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Mammoth Phylogeography South of the Ice MAMMOTH PHYLOGEOGRAPHY SOUTH OF THE ICE MAMMOTH PHYLOGEOGRAPHY SOUTH OF THE ICE: LARGE- SCALE SEQUENCING OF DEGRADED DNA FROM TEMPERATE DEPOSITS Jacob M. Enk, B.A., M.Sc. A Thesis Submitted to the School of Graduate Studies in Partial Fulfilment of the Requirements for the Degree Doctor of Philosophy McMaster University © Copyright by Jacob M. Enk, February 2014 Ph.D. Thesis – Jacob M. Enk; McMaster University – Department of Biology DOCTOR OF PHILSOPHY (2014) McMaster University (Biology) Hamilton, Ontario TITLE: Mammoth phylogeography south of the ice: large-scale sequencing of degraded DNA from temperate deposits AUTHOR: Jacob M. Enk, B.A. (Indiana University), M.Sc. (University of Utah) SUPERVISOR: Hendrik N. Poinar, Ph.D. NUMBER OF PAGES: (xii), 145 ii Ph.D. Thesis – Jacob M. Enk; McMaster University – Department of Biology ABSTRACT Extinct Pleistocene mammoths (Mammuthus) have been studied extensively at the genetic level. However due to both taphonomic and technological limitations, ancient DNA has been characterized from only one of several late Pleistocene mammoth species, the woolly mammoth (M. primigenius). This greatly limits our impression of their evolution and population history to the steppes of the northern latitudes, just one of several environments in which mammoths lived and went extinct. It also obscures the chronology of underlying population processes of this keystone megaherbivore, which prevents putting their history in the proper climatic and biogeographic context. Fortunately recent technological advances in high-throughput sequencing and targeted enrichment promise to expand mammoth and other Pleistocene faunal population phylogeography to non-permafrost, non- cave burial contexts. However the capacity and behavior of these combined technologies for characterizing poorly- preserved ancient DNA is largely unexplored, preventing efficient and routine use for population-level studies. In this thesis I test and apply these technologies to remains of mammoth species found in the temperate areas of North America. I first demonstrate their potential in sequencing DNA from these poorly-preserved remains, and then I evaluate new methods for their efficient application to large sample sets, as well as for capturing complete nuclear genomes. I then use these technologies to sequence dozens of mitochondrial genomes from Columbian (M. columbi) and other non-woolly mammoths, reconstructing their matrilineal phylogeography south of the ice. The revealed patterns not only imply a deep chronology for mammoth matrilineal diversity observed to date, but also that mammoth evolution in North America was likely characterized by separate episodes of interbreeding between resident and invading populations, and between ecotypes. Overall the biological and methodological discoveries afforded by this body of work outline several tools and avenues for future research on mammoth evolution, behavior, and extinction. iii Ph.D. Thesis – Jacob M. Enk; McMaster University – Department of Biology ACKNOWLEDGMENTS Hendrik Poinar is an inspiring scientist, incredibly supportive supervisor, and truly good person. I came to his laboratory intimidated by his and his group’s breadth of technical and conceptual expertise, but now leave it with the confidence to embrace and master new ways of doing things. Even during my episodes of resistance and exacerbation, he provided only patience and encouragement. And occasionally frisbee during work hours. Thanks to my committee members Brian Golding and Jim Quinn, for guidance and keen scrutiny over this past half decade of my research. Their novel and varied perspectives were invaluable in making this project address broader issues of animal behavior and evolution. I would not be involved in this science if it were not for Rika Kaestle. It was in her ancient DNA lab that I used my first pipette, did my first PCR, ran my first gel, and first sequenced DNA. I hope to honor her decision to let a rambunctious young undergrad like my former self work with sensitive ancient remains. Despite my short time working with Regis Debruyne, he taught me a tremendous amount and remains an inspiration. He also performed much of the work that would form the foundation of this project. Dennis O’Rourke, my Master’s supervisor, once asked “So I have this mammoth – do you want to work on it?” This is the result. Thanks especially to Dennis for that, and for encouraging me to follow wherever my curiosity led. Thanks also to Alan Rogers for always having time to bounce ideas around, and to Jack Broughton for teaching me to ask, “What is the research question?” I cannot describe how much the habit of asking that question has impacted my professional and personal frame of mind. We were a tight group at the McMaster Ancient DNA Centre. This project grew from countless hours of discussion and troubleshooting, especially with my friends and colleagues Alison Devault, Christine King, and Melanie Kuch. I thank them and all the present and former members of our lab for always being willing to discuss even the most numbing experimental details, and teaching me how to think. I especially thank my dear friend, Tina Li. Her unwavering companionship and simultaneous intolerance for bullshit allowed me to keep my emotional and mental sanctity through this process. And finally, thanks to my parents. It is impossible to list all the reasons. Much love to them both. iv Ph.D. Thesis – Jacob M. Enk; McMaster University – Department of Biology TABLE of CONTENTS I INTRODUCTION 1 1 Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths 4 1.1 Preface 4 1.2 Abstract 4 1.3 Background 4 1.4 Results and Discussion 5 1.5 Conclusions 9 1.6 Materials and Methods 9 1.6.1 Samples 9 1.6.2 Sequence Acquisition, Assembly, and Classification 10 1.6.3 Phylogenetic Analyses 10 1.7 Additional datafiles 10 1.8 Acknowledgments 10 1.9 Additional Datafile 1 – Materials and Methods 11 1.9.1 Laboratories 11 1.9.2 Operating procedures 11 1.9.3 Sample Selection 12 1.9.4 Huntington Mammoth Whole Mitochondrial Genome 12 1.9.4a DNA Extraction 12 1.9.4b Extraction qPCR Screen 12 1.9.4c DNA Size Distribution Measurement 13 1.9.4d Library Preparation 13 1.9.4e Library qPCR Evaluation 13 1.9.4f Sequencing with Illumina 14 1.9.4g Data Processing & Statistics 14 1.9.4h Sequence Assemblies 14 1.9.5 Sanger Sequencing of Huntington and Union Pacific mtDNA 15 1.9.5a DNA Extraction 15 1.9.5b PCR Amplification 15 1.9.5c Cloning and Sequencing 15 1.9.5d Sequence Replication 16 1.9.5e Preservation Evaluation 16 1.9.6 Whole Mitogenome of IK-99-70 16 1.9.6a DNA Extraction 17 1.9.6b Multiplex Primer Design & Optimization 17 1.9.6c Multiplex Amplification 18 1.9.6d Singleplex amplifications 18 1.9.6e Library Preparation 18 1.9.6f Sequencing on 454 GS FLX & Data Processing 18 1.9.6g Sequence Assembly & Fill-In 19 1.9.7 Phylogenetic Analysis 20 1.9.7a Cytochrome b, tRNAs, HVR 20 1.9.7b Whole Mitogenomes 21 1.9.8 Nuclear Genome Read Analysis 21 1.9.8a Read Classification 21 1.9.8b Nuclear Genome Divergence Estimate 22 1.10 Additional Datafile 2 – Supplementary Tables 22 1.11 Additional Datafile 3 – Supplementary Figures 28 v Ph.D. Thesis – Jacob M. Enk; McMaster University – Department of Biology 1.12 References 35 2 Quantitative PCR as a predictor of aligned ancient DNA read counts following targeted enrichment 38 2.1 Preface 38 2.2 Abstract 38 2.3 Introduction 38 2.4 Materials and Methods 39 2.4.1 Quantitative PCR assays 40 2.4.2 DNA extraction and library preparation 40 2.4.3 Bait design 41 2.4.4 Enrichment and re-amplification 41 2.4.5 Sequencing, demultiplexing 41 2.4.6 Curation 42 2.4.7 Alignment 42 2.5 Data availability 42 2.6 Results and discussion 42 2.7 Author contributions 46 2.8 Acknowledgements 46 2.9 Competing interests 46 2.10 Supplementary Figures 47 2.11 Supplementary Tables 59 2.12 References 75 3 Mitogenome phylogeography of Mammuthus from southern North America suggests a deep 78 interspecific chronology 3.1 Preface 78 3.2 Abstract 78 3.3 Introduction 78 3.4 Materials & Methods 80 3.4.1 Summary 80 3.4.2 Sample collection 81 3.4.3 DNA extraction 81 3.4.4 Quantitative PCR screens 82 3.4.5 Library preparation 82 3.4.6 Targeted enrichment 82 3.4.7 Illumina sequencing 82 3.4.8 Libraries with prefix “EID” 83 3.4.9 Shotgun sequencing 83 3.4.10 Data curation 83 3.4.11 Alignment and consensus calling 84 3.4.12 Second-round enrichment and sequencing 84 3.4.13 AMS radiocarbon dating 84 3.4.14 Maximum likelihood tree estimation 84 3.4.15 Mutation rate and tMRCA estimations 85 3.4.16 Bayesian Skygrid analyses 85 3.5 Results & Discussion 86 3.5.1 Mitogenome phylogeography 86 3.5.2 Chronology and mammoth biogeography 88 3.5.3 Population size dynamics 90 3.6 Conclusions 92 3.7 Data Availability 92 3.8 Acknowledgments 92 3.9 Author Contributions 92 vi Ph.D. Thesis – Jacob M. Enk; McMaster University – Department of Biology 3.10 Supplemental Figures 93 3.11 Supplemental Tables 95 3.12 References 124 4 Ancient whole genome enrichment using baits built from modern DNA 128 4.1 Preface 128 4.2 Abstract 128 4.3 Main text 128 4.4 Competing financial interests 130 4.5 Acknowledgments 130 4.6 Author contributions 130 4.7 Supplementary information 130 4.7.1 Elephant DNA extraction 130 4.7.2 Bait synthesis 131 4.7.3 Pleistocene fossil specimens 131 4.7.4 Mammoth and mylodon DNA extraction 131 4.7.5 Library preparation 132 4.7.6 Enrichment and re-amplification 132 4.7.7 Sequencing 132 4.7.8 Read processing and alignment 132 4.7.9 Complexity measurement and projection 133 4.7.10 Supplementary Tables 133 4.7.11 Supplementary Figures 136 4.8 References 137 II CONCLUSIONS 139 III REFERENCES 142 vii Ph.D.
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