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Genetic Diversity to Elucidate the Evolutionary Origin and Maintenance of the Sexual-System Diversity in M

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Genetic Diversity to Elucidate the Evolutionary Origin and Maintenance of the Sexual-System Diversity in M GENETIC VARIATION AND SEXUAL SYSTEM EVOLUTION IN THE ANNUAL MERCURIES DARREN J. OBBARD THE QUEENS COLLEGE - TRINITY TERM 2004 2 ABSTRACT The Mercurialis annua L. (Euphorbiaceae) species complex comprises a group of closely related lineages that present a wide range of sexual-systems, making it a valuable model for the study of plant sexual-system evolution. Within this polyploid complex, diploid populations are dioecious, and polyploid populations either monoecious or androdioecious (males coexist with functional hermaphrodites). The primary aim of this thesis was to use patterns of genetic diversity to elucidate the evolutionary origin and maintenance of the sexual-system diversity in M. annua. The phylogeny of the M. annua complex was reconstructed using chloroplast and ITS DNA sequence. This, in conjunction with morphometric analysis, showed that both hexaploid M. annua, and a novel species from the Canary Islands (newly described here as Mercurialis canariensis), were allopolyploid in origin. Such an origin for hexaploid M. annua suggests that androdioecy may have been able to arise in this group as a consequence of hybridisation between a monoecious lineage, tetraploid M. annua, and a dioecious lineage, M. huetii. Artificial crosses were used to show that hexaploid M. annua has disomic marker inheritance, and a statistical approach was developed to quantify genetic diversity and differentiation in polyploids with disomic inheritance. Strong gradients in genetic (allozyme) diversity at a pan-European scale were used to infer the existence of separate glacial refugia for dioecious and monoecious races of M. annua, at the eastern and western ends of the Mediterranean basin, respectively. A metapopulation model had previously been proposed to explain the ecological maintenance of androdioecy in M. annua. Here, population-level patterns of genetic diversity were used as an indirect test of this model. The discovery of lower within- population diversity, and of greater genetic differentiation between populations, for monoecious populations than for androdioecious populations was consistent with the metapopulation model, and suggests that androdioecy is maintained by the occurrence of regular local extinction. 3 4 ACKNOWLEDGEMENTS Within evolutionary biology, it seems traditional to start every large piece of text with a quote from Mr. Darwin. Here is mine: “What a very difficult thing it is to write correctly, I am only just beginning to feel my own inaccuracies.” (Darwin 1837) This was written with regard to the editing of a manuscript, and, whilst in my case there are as many inadequacies as inaccuracies, it is a sentiment that resonates. First and foremost I thank my supervisors, John Pannell and Stephen Harris. They have been unendingly friendly, helpful and enthusiastic (particularly in their criticism of my grammar). They have also put in far more work than I could ever have expected, consistently making themselves available whenever I had a crisis, a query, or merely a new gel photo. Many members of the Pannell and Harris labs have provided valuable help and advice, and within the department of Plant Sciences several people deserve mention for specific contributions, these include Alison Strugnell, Anne Sing, Colin Hughes, Donovan Bailey, John Baker, Richard Buggs, Rosemary Wise and Sarah Eppley. Vast numbers of people have supplied me with Mercurialis samples, including Avi Golan, Eirene Williams, Ettore Pacini, Fred Topliffe, Gill Campbell, Luis Fontes, Mark Harris, Pavel Hamouz, Phillip Schlüter, Renate Wesselingh, Tean Mitchell and Tim Rayden. I thank Yong-Ming Yuan, Cecelia Duraes and Salvador Talavera for providing me with particularly hard-to-get samples. Hiroyoshi Iwata and Patrick Meirmans helped me with their software, Johannes Vogel assisted at my initiation into the black art of polyploid isozymes, and Gil McVean helped me with the (marginally less black) art of coalescent simulation. I have been paid for by The Queens College (Oxford) and the Department of Plant Sciences, and The Genetics Society contributed to the cost of fieldwork. On a personal note, I wish to thank my parents, both generally, for their long-term emotional and financial encouragement over twenty years of full-time education, and specifically, for sacrificing their holiday to the discovery of Mercurialis canariensis. Finally, I want to express my everlasting love and gratitude to Dr. Elizabeth Bayne, who now has a psychological allergy to Mercurialis annua very nearly as strong as my physical one. 5 TABLE OF CONTENTS 1 GENERAL INTRODUCTION.................................................................. 10 1.1 Background................................................................................................... 10 1.2 Sexual-system and polyploid variation in Mercurialis annua...................... 11 1.3 Sexual-system evolution and genetic variation ............................................ 12 2 THE PHYLOGENETIC ORIGIN OF SEXUAL-SYSTEM VARIATION ......... 16 2.1 Introduction................................................................................................... 16 2.2 Materials and Methods ................................................................................. 19 2.3 Results........................................................................................................... 29 2.4 Discussion..................................................................................................... 41 3 DISTINGUISHING BETWEEN POLYPLOID GENOTYPES USING SELFED PROGENY ................................................................................................... 49 3.1 Introduction................................................................................................... 49 3.2 Methods ........................................................................................................ 53 3.3 Results........................................................................................................... 56 3.4 Discussion..................................................................................................... 60 4 POPULATION STRUCTURE IN POLYPLOIDS WITH DISOMIC INHERITANCE ............................................................................................ 66 4.1 Introduction................................................................................................... 66 4.2 Genetics summary statistics in polyploids.................................................... 67 4.3 Phenotype-based statistics............................................................................ 69 4.4 A new diversity statistic based on allele differences .................................... 73 4.5 The properties of phenotype-based statistics................................................ 74 4.6 Discussion..................................................................................................... 81 5 EVIDENCE FOR METAPOPULATION PROCESS AND POST-GLACIAL MIGRATION ............................................................................................... 88 5.1 Introduction................................................................................................... 88 5.2 Methods ........................................................................................................ 95 5.3 Results......................................................................................................... 101 6 5.4 Discussion................................................................................................... 111 6 GENERAL DISCUSSION...................................................................... 120 6.1 A hybrid origin for androdioecy................................................................. 120 6.2 Separate glacial refugia for monoecy and dioecy....................................... 122 6.3 Metapopulation structure and sexual system variation............................... 123 6.4 The genus Mercurialis as a model.............................................................. 124 7 REFERENCES .................................................................................... 127 8 APPENDICES ..................................................................................... 150 8.1 Chloroplast haplotype variation in Mercurialis annua............................... 150 8.2 PCR for intra-individual ITS variation ....................................................... 163 8.3 ITS and cpDNA gene trees not presented in the main text......................... 165 8.4 Manuscript: “A new species of Mercurialis endemic to the Canary Islands” 172 8.5 Photographs of plant morphology .............................................................. 187 8.6 Leaf shape variation in the annual mercuries ............................................. 189 8.7 The origin of samples used in the isozyme study ....................................... 192 8.8 The origin of samples used in the phylogenetic analysis ........................... 195 8.9 Example PGI isozyme gels......................................................................... 197 8.10 Isozyme allele frequencies in Mercurialis annua....................................... 198 8.11 The progeny from a self-fertilised hexaploid ............................................. 203 8.12 Allelic phenotype frequencies of selfed progeny ....................................... 204 8.13 FDASH documentation .............................................................................. 209 8.14 Published Paper: “Probing
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