Data supporting manuscript: "Transgenerational effects of heat shock on Drosophila melanogaster gene regulation and life history depend on adaptive environment"

Heat stress will increasingly affect populations, as climate change leads to higher temperatures and more extreme events such as heat waves. Adaptation is predicted to occur over long evolutionary timescales, but recent work suggests that interactions between the epigenome and transposable elements (TEs) could link environmental acclimation with rapid adaptation. However, combining all these factors in a tractable model system is difficult; consequently little is known about how these processes interact in natural genetic backgrounds to shape evolutionarily relevant phenotypes. To investigate these interactions, we carried out laboratory experiments to measure gene expression and chromatin accessibility responses to heat shock in female D. melanogaster from arid and temperate climates and their consequences for offspring phenotypes, and associated molecular responses with population variation in TEs. We then measured the same molecular and phenotypic traits three generations later to explore transgenerational inheritance. Expression and accessibility responses to heat shock varied between populations and were influenced by the presence of TEs, with more upregulated responses in the arid population. Effects of heat shock on transcription were still detectable after three generations, especially in the arid population, with many epigenetic genes transgenerationally expressed, although this was not driven by chromatin accessibility. Heat shock had negative phenotypic consequences on the initial offspring cohort, but later arid population cohorts developed quicker than controls, indicating hormesis, an effect still present in the great-great-grandoffspring. These results demonstrate the transgenerational inheritance of a potentially beneficial hormetic phenotype and associated patterns of gene expression in a natural insect population.