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A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection

Authors :
Jean-Marc Bonneville
Frederic Laporte
Ian W. Sutherland
Benedicte Fustec
Jeffrey C. Hertz
Tristan Cumer
Sébastien Marcombe
Julien Renaud
Thierry Gaude
Jean-Philippe David
Sébastien Boyer
Camille Noûs
Victor Arnaud
Chloé Haberkorn
Julien Cattel
Laboratoire d'Ecologie Alpine (LECA )
Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry])-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)
Naval Air Station Jacksonville (NAS Jacksonville)
United States Navy - U.S. Navy (USA)
Naval Medical Research Unit Two [Singapore] (NAMRU-2)
Naval Medical Research
Khon Kaen University [Thailand] (KKU)
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])
Institut Pasteur du Cambodge
Réseau International des Instituts Pasteur (RIIP)
Institut Pasteur du Laos
This work was conducted in the framework of the U.S. Naval Medical Research Unit TWO projects BIO‐LAO‐2 (work unit number D1425) and ARBOVEC‐PLUS (work unit number D1428), in support and funded by the Department of Defense Global Emerging Infections Surveillance Program and Military Infectious Disease Research Program. I (IWS and JCH) am a military Service member. This work was prepared as part of my official duties. Title 17, U.S.C., Section 105 provides that copyright protection under this title is not available for any work of the U.S. Government. Title 17, U.S.C., Section 101 defines a U.S. Government work as a work prepared by a military Service member or employee of the U.S. Government as part of that person's official duties. This publication was also supported by the project, Research Infrastructures for the control of vector‐borne diseases (Infravec2), which has received funding from the European Union's Horizon 2020 research and innovation program under grant agreement No 731060. Dr. Julien Cattel was supported by funding from the European Union's Horizon 2020 Research and Innovation Programme under ZIKAlliance Grant Agreement no. 734548. The field study in Cambodia was supported by ECOMORE 2 project, coordinated by Institut Pasteur and financially supported by AFD (Agence Française pour le Développement).
European Project: 731060,INFRAVEC2(2017)
European Project: 734548,ZIKAlliance(2016)
United States Navy Entomology
Laboratoire Cogitamus
Laboratoire d'Ecologie Alpine (LECA)
Université Joseph Fourier - Grenoble 1 (UJF)-Centre National de la Recherche Scientifique (CNRS)-Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry])
Source :
Evolutionary Applications, Vol 14, Iss 4, Pp 1009-1022 (2021), Evolutionary Applications, Evolutionary Applications, Blackwell, 2021, 14 (4), pp.1009-1022. ⟨10.1111/eva.13177⟩, Evolutionary Applications, 2021, 14 (4), pp.1009-1022. ⟨10.1111/eva.13177⟩
Publication Year :
2021
Publisher :
Wiley, 2021.

Abstract

By altering gene expression and creating paralogs, genomic amplifications represent a key component of short-term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxification enzymes, supporting the usefulness of these DNA markers for monitoring the dynamics of resistance alleles in the field. In this context, the present study aims to characterise a genomic amplification event associated with resistance to organophosphate insecticides in the mosquito Aedes aegypti and to develop a molecular assay to monitor the associated resistance alleles in the field. An experimental evolution experiment using a composite population from Laos supported the association between the over-transcription of multiple contiguous carboxylesterase genes on chromosome 2 and resistance to multiple organophosphate insecticides. Combining whole genome sequencing and qPCR on specific genes confirmed the presence of a ~100 Kb amplification spanning at least five carboxylesterase genes at this locus with the co-existence of multiple structural duplication haplotypes. Field data confirmed their circulation in South-East Asia and revealed high copy number polymorphism among and within populations suggesting a trade-off between this resistance mechanism and associated fitness costs. A dual-colour multiplex TaqMan assay allowing the rapid detection and copy number quantification of this amplification event in Ae. aegypti was developed and validated on field populations. The routine use of this novel assay will improve the tracking of resistance alleles in this major arbovirus vector.

Details

Language :
English
ISSN :
17524571 and 17524563
Volume :
14
Issue :
4
Database :
OpenAIRE
Journal :
Evolutionary Applications
Accession number :
edsair.doi.dedup.....270925fc9a895eb33458a2d82072739e
Full Text :
https://doi.org/10.1111/eva.13177⟩