Impact of selection regime and introgression on deltamethrin resistance in the arbovirus vector Aedes aegypti – a comparative study between contrasted situations in New Caledonia and French Guiana

Abstract

BACKGROUND: Pyrethroid insecticides such as deltamethrin have been massively used against Aedes aegypti leading to the spread of resistance alleles worldwide. In an insecticide resistance management context, we evaluated the temporal dynamics of deltamethrin resistance using two distinct populations carrying resistant alleles at different frequencies. Three different scenarios were followed: a continuous selection, a full release of selection, or a repeated introgression with susceptible individuals. The responses of each population to these selection regimes were measured across five generations by bioassays and by monitoring the frequency of knockdown resistance (kdr) mutations and the transcription levels and copy number variations of key detoxification enzymes. RESULTS: Knockdown resistance mutations, overexpression and copy number variations of detoxification enzymes as a mechanism of metabolic resistance to deltamethrin was found and maintained under selection across generations. On comparison, the release of insecticide pressure for five generations did not affect resistance levels and resistance marker frequencies. However, introgressing susceptible alleles drastically reduced deltamethrin resistance in only three generations. CONCLUSION: The present study confirmed that strategies consisting to stop deltamethrin spraying are likely to fail when the frequencies of resistant alleles are too high and the fitness cost associated to resistance is low. In dead-end situations like in French Guiana where alternative insecticides are not available, alternative control strategies may provide a high benefit for vector control, particularly if they favor the introgression of susceptible alleles in natural populations.

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

“…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).…”

Strong Positive Selection inAedes aegyptiand the Rapid Evolution of Insecticide Resistance

“…aegypti LVP_AGWG AaegL5.3) available through VectorBase. 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 et al 2021a , 2021b ; 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 99th percentile were significantly enriched at a P value of 0.05 for these genes in Colombia and the United States, but not the other four countries; however, the P value for enrichment in the Brazil cohort was 0.056.…”

Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations inAedes albopictusmosquito populations in Southern France

“…Although the French Agency for Food, Environmental and Occupational Health Safety (ANSES) established recommendations in 2020 regarding the use of insecticides and the surveillance of resistance in French populations, there is currently no national surveillance program in place 20 . While resistance of vector mosquitoes has been well-documented in overseas territories 11,21,22 , it remains poorly studied in metropolitan France. The presence of insecticide resistance alleles in Ae.…”