Abstract
Ongoing ambitions are to understand the evolution of costly polyandry and its consequences for species ecology and evolution. Emerging patterns could stem from feed‐back dynamics between the evolving mating system and its genetic environment, defined by interactions among kin including inbreeding. However, such feed‐backs are rarely considered in nonselfing systems. We use a genetically explicit model to demonstrate a mechanism by which inbreeding depression can select for polyandry to mitigate the negative consequences of mating with inbred males, rather than to avoid inbreeding, and to elucidate underlying feed‐backs. Specifically, given inbreeding depression in sperm traits, costly polyandry evolved to ensure female fertility, without requiring explicit inbreeding avoidance. Resulting sperm competition caused evolution of sperm traits and further mitigated the negative effect of inbreeding depression on female fertility. The evolving mating system fed back to decrease population‐wide homozygosity, and hence inbreeding. However, the net overall decrease was small due to compound effects on the variances in sex‐specific reproductive success and paternity skew. Purging of deleterious mutations did not eliminate inbreeding depression in sperm traits or hence selection for polyandry. Overall, our model illustrates that polyandry evolution, both directly and through sperm competition, might facilitate evolutionary rescue for populations experiencing sudden increases in inbreeding.
Highlights
Understanding key forces that drive the evolution and persistence of complex mating systems remains a central endeavor in evolutionary biology
Mating system evolution must depend on aspects of life-history variation and population ecology that shape the frequencies of different types of relatives that coexist within any population, and shape the opportunities for reproductive interactions among different relatives (e.g., Banks et al 2005; Hatchwell 2009; Beckerman et al 2011; Szulkin et al 2013; Pizzari et al 2015)
Even given the increased female remating rate resulting from low male investment in sperm traits, the mean number of offspring produced per female was substantially lower when sperm competition was excluded, especially given strong inbreeding depression (Fig. 3F)
Summary
Genetic and genotypic variation of other life-history traits and population viability. The relative importance of, and interactions among, these mechanisms will act alongside direct effects of polyandry on sibship structures (Cornell and Tregenza 2007) to determine the net effect of the evolving polyandrous mating system on individual and population-wide inbreeding and resulting homozygosity Such changes could potentially alter selection on mechanisms of inbreeding avoidance including mate choice and dispersal, thereby affecting the eco-evolutionary dynamics of inbreeding itself, and affecting population viability and evolution of other life-history traits (Fig. 1H). Seed beetles Callosobruchus maculatus inbred males’ ejaculates contained fewer sperm, meaning that females that mated with inbred males had reduced fertility (Fox et al 2012) Despite such established background, the hypothesis that inbreeding could drive evolution of polyandry through inbreeding depression in male gametic traits, and thereby drive feed-backs that affect inbreeding (Fig. 1), has not been explicitly considered. We examine the effect of the evolving mating system on female fertility, and consider the implications for population fitness (Fig. 1H)
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