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The Consequences of Life Without Sex an Examination Into Taxonomy and Evolution of the Anciently Asexual Bdelloid Rotifers

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The Consequences of Life Without Sex an Examination Into Taxonomy and Evolution of the Anciently Asexual Bdelloid Rotifers The Consequences of Life without Sex An Examination into Taxonomy and Evolution of the Anciently Asexual Bdelloid Rotifers Cuong Quoc Tang A thesis submitted for the degree of Doctor of Philosophy from the Department of Life Sciences, Imperial College London July 2014 59 The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution-Non Commercial-No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or distribution, researchers must make clear to others the licence terms of this work. 59 Abstract The anciently asexual bdelloid rotifers are a ubiquitous and ecologically important group coined “evolutionary scandals” owing to their diversification and persistence over evolutionary time despite the pressures of obligate parthenogenesis. Understanding the biodiversity of rotifers, in the context of reproductive mode, will aid in the understanding of how differences in sex and ecology drive biodiversity patterns. Given that resolved taxonomy is a prerequisite to investigating larger scale macroevolutionary patterns, and that rotifer taxonomy is confounded by morphostasis, cryptic diversity, and a dearth of expert taxonomists, this thesis first deals with the use of DNA taxonomy as a tool to alleviate the taxonomic crisis so prevalent in the group. Results from multiple meta-analyses exploring the effects of choice in gene, phylogenetic reconstruction methods, and species delimitation metrics, provide better guidelines for DNA taxonomy. The analyses suggest that coalescent-based DNA taxonomy using the Generalised Mixed Yule Coalescent model in conjunction with the cytochrome oxidase 1 subunit c gene analysed in a Bayesian inference phylogenetic framework using BEAST, provides realistic and tangible species clusters (evolutionarily significant units; ESU) in both asexual and sexual organisms. Using these ESUs, the efficacy of DNA barcoding for identifying rotifer species is examined. These analyses suggest that the sexual monogonont rotifers are more readily identifiable than the asexual bdelloid rotifers. Explicit comparison of genetic discreteness of asexual and sexual rotifers indicates that sexual rotifers are separated by larger genetic and phylogenetic gaps than asexual rotifers and thus are more discrete. Combined, these analyses indicate that sex, specifically reproductive isolation, is the predominant factor in explaining why species form discrete clusters rather than a continuum of forms. Finally, a dated multilocus molecular phylogeny of Bdelloidea is reconstructed. The phylogeny suggests that bdelloid rotifers have persisted for at least 40 million years, but that bdelloid higher taxa are typically polyphyletic. 3 Acknowledgements I would like to thank Diego and Tim for their support all the way through the PhD. From you I’ve learnt what it is to be a scientist, and your example is an inspiration and something I want to emulate. Of all of the candidates, I’m glad you picked me. I hope that through all this work I’ve been a valuable addition to your groups. Thanks for never saying no, irrespective of how odd things sounded. Everything I’ve done for this PhD is down to you both. Years in the Barralab and the ever expanding BLAB family have been a huge privilege. Thanks for all of the help and for being such a pleasure to work alongside. Your support has been a massive pick me up. In particular, Aelys Humphreys, Isobel Eyres, and Chris Wilson for their discussions on all things evolutionary and bdelloid, and Alejandra, Diane, Francesca, Chris, Matt, Shorok, Damian, Drew, and Laura, for making, sometimes, gruelling days much more enjoyable. Life at Silwood wouldn’t have been the same had it not been for the friends that I’ve been fortunate enough to make on the way, you are too numerous to name, but you know who you are. Thanks to nearly all of my housemates over the years, especially Shorok who has been looking after me and feeding me for the last few months. You’ve all given me respite from work and stopped me going really peculiar towards the end. Yet all of this wouldn’t have been possible without the support of my family. I dedicate this thesis to them. Your enthusiasm and pride for my academic career is only matched by the bemused expressions you have when I try to explain what it is I do. Cảm ơn bố và mẹ. To Elle, you make me a happier person. Always. And to Charlie, who would have been a better academic than me. 4 This thesis was funded by a NERC studentship. Declaration of originality I hereby declare that this thesis includes some work that has been the result of joint work. In all cases, the key ideas, primary contributions, experimental designs, data analysis, interpretation, and writing were performed by myself under the supervision of both Tim Barraclough and Diego Fontaneto, but specific chapters have been made possible by certain collaborators providing data. Chapter 2 has been published in a slightly modified form in: Tang CQ, Leasi F, Obertegger U, Kieneke A, Barraclough TG, Fontaneto D. (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences of the United States of America, 109, 16208–16212. Three of the 55 alignments used were generated by Francesca Leasi (Testudinella spp.), Ulrike Obertegger (Synchaeta spp.), and Alex Kieneke (Turbanella spp.). The rest of the datasets were generated either by myself, or collated by myself from GenBank. Chapter 3 is in press at Methods in Ecology and Evolution as: Tang, CQ, Humphreys, AM, Fontaneto, D, Barraclough, TG (2014) Effects of phylogenetic reconstruction method on the robustness of species delimitation using single‐locus data. Methods in Ecology and Evolution. All of the data was either downloaded from GenBank or provided by Chris Meyer (cowries dataset). The analyses and the manuscript was performed and written principally by myself, with helpful comments from Aelys Humphries. Chapter 5 is in press at Evolution as: Tang, C. Q., Obertegger, U., Fontaneto, D., & Barraclough, T. G. (2014). Sexual species are separated by larger genetic gaps than asexual species in rotifers. Evolution, 68(10), 2901–2916. The data were mostly downloaded from GenBank, but additional targeted sequencing was obtained by Ulrike Obertegger. Other than these targeted sequences, all of the data collection and analyses were performed by myself. Chapter 6 uses samples collected by myself, Nataliia Iakovenko, Chris G. Wilson, Carl W. Birky Jr, and Diego Fontaneto. Nuclear primers were designed using transcriptomic alignments provided by Isobel Eyres and Tim Barraclough. All of the subsequent lab work and analyses were performed by myself. Permission to reprint chapters 2, 3, and 5 can be found at the back of the thesis (pp208-210). 5 Table of contents Abstract ................................................................................................................................................... 3 Acknowledgements ................................................................................................................................. 4 Declaration of originality ........................................................................................................................ 5 Table of contents ..................................................................................................................................... 6 Figures and tables ................................................................................................................................. 10 Data accessibility .................................................................................................................................. 14 Abbreviations ........................................................................................................................................ 15 Chapter 1: Introduction ......................................................................................................................... 17 Rotifera ....................................................................................................................................... 18 Defining asexual species ............................................................................................................. 19 Ancient asexuality ...................................................................................................................... 20 Bdelloid rotifers ..................................................................................................................... 20 Oribatid mites (Acari: Arthropoda) ....................................................................................... 21 Darwinulid ostracods (Ostracoda: Arthropoda)..................................................................... 21 Timema stick insects (Pterygota: Arthropoda) ...................................................................... 22 Root knot nematodes (Secernentea: Nematoda) .................................................................... 22 Taxonomy ................................................................................................................................... 22 Molecular techniques and their limitations: Issues with using one locus instead of many ... 24 DNA barcoding ....................................................................................................................
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