A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito <i>Aedes aegypti</i>: From genomic characterization to high‐throughput field detection

Cattel, Julien; Haberkorn, Chloé; Laporte, Fréderic; Gaude, Thierry; Cumer, Tristan; Renaud, Julien; Sutherland, Ian W.; Hertz, Jeffrey C.; Bonneville, Jean Marc; Arnaud, Victor; Fustec, Benedicte; Boyer, Sébastien; Marcombe, Sébastien

doi:10.1111/eva.13177

Cited by 21 publications

(15 citation statements)

References 65 publications

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“…However, this system requires the production of capture libraries with overlapping RNA probes, becoming a more expensive and complicated approach than using multiplex PCR assays. Quantitative PCR, like the one developed by Cattel et al [ 60 ], is still a main approach for the rapid detection and copy number quantification in Ae . Aegypti .…”

Section: Discussionmentioning

confidence: 99%

A next generation targeted amplicon sequencing method to screen for insecticide resistance mutations in Aedes aegypti populations reveals a rdl mutation in mosquitoes from Cabo Verde

et al. 2022

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Aedes mosquito vectors transmit many viruses of global health concern, including dengue, chikungunya and Zika. These vector-borne viral diseases have a limited number of treatment options, and vaccines vary in their effectiveness. Consequently, integrated vector management is a primary strategy for disease control. However, the increasing emergence and spread of insecticide resistance is threatening the efficacy of vector control methods. Identifying mutations associated with resistance in vector populations is important to monitor the occurrence and evolution of insecticide resistance and inform control strategies. Rapid and cost-effective genome sequencing approaches are urgently needed. Here we present an adaptable targeted amplicon approach for cost-effective implementation within next generation sequencing platforms. This approach can identify single nucleotide polymorphisms (SNPs) and small insertions and deletions (indels) in genes involved in insecticide resistance in Aedes aegypti mosquitoes. We designed and tested eleven amplicons, which included segments of the ace-1 (carbamate target), the Voltage-Gated Sodium Channel (vgsc; pyrethroids, DDT and organochlorines), and rdl (dieldrin) genes; thereby covering established knockdown resistance (kdr) mutations (e.g., S989P, I1011M/V, V1016G/I and F1534C), with the potential to identify novel ones. The amplicon assays were designed with internal barcodes, to facilitate multiplexing of large numbers of mosquitoes at low cost, and were sequenced using an Illumina platform. Our approach was evaluated on 152 Ae. aegypti mosquitoes collected in Cabo Verde, an archipelago with a history of arbovirus outbreaks. The amplicon sequence data revealed 146 SNPs, including four non-synonymous polymorphisms in the vgsc gene, one in ace-1 and the 296S rdl mutation previously associated with resistance to organochlorines. The 296S rdl mutation was identified in 98% of mosquitoes screened, consistent with the past use of an organochlorine compound (e.g., DDT). Overall, our work shows that targeted amplicon sequencing is a rapid, robust, and cost-effective tool that can be used to perform high throughput monitoring of insecticide resistance.

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Section: Discussionmentioning

confidence: 99%

A next generation targeted amplicon sequencing method to screen for insecticide resistance mutations in Aedes aegypti populations reveals a rdl mutation in mosquitoes from Cabo Verde

et al. 2022

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“…To do this, we assembled a list of 152 cytochrome P450 genes, glutathione transferase genes, and carboxylesterase genes by searching the annotated gene file available through VectorBase (release 54). We then manually added AAEL023266 (Vgsc), and AAEL023844 (a carboxylesterase-like gene that is part of a cluster of CCE genes and has been extensively associated with insecticide resistance [ (Cattel, Haberkorn, et al 2021, Cattel, Minier, et al 2021, Sene et al 2021])-we note that the decision to include Vgsc in enrichment testing was made prior to conducting our SweepFinder2 scan. Outlier windows at the 99 th percentile were significantly enriched for these genes in Colombia, but not the other five countries (however, the p-value for enrichment in the Brazil cohort was 0.05).…”

Section: Selective Sweep Signatures Are Enriched For Insecticide Resi...mentioning

confidence: 99%

Strong positive selection in Aedes aegypti and the rapid evolution of insecticide resistance

Love

Sikder

Vivero

et al. 2022

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Aedes aegypti vectors the pathogens that cause dengue, yellow fever, Zika virus, and chikungunya, and is a serious threat to public health in tropical regions. Decades of work has illuminated many aspects of Ae. aegypti's biology and global population structure, and has identified insecticide resistance genes; however, the size and repetitive nature of the Ae. aegypti genome have limited our ability to detect positive selection in this mosquito. Combining new whole genome sequences from Colombia with publicly available data from Africa and the Americas, we identify multiple strong candidate selective sweeps in Ae. aegypti, many of which overlap genes linked to or implicated in insecticide resistance. We examine the voltage-gated sodium channel gene in three American cohorts, and find evidence for successive selective sweeps in Colombia. The most recent sweep encompasses an intermediate-frequency haplotype containing four candidate insecticide resistance mutations that are in near-perfect linkage disequilibrium with one another in the Colombian sample. We hypothesize that this haplotype may continue to rapidly increase in frequency and perhaps spread geographically in the coming years. These results extend our knowledge of how insecticide resistance has evolved in this species, and add to a growing body of evidence suggesting Ae. aegypti has an extensive genomic capacity to rapidly adapt to insecticide-based vector control.

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“…Over-transcription can be caused by gene Copy Number Variation (CNV) or transcriptional regulation. In mosquitoes, copy number variations (CNV) has been highlighted as a frequent mechanism leading to the over-expression of detoxification enzymes in response to insecticide selection (Cattel et al 2020b;Faucon et al 2015;Faucon et al 2017;Lucas et al 2019;Weetman et al 2018). By combining controlled crosses with targeted DNA-seq, (Cattel et al 2020a) identified multiple P450s affected by CNV in association with insecticide resistance in a multi-resistant population from French Guiana.…”

Section: Discussionmentioning

confidence: 99%

Molecular bases of P450-mediated resistance to the neonicotinoid insecticide imidacloprid in the mosquito Ae. aegypti

et al. 2021

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A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 21 publications

References 65 publications

A next generation targeted amplicon sequencing method to screen for insecticide resistance mutations in Aedes aegypti populations reveals a rdl mutation in mosquitoes from Cabo Verde

A next generation targeted amplicon sequencing method to screen for insecticide resistance mutations in Aedes aegypti populations reveals a rdl mutation in mosquitoes from Cabo Verde

Strong positive selection in Aedes aegypti and the rapid evolution of insecticide resistance

Molecular bases of P450-mediated resistance to the neonicotinoid insecticide imidacloprid in the mosquito Ae. aegypti

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