Discovery of super–insecticide-resistant dengue mosquitoes in Asia: Threats of concomitant knockdown resistance mutations

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Abstract

Aedes aegypti (Linnaeus, 1762) is the main mosquito vector for dengue and other arboviral infectious diseases. Control of this important vector highly relies on the use of insecticides, especially pyrethroids. The high frequency (>78%) of the L982W substitution was detected at the target site of the pyrethroid insecticide, the voltage-gated sodium channel (Vgsc) of A. aegypti collected from Vietnam and Cambodia. Alleles having concomitant mutations L982W + F1534C and V1016G + F1534C were also confirmed in both countries, and their frequency was high (>90%) in Phnom Penh, Cambodia. Strains having these alleles exhibited substantially higher levels of pyrethroid resistance than any other field population ever reported. The L982W substitution has never been detected in any country of the Indochina Peninsula except Vietnam and Cambodia, but it may be spreading to other areas of Asia, which can cause an unprecedentedly serious threat to the control of dengue fever as well as other Aedes-borne infectious diseases.

Abstract

Highly insecticide-resistant mosquito vectors are an emerging threat to controlling arbovirus infectious diseases.

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Most cited references 60

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MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms.

Sudhir Kumar, Glen Stecher, Michael KaWah Li … (2018)

The Molecular Evolutionary Genetics Analysis (Mega) software implements many analytical methods and tools for phylogenomics and phylomedicine. Here, we report a transformation of Mega to enable cross-platform use on Microsoft Windows and Linux operating systems. Mega X does not require virtualization or emulation software and provides a uniform user experience across platforms. Mega X has additionally been upgraded to use multiple computing cores for many molecular evolutionary analyses. Mega X is available in two interfaces (graphical and command line) and can be downloaded from www.megasoftware.net free of charge.

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A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.

Motoo Kimura (1980)

Some simple formulae were obtained which enable us to estimate evolutionary distances in terms of the number of nucleotide substitutions (and, also, the evolutionary rates when the divergence times are known). In comparing a pair of nucleotide sequences, we distinguish two types of differences; if homologous sites are occupied by different nucleotide bases but both are purines or both pyrimidines, the difference is called type I (or "transition" type), while, if one of the two is a purine and the other is a pyrimidine, the difference is called type II (or "transversion" type). Letting P and Q be respectively the fractions of nucleotide sites showing type I and type II differences between two sequences compared, then the evolutionary distance per site is K = -(1/2) ln [(1-2P-Q) square root of 1-2Q]. The evolutionary rate per year is then given by k = K/(2T), where T is the time since the divergence of the two sequences. If only the third codon positions are compared, the synonymous component of the evolutionary base substitutions per site is estimated by K'S = -(1/2) ln (1-2P-Q). Also, formulae for standard errors were obtained. Some examples were worked out using reported globin sequences to show that synonymous substitutions occur at much higher rates than amino acid-altering substitutions in evolution.

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CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP.

Joseph Felsenstein (1985)

The recently-developed statistical method known as the "bootstrap" can be used to place confidence intervals on phylogenies. It involves resampling points from one's own data, with replacement, to create a series of bootstrap samples of the same size as the original data. Each of these is analyzed, and the variation among the resulting estimates taken to indicate the size of the error involved in making estimates from the original data. In the case of phylogenies, it is argued that the proper method of resampling is to keep all of the original species while sampling characters with replacement, under the assumption that the characters have been independently drawn by the systematist and have evolved independently. Majority-rule consensus trees can be used to construct a phylogeny showing all of the inferred monophyletic groups that occurred in a majority of the bootstrap samples. If a group shows up 95% of the time or more, the evidence for it is taken to be statistically significant. Existing computer programs can be used to analyze different bootstrap samples by using weights on the characters, the weight of a character being how many times it was drawn in bootstrap sampling. When all characters are perfectly compatible, as envisioned by Hennig, bootstrap sampling becomes unnecessary; the bootstrap method would show significant evidence for a group if it is defined by three or more characters.

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Author and article information

Contributors

Shinji Kasai:

ORCID: https://orcid.org/0000-0002-3837-6551

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Kentaro Itokawa:

ORCID: https://orcid.org/0000-0003-1300-9883

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: Writing - original draft

Nozomi Uemura:

ORCID: https://orcid.org/0000-0001-8597-6704

Role: InvestigationRole: ValidationRole: Writing - review & editing

Aki Takaoka:

ORCID: https://orcid.org/0000-0002-5885-2121

Role: Data curationRole: Formal analysisRole: InvestigationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Shogo Furutani: Role: Investigation

Yoshihide Maekawa: Role: Investigation

Daisuke Kobayashi:

ORCID: https://orcid.org/0000-0002-5735-8404

Role: Investigation

Nozomi Imanishi-Kobayashi: Role: Investigation

Michael Amoa-Bosompem:

ORCID: https://orcid.org/0000-0003-0416-2878

Role: InvestigationRole: ResourcesRole: Writing - review & editing

Katsunori Murota:

ORCID: https://orcid.org/0000-0002-3053-9504

Role: InvestigationRole: ResourcesRole: Writing - review & editing

Yukiko Higa: Role: InvestigationRole: Resources

Hitoshi Kawada:

ORCID: https://orcid.org/0000-0002-1565-7596

Role: Investigation

Noboru Minakawa: Role: Resources

Tran Chi Cuong:

ORCID: https://orcid.org/0000-0002-0721-6248

Role: Resources

Nguyen Thi Yen: Role: Investigation

Tran Vu Phong: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Sath Keo: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing - review & editing

Kroesna Kang:

ORCID: https://orcid.org/0000-0002-6818-1982

Role: Project administrationRole: ResourcesRole: Validation

Kozue Miura:

ORCID: https://orcid.org/0000-0002-3233-0202

Role: InvestigationRole: Resources

Lee Ching Ng:

ORCID: https://orcid.org/0000-0003-2413-3863

Role: ConceptualizationRole: ResourcesRole: Writing - review & editing

Hwa-Jen Teng: Role: ResourcesRole: Writing - review & editing

Samuel Dadzie: Role: ConceptualizationRole: Data curationRole: InvestigationRole: ResourcesRole: SoftwareRole: ValidationRole: Writing - review & editing

Sri Subekti:

ORCID: https://orcid.org/0000-0003-4816-041X

Role: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Kris Cahyo Mulyatno:

ORCID: https://orcid.org/0000-0001-8926-3031

Role: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Kyoko Sawabe: Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administration

Takashi Tomita:

ORCID: https://orcid.org/0000-0002-5029-3169

Role: Data curationRole: InvestigationRole: ResourcesRole: Writing - review & editing

Osamu Komagata:

ORCID: https://orcid.org/0000-0002-8175-6402

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: December 2022

Publication date (Electronic, pub): 21 December 2022

Volume: 8

Issue: 51

Electronic Location Identifier: eabq7345

Affiliations

[ ¹ ]Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo 162-8640, Japan.

[ ² ]Kagoshima Research Station, National Institute of Animal Health, National Agriculture and Food Research Organization, Kagoshima 891-0105, Japan.

[ ³ ]Department of Vector Ecology and Environment, Institute of Tropical Medicine, Nagasaki University, Nagasaki 852-8523, Japan.

[ ⁴ ]Medical Entomology and Zoology Department, National Institute of Hygiene and Epidemiology, Hanoi, Vietnam.

[ ⁵ ]Faculty of Veterinary Medicine, Royal University of Agriculture, P.O. Box 2696, Phnom Penh, Cambodia.

[ ⁶ ]Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo 113-8657, Japan.

[ ⁷ ]Environmental Health Institute, National Environment Agency, Singapore 138667, Singapore.

[ ⁸ ]School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.

[ ⁹ ]Center for Diagnostics and Vaccine Development, Centers for Disease Control, Ministry of Health and Welfare, Taipei City 10050, Taiwan.

[ ¹⁰ ]Department of Parasitology, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, P.O. Box LG 581, Legon,, Ghana.

[ ¹¹ ]Entomology Study Group, Institute of Tropical Disease, Universitas Airlangga, Surabaya 60115, Indonesia.

Author notes

[* ]Corresponding author. Email: kasacin@ 123456niid.go.jp (S.Ka.); komagata@ 123456niid.go.jp (O.K.)

[†]

These authors contributed equally to this work.

Author information

Shinji Kasai https://orcid.org/0000-0002-3837-6551

Kentaro Itokawa https://orcid.org/0000-0003-1300-9883

Nozomi Uemura https://orcid.org/0000-0001-8597-6704

Aki Takaoka https://orcid.org/0000-0002-5885-2121

Daisuke Kobayashi https://orcid.org/0000-0002-5735-8404

Michael Amoa-Bosompem https://orcid.org/0000-0003-0416-2878

Katsunori Murota https://orcid.org/0000-0002-3053-9504

Hitoshi Kawada https://orcid.org/0000-0002-1565-7596

Tran Chi Cuong https://orcid.org/0000-0002-0721-6248

Kroesna Kang https://orcid.org/0000-0002-6818-1982

Kozue Miura https://orcid.org/0000-0002-3233-0202

Lee Ching Ng https://orcid.org/0000-0003-2413-3863

Sri Subekti https://orcid.org/0000-0003-4816-041X

Kris Cahyo Mulyatno https://orcid.org/0000-0001-8926-3031

Takashi Tomita https://orcid.org/0000-0002-5029-3169

Osamu Komagata https://orcid.org/0000-0002-8175-6402

Article

Publisher ID: abq7345

DOI: 10.1126/sciadv.abq7345

PMC ID: 9770935

PubMed ID: 36542722

SO-VID: 7b6c0762-b526-4f74-b939-865062bc3b89

Copyright © Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.