Genomic studies of mating system variation in flowering plants

The striking diversity of reproductive strategies that flowering plants exhibit remains one of the most intriguing conundrums in evolutionary biology. Pollination-related traits and mating system strategies have a major impact on the processes shaping plant evolution through their effects on genetic diversity and selection. In this thesis, I use population genomic methods to investigate the genetic underpinnings and genomic impact of cross- and self-fertilization in flowering plants. I first study the evolution and breakdown of the supergene that governs the balanced floral polymorphism of distyly in a wild flaxseed species (Linum tenue). Then I assess the consequences of shifts to self-fertilization on the intensity of sexual selection that populations experience, using the crucifer species Arabis alpina as a model. In chapters I, II and III, I investigated how the evolution of supergenes is impacted by their genetic architecture. Building on a de novo genome assembly, I used population genomic data to identify and characterize the distyly supergene in Linum tenue (chapter II). I found that the dominant allele at the distyly S-locus is defined by the presence of a 260-kb region carried in hemizygosity by thrum individuals. Importantly, the hemizygous region harbors, among others, a strong candidate gene for style length. S-linked genes did not exhibit signatures of relaxed purifying selection, consistent with expectations from previous empirical studies and forward simulations (chapter I) in suggesting that hemizygosity might slow down genetic degeneration of non-recombining haplotypes. In the light of similar studies conducted in independently evolved distylous lineages (reviewed in chapter I), our results indicate that distyly supergenes show convergent evolution at the molecular level. By conducting comparative studies of the genome sequences of L. tenue and closely related homostylous L. trigynum (chapter III), I identified candidate mutations for distyly breakdown at S-linked genes. I also investigated the genome-wide effects of the evolutionary transition to homostyly and self-fertilization in L. trigynum. I found that L. trigynum populations are highly inbred, and show significantly lower genetic diversity and more marked population structure than the obligately outcrossing L. tenue. However, I found only weak signatures of relaxed purifying selection in L. trigynum at the genome-wide scale, suggesting that self-fertilization has not had a major effect on the impact of selection. Finally, by analyzing whole-genome sequences from individuals of populations of A. alpina with contrasting mating strategies, I investigated if shifts to self-fertilization have a particularly marked impact on the evolution of genes involved in pollen-pollen competition (chapter IV). The results indicate that the reduced intensity of sexual selection that self-fertilizing populations experience translate into more pronounced signatures of relaxed purifying selection on genes expressed in male gametophyte components. Overall, this thesis contributes to our understanding of the genetic basis and evolution of plant reproductive strategies, and how they impact selection both locally and broadly across the genome