Reproducing in hot water: Experimental heatwaves deteriorate multiple reproductive traits in a freshwater ectotherm

1. 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. 2. 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. 3. 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. 4.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.