Recombination and the role of pseudo-overdominance in polyploid evolution

ABSTRACT Natural selection is an imperfect force that can under some conditions fail to prevent the buildup of deleterious mutations. Small population sizes and the lack of recombination are two such scenarios that reduce the efficiency of selection. Under these conditions, the disconnect between deleterious genetic load and individual fitness due to the masking of recessive deleterious mutations in heterozygous individuals may result in the emergence of pseudo-overdominance, wherein the buildup of haplotypes with complementary sets of deleterious mutations results in apparent heterozygote advantage and an increase in linked neutral diversity. In polyploids, the presence of additional allelic copies magnifies this masking effect and may therefore increase the probability of pseudo-overdominance. Here, we simulate the evolution of small diploid and autotetraploid populations to identify the conditions that support the evolution of pseudo-overdominance. We discover that pseudo-overdominance evolves under a much wider range of parameters in autotetraploids than in diploids with identical population sizes, and that in many parts of parameter space there is an inverse relationship between fitness and recombination rate. These results imply that pseudo-overdominance may be more common than previously thought. We conclude by discussing the current evidence for pseudo-overdominance in species with polyploid histories, as well as its implications in agriculture due to the prevalence of polyploidy in crops. ARTICLE SUMMARY Pseudo-overdominance is an extreme evolutionary phenomenon in which low recombination rates result in the buildup of alternative mutations on disparate haplotypes, rendering recombination events maladaptive because they disrupt the masking of recessive deleterious alleles. In polyploids, additional chromosomes accentuate this masking effect, potentially increasing the likelihood of pseudo-overdominance. We used forward-in-time simulations to test the hypothesis that polyploids are more likely to experience pseudo-overdominance–and find strong evidence in support of this hypothesis. Our results have implications for the evolution of recombination rates in all species, the evolution of polyploids generally, and the efficacy of selection in polyploid crops.