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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

Julien Cattel, Chloé Haberkorn, Fréderic Laporte, Thierry Gaude, Tristan Cumer, Julien Renaud, Ian W. Sutherland, Jeffrey C. Hertz, Jean-Marc Bonneville, Victor Arnaud, Camille Noûs, Bénédicte Fustec, Sébastien Boyer, Sébastien Marcombe, Jean-Philippe David
doi: https://doi.org/10.1101/2020.06.08.139741
Julien Cattel
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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  • For correspondence: juliencattel@gmail.com
Chloé Haberkorn
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Fréderic Laporte
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Thierry Gaude
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Tristan Cumer
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Julien Renaud
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Ian W. Sutherland
2United States Navy Entomology. Center of Excellence, NAS Jacksonville, Florida, United States of America
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Jeffrey C. Hertz
3US Naval Medical Research Unit No. 2, Singapore
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Jean-Marc Bonneville
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Victor Arnaud
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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Camille Noûs
4Laboratoire Cogitamus, 1 ¾ rue Descartes, 75005 Paris, France
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Bénédicte Fustec
5Department of Microbiology, Khon Kaen University, Khon Kaen, Thailand
6Institut de Recherche pour le Développement, UMR IRD 224-CNRS 5290-Université Montpellier. 911, avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, FRANCE
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Sébastien Boyer
7Medical and Veterinary Entomology, Institut Pasteur du Cambodge, P.O Box. 983 Phnom Penh, Cambodia
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Sébastien Marcombe
8Medical Entomology and Vector-Borne Disease Laboratory, Institut Pasteur du Laos, Vientiane, Laos
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Jean-Philippe David
1Laboratoire d’Ecologie Alpine (LECA), UMR 5553 CNRS – Université Grenoble-Alpes, 2233 rue de la piscine, Grenoble, France
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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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Version 4 of this preprint has been peer-reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100114)

  • https://zenodo.org/record/4243761#.X6JBUWgzZPZ

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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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
Julien Cattel, Chloé Haberkorn, Fréderic Laporte, Thierry Gaude, Tristan Cumer, Julien Renaud, Ian W. Sutherland, Jeffrey C. Hertz, Jean-Marc Bonneville, Victor Arnaud, Camille Noûs, Bénédicte Fustec, Sébastien Boyer, Sébastien Marcombe, Jean-Philippe David
bioRxiv 2020.06.08.139741; doi: https://doi.org/10.1101/2020.06.08.139741
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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
Julien Cattel, Chloé Haberkorn, Fréderic Laporte, Thierry Gaude, Tristan Cumer, Julien Renaud, Ian W. Sutherland, Jeffrey C. Hertz, Jean-Marc Bonneville, Victor Arnaud, Camille Noûs, Bénédicte Fustec, Sébastien Boyer, Sébastien Marcombe, Jean-Philippe David
bioRxiv 2020.06.08.139741; doi: https://doi.org/10.1101/2020.06.08.139741

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