Pollen selection in Arabis alpina

Competition between pollen during fertilization is a crucial stage of sexual selection in angiosperms. Pollen germinates on the stigma and extrudes a tube that elongates through the style and delivers two sperm cells to the embryo sac for fertilization. The intensity of sexual selection during this process should be affected by the number of competing genotypes deposited during pollination. As increased self-fertilization reduces the genetic diversity and heterozygosity of natural populations, it should thereby reduce pollen competition. However, despite the importance of pollen competition in plant reproduction and the prevalence of mating system shifts, direct tests of molecular signatures of sexual selection at different levels of pollen competition remain scarce. Here we analyzed whole-genome sequences from 13 natural populations of A. alpina, a species that shows mating system variation across its distribution, to test whether shifts from cross- to self-fertilization affect the strength of sexual selection on genes involved in pollen competition. We found evidence for efficient purifying and positive selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes is significantly stronger in more genetically diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing rates of self-fertilization.