Aceandace-like genes of invasive redlegged earth mite: Copy number variation, target-site mutations, and their associations with organophosphate insensitivity

Abstract

Pesticide resistance provides an intriguing system to study adaptative evolution because the candidate genes, the targets of pesticidal compounds, are often known a priori. In the redlegged earth mite, Halotydeus destructor (Trombidiformes: Penthaleidae, Tucker 1925), amplification of the acetylcholinesterase gene (ace), has led to the evolution of a gene complex. This gene complex has likely evolved in response to decades of organophosphate selection to control this invasive mite pest in the Australian grain and pasture industry. Using a pool-seq approach and experimental selection of H. destructor mites, we find that this ace gene complex likely contributes to organophosphate insensitivity in several ways. Firstly, we found that an increased copy number of individual ace genes within this complex is associated with organophosphate insensitivity. This effect may be general (increased copy number across all ace genes) or related to specific ace genes (the ancestral ace gene, HDE_14279, in a subset of populations). Secondly, target-site mutations (G119S, A201S, and F331Y) in the ancestral ace gene appear to be associated with evolved resistance to high doses of organophosphates. Thirdly, despite the low within-gene polymorphism, there were high levels among-gene polymorphisms at codons typically associated with resistance in other arthropods. These included fixed amino acids known to confer resistance (e.g., at codons 119, 201, 227, 331, and 441), but the functional effect of these mutations at amplified ace genes is yet to be characterised. Although we tested for the effects of other (non-ace) genes (e.g., detoxification on cuticular genes), our genome scans were equivocal and could not identify any other clear candidate genes contributing to organophosphate insensitivity. Our study makes headway on unravelling the intricacies of the ace gene complex in H. destructor and its phenotypic effects. We highlight the role of gene amplifications in adaptive evolution and its potential to generate polygenic-like mechanisms and non-convergent responses to selection among populations.

Ace and ace‐like genes of invasive redlegged earth mite: copy number variation, target‐site mutations, and their associations with organophosphate insensitivity

“…All sequencing data has been submitted under the GenBank Project PRJNA756307 and their accessions are listed in Supporting Information Table S1. All code and data required to run these analyses have been deposited into a Dryad archive 56 : https://doi.org/10.5061/dryad.dr7sqvb2m.…”