Females of many species mate repeatedly throughout their lives, often with many different males (polyandry). Females can secure genetic benefits by maximizing their diversity of mating partners, and might be expected, therefore, to forego matings with previous partners in favour of novel males. Indeed, a female preference for novel mating partners has been shown in several taxa, but the mechanism by which females distinguish between novel males and previous mates remains unknown. We show that female crickets (Gryllodes sigillatus) mark males with their own unique chemical signatures during mating, enabling females to recognize prior mates in subsequent encounters and to avoid remating with them. Because self-referent chemosensory cues provide females with a simple, but reliable mechanism of identifying individuals with whom they have mated without requiring any special cognitive ability, they may be a widespread means by which females across a broad range of animal mating systems maximize the genetic benefits of polyandry.

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Genetic benefits can enhance the fitness of polyandrous females through the high intrinsic genetic quality of females’ mates or through the interaction between female and male genes. I used a full diallel cross, a quantitative genetics design that involves all possible crosses among a set of genetically homogeneous lines, to determine the mechanism through which polyandrous female decorated crickets (Gryllodes sigillatus) obtain genetic benefits. I measured several traits related to fitness and partitioned the phenotypic variance into components representing the contribution of additive genetic variance (‘good genes’), nonadditive genetic variance (genetic compatibility), as well as maternal and paternal effects. The results reveal a significant variance attributable to both nonadditive and additive sources in the measured traits, and their influence depended on which trait was considered. The lack of congruence in sources of phenotypic variance among these fitness‐related traits suggests that the evolution and maintenance of polyandry are unlikely to have resulted from one selective influence, but rather are the result of the collective effects of a number of factors.

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The spermatophore transferred by male decorated crickets (Gryllodes sigillatus) at mating includes a large gelatinous spermatophylax that the female consumes after copulation. Although previous studies have shown that G. sigillatus females gain no nutritional bene¢ts from consuming food gifts, there may be other bene¢ts to their consumption. We examined potential hydration bene¢ts to females by experimentally manipulating both the availability of water and the number of food gifts that females consumed, and by measuring their e¡ect on female ¢tness. Analysis of the number of nymphs produced by females revealed a signi¢cant interaction between the number of spermatophylaxes consumed and water availability. When spermatophylaxes were not provided, females given water ad libitum produced signi¢cantly more nymphs than females subjected to water stress. Female longevity was signi¢cantly a¡ected by water availability, with an increase in the availability of water corresponding to a signi¢cant increase in female longevity. These data suggest that female G. sigillatus accrue ¢tness bene¢ts by consuming spermatophylaxes when alternative sources of water are unavailable. In addition, females appear to allocate water contained in spermatophylaxes towards reproduction as opposed to survival.