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The Evolution of Apomixis in the Asplenium Monanthes Fern Complex

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The Evolution of Apomixis in the Asplenium Monanthes Fern Complex The evolution of apomixis in the Asplenium monanthes fern complex Robert James Dyer A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy and the diploma of Imperial College London Department of Life Sciences Imperial College London March 2013 © The Natural History Museum, London. Asplenium monanthes. Copper plate by Daniel Mackenzie from the original drawing by Sydney Parkinson made during Captain James Cook’s first voyage across the Pacific, 1768-1771. Abstract Asexually reproducing eukaryotes provide a window into the evolution and maintenance of sexual reproduction, and are challenging our concept of a species. In plants, asexual reproduction (apomixis) is known to cause taxonomic problems and has been indicated to have a disparately high frequency in homosporous ferns. The reasons for such a high frequency of apomictic taxa are unclear, and only add to the enigmatic nature of these ferns. Contemporary studies in ferns are focussing on such questions, and are providing valuable insights into the evolutionary dynamics of apomictic ferns. In this thesis, I investigate the evolution of apomixis in the Asplenium monanthes complex. First, I perform a biosystematic study of the complex, based upon plastid and nuclear DNA sequence data, reproductive mode and polyploidy. I present evidence for reticulate evolution and multiple apomictic lineages. Second, I address the problem of species delimitation in an apomictic species complex. I performed a comparative analysis of AFLP data and sequence data using a variety of species delimitation methods. Results supported the inferences of independent lineages and reticulate evolution made in the previous chapter, but the AFLP data did not support inferences of parentage. Third, I investigated the evolution of genome size in the complex based on DNA C-value data, and tested the utilisation of spore size data to infer ploidy level based on the relationship between genome size and spore size. Genome size variation was shown not only to be due to polyploidy, but also due to expansion of the monoploid genome / chromosome size. Moreover, the evolution of spore size and genome size were not correlated, indicating that spore size is not a good indicator of ploidy level in apomictic complexes. Finally, I investigate the origins of apomixis in A.monanthes based upon AFLP data, sequence data and DNA C-values. I find evidence that the observed genetic and karyological diversity is explained by a single origin of apomixis followed by the spread of apomixis by hybridisation with closely related sexual species by the male function. There is also evidence for post genetic divergence by other mechanisms such as genetic segregation, somatic mutation and unequal meiosis. This thesis presents the first thorough investigation of this complex and has increased our understanding of the evolutionary dynamics of apomixis in ferns. Declaration of Authorship I confirm that the research presented in this thesis is my own work, and any assistance received has been appropriately acknowledged. Co-authors who have contributed to manuscripts prepared for publication have been acknowledged at the beginning of each chapter. Signed: Robert Dyer Date: 18/12/2012 Acknowledgements I am incredibly grateful to so many people who have helped, guided, inspired and supported me over the past four years. The thesis would simply not have been completed without them. First and foremost, I am truly indebted to Harald who has always made time for me, and whose passion and enthusiasm for this field of research has been an inspiration. Second, to Vincent who has navigated me through and kept me on my toes throughout. I thank you both for tolerating my relaxed concept of the deadline, and for you understanding during my more stressed moments. It has been an unforgettable journey and I will always appreciate the opportunity that you have given me. I have been privileged to meet and become friends with many wonderful people both in the museum and at Silwood Park. I leave both with a bag full of cherished memories. In the museum, I thank Anne, Sabine, Steve, Li, Ying, Jeannine, Norman, Cecile, Andie, Steve Russell, Alex Aitken, Tiina, Mark Carine, Alex Monro, Mark Lewis and Mark Spencer for all your help in the lab, discussions and general warmth. Thank you to all in the sequencing lab, Gabrielle, and Anna and Eileen in the postgraduate office. The museum would certainly not have been the same without the cake Wednesday girls, the mycology massive, and not forgetting Messrs Tom, Guy and Murray. Thank you all for some very happy times. In Silwood, I want to say a special thank you to Helen, Alex and Martyn who have really spurred me through the last phases, and generally kept me smiling. Also to Tim, CT, Rich, Omar, Paul, Jan, Andrew, Betty, Luis, Lyndsey, Yael, Hanno, and Guillame for helpful discussions and for ‘thinking big’. Thank you to the Mark, Charlie, Bearded Richard, Andy and everyone else in the cricket and football teams for lots of fun, the odd drink, and I’m pleased to say, even the odd victory. I would also like to thank Ilia and Jaume for the lovely time I spent at Kew. Thank you both for your friendliness and all your help with the manuscript. I must also thank Carl, James, Anders, George, Paul, Alex and Jorge for their invaluable help in the field, and those at Duke who helped me to edit the first chapter into a paper. I honestly don’t think I’d have made it here in as healthy a state, if at all, without the sustenance provided by my housemates, Charlie and Victoria. I will be forever grateful for your kindness, endless home cooked meals, and all the laughter we shared. Lunch times will not be the same without Tommy Walsh. Thank you also to all my other housemates. I have been incredibly fortunate to have the continuous support of so many close friends and family. Thank you James and La, and family, Fox Lloyd and family (including Richard), the Leighton family, Ben, Kate and Brenny, Julia and Matt, Alex, Polly and Otis, Uncle Kelvin, Auntie Lydia and Uncle Ray, and many more. To Vicky, thank you for supporting and enduring me. Your love and understanding has kept me going. A special mention goes to my grandparents who always encouraged me, and who I will always remember. And finally, to Mum, Dad, Naomi, Paul (and Wiggins), I am a very lucky person to have you all. You are a truly wonderful family. Contents Abstract ................................................................................................................................................ 4 Declaration of Authorship ............................................................................................................. 5 Acknowledgements .......................................................................................................................... 6 List of Figures .................................................................................................................................. 12 List of Tables ................................................................................................................................... 14 Chapter 1 .......................................................................................................................................... 17 General Introduction ....................................................................................................................... 17 1.1 Asexual reproduction and the paradox of sex .............................................................................. 17 1.2 Asexual reproduction in plants ........................................................................................................... 18 1.3 Apomictic reproduction in homosporous ferns ........................................................................... 20 1.3.1 An introduction to ferns ................................................................................................. 20 1.3.2 Reproduction in homosporous ferns .............................................................................. 21 1.3.3 Apomictic reproduction in homosporous ferns ............................................................. 22 1.3.4 The evolution of apomixis in homosporous ferns ......................................................... 24 1.4 The Asplenium monanthes complex: A model system for studying apomixis in ferns ................................................................................................................................................................ 25 1.4.1 Taxonomy and cytology ................................................................................................ 25 1.4.2 Geographic distribution ................................................................................................. 26 1.5 Outline of thesis ......................................................................................................................................... 26 Chapter 2 .......................................................................................................................................... 29 Apomixis and reticulate evolution in the Asplenium monanthes fern complex .......................... 29 2.1 Summary ...................................................................................................................................................... 30 2.2 Introduction ...............................................................................................................................................
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