The evolutionary origins of mating failures and multiple mating

Abstract

AbstractFemale ‘mating failures’ seem a paradox similar to the paradox of polyandry. To illustrate the twin paradoxes of female mating failures and polyandry, we assume that individuals, not sexes, trade‐off time available for mating with immediate fitness increments or decrements that would be conferred by alternative potential mates. We use Hubbell & Johnson's (1987) [analytical mating theory (H&J), the first sex‐neutral null model of stochastic demography on variance in lifetime mating and adaptive behavior, as well as another sex‐neutral null model, the Switch Point Theorem (SPT) (Gowaty & Hubbell, 2009). The H&J mating theory and SPT predict adaptive behavior of individuals accepting and rejecting potential mates without recourse to scenarios for the evolution of sex differences via anisogamy or parental investment. Sex‐neutral models begin with individuals, not sexes. Null models assume no pre‐existing sex‐specific adaptations. H&J's mating theory and the SPT are discrete time absorbing Markov models that count the times individuals enter states such as receptivity, mating, latency to onset to receptivity, and death. H&J's model and the SPT are analytical solutions for the variance in mating success and the variance in reproductive success, as well as for the fraction of potential mates that are acceptable as mates to a given individual when potential mates differ in the fitness that they would confer to a given mating partner. In H&J's model, there are only two qualities of mates; in the SPT, there are n qualities of mates, where n = the number of potential mates in the population. Thus, both models predict mating failures and multiple mating for both sexes under similar or different demographic circumstances, including the fitness background (the fitness distribution of the pool of potential mates) under which individuals make reproductive decisions. In addition, we conducted numerical experiments using DYNAMATE©, a dynamic, agent‐based (object‐oriented) simulation program that tracks dynamically the fate and interactions of all individuals in a single population over a reproductive season. DYNAMATE embodies the analytical solutions of the SPT as rules that determine individually adaptive reproductive decisions. With DYNAMATE we studied how moment‐to‐moment changes in demographic circumstances change individual behavior and trajectories of mating opportunities under the rules of the SPT that determined for each individual each of its adaptive (fitness enhancing) reproductive decisions. The models demonstrate that the pathways to life‐long virginity and multiple mating reside in: (1) variation in individual lifespan; (2) variation in encounters with potential mates; (3) adaptive acceptance or rejection of potential mates as actual mates, which in the case of rejection of all encountered potential mates, results in life‐long virginity, a ‘fitness trap’; (4) opposite‐sex acceptances or rejections of potential mates as mates; and/or (5) some combination of (1)–(4). The models make quantitative predictions about life‐long failures to mate. Results are consistent with the conclusions that the paradoxical twin riddles of females failing to mate or mating multiply can occur without any appeal to or requirement for pre‐existing fixed sex differences in ‘choosy’ or ‘indiscriminate’ behavior. It may be that the twin riddles of polyandry and female mating failures are only puzzling because the assumptions from parental investment and anisogamy theories about the fixed nature of female mating behavior are wrong.