Profiling of Dermanyssus gallinae genes involved in acaricide resistance

The poultry red mite (PRM), Dermanyssus gallinae, is a major threat for the poultry industry worldwide. Chemical compounds have been extensively used for PRM control, leading to selection of resistant mites. Molecular mechanisms of resistance have been investigated in arthropods, showing the role of target-site insensitivity and enhanced detoxification. Few studies are available about those mechanisms in D. gallinae, and none have yet focused on the expression levels of detoxification enzymes and other defense-related genes through RNA-seq. We tested PRM populations from Italy for their susceptibility to the acaricidal compounds phoxim and cypermethrin. Mutations in the voltage-gated sodium channel (vgsc) and in acetylcholinesterase (AChE) were investigated, detecting mutations known to be associated with acaricide/insecticide resistance in arthropods, including M827I and M918L/T in the vgsc and G119S in the AChE. RNA-seq analysis was performed to characterize metabolic resistance in fully susceptible PRM and in cypermethrin-resistant PRM exposed and unexposed to cypermethrin as well as phoxim resistant PRM exposed and unexposed to phoxim. Detoxification enzymes (including P450 monooxygenases and glutathione-S-transferases), ABC transporters and cuticular proteins were constitutively overexpressed in phoxim and cypermethrin resistant mites. In addition, heat shock proteins were found constitutively and inductively upregulated in phoxim resistant mites, while in cypermethrin resistant mites esterases and an aryl hydrocarbon receptor were constitutively highly expressed. The findings suggest that acaricide resistance in D. gallinae is due to both target-site insensitivity and overexpression of detoxification enzymes and other xenobiotic defense-related genes, which is mostly constitutive and not induced by treatment. Understanding the molecular basis of resistance could be useful to screen or test PRM populations in order to select targeted acaricides and to avoid the abuse/misuse of the few available compounds.