Experimental evolution reveals that males evolving within warmer thermal regimes improve reproductive performance under heatwave conditions in a model insect

Climate change is increasing mean temperatures, and intensifying heatwaves. Natural populations may respond to stress through shorter-term acclimation via plasticity and/or longer-term inter-generational evolution. However, if the pace and/or extent of thermal change is too great, local extinctions occur; one potential cause in ectotherms is identified to be the heat-liability of male reproductive biology. Recent data from several species, including the beetle Tribolium castaneum, confirmed that male reproductive biology is vulnerable to heatwaves, which may constrain populations. However, such reproductive-damage may be overestimated, if there is potential to adapt to elevated mean temperatures associated with climate change via evolution and/or acclimation. Here, we tested this to evaluate whether pre-exposures could improve heatwave tolerance (adaptation or acclimation), by experimentally evolving Tribolium castaneum populations to divergent thermal regimes (30 °C vs. 38 °C). Findings across assays revealed that relative to 30 °C-regime males, males from the 38 °C regime, maintained constantly at 8 °C warmer for 25 generations, displayed an increase; (i) in post heatwave (42 °C) reproductive fitness by 55%, (ii) survival by 33%, and (iii) 32% larger testes volumes. Unexpectedly, in the acclimation assay, warm-adapted males' post-heatwave survival and reproduction were best if they experienced cool developmental acclimation beforehand, suggesting a cost to adapting to 38 °C. These results help progress knowledge of the potential for survival and reproduction to adapt to climate change; trait specific adaptation to divergent thermal regimes can occur over relatively few generations, but this capacity depended on the interaction of evolutionary and thermal acclimatory processes.