The quantitative genetics of insecticide resistance in Drosophila melanogaster

Abstract

While understanding insecticide resistance in Drosophila melanogaster is informative for controlling pest insects that threaten agricultural yields and vector deadly diseases, it also serves as a powerful model of microevolution which can be interrogated with an exceptionally powerful genetic toolkit. The Drosophila Genetic Reference Panel (DGRP) provides the opportunity to study population-genetic signatures of natural selection in individuals that can be repeatedly measured for a range of phenotypes. In this work, genomic and transcriptomic data from the DGRP are compared with phenotypes from nine insecticidal compounds against the background of genome-wide signals of selection. The two most prominent signatures of selection in the population are attributable to insecticides from a single, widely-used chemical class, the organophosphates. Evidence suggests that insecticide-based selection is limited to these two loci, however the genetic bases of insecticide phenotypes appear to be complex. Insecticide-associated variation includes both structural effects through amino acid substitution and chimeric gene formation, and regulatory effects on transcript abundance by cis- and trans-acting factors. Resistance mechanisms exhibiting pleiotropic effects on insecticides from different chemical classes is found to be rare; one such case is correlated with constitutive, modular regulation of oxidative stress-related transcripts, the genetic basis of which is mapped to multiple trans-acting factors. Comparisons of the results from the DGRP with diverse population genomics data suggests that the outcomes of these analyses are applicable to populations of D. melanogaster worldwide.