Multiple mating rescues offspring sex ratio but not productivity in a haplodiploid exposed to developmental heat stress

Abstract

Reproduction is generally more sensitive to high temperatures than survival and arguably a better predictor of the response of populations to climate change than survival estimates. Still, how temperature simultaneously impacts male and female reproductive success, the mating system and the operational sex ratio remains an open question. Here, we addressed how a sublethal high temperature affects the reproductive system of the spider mite Tetranychus urticae. Males and females maintained at 25°C or 36°C during development were paired and the fertility of both sexes, their mating and remating eagerness, and the paternity of the offspring of females with different mating histories were measured. There was a decrease in female and male fertility at 36°C compared to 25°C that resulted in lower offspring production and a more male-biased sex ratio, respectively, because spider mites are haplodiploids. However, when females remated, the pattern of first male sperm precedence typically seen in this species was disrupted, with more than one male contributing to the offspring. This was accompanied by reduced mating eagerness in pairs with partially sterile males and increased remating eagerness in pairs in which at least one sex was partially sterile in the first mating. The observed temperature-induced changes in pre- and post-copulatory traits allowed restoring the offspring sex ratio but did not lead to the recovery of offspring number. Our results show that temperature induces changes in the spider mite mating behaviour and mating system, with potential impact on sexual selection and sexual conflict. However, such changes may not be sufficient to buffer the impact of extreme temperatures on their populations.