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Cited by 136Malaria Research and ControlInsect Resistance and GeneticsDengue and Mosquito Control Research

Impact of agriculture on the selection of insecticide resistance in the malaria vector Anopheles gambiae: a multigenerational study in controlled conditions

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Nkya, Theresia Estomih, Poupardin, Rodolphe, Laporte, Frederic, Akhouayri, Idir, Mosha, Franklin, Magesa, Stephen, Kisinza, William, David, Jean-Philippe·2014·Parasites & Vectors
DOI 10.1186/s13071-014-0480-zPMC PMC4201709
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Abstract

BACKGROUND: Resistance 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. METHODS: An 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. RESULTS: A 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. CONCLUSIONS: This 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.

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  • There is a relationship between pesticide use in agriculture and the emergence of insecticide resistance in disease vectors, as confirmed by voluminous literature.

    “there are voluminous amounts of literature confirming the relationship between pesticide used in agriculture and emergence of insecticide resistance in disease vectors [95, 116–120].”

    From Evolution of insecticide resistance and its mechanisms in Anopheles stephensi in the WHO Eastern Mediterranean Region (2020) · cites this paper as [118]

    The Conclusion reports that recurrent exposure to an agricultural pesticide mixture selected insecticide-resistance mechanisms in Anopheles gambiae, supporting the relationship. But the Abstract Background and Discussion say that only a few studies had validated or demonstrated this effect, so this source does not support the claim that voluminous literature confirms it. (LLM, conf=0.86)

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Authors
Nkya, T. E., Poupardin, R., Laporte, F., Akhouayri, I., Mosha, F., Magesa, S., Kisinza, W., & David, J.-P.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Liverpool School of Tropical Medicine (GB)
  • Tumaini University (TZ)
  • RTI International (US)
  • National Institute for Medical Research (TZ)
Corresponding author
David, Jean-Philippe
ORCID
Venue
Parasites & Vectors
Publisher
Springer Science and Business Media LLC
Published
2014-10-16
Volume
7
Issue
1
Pages
480-480
ISSN
1756-3305 (ISSN-L)
DOI
10.1186/s13071-014-0480-z
PMC
PMC4201709
OpenAlex
W2097581662
Cited by
136
References
5
Citations by year
2026: 3 · 2025: 13 · 2024: 14 · 2023: 17 · 2022: 13 · 2021: 16 · 2020: 13 · 2019: 9 · 2018: 12 · 2017: 14 · 2016: 7 · 2015: 5
FWCI
8.62
Type
journal article
Language
en
Open access
Licence
Locations
  • Parasites & Vectors (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • IHI Repository (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
European Commission (265660)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
  • Social Sciences › Sociology and Political Science › Dengue and Mosquito Control Research
Keywords
insecticide resistance, Anopheles gambiae, malaria vectors, agricultural pesticides, herbicides, deltamethrin, DDT, bendiocarb, kdr mutation, gene expression profiling, cuticular proteins, detoxification enzymes, synaptic transmission, resistance management
MeSH terms
Agriculture, Animals, Anopheles, Dose-Response Relationship, Drug, Gene Expression Regulation, Genotype, Insect Vectors, Insecticide Resistance, Insecticides, Malaria, Selection, Genetic, Reverse Transcriptase Polymerase Chain Reaction, Protein Array Analysis, Transcriptome

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