Genetic architecture of natural variation in cuticular hydrocarbon composition in Drosophila melanogaster

Abstract

Insect cuticular hydrocarbons (CHCs) prevent desiccation and serve as chemical signals that mediate social interactions. Drosophila melanogaster CHCs have been studied extensively, but the genetic basis for individual variation in CHC composition is largely unknown. We quantified variation in CHC profiles in the D. melanogaster Genetic Reference Panel (DGRP) and identified novel CHCs. We used principal component (PC) analysis to extract PCs that explain the majority of CHC variation and identified polymorphisms in or near 305 and 173 genes in females and males, respectively, associated with variation in these PCs. In addition, 17 DGRP lines contain the functional Desat2 allele characteristic of African and Caribbean D. melanogaster females (more 5,9-C27:2 and less 7,11-C27:2, female sex pheromone isomers). Disruption of expression of 24 candidate genes affected CHC composition in at least one sex. These genes are associated with fatty acid metabolism and represent mechanistic targets for individual variation in CHC composition.

DOI: http://dx.doi.org/10.7554/eLife.09861.001

eLife digest

The outermost layer of an insect’s body is called the epicuticle and is made of a blend of fat molecules. “Cuticular hydrocarbons” (or CHCs) are the most common fat molecules in the epicuticle, and play an important role in protecting the insect’s body from harsh, dry habitats. CHCs also have other roles in insect behavior. For example, these molecules act as chemical cues when insects search for mates (i.e. pheromones), and they can even contribute to camouflage.

Insects are amongst the most diverse groups of animals on Earth, and different species have different blends of CHC molecules in their epicuticles. Fruit flies are a useful model to understand the genetics of CHC production, including CHCs that act as sex pheromones. Previous research has analyzed the CHCs made by both sexes in several fruit fly strains. However this work was unable to uncover which genes influence how much of a given CHC an individual fly will make.

Dembeck et al. have now looked into CHC production in a collection of 205 different fly strains, all of which have already had their total genetic material sequenced and studied. Comparing these known sequences and looking for associations between genetic differences and particular CHCs uncovered 24 genes that may be involved in CHC manufacture. Only six of the genes had been identified previously. Dembeck et al. found that interfering with the activity of any of the 24 genes had a knock-on effect on many other CHCs present in the flies’ epicuticle.

These 24 genes could to be pieced together in a network that is needed to make and recycle CHCs. The complexity and flexibility of this network can explain in part how insects have been able to build epicuticles for almost every environment. These data set the stage for future work directed towards understanding the evolutionary significance of variation in CHC composition in many fruit fly populations.

DOI: http://dx.doi.org/10.7554/eLife.09861.002