical Structure plots for range wide subspecies 47 population genetic structure based on microsatellites Figure 2.3 Map showing population locations with genetic cluster 48 assignment based on Structure results in Figure 2.2 Figure 2.4 Morphology box plots 49 Figure 2.5 Ecological niche model predictions 50 Figure 3.1 Breeding ranges and contact zones of the three warbling vireo 79 subspecies in this study Figure 3.2 Map of Alberta and Saskatchewan with populations included 80 in cyt b screening Figure 3.3 Hierarchical Structure plots examining population genetic 81 structure and hybridization at contact zones with microsatellites Figure 3.4 Map showing population locations with genetic cluster 82 assignment based on
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