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The G119S ace-1 mutation confers adaptive organophosphate resistance in a nontarget amphipod.

ABSTRACT: Organophosphate (OP) and carbamate (CM) insecticides are widely used in the United States and share the same mode of toxic action. Both classes are frequently documented in aquatic ecosystems, sometimes at levels that exceed aquatic life benchmarks. We previously identified a population of the nontarget amphipod, Hyalella azteca, thriving in an agricultural creek with high sediment levels of the OP chlorpyrifos, suggesting the population may have acquired genetic resistance to the pesticide. In the present study, we surveyed 17 populations of H. azteca in California to screen for phenotypic resistance to chlorpyrifos as well as genetic signatures of resistance in the acetylcholinesterase (ace-1) gene. We found no phenotypic chlorpyrifos resistance in populations from areas with little or no pesticide use. However, there was ~3- to 1,000-fold resistance in H. azteca populations from agricultural and/or urban areas, with resistance levels in agriculture being far higher than urban areas due to greater ongoing use of OP and CM pesticides. In every case of resistance in H. azteca, we identified a glycine-to-serine amino acid substitution (G119S) that has been shown to confer OP and CM resistance in mosquitoes and has been associated with resistance in other insects. We found that the G119S mutation was always present in a heterozygous state. Further, we provide tentative evidence of an ace-1 gene duplication in H. azteca that may play a role in chlorpyrifos resistance in some populations. The detection of a genetically based, adaptive OP and CM resistance in some of the same populations of H. azteca previously shown to harbor a genetically based adaptive pyrethroid resistance indicates that these nontarget amphipod populations have become resistant to many of the insecticides now in common use. The terrestrial application of pesticides has provided strong selective pressures to drive evolution in a nontarget, aquatic species.

SUBMITTER: Major KM

PROVIDER: S-EPMC7086107 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCameroon is considering the implementation of indoor residual spraying (IRS) as a complementary measure to control malaria in the context of high pyrethroid resistance in major malaria vectors. Non-pyrethroid insecticide classes such as organophosphates and carbamates may be utilized in IRS due to widespread pyrethroid resistance. However, the success of this strategy depends on good knowledge of the resistance status of malaria vectors to carbamates and organophosphates. Here, we assessed the susceptibility profile of Anopheles gambiae sensu lato with respect to carbamates and organophosphate and the distribution of the molecular mechanism underlying resistance to these insecticides.MethodsAnopheles gambiae s.l. mosquitoes were collected from nine settings across the country and bio-assayed with bendiocarb, propoxur and pirimiphos-methyl. The Ace-1 target-site G119S mutation was genotyped using a TaqMan assay. To investigate the polymorphism in the Ace-1 gene, a region of 924 base pairs in a sequence of the gene was amplified from both live and dead females of An. gambiae exposed to bendiocarb.ResultsPirimiphos-methyl induced full mortality in An. gambiae s.l. from all study sites, whereas for carbamates, resistance was observed in four localities, with the lowest mortality rate recorded in Mangoum (17.78 ± 5.02% for bendiocarb and 18.61 ± 3.86% for propoxur) in the southern part of Cameroon. Anopheles coluzzii was found to be the predominant species in the northern tropical part of the country where it is sympatric with Anopheles arabiensis. In the localities situated in southern equatorial regions, this species was predominant in urban settings, while An. gambiae was the most abundant species in rural areas. The G119S Ace-1 target-site mutation was detected only in An. gambiae and only in the sites located in southern Cameroon. Phylogenetic analyses showed a clustering according to the phenotype.ConclusionThe occurrence of the Ace-1 target-site substitution G119S in An. gambiae s.l. populations highlights the challenge associated with the impending deployment of IRS in Cameroon using carbamates or organophosphates. It is therefore important to think about a resistance management plan including the use of other insecticide classes such as neonicotinoids or pyrrole to guarantee the implementation of IRS in Cameroon.

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The G119S ace-1 mutation confers adaptive organophosphate resistance in a nontarget amphipod.

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