Genetic basis of octanoic acid resistance in Drosophila sechellia: functional analysis of a fine-mapped region

J M Andrade López, S M Lanno, J M Auerbach, E C Moskowitz, L A Sligar, P J Wittkopp, J. D. Coolon

Abstract

Drosophila sechellia is a species of fruit fly endemic to the Seychelles islands. Unlike its generalist sister species, D. sechellia has evolved to be a specialist on the host plant Morinda citrifolia. This specialization is interesting because the plant’s fruit contains secondary defense compounds, primarily octanoic acid (OA), that are lethal to most other Drosophilids. Although ecological and behavioral adaptations to this toxic fruit are known, the genetic basis for evolutionary changes in OA resistance are not. Prior work showed that a genomic region on chromosome 3R containing 18 genes has the greatest contribution to differences in OA resistance between D. sechellia and D. simulans. To determine which gene(s) in this region might be involved in the evolutionary change in OA resistance, we knocked-down expression of each gene in this region in D. melanogaster with RNA interference (RNAi) (i) ubiquitously throughout development, (ii) during only the adult stage, and (iii) within specific tissues. We identified three neighboring genes in the Osiris family, Osiris 6 (Osi6), Osi7, and Osi8, that lead to decreased OA resistance when ubiquitously knocked-down. Tissue specific RNAi, however, showed that decreasing expression of Osi6 and Osi7 specifically in the fat body and/or salivary glands increased OA resistance. Gene expression analyses of Osi6 and Osi7 revealed that while standing levels of expression are higher in D. sechellia, Osi6 expression is significantly downregulated in salivary glands in response to OA exposure, suggesting that evolved tissue-specific environmental plasticity of Osi6 expression may be responsible for OA resistance in D. sechellia.

 Molecular Ecology. December 30, 2016. doi: 10.1111/mec.14001