Desiccation resistance differences in Drosophila species can be largely explained by variations in cuticular hydrocarbons

Abstract

Maintaining water balance is a universal challenge for organisms living in terrestrial environments, especially for insects, which have essential roles in our ecosystem. Although the high surface area to volume ratio in insects makes them vulnerable to water loss, insects have evolved different levels of desiccation resistance to adapt to diverse environments. To withstand desiccation, insects use a lipid layer called cuticular hydrocarbons (CHCs) to reduce water evaporation from the body surface. 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 which CHC components are important contributors to desiccation resistance and how these components can determine differences in desiccation resistance. In this study, we used machine learning algorithms, correlation analyses, and synthetic CHCs to investigate how different CHC components affect desiccation resistance in 50 Drosophila and related species. We showed that desiccation resistance differences across these species can be largely explained by variation in cuticular hydrocarbons. In particular, length variation in a subset of CHCs, the methyl-branched CHCs (mbCHCs), is a key determinant of desiccation resistance. We also showed a significant correlation between the evolution of longer mbCHCs and higher desiccation resistance. Given the ubiquitous presence of mbCHCs in insects, the evolution of mbCHCs may be a general mechanism of how insects evolve desiccation resistance and adapt to diverse and changing environments. SignificanceAs our planet is becoming more arid due to global warming, preventing dehydration is key to the survival of insects, an essential part of our ecosystem. However, factors that determine how insects may evolve resistance to desiccation are relatively unknown. Using Drosophila species from diverse habitats, we showed that variations in the composition of cuticular hydrocarbons (CHCs), a hydrophobic layer found on insects to prevent evaporative water loss, can largely explain desiccation resistance differences. In addition, the evolution of longer methyl-branched CHCs (mbCHCs), underlies the evolution of higher desiccation resistance in this genus. As mbCHCs are ubiquitously present in most insects, we suggest that evolutionary changes in mbCHCs may be a general determinant of desiccation resistance across insect species.