In principle, widespread polyandry (female promiscuity) creates potential for sexual selection in males both before and after copulation. However, the way polyandry affects pre-and postcopulatory episodes of sexual selection remains little understood. Resolving this fundamental question has been difficult because it requires extensive information on mating behavior as well as paternity for the whole male population. Here we show that in replicate seminatural groups of red junglefowl, Gallus gallus, polyandry eroded variance in male mating success, which simultaneously weakened the overall intensity of sexual selection but increased the relative strength of postcopulatory episodes. We further illustrate the differential effect of polyandry on pre-and postcopulatory sexual selection by considering the case of male social status, a key determinant of male reproductive success in this species. In low-polyandry groups, however, status was strongly sexually selected before copulation because dominants mated with more females. In high-polyandry groups, sexual selection for status was weakened and largely restricted after copulation because dominants defended paternity by mating repeatedly with the same female. These results reveal polyandry as a potent and dynamic modulator of sexual selection episodes.cryptic female choice | sperm competition | selection gradient | opportunity of selection P olyandry is a taxonomically widespread consequence of sexual reproduction and a key modulator of fundamental evolutionary processes (1), including sociality (2, 3), sex allocation (4), selfish genetic elements (5), speciation (6), inbreeding (7), and evolutionary conflicts [e.g., between diploid and haploid genomes (8), between parents and offspring (9), and between the sexes (10)]. The realization of widespread polyandry has been particularly revolutionary for our understanding of sexual selection (11). Darwin (12) proposed that sexual selection operates on individual variation in the number of partners (i.e., mating success) and their reproductive quality (e.g., fecundity) to promote traits that confer an advantage in intrasexual competition (see also refs. 13-15). By inducing the ejaculates of multiple males to compete for fertilization, polyandry introduces an additional postcopulatory source of variation in male reproductive success-variation in the proportion of a set of eggs fertilized by different males-creating additional episodes of selection after copulation, namely sperm competition and cryptic female choice (11). Although the study of postcopulatory sexual selection has mushroomed over the last 30 y, the way in which polyandry affects the operation of sexual selection remains unclear. A number of studies have concluded that polyandry increases the strength of sexual selection on males by promoting variation in male reproductive success (e.g., refs. 16-19). Other studies, however, have suggested that the amount of variation in male reproductive success caused by polyandry is limited and that polyandry might in fact wea...

Bateman's principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus, mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Bateman's principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Bateman's principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Bateman's principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.