Genomic Causes and Consequences of the Evolution of Self-fertilization in the Flowering Plant Genera Capsella and Collinsia

The shift in mating system from outcrossing to selfing is associated with many evolutionary changes including reduced flower size and changes in sex allocation, leading to a suite of morphological characteristics known as the selfing syndrome. Furthermore, the evolution of selfing is expected to have important effects on genetic variation and the efficacy of natural selection. However, the underlying genomic causes of morphological evolution and the extent of relaxed selection remain unresolved. In this thesis I use new genomic approaches to investigate the genetic basis of floral evolution as well as the consequences of the evolution of selfing in the genus Capsella (Brassicaceae), in which the highly selfing C. rubella evolved recently from the self-incompatible, obligately outcrossing C. grandiflora. Quantitative trait locus (QTL) mapping results suggest that few loci with major effects on multiple floral phenotypes underlie the evolution of the selfing syndrome. Patterns of neutral diversity in QTL regions from both resequencing and next-generation transcriptome sequencing suggest an important role for positive directional selection in the evolution of the selfing syndrome. Combined with the identification of differentially expressed genes, the signals of positive selection provide candidate regions for identifying the causal evolutionary changes. Analysis of whole-transcriptome polymorphism patterns shows a significant increase in the ratio of unique nonsynonymous to synonymous polymorphism in C. rubella, consistent with a genome-wide relaxation of selection. To investigate the evolution of selfing in the genus Collinsia, I combined transcriptome sequencing with Sanger resequencing of multiple populations of the large-flowered Collinsia linearis with its small flowered, more highly selfing sister species Collinsia rattanii. Patterns of nucleotide diversity suggest the recent divergence of C. rattanii associated with a severe population bottleneck. C. rattanii showed an increased proportion of nonsynonymous polymorphism, consistent with a relaxation of natural selection following the population bottleneck and shift to selfing. In general, my results using combined genome-wide polymorphism, QTL mapping and gene expression data allow for a powerful approach to investigate the targets of adaptive evolution following the shift to selfing, and highlight the potential for relaxation of selection associated with this transitionPh