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Molecular Population Genetic Consequences of Evolutionary Transitions from Outcrossing to Selfing in Plants

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Molecular Population Genetic Consequences of Evolutionary Transitions from Outcrossing to Selfing in Plants MOLECULAR POPULATION GENETIC CONSEQUENCES OF EVOLUTIONARY TRANSITIONS FROM OUTCROSSING TO SELFING IN PLANTS by Robert W. Ness A thesis submitted in conformity with the requirements for the degree of Doctorate of Philosophy Graduate Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Robert W. Ness 2011 MOLECULAR POPULATION GENETIC CONSEQUENCES OF EVOLUTIONARY TRANSITIONS FROM OUTCROSSING TO SELFING IN PLANTS Robert W. Ness Doctor of Philosophy, 2011 Department of Ecology and Evolutionary Biology University of Toronto ABSTRACT The transition from cross-fertilization to predominant self-fertilization is considered the most common evolutionary transition in flowering plants. This change in mating system has profound influences on the amounts and patterns of genetic diversity within and among populations, and on key genetic and demographic processes. The main goal of my thesis is to determine the molecular population genetic consequences of this transition in the annual neotropical aquatic plant Eichhornia paniculata (Pontederiaceae) using DNA sequence from individuals sampled from throughout the species’ geographic range. Populations exhibit a wide range of mating patterns associated the evolutionary breakdown of tristyly facilitating specific contrasts between outcrossing and selfing populations. Analysis of molecular variation supported the hypothesis of multiple origins of selfing, including the evolution of two morphologically distinct selfing variants from Central America and the Caribbean. A survey of 10 nuclear loci from 225 individuals sampled from 25 populations demonstrated the joint influence of mating system, population size and demographic bottlenecks in affecting patterns of nucleotide variation. Small selfing populations exhibited significantly lower genetic diversity compared with larger outcrossing and mixed mating populations. There was also evidence for higher population differentiation and a slower decay of linkage disequilibrium in predominately selfing populations from the ii Caribbean region. Coalescent simulations of the sequence data indicated a bottleneck associated with colonization of the Caribbean from Brazil ∼125,000 years ago. To investigate the consequences of transitions from outcrossing to selfing across the genome, I used high-throughput, short-read sequencing to assemble ~27,000 ESTs representing ∼24Mbp of sequence. Characterization of floral transcriptomes from this dataset identified 269 genes associated with floral development, 22 of which were differentially expressed in three independently derived selfing lineages compared to an outcrossing genotype. Evidence for relaxed selection in selfing lineages was obtained from an analysis of a subset of ~8000 orthologous sequences from each genotype, as predicted by theory. Selfing genomes showed an increase in the proportion of nonsynonymous to synonymous changes and relaxation of selection for codon usage bias. My thesis represents the most detailed investigation to date of the molecular population genetic consequences of intraspecific variation in the mating systems of plants. iii ACKNOWLEDGEMENTS Throughout my doctoral studies I received invaluable advice and support from many people, without which the research presented in this thesis would not have been possible. First, I would like to thank my supervisor Spencer Barrett for his loyalty and dedication to ensuring the success of my dissertation, and for continued financial support. His guidance has helped greatly in my scientific and intellectual development. I am grateful to John Willis (Duke University) for generously offering to serve as my external examiner. My supervisory committee David Guttman, Nicholas Provart and Stephen Wright have always been available for discussion, and provided critical advice towards many aspects of my project. I would also like to thank Asher Cutter, John Stinchcombe, Jannice Friedman, Rob Colautti, and Aneil Agrawal for valuable insights and conversation over the years. Thanks also to Pauline Wang and John Stavrinides both of whom provided invaluable laboratory advice, and to Justin Giancola for his patient computational assistance. My thesis has benefitted greatly from the fruitful collaborations that I have had with Sean Graham (Univ. of British Columbia), Stephen Wright, Paul Foxe and Mathieu Siol. I also thank Spencer Barrett, Neil White, Suzanne Barrett and Bill Cole for assistance with field collections of Eichhornia paniculata in Brazil and the Caribbean, and Sean Graham for DNA samples of Pontederiaceae and for hosting my visit to Vancouver. Several people have made my time at the University of Toronto a fun and stimulating place to do graduate training, including Sarah Yakimowski, Bill Cole, Marc Johnson, and Honour McCann and Danielle Marcos. I am also indebted to the whole Barrett lab, past and present, for valuable contributions to my research and for advice on presentations during my graduate work. Finally, I am forever grateful to my parents Janet and Gary Ness for their support and encouragement throughout my graduate and early education. I also owe Rosalind iv Murray my deepest gratitude for organizing my life, and for providing partnership, support, fun and distractions, especially over the final months of my thesis. The Natural Sciences and Engineering Research Council of Canada, Frederick P. Ide Graduate Award in EEB, and the University of Toronto provided financial support for my doctoral studies. The research in this thesis was supported by NSERC Discovery Grants and funding through the Canada Chair’s Program and a Premier’s Discovery Award in Life Sciences and Medicine from the Ontario Government to Spencer C.H. Barrett. v TABLE OF CONTENTS Abstract ..................................................................................................................................... ii Acknowledgements.................................................................................................................. iv Table of Contents..................................................................................................................... vi List of Tables .......................................................................................................................... xii List of Figures ........................................................................................................................ xiv CHAPTER ONE: GENERAL INTRODUCTION ................................................................... 1 Mating system variation and evolution............................................................................. 2 Molecular approaches to investigating the evolution of selfing ....................................... 5 Eichhornia paniculata as a study system.......................................................................... 9 Research objectives......................................................................................................... 12 CHAPTER TWO: GENOMIC CONSEQUENCES OF OUTCROSSING AND SELFING IN PLANTS ................................................................................................................................. 21 Summary ......................................................................................................................... 21 Introduction..................................................................................................................... 22 Inbreeding and the efficacy of natural selection ............................................................. 25 Evolution of recombination rate ..................................................................................... 30 Relations between mating system and genomic mutation rate ....................................... 34 Mating systems and genetic conflicts ............................................................................. 37 Transposable elements ................................................................................................ 38 B-Chromosomes ......................................................................................................... 41 Biased gene conversion............................................................................................... 42 Cytoplasmic male sterility .......................................................................................... 45 Evolution of genome size................................................................................................ 47 vi Conclusions and future directions................................................................................... 51 CHAPTER THREE: EVOLUTIONARY PATHWAYS TO SELF-FERTILIZATION IN A TRISTYLOUS PLANT SPECIES.......................................................................................... 57 Summary ......................................................................................................................... 57 Introduction..................................................................................................................... 58 Evolutionary pathways to selfing.................................................................................... 60 Multiple origins of selfing .............................................................................................. 63 Evidence from genetic relations among populations ...................................................... 63 Evidence from genetic control of mating-system modification...................................... 66
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