Abstract
Effective vector control is currently challenged worldwide by the evolution of resistance to all classes of chemical insecticides in mosquitoes. In Martinique, populations of the dengue vector Aedes aegypti have been intensively treated with temephos and deltamethrin insecticides over the last fifty years, resulting in heterogeneous levels of resistance across the island. Resistance spreading depends on standing genetic variation, selection intensity and gene flow among populations. To determine gene flow intensity, we first investigated neutral patterns of genetic variability in sixteen populations representative of the many environments found in Martinique and experiencing various levels of insecticide pressure, using 6 microsatellites. Allelic richness was lower in populations resistant to deltamethrin, and consanguinity was higher in populations resistant to temephos, consistent with a negative effect of insecticide pressure on neutral genetic diversity. The global genetic differentiation was low, suggesting high gene flow among populations, but significant structure was found, with a pattern of isolation-by-distance at the global scale. Then, we investigated adaptive patterns of divergence in six out of the 16 populations using 319 single nucleotide polymorphisms (SNPs). Five SNP outliers displaying levels of genetic differentiation out of neutral expectations were detected, including the kdr-V1016I mutation in the voltage-gated sodium channel gene. Association tests revealed a total of seven SNPs associated with deltamethrin resistance. Six other SNPs were associated with temephos resistance, including two non-synonymous substitutions in an alkaline phosphatase and in a sulfotransferase respectively. Altogether, both neutral and adaptive patterns of genetic variation in mosquito populations appear to be largely driven by insecticide pressure in Martinique.
Highlights
During their life-span, mosquitoes face multiple selective pressures, including climatic constraints linked to an obligate aquatic larval stage, together with intense insecticide pressure
This study showed that the insecticide resistance in Ae. aegypti populations was not homogeneously distributed across Martinique and that there were potential links existing between resistance distribution and vector control operations and other factors such as climate and urbanization
We investigated the association between insecticide resistance and 319 single nucleotide polymorphisms (SNPs) in 6 populations, in order to identify candidate genes for temephos and deltamethrin resistances in Ae. aegypti. We found that both neutral and adaptive (SNPs) genetic variation is affected by insecticide pressure in Ae. aegypti populations in Martinique
Summary
During their life-span, mosquitoes face multiple selective pressures, including climatic constraints linked to an obligate aquatic larval stage, together with intense insecticide pressure. Insecticide pressure has led to the spreading of resistance alleles in all target species, and the managing of insecticide resistance in vectors of pathogens represents a major challenge for humanity. Originating from Africa, Aedes aegypti (Diptera, Culicidae) has spread throughout the tropics in historical times [1]. This mosquito species is the primary vector for dengue fever, yellow fever, and chikungunya virus in urban and sub-urban tropical areas across the world. In Martinique Island, a French overseas department located in the eastern Caribbean in the Lesser Antilles, the dengue virus (Flaviviridae) is transmitted by Ae. aegypti following an endemo-epidemic pattern and is a major public health issue [2]. In the absence of vaccine or specific treatment against the disease, vector control by the use of chemical or biological agents against Ae. aegypti is currently the main method for reducing dengue transmission, in addition to environmental management and educational programs
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