Environmental predictability drives adaptive within- and transgenerational plasticity of heat tolerance across life stages and climatic regions

Although environmental variability and predictability have been proposed as the underlying ecological context in which transgenerational plasticity (TGP) arises, the adaptive significance and interaction with within-generation plasticity (WGP) in such scenarios is still poorly understood. To investigate these questions, we considered the tolerance to upper thermal limits of larvae and adults of the desert endemic Drosophila mojavensis adapted to different climatic regions (Desert vs. Mediterranean climate). Thermal plasticity was investigated by acclimating parents and offspring at 36°C (vs. at 25°C). We then used historical temperature variation data from both regions to perform individual-based simulations by modelling expected components of adaptive plasticity in multiple life stages. Our results indicated that thermal response to ramping heat shocks was more pronounced in larvae, where acclimation treatments in parents and offspring increased their heat-shock performance, while heat knockdown in adults was only increased by offspring acclimation of adults. The relative contribution of WGP and TGP was greater for the population from the more thermally variable Sonoran Desert. Similarly, individual-based simulations of evolving maternal effects indicated that variation in tolerance to upper thermal limits across life stages and climates is expected from its adaptive significance in response to environmental predictability. Our approach offers a new perspective and interpretation of adaptive plasticity, demonstrating that environmental predictability can drive thermal responses across generations and life stages in a scenario with regional climate variability. A free Plain Language Summary can be found within the Supporting Information of this article.