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Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis

BACKGROUND: Anopheles sinensis is one of the most abundant vectors of malaria and other diseases in Asia. Vector control through the use of insecticides is the front line control method of vector-borne diseases. Pyrethroids are the most commonly used insecticides due to their low toxicity to vertebr...

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Autores principales: Chang, Xuelian, Zhong, Daibin, Lo, Eugenia, Fang, Qiang, Bonizzoni, Mariangela, Wang, Xiaoming, Lee, Ming-Chieh, Zhou, Guofa, Zhu, Guoding, Qin, Qian, Chen, Xiaoguang, Cui, Liwang, Yan, Guiyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4842280/
https://www.ncbi.nlm.nih.gov/pubmed/27108406
http://dx.doi.org/10.1186/s13071-016-1513-6
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author Chang, Xuelian
Zhong, Daibin
Lo, Eugenia
Fang, Qiang
Bonizzoni, Mariangela
Wang, Xiaoming
Lee, Ming-Chieh
Zhou, Guofa
Zhu, Guoding
Qin, Qian
Chen, Xiaoguang
Cui, Liwang
Yan, Guiyun
author_facet Chang, Xuelian
Zhong, Daibin
Lo, Eugenia
Fang, Qiang
Bonizzoni, Mariangela
Wang, Xiaoming
Lee, Ming-Chieh
Zhou, Guofa
Zhu, Guoding
Qin, Qian
Chen, Xiaoguang
Cui, Liwang
Yan, Guiyun
author_sort Chang, Xuelian
collection PubMed
description BACKGROUND: Anopheles sinensis is one of the most abundant vectors of malaria and other diseases in Asia. Vector control through the use of insecticides is the front line control method of vector-borne diseases. Pyrethroids are the most commonly used insecticides due to their low toxicity to vertebrates and low repellency. However, the extensive use of insecticides has imposed strong selection pressure on mosquito populations for resistance. High levels of resistance to pyrethroid insecticides and various mutations and haplotypes in the para sodium channel gene that confers knockdown resistance (kdr) have been detected in An. sinensis. Despite the importance of kdr mutations in pyrethroid resistance, the evolutionary origin of the kdr mutations is unknown. This study aims to examine the evolutionary genetics of kdr mutations in relation to spatial population genetic structure of An. sinensis. METHODS: Adults or larvae of Anopheles sinensis were collected from various geographic locations in China. DNA was extracted from individual mosquitoes. PCR amplification and DNA sequencing of the para-type sodium channel gene were conducted to analyse kdr allele frequency distribution, kdr codon upstream and downstream intron polymorphism, population genetic diversity and kdr codon evolution. The mitochondrial cytochrome c oxidase COI and COII genes were amplified and sequenced to examine population variations, genetic differentiation, spatial population structure, population expansion and gene flow patterns. RESULTS: Three non-synonymous mutations (L1014F, L1014C, and L1014S) were detected at the kdr codon L1014 of para-type sodium channel gene. A patchy distribution of kdr mutation allele frequencies from southern to central China was found. Near fixation of kdr mutation was detected in populations from central China, but no kdr mutations were found in populations from southwestern China. More than eight independent mutation events were detected in the three kdr alleles, and at least one of them evolved multiple times subsequent to their first divergence. Based on sequence analysis of the mitochondrial COI and COII genes, significant and large genetic differentiation was detected between populations from southwestern China and central China. The patchy distribution of kdr mutation frequencies is likely a consequence of geographic isolation in the mosquito populations and the long-term insecticide selection. CONCLUSION: Our results indicate multiple origins of the kdr insecticide-resistant alleles in An. sinensis from southern and central China. Local selection related to intense and prolonged use of insecticide for agricultural purposes, as well as frequent migrations among populations are likely the explanations for the patchy distribution of kdr mutations in China. On the contrary, the lack of kdr mutations in Yunnan and Sichuan is likely a consequence of genetic isolation and absence of strong selection pressure. The present study compares the genetic patterns revealed by a functional gene with a neutral marker and demonstrates the combined impact of demographic and selection factors on population structure. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1513-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-48422802016-04-25 Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis Chang, Xuelian Zhong, Daibin Lo, Eugenia Fang, Qiang Bonizzoni, Mariangela Wang, Xiaoming Lee, Ming-Chieh Zhou, Guofa Zhu, Guoding Qin, Qian Chen, Xiaoguang Cui, Liwang Yan, Guiyun Parasit Vectors Research BACKGROUND: Anopheles sinensis is one of the most abundant vectors of malaria and other diseases in Asia. Vector control through the use of insecticides is the front line control method of vector-borne diseases. Pyrethroids are the most commonly used insecticides due to their low toxicity to vertebrates and low repellency. However, the extensive use of insecticides has imposed strong selection pressure on mosquito populations for resistance. High levels of resistance to pyrethroid insecticides and various mutations and haplotypes in the para sodium channel gene that confers knockdown resistance (kdr) have been detected in An. sinensis. Despite the importance of kdr mutations in pyrethroid resistance, the evolutionary origin of the kdr mutations is unknown. This study aims to examine the evolutionary genetics of kdr mutations in relation to spatial population genetic structure of An. sinensis. METHODS: Adults or larvae of Anopheles sinensis were collected from various geographic locations in China. DNA was extracted from individual mosquitoes. PCR amplification and DNA sequencing of the para-type sodium channel gene were conducted to analyse kdr allele frequency distribution, kdr codon upstream and downstream intron polymorphism, population genetic diversity and kdr codon evolution. The mitochondrial cytochrome c oxidase COI and COII genes were amplified and sequenced to examine population variations, genetic differentiation, spatial population structure, population expansion and gene flow patterns. RESULTS: Three non-synonymous mutations (L1014F, L1014C, and L1014S) were detected at the kdr codon L1014 of para-type sodium channel gene. A patchy distribution of kdr mutation allele frequencies from southern to central China was found. Near fixation of kdr mutation was detected in populations from central China, but no kdr mutations were found in populations from southwestern China. More than eight independent mutation events were detected in the three kdr alleles, and at least one of them evolved multiple times subsequent to their first divergence. Based on sequence analysis of the mitochondrial COI and COII genes, significant and large genetic differentiation was detected between populations from southwestern China and central China. The patchy distribution of kdr mutation frequencies is likely a consequence of geographic isolation in the mosquito populations and the long-term insecticide selection. CONCLUSION: Our results indicate multiple origins of the kdr insecticide-resistant alleles in An. sinensis from southern and central China. Local selection related to intense and prolonged use of insecticide for agricultural purposes, as well as frequent migrations among populations are likely the explanations for the patchy distribution of kdr mutations in China. On the contrary, the lack of kdr mutations in Yunnan and Sichuan is likely a consequence of genetic isolation and absence of strong selection pressure. The present study compares the genetic patterns revealed by a functional gene with a neutral marker and demonstrates the combined impact of demographic and selection factors on population structure. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1513-6) contains supplementary material, which is available to authorized users. BioMed Central 2016-04-23 /pmc/articles/PMC4842280/ /pubmed/27108406 http://dx.doi.org/10.1186/s13071-016-1513-6 Text en © Chang et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Chang, Xuelian
Zhong, Daibin
Lo, Eugenia
Fang, Qiang
Bonizzoni, Mariangela
Wang, Xiaoming
Lee, Ming-Chieh
Zhou, Guofa
Zhu, Guoding
Qin, Qian
Chen, Xiaoguang
Cui, Liwang
Yan, Guiyun
Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis
title Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis
title_full Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis
title_fullStr Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis
title_full_unstemmed Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis
title_short Landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in Anopheles sinensis
title_sort landscape genetic structure and evolutionary genetics of insecticide resistance gene mutations in anopheles sinensis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4842280/
https://www.ncbi.nlm.nih.gov/pubmed/27108406
http://dx.doi.org/10.1186/s13071-016-1513-6
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