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Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes

Organophosphate and carbamate insecticides have largely been used worldwide to control mosquito populations. As a response, the same amino acid substitution in the ace-1 gene (G119S), conferring resistance to both insecticides, has been selected independently in many mosquito species. In Anopheles g...

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Autores principales: Milesi, Pascal, Claret, Jean-Loup, Unal, Sandra, Weill, Mylène, Labbé, Pierrick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9783466/
https://www.ncbi.nlm.nih.gov/pubmed/36550589
http://dx.doi.org/10.1186/s13071-022-05599-8
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author Milesi, Pascal
Claret, Jean-Loup
Unal, Sandra
Weill, Mylène
Labbé, Pierrick
author_facet Milesi, Pascal
Claret, Jean-Loup
Unal, Sandra
Weill, Mylène
Labbé, Pierrick
author_sort Milesi, Pascal
collection PubMed
description Organophosphate and carbamate insecticides have largely been used worldwide to control mosquito populations. As a response, the same amino acid substitution in the ace-1 gene (G119S), conferring resistance to both insecticides, has been selected independently in many mosquito species. In Anopheles gambiae, it has recently been shown that the G119S mutation is actually part of homogeneous duplications that associate multiple resistance copies of the ace-1 gene. In this study, we showed that duplications of resistance copies of the ace-1 gene also exist in the Culex pipiens species complex. The number of copies is variable, and different numbers of copies are associated with different phenotypic trade-offs: we used a combination of bioassays and competition in population cages to show that having more resistance copies conferred higher resistance levels, but was also associated with higher selective disadvantage (or cost) in the absence of insecticide. These results further show the versatility of the genetic architecture of resistance to organophosphate and carbamate insecticides around the ace-1 locus and its role in fine-tuned adaptation to insecticide treatment variations. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05599-8.
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spelling pubmed-97834662022-12-24 Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes Milesi, Pascal Claret, Jean-Loup Unal, Sandra Weill, Mylène Labbé, Pierrick Parasit Vectors Research Organophosphate and carbamate insecticides have largely been used worldwide to control mosquito populations. As a response, the same amino acid substitution in the ace-1 gene (G119S), conferring resistance to both insecticides, has been selected independently in many mosquito species. In Anopheles gambiae, it has recently been shown that the G119S mutation is actually part of homogeneous duplications that associate multiple resistance copies of the ace-1 gene. In this study, we showed that duplications of resistance copies of the ace-1 gene also exist in the Culex pipiens species complex. The number of copies is variable, and different numbers of copies are associated with different phenotypic trade-offs: we used a combination of bioassays and competition in population cages to show that having more resistance copies conferred higher resistance levels, but was also associated with higher selective disadvantage (or cost) in the absence of insecticide. These results further show the versatility of the genetic architecture of resistance to organophosphate and carbamate insecticides around the ace-1 locus and its role in fine-tuned adaptation to insecticide treatment variations. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05599-8. BioMed Central 2022-12-22 /pmc/articles/PMC9783466/ /pubmed/36550589 http://dx.doi.org/10.1186/s13071-022-05599-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Milesi, Pascal
Claret, Jean-Loup
Unal, Sandra
Weill, Mylène
Labbé, Pierrick
Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
title Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
title_full Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
title_fullStr Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
title_full_unstemmed Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
title_short Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes
title_sort evolutionary trade-offs associated with copy number variations in resistance alleles in culex pipiens mosquitoes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9783466/
https://www.ncbi.nlm.nih.gov/pubmed/36550589
http://dx.doi.org/10.1186/s13071-022-05599-8
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