Experimental evolution of female multiple mating in spatially structured populations: inbreeding and fertility assurance

Female multiple mating (FMM) is widespread across taxa. Yet, explaining its evolution and persistence remains a challenge, especially when costly to females. Inbreeding avoidance and fertility assurance are two drivers that have been hypothesized to maintain FMM despite costs. Most theoretical studies to date concluded that the indirect selection from inbreeding avoidance is unlikely to outweigh direct costs. However, the relatedness structure emerging in spatially structured populations, and the consequent dynamics of inbreeding depression, may impact the selective advantage of FMM. Two recent theoretical studies predicted evolution of FMM in spatially structured populations as means of inbreeding avoidance and bet-hedging for fertility assurance. To test these predictions, we experimentally evolved the seed beetle Callosobruchus maculatus for 25 generations in spatially structured populations with three different levels of dispersal. Results revealed temporally changing dynamics of female multiple mating intertwined with potential feedbacks with female fecundity, male fertility, and the dynamics of the genetic load in the population, suggesting a prominent role of fertility assurance in driving FMM in small and spatially structured populations. Additionally, we observed changes in female’s egg allocation through time, moving towards a more homogeneous distribution of eggs across multiple mating, pointing towards a bet-hedging strategy against infertility.