Trade-offs of strategic sperm adjustments and their consequences under phenotype–environment mismatches in guppies

In polyandrous species males invest significant resources in producing large and high-quality ejaculates. As ejaculates are costly, males are expected to modulate their investment in response to social cues associated with the expected level of sperm competition or mating opportunity, to anticipate future mating conditions. Another consequence of ejaculate costs is that the increase in ejaculate production may be traded against traits linked to mate acquisition. In such cases, the effect of this anticipatory plasticity in ejaculate investment on a male's reproductive success will depend on the balance between postcopulatory benefits and precopulatory costs in the sociosexual context subsequently encountered. Here, we used the guppy, Poecilia reticulata, a live-bearing fish characterized by intense sperm competition, to investigate how mismatches between anticipatory phenotypes and the social conditions subsequently experienced affect male reproductive success. Male guppies kept in visual contact with females, a social stimulus predicting high mating opportunities, increase their sperm production compared to female-deprived males which foresee fewer opportunities to mate, but simultaneously reduce their courtship rate. Using a paired experimental design, we manipulated the male's perceived mating opportunities by housing them in the presence (FP) or in the absence (FA) of females. We then measured male mating and insemination success under two conditions: (1) a female-biased sex ratio, matching expected FP cues; and (2) a male-biased sex ratio, matching expected FA cues. Under a female-biased sex ratio, mating and insemination success were not affected by previous exposure to females, although FP males experienced a lower risk of sperm depletion after several copulations. However, FP males showed a small, but significant, reduction in their mating success under a male-biased sex ratio, when directly competing with an FA male. Males showed significant repeatability in mating and insemination success within a sex ratio context, suggesting that the costs of mismatching anticipatory ejaculate responses are probably low in this species.