Genetic benefits of extreme sequential polyandry in a terrestrial-breeding frog

Abstract

Sequential polyandry may evolve as an insurance mechanism to reduce the risk that females choose mates that are genetically inferior (intrinsic male quality hypothesis) or genetically incompatible (genetic incompatibility hypothesis). The prevalence of such indirect benefits remains controversial, however, because studies estimating the contributions of additive and non-additive sources of genetic variation to offspring fitness have been limited to a small number of taxonomic groups. Here, we use artificial fertilisation techniques combined with a cross-classified breeding design (North Carolina Type II) to simultaneously test the ‘good genes hypothesis’ and the ‘genetic incompatibility hypothesis’ in the brown toadlet (Pseudophryne bibronii); a terrestrial breeding species with extreme sequential polyandry. Our results revealed no significant additive or non-additive genetic effects on fertilisation success. Moreover, they revealed no significant additive genetic effects, but highly significant non-additive genetic effects (sire by dam interaction effects), on hatching success and larval survival to initial and complete metamorphosis. Taken together, these results indicate that offspring viability is significantly influenced by the combination of parental genotypes, and that negative interactions between parental genetic elements manifest during embryonic and larval development. More broadly, our findings provide quantitative genetic evidence that insurance against genetic incompatibility favours the evolution and maintenance of sequential polyandry.