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Conceptual and Empirical Investigations of Eukaryotic Transposable Element Evolution

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Conceptual and Empirical Investigations of Eukaryotic Transposable Element Evolution Conceptual and Empirical Investigations of Eukaryotic Transposable Element Evolution by Tyler Adam Elliott A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Integrative Biology Guelph, Ontario, Canada © Tyler Adam Elliott, December, 2016 ABSTRACT Conceptual and Empirical Investigations of Eukaryotic Transposable Element Evolution Tyler Adam Elliott Advisor: University of Guelph, 2016 Professor T.R. Gregory Transposable elements (TEs), mobile pieces of self-replicating DNA, are one of the driving forces behind genomic evolution in eukaryotic organisms. Their contribution to genome size variation and as mutagens has led researchers to pursue their study in the hope of better understanding the evolution of genomic properties and organismal phenotypes But TEs can also be thought of in a multi-level evolutionary context, with TEs best understood as evolving populations residing within (and interacting with) the host genome. I argue, with empirical evidence from the literature, that the multi-level approach advocated by the classic ―selfish DNA‖ papers of 1980 has become less commonly invoked over the past 35 years, in a favour of a strictly organism-centric view. I also make the case that an exploration of evolution at the level of TEs within genomes is required, one which articulates the similarities and differences between a TE population and a traditional population of organisms. A comprehensive analysis of sequenced eukaryote genomes outlines the landscape of how TE superfamilies are distributed, but also reveals that how TEs are reported needs to be addressed. A proper exploration of evolution at the TE level will require a dramatic change to how TE information is annotated, curated, and stored, and I make several specific recommendations in this regard. ACKNOWLEDGEMENTS This thesis represent the most taxing work I‘ve done, for various reasons, and there are many people to thank for it finally coming to fruition. I‘d like to thank my advisor Ryan Gregory for guiding me through this sometimes strange PhD experience. I‘ll always be grateful for the opportunities I‘ve been given by working with an advisor who is always willing to help me explore interesting and new areas of research. Dr. Stefan Linquist introduced me to the world of philosophy years ago, and I greatly value his friendship, and the new perspective this had afforded me. Dr. Teri Crease has always been a sympathetic and wise ear when I was having a problem, and is nearly always able to answer the questions I have so very easily. She is a font of knowledge that all graduate students should be so lucky to have her just two doors away. My thanks go to Dr. Cort Griswold, for being subjected to countless meetings where we discussed TEs. Although that particular project didn‘t come to fruition, I know that Cort has incorporated TEs into his lectures. I consider that an immense win. Without the support of my lab mates and colleagues, graduate school would have been way less enjoyable. Dr. Nick Jeffery was a joy to sit beside for 5 years, and in him I will always have a life-long friend. Brent Saylor was always there when I needed a fellow TE person to complain to about the quirks of our field, and his bioinformatics knowledge was invaluable to this PhD. And it amazes me that we never drove each other nuts on the 10 hour long drives to TE meetings at Cold Spring Harbor and Woods Hole. I would also like to thank all past members of the Gregory, Hebert, Crease, Lynn and Adamowicz labs for their friendship and help over the years. To Haley, Darren, Katherine and Ella, thank-you for bringing countless smiles to my face this past year. iii Many others contributed in smaller ways to this thesis, in the form of advice, both in person, at the pub and through mail, electronic or otherwise. These include: Dr. Sally Adamowicz, Dr. Peter Cock and the Biostar forum, the TE community on Twitter, Dr. Gabriel da Luz Wallau, Dr. Arnaud Le Rouzic, Dr. Roland Vergilino, Dr. Ilia Leitch, Dr. Arvid Ågren, Dr. Peter A. Peterson, and Dr. Ellen Clarke. I would also like to thank Dr. Roy G. Danzmann and Dr. Cedric Feschotte for serving on my defence committee and providing useful suggestions and stimulating conversation. To the Science and Philosophy squad (I guess that‘s what we are now): Dr. Karl Cottenie, Dr. Stefan Kremer, Dr. Stefan Linquist, Ryan and Brent. Our weekly meetings were always enlightening, even the ones where we got side-tracked on inexplicable tangents that had nothing to do with TEs, community ecology, computer science or philosophy. NSERC grants to Ryan, and OGS and OGSST grants to myself, provided the resources to be able to learn as a vocation. We all know academic departments cannot run smoothly without the efforts of wonderful staff. Thanks go to Lori Ferguson, Monica McKay, Debbie Bailey and Mary Ann Davis. That which has kept me sane over these 5 years deserves accolades: Mike, Joel, the Mads and the Bots, Ed Greenwood and his Forgotten Realms, the Tell‘Em Steve-Dave podcast, and the folks at Red Letter Media. My friends Dan, Victoria, Matt, Bill, Brandon, Ryan and Shane were always there throughout the years to provide laughs and comfort. I look forward to being able to spend more time with them in the future, and being able to respond with more than ―finishing my thesis‖ when they ask what I‘m doing. My family has always been there for me. I‘m grateful to have grown up with four sisters iv whom I admire, love and respect. And without my brother-in-law, I wouldn‘t know the power of positive thinking. To Shannon, Derek, Kirstin, Marissa, Rhianna, Adrian, Kevin, Christina and Oliver; I love you all. More so than any other people, I owe the greatest thanks to my parents, Douglas Elliott and Sonia O‘Brien. They must have seen the budding scientist in me all those many decades ago and never stopped encouraging me. I dedicate this thesis to them. v STATEMENT OF AUTHORSHIP AND CONTRIBUTIONS All chapters herein were written by the author of this thesis alone. Chapter 3 is based upon two publications published in The Philosophical Transactions of the Royal Society of London B (2015, Vol. 370, pg. 20140331) and BMC Evolutionary Biology (2015, Vol. 15, pg. 69), both co-authored with Dr. T. Ryan Gregory. For these papers, and for Chapter 2, both co- authors had input on study design, but data collection and analysis were performed by me. The ideas from Chapter 4 were conceived of by the author of this thesis, with some input from Dr. T. Ryan Gregory. vi TABLE OF CONTENTS ACKNOWLEDGEMENTS………………………………………………………...…..……...iii STATEMENT OF AUTHORSHIP AND CONTRIBUTIONS…………………………...….vi TABLE OF CONTENTS……………………………………………………………………....vii LIST OF TABLES…………………………………………………………………………...…xii LIST OF FIGURES…………………………………………………………………………....xiii LIST OF ABBREVIATIONS……………………………………………………………...….xvi LIST OF APPENDICES………………………………………………………………...…….xix Chapter 1 A general introduction to transposable element biology and evolution………...............……1 Abstract…………………………………………………………………………...………1 Introduction……………………………………………………………………………....2 The diversity and evolution of eukaryotic transposable elements…………………….3 Class I- Retrotransposons…………………………………………………………5 i)Penelope………………………………………………………………....6 ii) LINEs/Non-LTRS…………………………………………………...…6 iii) SINEs………………………………………………………………….8 iv) Long terminal repeat retrotransposons (Ty3/Gypsy, Ty1/Copia, BEL/Pao)………………………………………………………………………………………..…9 v )Dictyostelium intermediate repeat sequences (DIRS) and relatives…..11 vi) Miscellaneous non-autonomous retrotransposons………………...….12 Class I – DNA Transposons…………………………………………………...…13 vii i) Inverted terminal repeat elements…………………………………..…13 ii) Maverick/Polinton………………………………………………….....15 iii) Helitrons……………………………………………………………...16 iv) Cryptons……………………………………………………………...17 v) Miscellaneous non-autonomous DNA transposons…………………..18 TE biology and behavior…………………………………………………………….…20 Vertical inheritance and horizontal transmission………………………………..22 TE-organisms interactions……………………………………………………………..24 Overview of this thesis……………………………………………………………….…30 Where we have been…………………………………………………………...…31 What we know……………………………………………………………...…….32 Where we are going………………………………………………………..…….33 Tables and figures…………………………………………………………………..…..35 Chapter 2 Where we have been: the Selfish DNA hypothesis, then and now …………………….……42 Abstract……………………………….…………………………………………….…...42 Introduction……………………………………………………………………………..43 Setting the context: views on genome function before 1980………………………….46 The concept of selfish DNA before 1980 ………………………………………...……50 What the 1980 papers on selfish DNA did not say……………………………………52 Doolittle and Sapienza, 1980…………………………………………………….52 Orgel and Crick, 1980…………………………………………………………...54 viii Misconception about the selfish DNA hypothesis………………………………..56 Early reactions to the selfish DNA papers…………………………………………….57 Elaboration of the selfish DNA concept…………………………………………….....61 How the selfish DNA papers have been cited over the past 35 years………………..64 An updated view of selfish DNA……………………………………………………….68 Concluding remarks…………………………………………………………………....71 Tables and figures..........................................................................................................73 Chapter 3 Where we are: Transposable element abundance and diversity in genomes of different sizes………………………………………………………………………………………………75 Abstract……………………………….…………………………………………………75 Introduction…………………………………………………………………………..…76 Methods………………………………………………………………………………….80
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