Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors
Abstract The introduction of neonicotinoids for managing insecticide resistance in mosquitoes is of high interest as they interact with a biochemical target not previously used in public health. In this concern, Bayer developed a combination of the neonicotinoid clothianidin and the pyrethroid delta...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2021-09-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-99061-x |
| _version_ | 1818997765675417600 |
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| author | Marius Gonse Zoh Jean-Marc Bonneville Jordan Tutagata Frederic Laporte Behi K. Fodjo Chouaibou S. Mouhamadou Christabelle Gba Sadia Justin McBeath Frederic Schmitt Sebastian Horstmann Stephane Reynaud Jean-Philippe David |
| author_facet | Marius Gonse Zoh Jean-Marc Bonneville Jordan Tutagata Frederic Laporte Behi K. Fodjo Chouaibou S. Mouhamadou Christabelle Gba Sadia Justin McBeath Frederic Schmitt Sebastian Horstmann Stephane Reynaud Jean-Philippe David |
| author_sort | Marius Gonse Zoh |
| collection | DOAJ |
| description | Abstract The introduction of neonicotinoids for managing insecticide resistance in mosquitoes is of high interest as they interact with a biochemical target not previously used in public health. In this concern, Bayer developed a combination of the neonicotinoid clothianidin and the pyrethroid deltamethrin (brand name Fludora Fusion) as a new vector control tool. Although this combination proved to be efficient against pyrethroid-resistant mosquitoes, its ability to prevent the selection of pyrethroid and neonicotinoid resistance alleles was not investigated. In this context, the objective of this work was to study the dynamics and the molecular mechanisms of resistance of An. gambiae to the separated or combined components of this combination. A field-derived An. gambiae line carrying resistance alleles to multiple insecticides at low frequencies was used as a starting for 33 successive generations of controlled selection. Resistance levels to each insecticide and target site mutation frequencies were monitored throughout the selection process. Cross resistance to other public health insecticides were also investigated. RNA-seq was used to compare gene transcription variations and polymorphisms across all lines. This study confirmed the potential of this insecticide combination to impair the selection of resistance as compared to its two separated components. Deltamethrin selection led to the rapid enrichment of the kdr L1014F target-site mutation. Clothianidin selection led to the over-transcription of multiple cytochrome P450s including some showing high homology with those conferring neonicotinoid resistance in other insects. A strong selection signature associated with clothianidin selection was also observed on a P450 gene cluster previously associated with resistance. Within this cluster, the gene CYP6M1 showed the highest selection signature together with a transcription profile supporting a role in clothianidin resistance. Modelling the impact of point mutations selected by clothianidin on CYP6M1 protein structure showed that selection retained a protein variant with a modified active site potentially enhancing clothianidin metabolism. In the context of the recent deployment of neonicotinoids for mosquito control and their frequent usage in agriculture, the present study highlights the benefit of combining them with other insecticides for preventing the selection of resistance and sustaining vector control activities. |
| first_indexed | 2024-12-20T21:50:50Z |
| format | Article |
| id | doaj.art-3662cd03125b42229b6182058aa20a36 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-20T21:50:50Z |
| publishDate | 2021-09-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-3662cd03125b42229b6182058aa20a362022-12-21T19:25:34ZengNature PortfolioScientific Reports2045-23222021-09-0111111610.1038/s41598-021-99061-xExperimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectorsMarius Gonse Zoh0Jean-Marc Bonneville1Jordan Tutagata2Frederic Laporte3Behi K. Fodjo4Chouaibou S. Mouhamadou5Christabelle Gba Sadia6Justin McBeath7Frederic Schmitt8Sebastian Horstmann9Stephane Reynaud10Jean-Philippe David11Laboratoire d’Ecologie Alpine (LECA) UMR 5553 CNRS Grenoble-Alpes UniversityLaboratoire d’Ecologie Alpine (LECA) UMR 5553 CNRS Grenoble-Alpes UniversityLaboratoire d’Ecologie Alpine (LECA) UMR 5553 CNRS Grenoble-Alpes UniversityLaboratoire d’Ecologie Alpine (LECA) UMR 5553 CNRS Grenoble-Alpes UniversityCentre Suisse de La Recherche Scientifique (CSRS)Centre Suisse de La Recherche Scientifique (CSRS)Centre Suisse de La Recherche Scientifique (CSRS)Bayer CropScience LtdBayer SASBayer AGLaboratoire d’Ecologie Alpine (LECA) UMR 5553 CNRS Grenoble-Alpes UniversityLaboratoire d’Ecologie Alpine (LECA) UMR 5553 CNRS Grenoble-Alpes UniversityAbstract The introduction of neonicotinoids for managing insecticide resistance in mosquitoes is of high interest as they interact with a biochemical target not previously used in public health. In this concern, Bayer developed a combination of the neonicotinoid clothianidin and the pyrethroid deltamethrin (brand name Fludora Fusion) as a new vector control tool. Although this combination proved to be efficient against pyrethroid-resistant mosquitoes, its ability to prevent the selection of pyrethroid and neonicotinoid resistance alleles was not investigated. In this context, the objective of this work was to study the dynamics and the molecular mechanisms of resistance of An. gambiae to the separated or combined components of this combination. A field-derived An. gambiae line carrying resistance alleles to multiple insecticides at low frequencies was used as a starting for 33 successive generations of controlled selection. Resistance levels to each insecticide and target site mutation frequencies were monitored throughout the selection process. Cross resistance to other public health insecticides were also investigated. RNA-seq was used to compare gene transcription variations and polymorphisms across all lines. This study confirmed the potential of this insecticide combination to impair the selection of resistance as compared to its two separated components. Deltamethrin selection led to the rapid enrichment of the kdr L1014F target-site mutation. Clothianidin selection led to the over-transcription of multiple cytochrome P450s including some showing high homology with those conferring neonicotinoid resistance in other insects. A strong selection signature associated with clothianidin selection was also observed on a P450 gene cluster previously associated with resistance. Within this cluster, the gene CYP6M1 showed the highest selection signature together with a transcription profile supporting a role in clothianidin resistance. Modelling the impact of point mutations selected by clothianidin on CYP6M1 protein structure showed that selection retained a protein variant with a modified active site potentially enhancing clothianidin metabolism. In the context of the recent deployment of neonicotinoids for mosquito control and their frequent usage in agriculture, the present study highlights the benefit of combining them with other insecticides for preventing the selection of resistance and sustaining vector control activities.https://doi.org/10.1038/s41598-021-99061-x |
| spellingShingle | Marius Gonse Zoh Jean-Marc Bonneville Jordan Tutagata Frederic Laporte Behi K. Fodjo Chouaibou S. Mouhamadou Christabelle Gba Sadia Justin McBeath Frederic Schmitt Sebastian Horstmann Stephane Reynaud Jean-Philippe David Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors Scientific Reports |
| title | Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors |
| title_full | Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors |
| title_fullStr | Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors |
| title_full_unstemmed | Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors |
| title_short | Experimental evolution supports the potential of neonicotinoid-pyrethroid combination for managing insecticide resistance in malaria vectors |
| title_sort | experimental evolution supports the potential of neonicotinoid pyrethroid combination for managing insecticide resistance in malaria vectors |
| url | https://doi.org/10.1038/s41598-021-99061-x |
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