Natural and sexual selection on phenotypic plasticity favour thermal canalization

Abstract

Climate change affects organisms worldwide with profound ecological and evolutionary consequences, often increasing population extinction risk. Climatic factors can increase the strength, variability or direction of natural selection on phenotypic traits, potentially driving adaptive evolution. Phenotypic plasticity in relation to temperature can allow organisms to maintain fitness in response to increasing temperatures, thereby "buying time" for subsequent genetic adaptation and promoting evolutionary rescue. Although many studies have shown that organisms respond plastically to increasing temperatures, it is unclear if such thermal plasticity is adaptive. Moreover, we know little about how natural and sexual selection operate on thermal reaction norms reflecting such plasticity. Here, we investigate how natural and sexual selection shape phenotypic plasticity in two congeneric and phenotypically similar sympatric insect species. We show that the thermal optima for longevity and mating success differ, suggesting temperature-dependent trade-offs between survival and reproduction. Males in these species have similar thermal reaction norm slopes but have diverged in baseline body temperature (intercepts), being higher for the more northern species. Natural selection favoured reduced thermal reaction norm slopes at high ambient temperatures, suggesting that the current level of thermal plasticity is maladaptive in the context of anthropogenic climate change and that selection now promotes thermal canalization and robustness. Our results show that ectothermic animals also at high latitudes can suffer from overheating and challenge the common view of phenotypic plasticity as being beneficial in harsh and novel environments. Significance StatementOrganisms are increasingly challenged by increasing temperatures due to climate change. In insects, body temperatures are strongly affected by ambient temperatures, and insects are therefore expected to suffer increasingly from heat stress, potentially reducing survival and reproductive success leading to elevated extinction risks. We investigated how ambient temperature affected fitness in two insect species in the temperate zone. Male and female survivorship benefitted more from low temperatures than did reproductive success, which increased with higher temperatures, revealing a thermal conflict between fitness components. Male body temperature plasticity reduced survival, and natural and sexual selection operated on such thermal plasticity. Our results reveal the negative consequences of thermal plasticity and show that these insects have limited ability to buffer heat stress.