Gametic selection and mating systems show mutually dependent evolution

Abstract

Competition among pollen or sperm (gametic selection) can cause evolution. Mating systems shape the intensity of gametic selection by determining the competitors involved, which can in turn cause mating system evolution. We model the bidirectional relationship between gametic selection and mating systems, focussing on variation in female mating frequency (monandry-polyandry) and self-fertilisation (selfing-outcrossing). First, we find that mating systems affect evolutionary responses to gametic selection, with more effective gametic selection when fertilisation success depends on haploid genotypes, rather than the diploid genotype of the father. Monandry and selfing both reduce the efficacy of gametic selection despite creating intense selection among pollen/sperm from heterozygous males with haploid expression. This effect means selfing can increase mutation load, in contrast to classic predictions where selfing purges deleterious mutations. Second, we show that mating systems can evolve via their effect on gametic selection, with polyandry evolving because it removes deleterious alleles more efficiently and increases offspring fitness. Our population genetic models reveal that this good sperm effect could plausibly give a selective advantage for polyandry over monandry of only around 1%. Selection for polyandry is lessened further if some loci experience balancing selection and is likely to be overwhelmed by any direct fitness effects of mating systems. Similarly, the indirect benefits from manipulating gametic selection have a weak influence on the evolution of selfing, which is dominated by automatic selection and inbreeding depression in our model. Nevertheless, gametic selection can be potentially decisive for selfing evolution because it significantly reduces inbreeding depression, which favours selfing. One test of the predicted interactions between gametic selection and mating system evolution would be to compare evolutionary rates in genes with different expression patterns across different mating systems.