Resistance to pirimiphos-methyl in West African Anopheles is spreading via duplication and introgression of the Ace1 locus
| Autor: | Grau-Bové, Xavier, Lucas, Eric, Pipini, Dimitra, Rippon, Emily, van ‘t Hof, Arjèn E., Constant, Edi, Dadzie, Samuel, Egyir-Yawson, Alexander, Essandoh, John, Chabi, Joseph, Djogbénou, Luc, Harding, Nicholas J., Miles, Alistair, Kwiatkowski, Dominic, Donnelly, Martin J., Weetman, David, Jorge Edouardo Amaya-Romero, Diego, Ayala, Battey, C. J., Philip, Bejon, Besansky, Nora J., Austin, Burt, Jorge, Cano, Caputo, Beniamino, Edi, Constant, Carlo, Costantini, Boubacar, Coulibaly, DELLA TORRE, Alessandra, Abdoulaye, Diabate´, João, Dinis, Eleanor, Drury, Jorge, Edouardo, Nohal, Elissa, John, Essandoh, Fontaine, Michael C., Godfray, H. Charles J., Hahn, Matthew W., Christa, Henrichs, Christina, Hubbart, Isaacs, Alison T., Musa, Jawara, Jeffreys, Anna E., Dushyanth, Jyothi, Maryam, Kamali, Kern, Andrew D., Kwiatkowski, Dominic P., Clarkson, Chris S., Lawniczak, Mara K. N., Gilbert Le Goff, Lucas, Eric R., Cinzia, Malangone, Mawejje, Henry D., Charles, Mbogo, Daniel, Mead, Janet, Midega, Alistair, Miles, Nwakanma, Davis C., Samantha, O’Loughlin, João, Pinto, Riehle, Michelle M., Vincent, Robert, Rockett, Kirk A., Rohatgi, Kyanne R., Kate, Rowlands, Schrider, Daniel R., Igor, Sharakhov, Victoria, Simpson, Jim, Stalker, Troco, Arlete D., Vernick, Kenneth D., David, Weetman, White, Bradley J., Wilding, Craig S. |
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| Přispěvatelé: | IRTA, Institute of Molecular Biology and Biotechnology (IMBB-FORTH), Foundation for Research and Technology - Hellas (FORTH), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre de Recherche Entomologique de Cotonou (CREC), Ministère de la Santé, The Wellcome Trust Centre for Human Genetics [Oxford], University of Oxford [Oxford], Liverpool School of Tropical Medicine (LSTM), Instituto de Higiene e Medicina Tropical (IHMT), Global Health and Tropical Medicine (GHTM), Vector borne diseases and pathogens (VBD), Institut de Recerca i Tecnologia Agroalimentàries = Institute of Agrifood Research and Technology (IRTA), University of Oxford, Fontaine lab |
| Jazyk: | angličtina |
| Rok vydání: | 2021 |
| Předmět: |
Cancer Research
Insecticides Heredity Introgression Anopheles gambiae Anopheles Gambiae QH426-470 Disease Vectors Mosquitoes Ghana Insecticide Resistance Geographical Locations пиримифос-метил 0302 clinical medicine Medical Conditions [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases Invertebrate Genomics Medicine and Health Sciences Genetics(clinical) Copy-number variation Association mapping Genetics (clinical) SDG 15 - Life on Land Data Management Genetics 0303 health sciences education.field_of_study biology malaria vectors genomics insecticide resistance anopheles gambiae anopheles coluzzii Anopheles Eukaryota Phylogenetic Analysis Agriculture Genomics 3. Good health Insects Phylogenetics Africa Western Genetic Mapping Infectious Diseases [SDE]Environmental Sciences Acetylcholinesterase Agrochemicals Research Article Computer and Information Sciences африканские комары Evolutionary Processes DNA Copy Number Variations Arthropoda 030231 tropical medicine Population Locus (genetics) Mosquito Vectors Genetic Introgression 03 medical and health sciences SDG 3 - Good Health and Well-being Genes Duplicate Animals Humans Evolutionary Systematics education Molecular Biology Ecology Evolution Behavior and Systematics 030304 developmental biology Taxonomy Evolutionary Biology Haplotype Organisms Biology and Life Sciences Organothiophosphorus Compounds biology.organism_classification Invertebrates Malaria Insect Vectors Species Interactions Haplotypes Animal Genomics Vector (epidemiology) People and Places Africa [SDE.BE]Environmental Sciences/Biodiversity and Ecology Zoology Entomology |
| Zdroj: | PLoS Genetics PLoS Genetics, Public Library of Science, 2021, 17 (1), pp.e1009253. ⟨10.1371/journal.pgen.1009253⟩ PLOS Genetics. 2021. Vol. 17, № 1. P. 1009253 (1-34) PLoS Genetics, 2021, 17 (1), pp.e1009253. ⟨10.1371/journal.pgen.1009253⟩ PLoS Genetics, Vol 17, Iss 1, p e1009253 (2021) Repositório Científico de Acesso Aberto de Portugal Repositório Científico de Acesso Aberto de Portugal (RCAAP) instacron:RCAAP PLoS genetics, 17(1):e1009253. PUBLIC LIBRARY SCIENCE |
| ISSN: | 1553-7390 1553-7404 |
| Popis: | Vector population control using insecticides is a key element of current strategies to prevent malaria transmission in Africa. The introduction of effective insecticides, such as the organophosphate pirimiphos-methyl, is essential to overcome the recurrent emergence of resistance driven by the highly diverse Anopheles genomes. Here, we use a population genomic approach to investigate the basis of pirimiphos-methyl resistance in the major malaria vectors Anopheles gambiae and A. coluzzii. A combination of copy number variation and a single non-synonymous substitution in the acetylcholinesterase gene, Ace1, provides the key resistance diagnostic in an A. coluzzii population from Côte d’Ivoire that we used for sequence-based association mapping, with replication in other West African populations. The Ace1 substitution and duplications occur on a unique resistance haplotype that evolved in A. gambiae and introgressed into A. coluzzii, and is now common in West Africa primarily due to selection imposed by other organophosphate or carbamate insecticides. Our findings highlight the predictive value of this complex resistance haplotype for phenotypic resistance and clarify its evolutionary history, providing tools to for molecular surveillance of the current and future effectiveness of pirimiphos-methyl based interventions. Author summary Control of mosquito populations via insecticidal tools or interventions is a mainstay of campaigns to reduce malaria transmission. However, especially in sub-Saharan Africa, continued insecticidal selection pressure on the most important species of Anopheles malaria mosquitoes has favoured the evolutionary selection of increasingly effective resistance mechanisms. We investigate the genetic basis of resistance to the organophosphate pirimiphos-methyl, the dominant insecticide now used for indoor residual spraying campaigns in Africa. Genome-wide association analysis of a population from Cote d’Ivoire showed that resistant specimens share a unique combination of mutations in one gene, the acetylcholinesterase enzyme, which constitute the prime cause of pirimiphos-methyl resistance. Further testing of these mutations in diagnostic assays involving two major malaria vectors, A. coluzzii and A. gambiae, validate their use as informative predictors of pirimiphos-methyl resistance. Using data from a large collection of whole genome sequenced specimens from a broader range of locations (Burkina-Faso, Côte d’Ivoire, Ghana, and Guinea), our evolutionary analyses demonstrate that these mutations emerged in A. gambiae and transferred into A. coluzzii by inter-specific hybridisation. Our results show how resistance mechanisms in key malaria vectors have developed and spread, and provide validated tools for molecular surveillance to inform public health campaigns. |
| Databáze: | OpenAIRE |
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