Evolutionary changes in a fatty acyl-CoA elongase gene underlie high levels of desiccation resistance in a desert Drosophila species

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 prevent water from evaporation and therefore, withstand desiccation stress. Previous studies have shown that the length of a subset of these CHCs, the methyl-branched CHCs (mbCHCs), is positively associated with desiccation resistance. For example, the desert fruit fly, Drosophila mojavensis, has the longest mbCHCs and the highest desiccation resistance among Drosophila species, suggesting these very-long-chained mbCHCs could be the basis of their high desiccation resistance. However, the underlying molecular mechanisms are not known. In our study, we investigated the genetic basis underlying the synthesis of these very-long-chained mbCHCs in D. mojavensis. Using a candidate gene approach and CRISPR/Cas9 gene editing, we identified a fatty acyl-CoA elongase gene in D. melanogaster, which we named mElo, responsible for the elongation of median-chained mbCHCs in this species. We hypothesized that mElo ortholog in D. mojavensis could be responsible for the elongation of very-long-chained mbCHCs. To test this hypothesis, we overexpressed the mElo ortholog of D. mojavensis, Dmoj/mElo, in D. melanogaster. We showed the overexpression led to longer-chained mbCHCs and higher desiccation resistance, suggesting protein-coding changes in Dmoj/mElo in this species. Our results suggest that the evolution of high levels of desiccation resistance in the desert D. mojavensis may be due to protein-coding evolution in a single gene.