Independently evolved and gene flow‐accelerated pesticide resistance in two‐spotted spider mites

Abstract

Pest species are often able to develop resistance to pesticides used to control them, depending on how rapidly resistance can emerge within a population or spread from another resistant population. We examined the evolution of bifenazate resistance in China in the two‐spotted spider mite (TSSM) Tetranychus uticae Koch (Acari: Tetranychidae), one of the most resistant arthropods, by using bioassays, detection of mutations in the target cytb gene, and population genetic structure analysis using microsatellite markers. Bioassays showed variable levels of resistance to bifenazate. The cytb mutation G126S, which confers medium resistance in TSSM to bifenazate, had previously been detected prior to the application of bifenazate and was now widespread, suggesting likely resistance evolution from standing genetic variation. G126S was detected in geographically distant populations across different genetic clusters, pointing to the independent origin of this mutation in different TSSM populations. A novel A269V mutation linked to a low‐level resistance was detected in two southern populations. Widespread resistance associated with a high frequency of the G126S allele was found in four populations from the Beijing area which were not genetically differentiated. In this case, a high level of gene flows likely accelerated the development of resistance within this local region, as well as into an outlying region distant from Beijing. These findings, therefore, suggest patterns consistent with both local evolution of pesticide resistance as well as an impact of migration, helping to inform resistance management strategies in TSSM.

The G126S substitution in mitochondrially encoded cytochrome b does not confer bifenazate resistance in the spider mite Tetranychus urticae

“…Later studies have revealed additional mutations using targeted cytochrome b sequencing, combined with crosses between strains to reveal maternal inheritance (Van Nieuwenhuyse et al 2009;Van Leeuwen et al 2011;Riga et al 2017;Fotoukkiaii et al 2019). Because the G126S mutation was found in a strain with low resistance ratio, and even more so because of the fact that G126S in combination with S141F or I136T provides very high levels of resistance (Van Leeuwen et al 2008), some studies have determined the frequency of this mutation alone in the context of bifenazate resistance (Piraneo et al 2015;Shi et al 2019;Kim et al 2019;Maeoka et al 2020;Zhang et al 2021). However, the role of a G126S substitution in the cd1-helix, without additional substitutions, is not validated in T. urticae, as maternal inheritance tests were never reported.…”

“…Since then, cytochrome b genotypes with only G126S in the cd1-helix have been identified in a variety of different field populations across continents. This mutation was often considered a resistance mutation on its own, yet the specific contribution of G126S remained unclear or was not investigated in these field populations (Table 1) (Piraneo et al 2015;Shi et al 2019;Sugimoto and Osakabe 2019;Wu et al 2019;Maeoka et al 2020). In one study the incidence and frequency of the G126S mutation was used to characterize the origins of bifenazate resistance and to study gene flow in the context of resistance development (Shi et al 2019), but also in this case without proper association to a resistant phenotype by maternal inheritance tests.…”

Identification and characterization of new mutations in mitochondrial cytochrome b that confer resistance to bifenazate and acequinocyl in the spider miteTetranychus urticae

“…). Although a number of other mutations has been reported, formal evidence of their contribution to bifenazate resistance is lacking . The same is true for G126S, which was reported initially in combination with other cd1‐helix mutations, but the mutation alone has never been validated to confer a resistant phenotype, despite a recent report .…”

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

“…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).…”