A Deep Dive Into the Genomic History of the Sea Otter

UNIVERSITY OF CALIFORNIA Los Angeles Aquatic Adaptation and Fur Trade Devastation: A Deep Dive into the Genomic History of the Sea Otter A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Biology by Annabel Carroll Beichman 2020 © Copyright by Annabel Carroll Beichman 2020 ABSTRACT OF THE DISSERTATION Aquatic Adaptation and Fur Trade Devastation: A Deep Dive into the Genomic History of the Sea Otter by Annabel Carroll Beichman Doctor of Philosophy in Ecology and Evolutionary Biology University of California, Los Angeles, 2020 Professor Kirk Edward Lohmueller, Co-Chair Professor Robert Wayne, Co-Chair Sea otters (Enhydra lutris) were hunted to the verge of extinction by fur traders in the 18th-19th centuries and provide a remarkable example of survival after an extreme population bottleneck. In this dissertation, I generated and analyzed sea otter genomic data to detect signals of the species’ recent evolutionary transition to marine life and to reveal the impact of the fur trade across the species range. I first explored different methods of demographic inference from genomic data. The inference of historical population size changes, splits, and migrations is one of the primary goals of population genetics and gives profound insights into our own history and that of the species around ii us. In my first chapter I compared several demographic inference methods, determining how well they generate models that fit empirical human population genetic data. I then produced a review of the various demographic inference methods available, with a focus on applying them to non-model organisms. In my second chapter, I sequenced and annotated the sea otter genome and explored the evolutionary history of the sea otter and its distant relative, the giant otter (Pteronura brasiliensis). I found changes to both species’ genomes due to otters’ semi-aquatic lifestyle, including a loss of olfactory receptors. I also discovered that the sea otter has extremely low genetic diversity and elevated levels of putatively deleterious variation. In my final chapter, I sequenced regions of the genome from 122 sea otters from across the species’ global range. I also generated ancient sea otter DNA from three samples dating from 300-1500 years ago. I found that sea otters in California are the last remnants of a highly diverged sea otter lineage and that the pre-fur trade genetic structure of sea otter populations has been preserved. I used the demographic methods examined in Chapter I to detect a signal of extreme population decline in every sea otter population, likely caused by the fur trade bottleneck. I then used simulations to show how this decline may have increased the burden of harmful genetic variation. My dissertation gives new insights into the evolutionary history of the sea otter, a keystone species of profound ecological importance. The work as a whole provides a model for genomic analyses of a non-model organism and illustrates how demographic inference and simulations can be powerful tools for studying the decline of wild populations. iii The dissertation of Annabel Carroll Beichman is approved. Janet S. Sinsheimer Kirk Edward Lohmueller, Committee Co-Chair Robert Wayne, Committee Co-Chair University of California, Los Angeles 2020 iv Dedicated to Gidget Photograph courtesy of the Monterey Bay Aquarium v TABLE OF CONTENTS ACKNOWLEDGEMENTS ......................................................................................................................... X CURRICULUM VITAE .......................................................................................................................... XVI CHAPTER I, PART ONE: COMPARISON OF SINGLE GENOME AND ALLELE FREQUENCY DATA REVEALS DISCORDANT DEMOGRAPHIC HISTORIES ........................................................................... 1 ABSTRACT ................................................................................................................................................... 2 INTRODUCTION ............................................................................................................................................ 3 METHODS ................................................................................................................................................... 9 RESULTS ................................................................................................................................................... 18 DISCUSSION .............................................................................................................................................. 28 ACKNOWLEDGEMENTS ................................................................................................................................ 37 AUTHOR CONTRIBUTIONS ............................................................................................................................ 37 TABLES ..................................................................................................................................................... 38 Table 1 ................................................................................................................................................ 38 FIGURES ................................................................................................................................................... 39 Figure 1 .............................................................................................................................................. 39 Figure 2 .............................................................................................................................................. 40 Figure 3 .............................................................................................................................................. 41 Figure 4 .............................................................................................................................................. 42 Figure 5 .............................................................................................................................................. 43 Figure 6 .............................................................................................................................................. 44 Figure 7 .............................................................................................................................................. 45 REFERENCES ............................................................................................................................................. 46 vi CHAPTER I, PART TWO: USING GENOMIC DATA TO INFER HISTORIC POPULATION DYNAMICS OF NON-MODEL ORGANISMS .................................................................................................................. 54 ABSTRACT ................................................................................................................................................. 55 1. WHY GENOMIC DATA? ............................................................................................................................ 55 2. METHODS FOR DEMOGRAPHIC INFERENCE ................................................................................................. 57 3. DEMOGRAPHIC INFERENCE IN NON-MODEL SPECIES ..................................................................................... 74 4. RECOMMENDATIONS .............................................................................................................................. 82 FIGURES ................................................................................................................................................... 89 Figure 1 .............................................................................................................................................. 89 Figure 2 .............................................................................................................................................. 90 Figure 3 .............................................................................................................................................. 91 Figure 4 .............................................................................................................................................. 92 ACKNOWLEDGMENTS .................................................................................................................................. 93 AUTHOR CONTRIBUTIONS ........................................................................................................................... 93 REFERENCES ............................................................................................................................................. 94 CHAPTER II: AQUATIC ADAPTATION AND DEPLETED DIVERSITY: A DEEP DIVE INTO THE GENOMES OF THE SEA OTTER AND GIANT OTTER. ........................................................................ 105 ABSTRACT ............................................................................................................................................... 106 BACKGROUND .......................................................................................................................................... 107 RESULTS ................................................................................................................................................. 111 DISCUSSION ...........................................................................................................................................

Load more