Genomic Signatures of Sexual Selection on Pollen-Expressed Genes in Arabis alpina

Abstract

Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying 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 was significantly stronger in genetically more 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 self-fertilization rates.

Genetic causes and genomic consequences of breakdown of distyly inLinum trigynum

“…Using a version of the McDonald-Kreitman test that corrects for biases resulting from weakly deleterious mutations (Messer and Petrov 2013), we found that the proportion of nonsynonymous fixations driven by positive selection was significantly lower (and not significantly different from zero) for the homostylous L. trigynum, in contrast to the distylous L. tenue which had evidence for a significant contribution of positive selection to nonsynonymous divergence. While detailed analyses separately assessing selection on specific classes of genes, such as those involved in the evolution of the selfing syndrome or pollen competition (Gutiérrez-Valencia et al 2022b) would be warranted for a more complete understanding of the impact of shifts to selfing on selection across the genome, our results so far demonstrate genomic signatures consistent with relaxed purifying and positive selection on nonsynonymous mutations in association with loss of distyly. These results are in line with those in a previous study on the genomic impact of loss of distyly in Primula (Wang et al 2021), and with a wealth of studies on the genomic impact of shifts to selfing in other plant lineages (e.g, Slotte et al 2010, Laenen et al 2018, Mattila et al 2020, Yi et al 2022.…”

“…The VCF file was processed to keep only biallelic SNPs and invariant sites, and then filtered based on the maximum proportion of missing data (pm = 0.1) and read depth (5 < dp < 200). To avoid false heterozygous calls based on a low number of alternate alleles, we used a combination of allele balance and coverage filtering, which has previously been successful for highly repetitive plant genomes (see Laenen et al 2018,Gutiérrez-Valencia et al 2022b for a detailed description).…”