Transgenerational effects of heat shock on gene regulation and fitness-related traits in natural Drosophila populations.

Heat stress will increasingly affect populations as climate change leads to higher temperatures and more frequent heat waves. Recent work suggests that interactions between the epigenome and transposable elements (TEs) could link environmental acclimation with rapid evolution. Yet little is known about how these processes interact in natural genetic backgrounds or shape evolutionarily relevant phenotypes. To investigate these interactions, we carried out laboratory experiments measuring gene expression and chromatin accessibility responses to heat shock in female D. melanogaster from arid and cold climates, their associations with population variation in TEs, and fitness-related phenotypes including viability and development time in the offspring. We also measured expression, accessibility and phenotypic traits three generations later to explore transgenerational inheritance. Expression and accessibility responses to heat shock varied between populations and were influenced by TE presence, with more upregulated responses in the arid population. Effects of heat shock on transcription were detected three generations later, especially in the arid population, although this was not driven by chromatin accessibility. Among offspring of heat shocked flies, phenotypes of the initial cohort (eggs laid within 2 d of heat shock) were negatively affected in both populations, but later cohorts (eggs laid more than 2 d after heat shock) from the arid population developed quicker than controls, indicating hormesis. This effect was still present four generations after the heat shock in the great-great-grandoffspring, demonstrating transgenerational inheritance of potentially beneficial phenotypes and gene expression in a natural insect population.