Deleterious Mutation Accumulation in Arabidopsis thaliana Pollen Genes: A Role for a Recent Relaxation of Selection

In many studies, sex-related genes have been found to evolve rapidly. We therefore expect plant pollen genes to evolve faster than sporophytic genes. In addition, pollen genes are expressed as haploids which can itself facilitate rapid evolution because recessive advantageous and deleterious alleles are not masked by dominant alleles. However, this mechanism is less straightforward to apply in the model plant species Arabidopsis thaliana. For 1 Myr, A. thaliana has been self-compatible, a life history switch that has caused: a reduction in pollen competition, increased homozygosity, and a dilution of masking in diploid expressed, sporophytic genes. In this study, we have investigated the relative strength of selection on pollen genes compared with sporophytic genes in A. thaliana. We present two major findings: 1) before becoming self-compatible, positive selection was stronger on pollen genes than sporophytic genes for A. thaliana and 2) current polymorphism data indicate that selection is weaker on pollen genes compared with sporophytic genes. This weaker selection on pollen genes can in part be explained by their higher tissue specificity, which in outbreeding plants can be outweighed by the effects of haploid expression and pollen competition. These results indicate that since A. thaliana has become self-compatible, selection on pollen genes has become more relaxed. This has led to higher polymorphism levels and a higher build-up of deleterious mutations in pollen genes compared with sporophytic genes.