Metabolic resistance of the tiger mosquito to pyrethroid insecticides in la Réunion Island likely results from local adaptation

Abstract

The resistance of mosquitoes to insecticides is a valuable model system for studying the genetic bases of xenobiotic adaptation in insects. The spread of the Asian tiger mosquito Aedes albopictus, combined with the massive use of pyrethroid insecticides to limit arbovirus transmission, resulted in the rise of resistance in various continents. Here, we investigated the genetic mechanisms underlying the recent adaptation of this mosquito to deltamethrin in La Réunion Island. Bioassays confirmed the presence of resistance alleles in field populations. The resistance phenotype was further enhanced in the laboratory following a few generations of controlled selection. Combining whole genome Pool-seq and RNA-seq revealed no evidence of target-site resistance mutations, but the over-expression and variant selection of detoxification enzymes associated with pyrethroid metabolism, including cytochrome P450s, transferases, and ABC-transporters. Among over-expressed detoxification genes, only one was linked to a gene duplication, while polymorphism data suggest most of them are trans-regulated. Genome-wide selection signatures revealed a 9 Mb inversion acting as a superlocus responding to controlled selection. Altogether, this study indicates that the multigenic metabolic resistance phenotype observed in this insular territory mainly results from local adaptation. From an applied perspective, this study provides a set of markers to track pyrethroid resistance in the tiger mosquito in the South-West Indian Ocean. As this region is subjected to recurrent arbovirus outbreaks, the additive resistance phenotype that may arise from the introduction of Kdr mutations from other territories also calls for improving resistance surveillance at the regional scale.