Evolution of female multiple mating: A quantitative model of the “sexually selected sperm” hypothesis

Explaining the evolution and maintenance of polyandry remains a key challenge in evolutionary ecology. One appealing explanation is the sexually selected sperm (SSS) hypothesis, which proposes that polyandry evolves due to indirect selection stemming from positive genetic covariance with male fertilization efficiency, and hence with a male's success in postcopulatory competition for paternity. However, the SSS hypothesis relies on verbal analogy with “sexy-son” models explaining coevolution of female preferences for male displays, and explicit models that validate the basic SSS principle are surprisingly lacking. We developed analogous genetically explicit individual-based models describing the SSS and “sexy-son” processes. We show that the analogy between the two is only partly valid, such that the genetic correlation arising between polyandry and fertilization efficiency is generally smaller than that arising between preference and display, resulting in less reliable coevolution. Importantly, indirect selection was too weak to cause polyandry to evolve in the presence of negative direct selection. Negatively biased mutations on fertilization efficiency did not generally rescue runaway evolution of polyandry unless realized fertilization was highly skewed toward a single male, and coevolution was even weaker given random mating order effects on fertilization. Our models suggest that the SSS process is, on its own, unlikely to generally explain the evolution of polyandry.