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University of California UNIVERSITY OF CALIFORNIA Los Angeles The effects of small population size and inbreeding on patterns of deleterious variation in Channel Island foxes and Isle Royale gray wolves A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Biology by Jacqueline Anita Robinson 2017 © Copyright by Jacqueline Anita Robinson 2017 ABSTRACT OF THE DISSERTATION The effects of small population size and inbreeding on patterns of deleterious variation in Channel Island foxes and Isle Royale gray wolves by Jacqueline Anita Robinson Doctor of Philosophy in Biology University of California, Los Angeles, 2017 Professor Robert Wayne, Chair In small isolated populations the fate of mutations is governed largely by chance rather than natural selection. Most mutations are deleterious, thus the inability of selection to effectively eradicate them incurs a cost to the genetic health of individuals in small populations. These detrimental consequences have been observed in numerous captive and wild populations, such as the gray wolves (Canis lupus) of Isle Royale, which suffer from severe inbreeding depression. However, other small populations appear healthy, and even persist for thousands of generations, such as the foxes (Urocyon littoralis) of the Channel Islands near the coast of Southern California. In this dissertation, we explore the genome-wide effects of small population size and isolation in these two extreme examples. First, we show that long-term small population size and isolation has led to a striking lack of diversity in island foxes, particularly in San Nicolas foxes, ii which are virtually monomorphic across the entire genome. Additionally, island foxes have an elevated burden of deleterious mutations relative to mainland gray foxes (U. cinereoargenteus), but show no signs of inbreeding depression. Second, we explore the possibility that strongly deleterious recessive alleles have been purged from island fox populations, facilitating their persistence, and allowing them to recover rapidly from extreme bottlenecks. We found that recent, short-term bottlenecks have had little impact on island fox genomes, and confirm through simulations that island populations are expected to have a reduced burden of strongly deleterious recessive alleles relative to mainland foxes. In contrast, Isle Royale wolves suffer from severe inbreeding depression, and are on the verge of extinction less than a century after the population was founded. Third, we show through whole genome sequencing of Isle Royale wolves that intense inbreeding has eliminated variation in large genomic segments, causing the increased homozygosity of deleterious mutations. Our results suggest that persistence is possible in small populations large enough for selection to purge strongly deleterious recessive alleles without causing extinction, although the long-term effects of the elevated burden of weakly deleterious alleles and the loss of diversity in these small populations are difficult to predict. iii The dissertation of Jacqueline Anita Robinson is approved. Kirk Edward Lohmueller Howard Bradley Shaffer Bridgett vonHoldt Robert Wayne, Committee Chair University of California, Los Angeles 2017 iv This dissertation is dedicated with utmost gratitude to Jean and Richard Robinson. v TABLE OF CONTENTS List of Figures and Tables……………………………………………………………………...vii Acknowledgments……………………………………………………………………………...viii Vita………………………………………………………………………………………………..x Chapter 1: Genomic flatlining in the endangered island fox……………………..…………...1 Summary…………………………………………………………………………………..1 Results and Discussion……………………………………………………………………2 Materials and Methods…………………………………………………………………….9 Figures……………………………………………………………………………………12 Tables…………………………………………………………………………………….18 Appendix 1-I: Supplemental Methods...................................……………………………22 Bibliography……………………………………………………………………………..39 Chapter 2: Purging of deleterious alleles implicated in the absence of inbreeding depression in genetically depauperate island foxes…………………………………………….………….46 Abstract…………………………………………………………………………………..46 Introduction………………………………………………………………………………46 Materials and Methods…………………………………………………………………...52 Results……………………………………………………………………………………57 Discussion………………………………………………………………………………..64 Figures……………………………………………………………………………………73 Appendix 2-I: Supplemental Tables……………………………………………………..81 Appendix 2-II: Supplemental Figures……………………………………………………89 Bibliography……………………………………………………………………………..90 Chapter 3: Genomic signatures of inbreeding in Isle Royale wolves, a population on the threshold of extinction………………………………………………………………………….99 Abstract…………………………………………………………………………………..99 Introduction………………………………………………………………………………99 Results…………………………………………………………………………………..104 Discussion………………………………………………………………………………115 Materials and Methods………………………………………………………………….122 Figures…………………………………………………………………………………..125 Tables…………………………………………………………………………………...134 Bibliography……………………………………………………………………………137 vi LIST OF FIGURES AND TABLES Figure 1-1.......................................................................................................................................12 Figure 1-2.......................................................................................................................................13 Figure 1-3.......................................................................................................................................14 Figure 1-4.......................................................................................................................................15 Figure 1-5.......................................................................................................................................16 Figure 1-6.......................................................................................................................................17 Figure 2-1.......................................................................................................................................73 Figure 2-2.......................................................................................................................................74 Figure 2-3.......................................................................................................................................75 Figure 2-4.......................................................................................................................................76 Figure 2-5.......................................................................................................................................77 Figure 2-6.......................................................................................................................................78 Figure 2-7.......................................................................................................................................79 Figure 2-8.......................................................................................................................................80 Figure S2-1.....................................................................................................................................89 Figure 3-1……………………………………………………………………………………….125 Figure 3-2……………………………………………………………………………………….126 Figure 3-3……………………………………………………………………………………….127 Figure 3-4……………………………………………………………………………………….128 Figure 3-5……………………………………………………………………………………….129 Figure 3-6……………………………………………………………………………………….130 Figure 3-7……………………………………………………………………………………….131 Figure 3-8……………………………………………………………………………………….132 Figure 3-9……………………………………………………………………………………….133 Table 1-1........................................................................................................................................18 Table 1-2........................................................................................................................................19 Table 1-3........................................................................................................................................20 Table S2-1......................................................................................................................................81 Table S2-2......................................................................................................................................82 Table S2-3......................................................................................................................................85 Table S2-4......................................................................................................................................88 Table 3-1......................................................................................................................................134 Table 3-2......................................................................................................................................135 Table 3-3......................................................................................................................................136 vii ACKNOWLEDGMENTS To adapt a phrase, it takes a village to complete a dissertation. I therefore begin by acknowledging a few of the people who were truly instrumental in the process of bringing forth this one, while recognizing that there are many others who played a part that I shall fail to mention in these few pages. First, I thank my committee members, Dr. Bridgett vonHoldt, Dr. H. Bradley Shaffer, Dr.
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