Elucidating the fitness effects of natural genetic variants is one of the current major challenges in evolutionary biology. Understanding the interplay between genotype, phenotype and environment is necessary to make accurate predictions of important biological outcomes such as stress resistance or yield in economically important plants and animals, and disease in humans. Based on population frequency patterns and footprints of selection at the DNA level, the transposable element Bari-Jheh, inserted in the intergenic region of Juvenile Hormone Epoxy Hydrolase (Jheh) genes, was previously identified as putatively adaptive. However, the adaptive effect of this mutation remained elusive. In this work, we integrate information on transcription factor binding sites, available ChIP-Seq data, gene expression analyses and phenotypic assays to identify the functional and the mechanistic underpinnings of Bari-Jheh. We show that Bari-Jheh adds extra antioxidant response elements upstream of Jheh1 and Jheh2 genes. Accordingly, we find that Bari-Jheh is associated with upregulation of Jheh1 and Jheh2 and with resistance to oxidative stress induced by two different compounds relevant for natural D. melanogaster populations. We further show that TEs other than Bari-Jheh might be playing a role in the D. melanogaster response to oxidative stress. Overall our results contribute to the understanding of resistance to oxidative stress in natural populations and highlight the role of transposable elements in environmental adaptation. The replicability of fitness effects on different genetic backgrounds also suggests that epistatic interactions do not seem to dominate the genetic architecture of oxidative stress resistance.
Keywords: Juvenile Hormone Epoxy Hydrolase; antioxidant response elements; cap'n'collar; environmental adaptation; insecticide resistance; regulatory networks.
© 2014 John Wiley & Sons Ltd.