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Abstract The role, magnitude, and molecular nature of trans-driven expression variation underlying the upregulation of detoxification genes in pesticide resistant arthropod populations has remained enigmatic. In this study, we performed expression quantitative trait locus (eQTL) mapping (n = 458) between a pesticide resistant and a susceptible strain of the generalist herbivore and crop pest Tetranychus urticae. We found that a single trans eQTL hotspot controlled large differences in the expression of a subset of genes in different detoxification gene families, as well as other genes associated with host plant use. As established by additional genetic approaches including RNAi gene knockdown, a duplicated gene with a nuclear hormone receptor HR96-related ligand-binding domain was identified as causal for the expression differences between strains. The presence of a large family of HR96-related genes in T. urticae may enable modular control of detoxification and host plant use genes, facilitating this species’ known and rapid evolution to diverse pesticides and host plants.

Abstract Pesticide resistance relies on a myriad of mechanisms, ranging from single mutations to a complex and polygenic architecture, and it involves mechanisms such as target‐site insensitivity, metabolic detoxification, or a combination of these, with either additive or synergistic effects. Several resistance mechanisms against abamectin, a macrocyclic lactone widely used in crop protection, have been reported in the cosmopolitan pest Tetranychus urticae. However, it has been shown that a single mechanism cannot account for the high levels of abamectin resistance found across different mite populations. Here, we used experimental evolution combined with bulked segregant analyses to map quantitative trait loci (QTL) associated with abamectin resistance in two genetically unrelated populations of T. urticae. In these two independent QTL mapping experiments, three and four QTLs were identified, of which three were shared between experiments. Shared QTLs contained genes encoding subunits of the glutamate‐gated chloride channel (GluCl) and harboured previously reported mutations, including G314D in GluCl1 and G326E in GluCl3, but also novel resistance candidate loci, including DNA helicases and chemosensory receptors. Surprisingly, the fourth QTL, present only in only one of the experiments and thus unique for one resistant parental line, revealed a non‐functional variant of GluCl2, suggesting gene knock‐out as resistance mechanism. Our study uncovers the complex basis of abamectin resistance, and it highlights the intraspecific diversity of genetic mechanisms underlying resistance in a cosmopolitan pest.

Host plant specialisation can promote evolutionary divergence between herbivore populations associated with different plant species. While the mechanisms by which specialist species exploit their hosts have been studied widely across taxa, less is known about the mechanisms that allow intraspecific variants to arise and to be maintained across spatial and temporal scales. To understand whether adaptations to plant defences against herbivory contribute to the co-existence of genetically distinct populations of an herbivore, we investigate the interaction between honeysuckle (Lonicera periclymenum) and sympatric specialist and generalist populations of the spider mite Tetranychus urticae. We found that mite folivory induces the production of sticky droplets on honeysuckle, which have a defensive role: they increase mite mortality directly, and potentially indirectly by increasing the arrestment of a predator. We show that droplet induction and the preference to feed on honeysuckle depend on mite genotype, where the generalist avoids this host and the specialist suppresses droplet production. These traits are heritable and dominant in F1 hybrids between generalists and specialists. Selection pressure from honeysuckle and differences in host preference likely reduce the opportunity of mating encounters on this host. We propose that the interplay between selection from host plant defences and ecological barriers to hybridisation contribute to the persistence of genetically distinct populations of a single species in sympatry.