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The Evolutionary Paths to Diversity

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University of Reading The evolutionary paths to diversity Ciara O’Donovan PhD Thesis School of Biological Sciences September, 2018 This thesis is dedicated to the ancestors of my own lineage To Charles Sharp - with whom I would have loved to discuss all this – and to his wife Anne-Marie, their daughter Leonie Lazarus and grand-daughter Corinne O’Donovan. To Margaret ‘Peggy’ O’Donovan – who prayed for so many years - and to her husband John and their son Bryan O’Donovan. The apple never falls far from the tree i ii Declaration I confirm that this is my own work and the use of all material from other sources has been properly and fully acknowledged. Chapter 1 is published as: O’Donovan, C., Meade, A. and Venditti, C. (2018). Dinosaurs reveal the geographical signature of an evolutionary radiation. Nature Ecology and Evolution. 2, 452-458 Author contributions are as follows: - Hypothesis formulation: COD, CV and AM - Data collection: COD - Analyses: COD - Writing: initial manuscript draft written by COD with CV and AM contributing to subsequent drafts. Ciara O’Donovan iii iv Abstract At the heart of diversity lies evolution, a continually acting process that has shaped and honed the enormous variety of life forms on Earth. To study evolutionary tempos and modes at a high resolution this thesis uses ancestral state reconstruction. This powerful, statistical method works within the framework of a novel, phylogenetic model which flexibly embraces the temporal and taxonomic complexity of the evolutionary process. Consistently across geographical and morphological data covering a wide range of species from dinosaurs to angiosperms to fish, evolutionary mode is broadly characterised by an overwhelming majority of negligible and small sized changes, interspersed with comparatively rare, exceptionally large ones. However, importantly, evolution is shown to work on a continuous scale without such categorical distinction. At a finer level, the magnitude of evolution’s steps differs depending on the direction of change being selected for, organisms’ biological history and the environment an organism evolves in. Changes to morphology of an exceptional magnitude have contributed to the process of undergoing major evolutionary transitions such as those seen in cetaceans and bats. These exceptional changes also differentially affect speciation and body size evolution depending on the nature of an organism’s environment. The signatures of evolutionary and ecological processes through time are revealed, for the first time showing that global scale movement across a famous evolutionary radiation universally follows an early burst pattern, moderated by speciation. On a larger temporal and taxonomic scale evolutionary changes increase in magnitude constantly through time suggesting that despite physical space filling up, there is no limit to evolutionary potential or to the diversity it creates. Current results spanning varying scales are viewed in the light of historical concepts of adaptive landscapes with leaps between and within peaks and zones, and are reconciled within the framework of this complex biological paradigm. v vi Acknowledgements “It doesn’t matter how you get from A to B, so long as you get there!” Chris Venditti, (2014)1 Without doubt my first thanks go to Chris Venditti without whom I would not have attempted a PhD, less, completed one. He has worked patiently and tirelessly to teach me how to conduct new and exciting research. Chris has listened to talks being practiced, viewed posters, convinced me to face the worlds of statistics and learning R and has stood by me throughout, even on the hardest of days. He has been committed to me as a student and has been a truly wonderful supervisor and friend, both of which must have been challenging at times. He has nurtured my interests, both allowing and facilitating work that I could never have been more captivated by. Through his hard work primarily, I have become a scientist and I feel grateful, honoured and lucky to have been able to spend the last four years working so closely with him. Huge thanks also go to my second supervisor, Andrew Meade without whom I would never have been able to produce work of the scale and impact that is presented in this thesis. He has written and developed new code, taught me how to ‘speak’ to computers, helped me to run thousands of analyses over and over until they were right and never once lost his patience or good nature despite being faced with a student who at times probably lost both. Andrew has been a kind and constant help and I am incredibly grateful to know and have worked with him. The Evolution Group at the University of Reading is a prestigious one, and it has been a pleasure and an honour to be a part of it. I would like to thank Mark Pagel who has been an enormous support throughout the last few years. His faith in my potential and the constant intellectual nourishment that he has provided have helped to make me into a more rounded and thoughtful researcher and person generally. Joanna Baker and Manabu Sakamoto have both been a huge part of my PhD experience. They have always been generous with their time and knowledge, helping with anything they could but particularly with programmes such as R and Inkscape at the slightest sign of trouble. Other invaluable members of this group include Louise Johnson, Annemarie Verkerk, Rebecca Grollemund, Renske Gudde, Simon Branford, Henry Ferguson-Gow, Igor Siveroni, Sammy Field, Jorge Avaria-Llautureo, Kirsten Farncombe and last but by no 1 Venditti, C. (2014). Personal communication. vii means least George Butler. These people have been important and wonderful figures both within and outside of the office environment. The last four years has encompassed a whole spectrum of life ranging from the extremes of happiness to those of being less so. Throughout all of this my family and friends have surrounded me with support and encouragement, reminding me that it will all be okay in the end. They have repeatedly forgiven my long absences both physical and emotional and continue to stand by me, cushioning my falls and championing my successes. My parents, grandmother and godmother have been unflappable constants, offering unbounded measures of love, kindness and help, all of which I have called upon and could not have done without. They have talked me down from hysteria and guided me through times when things felt insurmountable. Making these four incredible family members proud has been a major source of motivation. Mention must specifically also go to Pri and Charlotte – better friends than anyone could dream of. Late night conversations, daily messages, visits and prosecco drinking, they too have been constant figures in my life with the last few years being no exception. I am so grateful to them for their warmth and love, for always being there, always helping and always knowing what to say to make things better. They have never failed to bring laughter, comfort and pure happiness to my life. I feel honoured and lucky to have a support network that has the strength of steel and which has made me feel encircled by friends, some of whom need to be named are Tilly, Rachel, Jo R, Sue, Anna, Emily, Shef, Frankie, Sally and Margery. These friends have protected me, anchored me and reminded me of who I am during times when I was lost, or at least felt that way. They have sent words of support and motivation along with crazy photos and videos that always make me laugh; collectively and individually they are my home. Over the last four years I have adapted and evolved in wonderful and unexpected ways and certainly more resemble an animal suited to the academic environment now than four years ago. I have been spoilt with the knowledge and expertise that have surrounded me. In addition to this, I have learnt my own strength and resilience in the face of personal and academic adversity. These years provide my foundation as an adult and as a scientist who can move forward and stand on the shoulders of giants. To the eleven year old girl who wanted to be ‘a scientist’ when she grew up, with the help of everyone mentioned and more, we have done it! viii Contents Declaration…………………………………………………………………………………………………………..…........iii Abstract……………………………………………………………………………………………………………..................v Acknowledgements…………………………………………………………………………………………...............vii Introduction…………………………………………………………………………………………………………............1 References…………………………………………………………………………………………………….......13 Chapter 1 – Dinosaurs reveal the geographical signature of an evolutionary radiation….....................................................................................................................................................21 Abstract………………………………………………………………………………………………………..……21 Introduction………………………………………………………………………………………………..……..22 Results and Discussion………………………………………………………………………………..…….22 Conclusion…………………………………………………………………………………………………..…….29 Methods………………………………………………………………………………………………..…………..30 References…………………………………………………………………………………………………..…….40 Appendix 1…………………………………………………………………………………………………..……45 Chapter 2 – The nature of morphological change...................................................................57 Abstract………………………………………………………………………………………………..……………57 Introduction………………………………………………………………………………………………..……..58 Methods……………………………………………………………………………………..……………………..59 Results………………………………………………………………………………………………..……………..65 Discussion…………………………………………………………………………………………..………….....70 References………………………………………………………………………………..……………………….79
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