Long methyl-branched cuticular hydrocarbons underlie desert adaptation in Drosophila

Adaptation to diverse and extreme environments is key to long-term species persistence. One of the largest challenges for organisms living in terrestrial environments is water loss. Insects use cuticular hydrocarbons (CHCs), a lipid layer on the body surface, to reduce water from evaporation and withstand desiccation stress. It has long been hypothesized that the waterproofing capability of this CHC layer, which can confer different levels of desiccation resistance, depends on its chemical composition. However, it is unknown how the evolution of CHC components determines differences in desiccation resistance in insects and how insect species can evolve high levels of desiccation resistance. In this study, we determined desiccation resistance and CHC compositions across 50 Drosophila and related species We showed that the length variation in a subset of these CHCs, the methyl-branched CHCs (mbCHCs), is a key determinant of desiccation resistance in Drosophila. In particular, the evolution of longer mbCHCs underlies the evolution of higher desiccation resistance. We identified a fatty acyl-CoA elongase gene in D. melanogaster and D. mojavensis, which we named mElo, responsible for the elongation of mbCHCs. We showed that the overexpression of Dmoj/mElo in D. melanogaster led to longer chain mbCHCs and significantly higher desiccation resistance. In addition, CRISPR/Cas9 knockout of Dmoj/mElo in D. mojavensis led to loss of longer mbCHC production and a significant reduction of desiccation resistance at a temperature relevant to desert environments. Phylogenetic analysis showed that the mElo gene is specific to the Drosophila genus, suggesting a lineage-specific mechanism.