Transgenerational effects of heat shock on gene regulation and fitness-related traits are stronger in arid than temperate Drosophila populations

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. Yet combining all these factors in a tractable model system remains challenging; consequently 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 temperate climates and their associations with population variation in TEs. The consequences for fitness-related phenotypes were characterised in the offspring, and we also measured expression, chromatin 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 the presence of TEs, with more upregulated responses in the arid population. Effects of heat shock on transcription were detected three generations later, especially in the arid population, with many epigenetic genes transgenerationally expressed, although this was not driven by chromatin accessibility. Heat shock negatively affected phenotypes in 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. Significance StatementGlobal warming will lead to heat stress for many organisms. Interactions between the epigenome (the machinery controlling gene expression) and transposable elements, (TEs; mobile elements within the genome) are likely to influence the response to stress. In transgenerational laboratory heat shock experiments we investigated how the epigenome and TEs affected gene expression and phenotypes of arid and temperate populations of Drosophila melanogaster. The arid population showed clearer upregulation of epigenome and gene expression and transgenerational inheritance of gene expression following heat shock, and we identified TE insertions associated with stress-responsive genes. We also observed potentially beneficial transgenerational phenotypic responses in this population. Integrating molecular systems and measuring relevant phenotypes improves our understanding of acclimatory and evolutionary responses to environmental stress.