Exposure of Anopheles gambiae larvae to a sub-lethal dose of an agrochemical mixture induces tolerance to adulticides used in vector control management

Zoh, Marius Gonse; Tutagata, Jordan; Fodjo, Behi K.; Mouhamadou, Chouaïbou S.; Sadia, Christabelle G.; McBeath, Justin; Schmitt, Frederic; Horstmann, Sebastian; Reynaud, Stéphane

doi:10.1016/j.aquatox.2022.106181

Cited by 16 publications

(10 citation statements)

References 62 publications

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“…The role of agriculture in the development of insecticide resistance in mosquitoes is increasingly being recognized. Indeed, laboratory work has shown the potential of agrochemicals to induce or select for an overexpression of resistance genes in both larvae and adults [ 44 , 59 ]. In the field, susceptibility testing of adult mosquitoes in areas of high agricultural activity often revealed an increased resistance associated with the expression of detoxification enzymes [ 19 , 42 ].…”

Section: Discussionmentioning

confidence: 99%

The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics

Sadia,

Bonneville,

Zoh

et al. 2024

Malar J

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Background There are several indications that pesticides used in agriculture contribute to the emergence and spread of resistance of mosquitoes to vector control insecticides. However, the impact of such an indirect selection pressure has rarely been quantified and the molecular mechanisms involved are still poorly characterized. In this context, experimental selection with different agrochemical mixtures was conducted in Anopheles gambiae. The multi-generational impact of agrochemicals on insecticide resistance was evaluated by phenotypic and molecular approaches. Methods Mosquito larvae were selected for 30 generations with three different agrochemical mixtures containing (i) insecticides, (ii) non-insecticides compounds, and (iii) both insecticide and non-insecticide compounds. Every five generations, the resistance of adults to deltamethrin and bendiocarb was monitored using bioassays. The frequencies of the kdr (L995F) and ace1 (G119S) target-site mutations were monitored every 10 generations. RNAseq was performed on all lines at generation 30 in order to identify gene transcription level variations and polymorphisms associated with each selection regime. Results Larval selection with agrochemical mixtures did not affect bendiocarb resistance and did not select for ace1 mutation. Contrastingly, an increased deltamethrin resistance was observed in the three selected lines. Such increased resistance was not majorly associated with the presence of kdr L995F mutation in selected lines. RNA-seq identified 63 candidate resistance genes over-transcribed in at least one selected line. These include genes coding for detoxification enzymes or cuticular proteins previously associated with insecticide resistance, and other genes potentially associated with chemical stress response. Combining an allele frequency filtering with a Bayesian FST-based genome scan allowed to identify genes under selection across multiple genomic loci, supporting a multigenic adaptive response to agrochemical mixtures. Conclusion This study supports the role of agrochemical contaminants as a significant larval selection pressure favouring insecticide resistance in malaria vectors. Such selection pressures likely impact kdr mutations and detoxification enzymes, but also more generalist mechanisms such as cuticle resistance, which could potentially lead to cross-tolerance to unrelated insecticide compounds. Such indirect effect of global landscape pollution on mosquito resistance to public health insecticides deserves further attention since it can affect the nature and dynamics of resistance alleles circulating in malaria vectors and impact the efficacy of control vector strategies.

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Section: Discussionmentioning

confidence: 99%

The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics

Sadia,

Bonneville,

Zoh

et al. 2024

Malar J

Self Cite

View full text Add to dashboard Cite

show abstract

“…The role of agriculture in the development of insecticide resistance in mosquitoes is increasingly being recognized. Indeed, laboratory work has shown the potential of agrochemicals to induce or select for an overexpression of resistance genes in both larvae and adults (42,59). In the eld, susceptibility testing of adult mosquitoes in areas of high agricultural activity often revealed an increased resistance associated with the expression of detoxi cation enzymes (19,40).…”

Section: Discussionmentioning

confidence: 99%

“…broad spectrum detoxi cation enzymes, sequestration proteins, cuticle modi cations) as opposed to more speci c resistance mechanisms (e.g. target-site mutations and a few detoxi cation enzymes) that are often selected by vector control interventions (36,37,42,59). Though no cross-resistance between deltamethrin and bendiocarb was observed in our selected lines, the diversity and generalist nature of the resistance alleles selected by agrochemical mixtures agrees with the multi-resistance phenotypes frequently observed in intense agriculture areas (42,43,102).…”

Section: Agrochemicals As a Selection Pressure Contributing To Insect...mentioning

confidence: 99%

Impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae. Insights from experimental evolution and transcriptomics

Sadia

Bonneville

Zoh

et al. 2023

Preprint

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Context: There are several indications that pesticides used in agriculture contribute to the emergence and spread of resistance of mosquitoes to vector control insecticides. However, the impact of such indirect selection pressure has rarely been quantified and the molecular mechanisms involved are still poorly characterised. In this context, experimental selection with different agrochemical mixtures was conducted in An. gambiae and the impact on insecticide resistance was evaluated by phenotypic and molecular approaches. Methods: Mosquito larvae were selected for 30 generations with three different mixtures of agrochemicals containing i) insecticides, ii) non-insecticides compounds and iii) both agrochemical types. Each five generations, the resistance of adults to deltamethrin and bendiocarb was monitored using bioassays. The frequencies of the kdr west (L1014F) and Ace1 (G119S) target-site mutations were evaluated every 10 generations. Gene expression and polymorphism variations associated with each selection regime were investigated after 30 generations by RNA-seq. Results: Larval selection with agrochemical mixtures did not affect bendiocarb resistance and did not select for Ace1 mutation. Contrastingly, an increased deltamethrin resistance was observed in the three selected lines as compared to the non-selected line. Such increased resistance was associated with an increased frequency of the Kdr west mutation in the insecticide and non-insecticide selected lines. RNA-seq identified 63 candidate resistance genes over-transcribed in at least one selected line as compared to the non-selected line. These include genes coding for detoxification enzymes or cuticular proteins previously associated with insecticide resistance, and other genes potentially associated with chemical stress response. Polymorphism analyses identified several genes under selection in each line across multiple genomic loci supporting a multigenic adaptive response to agrochemical mixtures. Conclusion: This study supports the role of agrochemical contaminants as a significant larval selection pressure favouring insecticide resistance in malaria vectors. Such selection pressures impact Kdr mutations, detoxification enzymes but also other more generalist resistance mechanisms which could potentially lead to cross-tolerance to unrelated insecticide compounds. Such indirect effect of global landscape pollution on mosquito resistance to public health insecticides deserves further attention since it can affect the nature and dynamics of resistance alleles circulating in malaria vectors and impact the efficacy of control vector strategies.

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“…Among those speci cally over-transcribed in the Trans u-R line, ABCG3 and ABCG4 orthologs were also found over-transcribed in pyrethroid-resistant Aedes aegypti and DDT-resistant Anopheles arabiensis populations [56], while ABCH3 was associated with clothianidin resistance in An. gambiae [27,57]. Finally, various nicotinic receptor subunits were over-transcribed in the Delta-R and Trans u-R lines.…”

Section: Discussionmentioning

confidence: 99%

Deltamethrin and Transfluthrin select for distinct transcriptomic responses in the malaria vector Anopheles gambiae.

Zoh

Bonneville

Laporte

et al. 2023

Preprint

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Background The widespread use of pyrethroid insecticides in Africa has led to the development of strong resistance in Anopheles mosquitoes. Introducing new active ingredients can contribute to overcome this phenomenon and ensure the effectiveness of vector control strategies. Transfluthrin is a polyfluorinated pyrethroid whose structural conformation was thought to prevent its metabolism by cytochrome P450 monooxygenases in malaria vectors, thus representing a potential alternative for managing P450-mediated resistance occurring in the field. In this study, we used controlled selection to compare the dynamics of resistance between transfluthrin and the widely used pyrethroid deltamethrin in the mosquito Anopheles gambiae. Then, we investigated the associated molecular mechanisms using target-site mutation genotyping and RNA-seq. Methods A field-derived line of Anopheles gambiae carrying resistance alleles at low frequencies was used as starting material for a controlled selection experiment. Adult females were selected across 33 generations with deltamethrin or transfluthrin, resulting in three distinct lines: the Delta-R line (selected with deltamethrin), the Transflu-R line (selected with transfluthrin) and the Tiassale-S line (maintained without selection). Deltamethrin and transfluthrin resistance levels were monitored in each selected line throughout the selection process, as well as the frequency of the L1014F kdr mutation. At generation 17, cross-resistance to other public health insecticides was investigated and transcriptomes were sequenced to compare gene transcription variations and polymorphisms associated with adaptation to each insecticide. Results A rapid increase in resistance to deltamethrin and transfluthrin was observed throughout the selection process in each selected line in association with an increased frequency of the L1014F kdr mutation. Transcriptomic data support a broader response to transfluthrin selection as compared to deltamethrin selection. For instance, multiple detoxification enzymes and cuticle proteins were specifically over-transcribed in the Transflu-R line including the known pyrethroid metabolisers CYP6M2, CYP9K1 and CYP6AA1together with other genes previously associated with resistance in Anopheles gambiae. Conclusion This study confirms that recurrent exposure of adult mosquitoes to pyrethroids in a public health context can rapidly select for various resistance mechanisms. In particular, it indicates that in addition to target site mutations, the polyfluorinated pyrethroid transfluthrin can select for a broad metabolic response which includes some P450s previously associated to resistance to classical pyrethroids. This unexpected finding highlights the need for an in-depth study on the adaptive response of mosquitoes to newly introduced active ingredients in order to effectively guide and support decision-making programmes in malaria control.

show abstract

Exposure of Anopheles gambiae larvae to a sub-lethal dose of an agrochemical mixture induces tolerance to adulticides used in vector control management

Cited by 16 publications

References 62 publications

The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics

The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics

Impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae. Insights from experimental evolution and transcriptomics

Deltamethrin and Transfluthrin select for distinct transcriptomic responses in the malaria vector Anopheles gambiae.

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