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An Evolutionary History of the Peregrine Epigeic Earthworm Lumbricus Rubellus

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An Evolutionary History of the Peregrine Epigeic Earthworm Lumbricus Rubellus An evolutionary history of the peregrine epigeic earthworm Lumbricus rubellus Pierfrancesco Sechi Thesis submitted to Cardiff University in candidature for the degree of Doctor of Philosophy September 2013 Cardiff School of Biosciences Cardiff University DECLARATION This work has not previously been accepted in substance for any degree and is not concurrently submitted in candidature for any degree. Signed ................................................ (candidate) Date ........................... STATEMENT 1 This thesis is being submitted in partial fulfilment of the requirements for the degree of PhD. Signed ................................................ (candidate) Date ........................... STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. Signed ................................................ (candidate) Date ........................... STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter- library loan, and for the title and summary to be made available to outside organisations. Signed ................................................ (candidate) Date ........................... STATEMENT 4 – BAR ON ACCESS APPROVED I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter- library loans after expiry of a bar on access previously approved by the Graduate Development Committee. Signed ................................................ (candidate) Date ......................... An evolutionary history of the peregrine epigeic earthworm Lumbricus rubellus Pierfrancesco Sechi* Supervisors: Prof. Michael W. Bruford Organisms and the Environment research group, Cardiff School of Biosciences, Cardiff University, UK Address: The Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX Prof. Peter Kille Organisms and the Environment research group, Cardiff School of Biosciences, Cardiff University, UK Address: Main building, Museum Avenue, Cardiff, Cf10 3AT This work was financed by Agenzia regionale per il lavoro, Regione Sardegna (Italy) with a PhD grant relative to the Master and Back program – Alta Formazione (High Education), ref. n. 9847. *Email for correspondence: [email protected] II “Still round the corner there may wait A new road or a secret gate, And though we pass them by today, Tomorrow we may come this way And take the hidden paths that run Towards the Moon or to the Sun.” John Ronald Reuel Tolkien III Summary Recent studies have indicated the presence of a high degree of cryptic genetic diversity in some clitellate sentinel species. One of these species, the earthworm Lumbricus rubellus, has been recently found to comprise two divergent clades in the UK, and are possibly cryptic species. L. rubellus is commonly used in ecotoxicological assays, where undetected differences in contaminant responses between cryptic lineages may lead to confusing or misleading results. Furthermore, given the key role that earthworm species play in the soil ecosystem, a better understanding of cryptic diversity is necessary to investigate whether divergent lineages play different roles within their ecosystems. In this study, the phylogenomics of the acid-tolerant, cosmopolitan, epigeic species Lumbricus rubellus was investigated, with regard to demography during the glacial stages of the Pleistocene and the recent post-glacial colonization of North Europe using mitochondrial DNA markers, next-generation sequencing and environmental niche modelling tools. The niche suitability of L.rubellus during the last 120.000 years was inferred, allowing hypotheses on survival and recolonisation to be constructed. Phylogenetic, population structure and coalescent-based analyses resulted in the discovery of 11 deep divergent lineages (with levels of divergence up to 18% for mitochondrial markers), which most likely survived in refugia during Pleistocene glaciations. Signatures of expansions point to a possible recolonisation of central Europe during the last Glaciation, survival of one of the clades in a northern cryptic glacial refugium and a consequent recolonisation of northern Europe during the last 10,000 years. Genetic evidence and divergence time ultimately suggest that L. rubellus is a cryptic species complex, which clades diverged as far as ~5MY ago. The entire mitochondrial genome of the species complex is described here for the first time, and a survey of the deep phylogenetic signal over the mitochondrial genomes of eight selected individuals was carried out, supporting and deepening the phylogeny constructed using only two mitochondrial genes. Finally, whole genome analysis of genetic divergence supported the hypothesis of cryptic divergence for the two most divergent lineages selected. IV To my Father Vittorio, my Mother Speranza and my Brother Antonello with all my love and gratitude V ACKNOWLEDGEMENTS I am not afraid to overstate when I describe this experience as one of the most terrifying, thrilling, painful, exciting, instructive (in terms of life as much as in terms of science) and important experiences of my life. Words cannot express how much these four years changed me and, I think, made me a better person. It was a fantastic trip, and I wish to thank with all my heart all the companions I met along the road. First of all, I’d like to thank my supervisors. Mike, thank you for your relentless support and the endless trust in me, even in those moments when I was short of it. Thanks for teaching me the real meaning of being a professional, of not giving up in difficult times, and for being an example of what it means to be a great scientist without forgetting to be a human being. It was a privilege to have the opportunity to work with you! Pete, thank you for your great help and support and for inspiring me with your inexhaustible enthusiasm and your precious suggestions. Every chat with you was like a roller coaster in your incredible scientific mind! It’s been great to have the opportunity to share your ideas and work together at this project. I hope I’ll have many opportunities to collaborate with both of you in the future. To all my colleagues in the lab, for the many adventures we shared: thank you!!! Leila, Rui, Joana, Tania, Renata, Silke, Neeza, Dave, Niall, Jen, Hannah, Xiang Jiang; all the people at PK’s lab: Ceri, Craig, Marta, Dan, Yaser, Gonçalo and Luis; thanks to John, for all the enlightening conversations, for being there at the right time. Thanks to the Portuguese “children”, with whom I had great fun during my third year: Jorge and Renatinha. Thanks to my dear ladies, Mafalda and Isa, for the many dinners, drinks, jokes, discussions and laughs, for your constant help with life and work, and for being always close to me. Thanks to Rob, the best companion for worm hunting ever! A special thanks to two persons which arrival literally turned the tide of my Ph. D.: thanks to Pablo, for supporting me, directing me, teaching me, making me believe that I could do it. I cannot imagine how I could have completed this without you. Oh and also thanks for all the attempts to make me drunk (yeah, you succeeded a couple of times…)! Thanks to Mario, for deciding to come here, for all the fun, laughs and jokes, and for the many challenges faced together. A good friend on your side always makes things easier. VI Thank you to all my friends outside the lab. First of all, thanks to Lara. I would not be here if it wasn’t for you! Eleni, Osian and Axileas: you’re a constant in my Cardiff life! My beloved Doctor Arianna: thanks for your endless and unconditioned love and friendship. Thanks to Morena, for all the chats, and cakes, and laughs in our house! And thanks to my former supervisor and colleague Laura… all my gratitude for the cheerleading. It really helped! Thanks to all the friends whose lives are now unfolding in other countries. Even though you went away and you’re not close anymore, I will never forget you. Danilo, Argyro, and their beautiful son Alexandros; my little Malaysian sister Faezah; Leonidas, the bloody genius; Juan Carlos and his beautiful family. I look forward to see you all again. Thanks to all my friends of a life, back in the beautiful Sardinia: Daniele Sani, Daniele Campus, Ignazio, Luigi. Thanks to my former rock band Colt: Luca, Antonio, Bruno and my “surrogate”, Francesco! And thanks to my “acquired brothers”, Gianni and Joe, and to their ladies Maria Giovanna and Mary. Every time I went back, you made me feel like I’d never left. Thanks to my family, with all my heart. Thank you for patiently listening my whining in bad moments and sharing my joy in good moments, for the constant encouragement and support and for all the love. Finally, thank you, Margherita. It was a long and hard path, but you were always on my side on the way long. With you, I feel completed. VII TABLE OF CONTENTS DECLARATION……………………………………………………………………..I SUMMARY……………………………………………………………..…………..IV DEDICATION……………………………………………………………………….V ACKNOWLEDGEMENTS………………………………………………...……...VI TABLE OF CONTENTS…………………………………………….…………..VIII LIST OF FIGURES………………………………………………………………...XI LIST OF TABLES…………………………………………………………………XV CHAPTER 1 GENERAL INTRODUCTION ......................................................... 1 1.1 Foreword .................................................................................................................... 2 1.2 Soil ecosystem engineers ..........................................................................................
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