Origin of resistance to pyrethroids in the redlegged earth mite (Halotydeus destructor) in Australia: repeated local evolution and migration

Abstract

BACKGROUND: Halotydeus destructor is a major pest of crops and pastures across southern parts of Australia. This invasive mite has been chemically controlled for over 50 years, but resistance to synthetic pyrethroids and organophosphates is developing. Understanding processes behind the emerging resistance is important for effective management efforts. We undertook a ddRAD pool-sequencing approach to analyse genome-wide single nucleotide polymorphism variation in H. destructor population samples at two scales: local resistance across a set of fields, and regional resistance across their Australian range, along with toxicology bioassays to screen for pyrethroid resistance.RESULTS: Spatial patterns of genomic variation and resistance at a local scale indicated that genetic similarity among samples was more closely correlated with distance along roads and fence-lines than with straight-line geographic distance. This pattern was particularly strong in resistant samples, which were also more related than susceptible samples, suggesting local spread of resistance within an area after it emerged. By contrast, regional data suggest resistance has emerged repeatedly within parts of Australia. Our de novo annotation of the H. destructor draft genome sequence and Bayesian analysis identified several candidate loci strongly associated with population-level resistance to pyrethroids, located in genomic regions that code for transmembrane transport and signalling proteins that have previously been linked to insecticide resistance in other arthropods. CONCLUSION: Our findings highlight multiple independent evolutionary events leading to resistance in H. destructor, and demonstrate the utility and cost-effectiveness of a cross-population, genome-wide association study to reveal processes underlying adaptive evolution in a non-model invasive species.

Heterogeneous genetic invasions of three insecticide resistance mutations in Indo‐Pacific populations of Aedes aegypti (L.)

“…While the role of human transportation in establishing geographical distributions of Aedes mosquitoes is already well recognised (Tatem, Hay, & Rogers, 2006), these results indicate that dispersal along transportation networks has also helped to establish current distributions of pyrethroid resistance mutations. These results stand in contrast to a similar investigation of pyrethroid resistance in Australian red‐legged earth mite ( Halotydeus destructor ) populations, which showed that the present distribution of resistance had been attained by multiple de novo mutations (Yang et al., 2020).…”

“…This in turn will depend on whether the incursive populations carry pesticide resistance alleles, which can arise through in situ evolution of resistance alleles and/or through the introduction of resistance alleles from other established populations. Both processes can be important in pest and disease vector control: examples of local evolution of resistance include pyrethroid resistance in the earth mite Halotydeus destructor (Yang et al., 2020) and organophosphate resistance in the whitefly Bemisia tabaci (Gauthier et al, 2014), whereas the long distance introduction of resistance genes is typified by pyrethroid resistance in the mosquito Culex pipiens (Chevillon, Raymond, Guillemaud, Lenormand, & Pasteur, 1999); the contribution of both these factors in invading populations is highlighted by pesticide resistance in the spider mite Tetranychus urticae (Shi et al., 2019) and the moth Spodoptera frugiperda (Nagoshi et al., 2017).…”

“…To resolve how broad‐scale resistance patterns are produced, the distribution of resistance alleles can be compared to patterns of genetic differentiation in high resolution single nucleotide polymorphism (SNP) markers (Yang et al., 2020). As the recently developed genome assembly AaegL5 (Matthews et al., 2018) provides a precise genomic location for almost every SNP in Ae.…”

Heterogeneous genetic invasions of three insecticide resistance mutations in Indo-Pacific populations ofAedes aegypti(L.)

“…These results stand in contrast to a similar investigation of pyrethroid resistance in Australian red-legged earth mite (Halotydeus destructor) populations, which showed that the present distribution of resistance had been attained by multiple de novo mutations (Yang et al, 2019).…”

“…To resolve the importance of local mutation/selection and the movement of resistance alleles between populations, the distribution of resistant alleles can be compared to high resolution patterns of genetic differentiation among populations (Yang et al, 2019). Genomic approaches using single nucleotide polymorphism (SNP) markers have been highly effective at identifying differentiation among Ae.…”