In many species, females mate with multiple partners, meaning that sexual selection on male traits operates across a spectrum that encompasses the competition for mates (that is, before mating) and fertilizations (after mating). Despite being inextricably linked, pre- and postcopulatory sexual selection are typically studied independently, and we know almost nothing about how sexual selection operates across this divide. Here we bridge this knowledge gap using the livebearing fish Poecilia reticulata. We show that both selective episodes, as well as their covariance, explain a significant component of variance in male reproductive fitness. Moreover, linear and nonlinear selection simultaneously act on pre- and postcopulatory traits, and interact to generate multiple phenotypes with similar fitness.

Mate choice can continue after mating via chemical communication between the female reproductive system and sperm. While there is a growing appreciation that females can bias sperm use and paternity by exerting cryptic female choice for preferred males, we know surprisingly little about the mechanisms underlying these post-mating choices. In particular, whether chemical signals released from eggs (chemoattractants) allow females to exert cryptic female choice to favour sperm from specific males remains an open question, particularly in species (including humans) where adults exercise pre-mating mate choice. Here, we adapt a classic dichotomous mate choice assay to the microscopic scale to assess gamete-mediated mate choice in humans. We examined how sperm respond to follicular fluid, a source of human sperm chemoattractants, from either their partner or a non-partner female when experiencing a simultaneous or non-simultaneous choice between follicular fluids. We report robust evidence under these two distinct experimental conditions that follicular fluid from different females consistently and differentially attracts sperm from specific males. This chemoattractant-moderated choice of sperm offers eggs an avenue to exercise independent mate preference. Indeed, gamete-mediated mate choice did not reinforce pre-mating human mate choice decisions. Our results demonstrate that chemoattractants facilitate gamete-mediated mate choice in humans, which offers females the opportunity to exert cryptic female choice for sperm from specific males.

Traits associated with mating and fertilization success are expected to senesce with age, but limited information is available on their relative rates of senescence. In polyandrous species, male reproductive fitness depends on both mating and fertilization success. Because successful mating is a prerequisite for post-copulatory sexual selection, ejaculate traits are expected to senesce faster than pre-copulatory traits, as pre-copulatory sexual selection is often deemed to be stronger than post-copulatory sexual selection. This pattern has generally been found in the few empirical studies conducted so far. We tested this prediction in the guppy ( Poecilia reticulata ), a livebearing fish characterized by intense sperm competition, by comparing the expression of male sexual traits at two ages (four and nine months). Contrary to prediction, we found that post-copulatory traits senesced at a significantly slower rate than pre-copulatory traits. We also looked at whether early investment in those sexual traits affects longevity, and the interaction between sperm age (duration of sperm storage inside the male) and male age. Our results suggest that the relative senescence rate of pre- and post-copulatory sexual traits may vary among species with different mating systems and ecology.

Heatwaves are occurring at an increasing frequency and intensity under ongoing climate change. As many reproductive traits—including mating behaviour and gamete traits—are sensitive even to small temperature changes, the impact of heatwaves on reproduction and sexual selection processes is likely to be vast. Also, evaluating whether the sexes respond differently to these extreme events is crucial to understand the impact on fecundity and the consequences at the population level. Nonetheless, our knowledge of the effects of heatwaves on these key aspects of animal life is still limited. Here, we expose recently mated male and female guppies Poecilia reticulata to an experimental heatwave (32°C, 6°C above the control, for 5 days) to determine its effects on several traits, including sexual behaviour, condition, ornamentation and fertility. Using this design, in contrast to alternative experimental setups, we had the possibility to attribute the effects of the heatwave to males' and females' reproductive traits independently. Overall, our results indicate that heatwaves can drastically affect key reproductive traits and unravel sex‐specific responses. In males, there was no effect of the heatwave on survival, but both pre‐ and postcopulatory reproductive traits were affected. After the heatwave, we detected a decrease in orange colouration (the most important ornament on which female choice is based) and the overall level of sexual activity, and a shift in the preferred mating tactic towards forced copulation attempts. The latter suggests implications in sexual conflict dynamics, as forced copulations override female mate choice. Also, after the heatwave, males had more sperm but of lower quality, and, in addition, an increased variance in sperm number. Overall, heatwaves may thus result in a compromised ability to secure matings and fertilizations. In females, the heatwave significantly affected survival, with increased mortality in the short term, and impaired fecundity, with many females from the heatwave treatment not reproducing at all. The negative effects of heatwaves on key reproductive traits unravelled by our study could have major implications for population dynamics and persistence. It highlights the need for further studies on how these extreme events affect reproduction, to improve our understanding of the impacts of climate change. Read the free Plain Language Summary for this article on the Journal blog.

Male mate choice occurs in a wide range of species, and males can increase their reproductive success by distinguishing between females based on their fecundity (e.g., large body size) or their expected sperm competition risk (e.g., virgins). However, patterns of male mate choice could be mitigated by variation in female physiological receptivity, as males can benefit by directing their mating efforts toward females that are at a point in their reproductive cycle when fertilization probability is highest. Here, we perform three experiments to assess whether male mate choice is influenced by cues of female physiological receptivity, fecundity, or sperm competition risk in the pygmy halfbeak (Dermogenys collettei), a small livebearing fish. Female halfbeaks possess a “gravid spot”—an orange abdominal marking that is caused by pigmentation of the females’ skin and variation in embryo development and pigmentation during pregnancy. We show that gravid spot size increases toward parturition and is largest right before giving birth, independent of abdominal width or body size. Males consistently chose females with large gravid spots over females with small gravid spots. In contrast, males did not prefer larger females over smaller females or virgin females over mated females. As female halfbeaks store sperm prior to fertilizations, we suggest that males use the size of the gravid spot as a cue to direct their mating efforts to those females where the chance of fertilization is highest.