Abstract
BackgroundResistance of mosquitoes to insecticides is mainly attributed to their adaptation to vector control interventions. Although pesticides used in agriculture have been frequently mentioned as an additional force driving the selection of resistance, only a few studies were dedicated to validate this hypothesis and characterise the underlying mechanisms. While insecticide resistance is rising dramatically in Africa, deciphering how agriculture affects resistance is crucial for improving resistance management strategies. In this context, the multigenerational effect of agricultural pollutants on the selection of insecticide resistance was examined in Anopheles gambiae.MethodsAn urban Tanzanian An. gambiae population displaying a low resistance level was used as a parental strain for a selection experiment across 20 generations. At each generation larvae were selected with a mixture containing pesticides and herbicides classically used in agriculture in Africa. The resistance levels of adults to deltamethrin, DDT and bendiocarb were compared between the selected and non-selected strains across the selection process together with the frequency of kdr mutations. A microarray approach was used for pinpointing transcription level variations selected by the agricultural pesticide mixture at the adult stage.ResultsA gradual increase of adult resistance to all insecticides was observed across the selection process. The frequency of the L1014S kdr mutation rose from 1.6% to 12.5% after 20 generations of selection. Microarray analysis identified 90 transcripts over-transcribed in the selected strain as compared to the parental and the non-selected strains. Genes encoding cuticle proteins, detoxification enzymes, proteins linked to neurotransmitter activity and transcription regulators were mainly affected. RT-qPCR transcription profiling of candidate genes across multiple generations supported their link with insecticide resistance.ConclusionsThis study confirms the potency of agriculture in selecting for insecticide resistance in malaria vectors. We demonstrated that the recurrent exposure of larvae to agricultural pollutants can select for resistance mechanisms to vector control insecticides at the adult stage. Our data suggest that in addition to selected target-site resistance mutations, agricultural pollutants may also favor cuticle, metabolic and synaptic transmission-based resistance mechanisms. These results emphasize the need for integrated resistance management strategies taking into account agriculture activities.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-014-0480-z) contains supplementary material, which is available to authorized users.
Highlights
Resistance of mosquitoes to insecticides is mainly attributed to their adaptation to vector control interventions
An increasing number of studies suggested that the use of pesticides in agriculture contributes to the selection of resistance in mosquitoes, threatening the efficacy of vector control interventions [8,9,10,11,12,13,14]
As most insecticides used in agriculture are of the same chemical classes and share the same targets and modes of action as those used for vector control, they have the potential to select for resistance in mosquitoes [12]
Summary
Resistance of mosquitoes to insecticides is mainly attributed to their adaptation to vector control interventions. While insecticide resistance is rising dramatically in Africa, deciphering how agriculture affects resistance is crucial for improving resistance management strategies. In this context, the multigenerational effect of agricultural pollutants on the selection of insecticide resistance was examined in Anopheles gambiae. Malaria vector control programmes have shown success in the last few years through the use of chemical insecticides presented as insecticide treated bed nets (ITNs) or indoor residual spraying (IRS). These tools have been shown to be effective in reducing malaria transmission [1,2]. The agricultural selection pressure may differ from the ones caused by vector control activities in term of mode of exposure (larvae likely exposed to agrochemical leachates versus adults only targeted by vector control) and the nature of chemicals (complex mixtures of agrochemicals versus single insecticide molecules), which may select for different resistance phenotypes this has not been deeply investigated
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