Evolution of a fatty acyl-CoA elongase underlies desert adaptation in Drosophila

To survive in extreme environments such as hot-arid deserts, desert-dwelling species have evolved physiological traits to withstand the high temperatures and low aridity beyond the physiologically tolerable ranges of most species. Such traits which include reducing water loss have independently evolved in multiple taxa. However, the genetic and evolutionary mechanisms underlying these traits have thus far not been elucidated. Here we show that Drosophila mojavensis, a fruitfly species endemic to the Sonoran and Mojave deserts, had evolved extremely high desiccation resistance, by producing very long chained methylbranched cuticular hydrocarbons (mbCHCs) that contributes to a cuticular waterproofing lipid layer reducing water loss. We show that the ability to synthesize these longer mbCHCs is due to evolutionary changes in a fatty acyl-CoA elongase (mElo). CRISPR/Cas9 knockout of mElo in D. mojavensis led to loss of longer mbCHC production and significant reduction of desiccation resistance at high temperatures but did not affect mortality at high temperatures or desiccating conditions individually, indicating that this gene is crucial for desert adaptation. Phylogenetic analysis showed that mElo is a Drosophila specific gene with no clear ortholog outside Diptera. This suggests that while the physiological mechanisms underlying desert adaptation are general, the genetic mechanisms may be lineage-specific.