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.

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. © 2021 Society of Chemical Industry.

Spatiotemporal multiple insecticide resistance in Aedes aegypti populations in French Guiana: need for alternative vector control.

BACKGROUND: Aedes aegypti is the sole vector of urban arboviruses in French Guiana. Overtime, the species has been responsible for the transmission of viruses during yellow fever, dengue, chikungunya and Zika outbreaks. Decades of vector control have produced resistant populations to deltamethrin, the sole molecule available to control adult mosquitoes in this French Territory. OBJECTIVES: Our surveillance aimed to provide public health authorities with data on insecticide resistance in Ae. aegypti populations and other species of interest in French Guiana. Monitoring resistance to the insecticide used for vector control and to other molecule is a key component to develop an insecticide resistance management plan. METHODS: In 2009, we started to monitor resistance phenotypes to deltamethrin and target-site mechanisms in Ae. aegypti populations across the territory using the WHO impregnated paper test and allelic discrimination assay. FINDINGS: Eight years surveillance revealed well-installed resistance and the dramatic increase of alleles on the sodium voltage-gated gene, known to confer resistance to pyrethroids (PY). In addition, we observed that populations were resistant to malathion (organophosphorous, OP) and alpha-cypermethrin (PY). Some resistance was also detected to molecules from the carbamate family. Finally, those populations somehow recovered susceptibility against fenitrothion (OP). In addition, other species distributed in urban areas revealed to be also resistant to pyrethroids. CONCLUSION: The resistance level can jeopardize the efficiency of chemical adult control in absence of other alternatives and conducts to strongly rely on larval control measures to reduce mosquito burden. Vector control strategies need to evolve to maintain or regain efficacy during epidemics.

Vector Competence of Aedes aegypti, Aedes albopictus and Culex quinquefasciatus from Brazil and New Caledonia for Three Zika Virus Lineages.

Zika virus (ZIKV) has caused severe epidemics in South America beginning in 2015, following its spread through the Pacific. We comparatively assessed the vector competence of ten populations of Aedes aegypti and Ae. albopictus from Brazil and two of Ae. aegypti and one of Culex quinquefasciatus from New Caledonia to transmit three ZIKV isolates belonging to African, Asian and American lineages. Recently colonized mosquitoes from eight distinct sites from both countries were orally challenged with the same viral load (107 TCID50/mL) and examined after 7, 14 and 21 days. Cx. quinquefasciatus was refractory to infection with all virus strains. In contrast, although competence varied with geographical origin, Brazilian and New Caledonian Ae. aegypti could transmit the three ZIKV lineages, with a strong advantage for the African lineage (the only one reaching saliva one-week after challenge). Brazilian Ae. albopictus populations were less competent than Ae. aegypti populations. Ae. albopictus generally exhibited almost no transmission for Asian and American lineages, but was efficient in transmitting the African ZIKV. Viral surveillance and mosquito control measures must be strengthened to avoid the spread of new ZIKV lineages and minimize the transmission of viruses currently circulating.

Spatiotemporal multiple insecticide resistance in Aedes aegypti populations in French Guiana: need for alternative vector control

BACKGROUND Aedes aegypti is the sole vector of urban arboviruses in French Guiana. Overtime, the species has been responsible for the transmission of viruses during yellow fever, dengue, chikungunya and Zika outbreaks. Decades of vector control have produced resistant populations to deltamethrin, the sole molecule available to control adult mosquitoes in this French Territory. OBJECTIVES Our surveillance aimed to provide public health authorities with data on insecticide resistance in Ae. aegypti populations and other species of interest in French Guiana. Monitoring resistance to the insecticide used for vector control and to other molecule is a key component to develop an insecticide resistance management plan. METHODS In 2009, we started to monitor resistance phenotypes to deltamethrin and target-site mechanisms in Ae. aegypti populations across the territory using the WHO impregnated paper test and allelic discrimination assay. FINDINGS Eight years surveillance revealed well-installed resistance and the dramatic increase of alleles on the sodium voltage-gated gene, known to confer resistance to pyrethroids (PY). In addition, we observed that populations were resistant to malathion (organophosphorous, OP) and alpha-cypermethrin (PY). Some resistance was also detected to molecules from the carbamate family. Finally, those populations somehow recovered susceptibility against fenitrothion (OP). In addition, other species distributed in urban areas revealed to be also resistant to pyrethroids. CONCLUSION The resistance level can jeopardize the efficiency of chemical adult control in absence of other alternatives and conducts to strongly rely on larval control measures to reduce mosquito burden. Vector control strategies need to evolve to maintain or regain efficacy during epidemics.

Insecticide resistance in the dengue vector Aedes aegypti from Martinique: distribution, mechanisms and relations with environmental factors.

Dengue is an important mosquito borne viral disease in Martinique Island (French West Indies). The viruses responsible for dengue are transmitted by Aedes aegypti, an indoor day-biting mosquito. The most effective proven method for disease prevention has been by vector control by various chemical or biological means. Unfortunately insecticide resistance has already been observed on the Island and recently showed to significantly reduce the efficacy of vector control interventions. In this study, we investigated the distribution of resistance and the underlying mechanisms in nine Ae. aegypti populations. Statistical multifactorial approach was used to investigate the correlations between insecticide resistance levels, associated mechanisms and environmental factors characterizing the mosquito populations. Bioassays revealed high levels of resistance to temephos and deltamethrin and susceptibility to Bti in the 9 populations tested. Biochemical assays showed elevated detoxification enzyme activities of monooxygenases, carboxylesterases and glutathione S-tranferases in most of the populations. Molecular screening for common insecticide target-site mutations, revealed the presence of the "knock-down resistance" V1016I Kdr mutation at high frequency (>87%). Real time quantitative RT-PCR showed the potential involvement of several candidate detoxification genes in insecticide resistance. Principal Component Analysis (PCA) performed with variables characterizing Ae. aegypti from Martinique permitted to underline potential links existing between resistance distribution and other variables such as agriculture practices, vector control interventions and urbanization. Insecticide resistance is widespread but not homogeneously distributed across Martinique. The influence of environmental and operational factors on the evolution of the resistance and mechanisms are discussed.