Sex-specific variation in thermal sensitivity has multiple negative effects on reproductive trait performance

Understanding how increasing temperatures influence ectotherm population growth rate is necessary for predicting population persistence. Population growth rate depends on the thermal performance of multiple life-history traits that have different thermal sensitivities. Reproductive traits are considered more thermally sensitive than other life-history traits, such as survival and development rate. Moreover, the thermal sensitivity of reproductive traits can be sex-specific, which may differentially affect population growth. However, research concurrently assessing the sex-specific influence of heat stress on multiple reproductive traits is limited. We investigated the effect of heat stress on pupal survival and reproductive traits in both sexes to determine sex-specific thermal sensitivity and reproductive performance. Individuals of the butterfly Pieris napi were reared at either 22°C or 29°C throughout the larval and pupal stages. The latter temperature reflects the fastest development rate in this population, influencing generation time, a common population growth rate metric. We recorded pupal survival and adult body weight in both sexes. After eclosion, males and females from both treatments were allowed to interact, and mating success, copulation duration, egg production, fertility and male sterility recovery were measured. A subset of mated females was dissected to assess the number and length of fertilising eupyrene and non-fertilising apyrene sperm transferred by males of each treatment. While elevated temperatures reduced pupal survival and resulted in smaller body weights in both sexes, more substantial sex-specific effects on reproductive traits were observed. Mating success was reduced in heat-stressed females but not in males. In contrast, egg production and fertility were unaffected by heat stress in females, while heat-stressed males, despite having longer copulation durations, exhibited near-complete sterility. Male heat-induced sterility was mediated by a disruption to both eupyrene and apyrene sperm production or transfer. Male remating did not recover fertility, suggesting continued negative effects on sperm production. Our results highlight how increasing temperatures affect reproduction, illustrating that temperatures generating optimal performance for non-reproductive traits, like development rate, can negatively and differentially impact sex-specific reproductive fitness. These negative reproductive consequences may impact population persistence, highlighting the necessity to incorporate these findings into future advanced models predicting species' responses to climate warming.