Dataset Information

Rapid evolution of knockdown resistance haplotypes in response to pyrethroid selection in Aedes aegypti.

ABSTRACT: This study describes the evolution of knockdown resistance (kdr) haplotypes in Aedes aegypti in response to pyrethroid insecticide use over the course of 18 years in Iquitos, Peru. Based on the duration and intensiveness of sampling (~10,000 samples), this is the most thorough study of kdr population genetics in Ae. aegypti to date within a city. We provide evidence for the direct connection between programmatic citywide pyrethroid spraying and the increase in frequency of specific kdr haplotypes by identifying two evolutionary events in the population. The relatively high selection coefficients, even under infrequent insecticide pressure, emphasize how quickly Ae. aegypti populations can evolve. In our examination of the literature on mosquitoes and other insect pests, we could find no cases where a pest evolved so quickly to so few exposures to low or nonresidual insecticide applications. The observed rapid increase in frequency of resistance alleles might have been aided by the incomplete dominance of resistance-conferring alleles over corresponding susceptibility alleles. In addition to dramatic temporal shifts, spatial suppression experiments reveal that genetic heterogeneity existed not only at the citywide scale, but also on a very fine scale within the city.

SUBMITTER: Baltzegar J

PROVIDER: S-EPMC8372076 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Rapid evolution of knockdown resistance haplotypes in response to pyrethroid selection in Aedes aegypti.

Baltzegar Jennifer J Vella Michael M Gunning Christian C Vasquez Gissella G Astete Helvio H Stell Fred F Fisher Michael M Scott Thomas W TW Lenhart Audrey A Lloyd Alun L AL Morrison Amy A Gould Fred F

Evolutionary applications 20210709 8

This study describes the evolution of knockdown resistance (kdr) haplotypes in Aedes aegypti in response to pyrethroid insecticide use over the course of 18 years in Iquitos, Peru. Based on the duration and intensiveness of sampling (~10,000 samples), this is the most thorough study of kdr population genetics in Ae. aegypti to date within a city. We provide evidence for the direct connection between programmatic citywide pyrethroid spraying and the incre ...[more]

PMID: 34429751

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Project description:BackgroundControl of Aedes aegypti, the mosquito vector of dengue, chikungunya and yellow fever, is a challenging task. Pyrethroid insecticides have emerged as a preferred choice for vector control but are threatened by the emergence of resistance. The present study reports a focus of pyrethroid resistance and presence of two kdr mutations--F1534C and a novel mutation T1520I, in Ae. aegypti from Delhi, India.Methodology/principal findingsInsecticide susceptibility status of adult-female Ae. aegypti against DDT (4%), deltamethrin (0.05%) and permethrin (0.75%) was determined using WHO's standard insecticide susceptibility kit, which revealed resistance to DDT, deltamethrin and permethrin with corrected mortalities of 35%, 72% and 76% respectively. Mosquitoes were screened for the presence of kdr mutations including those reported earlier (I1011V/M, V1016G/I, F1534C, D1794Y and S989P), which revealed the presence of F1534C and a novel mutation T1520I. Highly specific PCR-RFLP assays were developed for genotyping of these two mutations. Genotyping using allele specific PCR and new PCR-RFLP assays revealed a high frequency of F1534C (0.41-0.79) and low frequency of novel mutation T1520I (0.13). The latter was observed to be tightly linked with F1534C and possibly serve as a compensatory mutation. A positive association of F1534C mutation with DDT and deltamethrin resistance in Ae. aegypti was established. However, F1534C-kdr did not show significant protection against permethrin.Conclusions/significanceThe Aedes aegypti population of Delhi is resistant to DDT, deltamethrin and permethrin. Two kdr mutations, F1534C and a novel mutation T1520I, were identified in this population. This is the first report of kdr mutations being present in the Indian Ae. aegypti population. Highly specific PCR-RFLP assays were developed for discrimination of alleles at both kdr loci. A positive association of F1534C mutation with DDT and deltamethrin resistance was confirmed.

Project description:In Colombia Aedes (Stegomyia) aegypti is the main vector of urban arboviruses such as dengue, chikungunya and Zika. This urban mosquito has a well-established capacity to develop insecticide resistance to different types of insecticides (pyrethroids, organochlorides, organophosphates), using multiple resistance mechanisms. An understanding of ongoing resistance mechanisms is critical to determining the activities of vector control programs. In order to identify the biochemical and molecular mechanisms associated with pyrethroid resistance in Colombia, three laboratory-selected strains resistant to DDT, Propoxur and lambdacyhalothrin, and 7 field-collected strains were evaluated. CDC bioassays were performed to measure the susceptibility status to pyrethroid type I (permethrin) and II (deltamethrin and lambdacyhalothrin), and potential cross-resistance to different types of insecticides; organochlorine (DDT), carbamates (propoxur) and organophosphates (malathion). The enzymatic activity of esterases, glutathione S-transferases (GST) and P450 monooxygenases were biochemically determined. Frequencies of kdr mutations Val1016Ile and Phe1534cys were determined through real-time PCR. The Rockefeller strain of Aedes (Stegomyia) aegypti was used as the susceptible control. The laboratory-selected strains "propoxur" and "lambdacyhalothrin" and one field population (Medellín (BF) F2 were resistant to all evaluated pyrethroids. Six of the seven field populations as well as the laboratory- selected "DDT" strain were resistant to permethrin. All the evaluated strains were resistant to DDT. Cross-resistance between lambdacyhalothrin and propoxur was observed in the laboratory-selected strains; however, all field-collected strains were susceptible to propoxur and no evidence of malathion resistance was found. The main biochemical mechanism for resistance observed in the field-collected strains was related to the enzyme GST. Further, the frequencies of kdr mutations alleles associated with insecticide resistance were high and ranged from 0.02 to 0.72 for Ile1016 and from 0.44 to 0.99 for Cys1534. Strains with high frequencies of both kdr mutations were resistant to both type I and II pyrethroids. These results suggest that Ae. aegypti from Colombia have developed multiple resistance mechanisms associated with pyrethroid resistance; therefore a resistance management strategy against these field populations of Ae. Aegypti, incorporating these findings is strongly recommended.

Project description:Association mapping of factors that condition pyrethroid resistance in Aedes aegypti has consistently identified genes in multiple functional groups. Toward better understanding of the mechanisms involved, we examined high throughput sequencing data (HTS) from two Aedes aegypti aegypti collections from Merida, Yucatan, Mexico treated with either permethrin or deltamethrin. Exome capture enrichment for coding regions and the AaegL5 annotation were used to identify genes statistically associated with resistance. The frequencies of single nucleotide polymorphisms (SNPs) were compared between resistant and susceptible mosquito pools using a contingency χ2 analysis. The -log10(χ2 p value) was calculated at each SNP site, with a weighted average determined from all sites in each gene. Genes with -log10(χ2 p value) ≥ 4.0 and present among all 3 treatment groups were subjected to gene set enrichment analysis (GSEA). We found that several functional groups were enriched compared to all coding genes. These categories were transport, signal transduction and metabolism, in order from highest to lowest statistical significance. Strikingly, 21 genes with demonstrated association to synaptic function were identified. In the high association group (n = 1,053 genes), several genes were identified that also genetically or physically interact with the voltage-gated sodium channel (VGSC). These genes were eg., CHARLATAN (CHL), a transcriptional regulator, several ankyrin-domain proteins, PUMILIO (PUM), a translational repressor, and NEDD4 (E3 ubiquitin-protein ligase). There were 13 genes that ranked among the top 10%: these included VGSC; CINGULIN, a predicted neuronal gap junction protein, and the aedine ortholog of NERVY (NVY), a transcriptional regulator. Silencing of CHL and NVY followed by standard permethrin bottle bioassays validated their association with permethrin resistance. Importantly, VGSC levels were also reduced about 50% in chl- or nvy-dsRNA treated mosquitoes. These results are consistent with the contribution of a variety of neuronal pathways to pyrethroid resistance in Ae. aegypti.

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Rapid evolution of knockdown resistance haplotypes in response to pyrethroid selection in Aedes aegypti.

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Rapid evolution of knockdown resistance haplotypes in response to pyrethroid selection in <i>Aedes aegypti</i>.

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