Heat tolerance, oxidative stress response tuning, and robust gene activation in early-stage Drosophila melanogaster embryos

Abstract

In organisms with complex life cycles, life stages that are most susceptible to environmental stress may determine species persistence in the face of climate change. Early embryos of Drosophila melanogaster are particularly sensitive to acute heat stress, yet tropical embryos have higher heat tolerance than temperate embryos, suggesting adaptive variation in embryonic heat tolerance. We compared transcriptomic responses to heat stress among tropical and temperate embryos to elucidate the gene regulatory basis of divergence in embryonic heat tolerance. The transcriptomes of tropical and temperate embryos were differentiated by the expression of relatively few genes, including genes involved in oxidative stress. But most of the transcriptomic response to heat stress was shared among all embryos. Further, embryos shifted the expression of thousands of genes and showed robust gene activation, demonstrating that, contrary to previous reports, early embryos are not transcriptionally silent. The involvement of oxidative stress genes in embryonic heat tolerance corroborates recent reports on the critical role of redox homeostasis in coordinating developmental transitions. By characterizing adaptive variation in the transcriptomic basis of embryonic heat tolerance, this study is a novel contribution to the literature on developmental physiology and genetics, which often lacks ecological and evolutionary context.