Facultative polyandry under heat stress and the evolutionary potential for climate-driven shifts in mating systems

The ecology of mating interactions determines a species' mating system, yet whether environmental change can alter the mating system of a species remains unclear. Elevated temperatures can cause male sterility, prompting females to remate for fertility assurance. In monandrous systems, heat-induced male infertility poses a significant extinction risk, as females may mate exclusively with infertile males. A key question is whether male sterility could drive polyandry in a typically monandrous system. Here we address this by examining genetic variance underlying both male fertility resilience to heat stress and facultative polyandry, and assessing the fitness consequences of each mating system. We used isofemales lines of Drosophila subobscura, a monandrous species, exposing males to developmental heat stress. Male heat stress generated sterility and females mated to these males typically remated. While significant genetic variation in male fertility sensitivity and female remating emerged at moderate to high temperatures, we found little genetic variation in plasticity for polyandry. These results indicate evolutionary potential in both traits, but that a shift in mating system would arise through selection on genes associated with polyandry, rather than plasticity. Polyandry improved offspring production after initially mating to a sterile male, but did not fully restore reproductive output relative to fertile monandrous pairs, and mating with heat-stressed males increased female mortality. Heat stress also altered mating behaviour which could impact female mate choice. Together, these findings show that increasing temperatures may shape species' mating systems and the interplay between thermal ecology and sexual selection under climate change.