The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity
Abstract Background Worldwide invasion and expansion of Aedes albopictus, an important vector of dengue, chikungunya, and Zika viruses, has become a serious concern in global public health. Chemical insecticides are the primary means currently available to control the mosquito populations. However,...
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| Format: | Article |
| Language: | English |
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BMC
2023-09-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01693-0 |
| _version_ | 1797451464944123904 |
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| author | Yijia Guo Ke Hu Jingni Zhou Zhensheng Xie Yijie Zhao Siyu Zhao Jinbao Gu Xiaohong Zhou Guiyun Yan Anthony A. James Xiao-Guang Chen |
| author_facet | Yijia Guo Ke Hu Jingni Zhou Zhensheng Xie Yijie Zhao Siyu Zhao Jinbao Gu Xiaohong Zhou Guiyun Yan Anthony A. James Xiao-Guang Chen |
| author_sort | Yijia Guo |
| collection | DOAJ |
| description | Abstract Background Worldwide invasion and expansion of Aedes albopictus, an important vector of dengue, chikungunya, and Zika viruses, has become a serious concern in global public health. Chemical insecticides are the primary means currently available to control the mosquito populations. However, long-term and large-scale use of insecticides has selected for resistance in the mosquito that is accompanied by a genetic load that impacts fitness. Results A number of laboratory strains representing different resistance mechanisms were isolated and identified from laboratory-derived, deltamethrin-resistant Ae. albopictus recovered in previous work. Resistance levels and fitness costs of the strains were evaluated and compared to characterize the evolution of the resistance genotypes and phenotypes. The heterozygous F1534S mutation (1534F/S) in the voltage gated sodium channel (vgsc) gene product (VGSC), first detected in early stages of resistance evolution, not only confers high-level resistance, but also produces no significant fitness costs, leading to the rapid spread of resistance in the population. This is followed by the increase in frequency of homozygous F1534S (1534S/S) mosquitoes that have significant fitness disadvantages, prompting the emergence of an unlinked I1532T mutation with fewer side effects and a mating advantage better adapted to the selection and reproductive pressures imposed in the experiments. Metabolic resistance with no significant fitness cost and mediating a high-tolerance resistance phenotype may play a dominant role in the subsequent evolution of resistance. The different resistant strains had similar vector competence for dengue virus type-2 (DENV-2). Furthermore, a comparative analysis of vectorial capacity revealed that increased survival due to deltamethrin resistance balanced the negative fitness cost effects and contributed to the risk of dengue virus (DENV) transmission by resistant populations. The progressive evolution of resistance results in mosquitoes with both target-site insensitivity and metabolic resistance with lower fitness costs, which further leads to resistant populations with both high resistance levels and vectorial capacity. Conclusions This study reveals a possible mechanism for the evolution of deltamethrin resistance in Aedes albopictus. These findings will help guide practical strategies for insecticide use, resistance management and the prevention and control of mosquito-borne disease. |
| first_indexed | 2024-03-09T14:55:03Z |
| format | Article |
| id | doaj.art-440825cf409a4fe4bd68da729a9aa6ab |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-09T14:55:03Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-440825cf409a4fe4bd68da729a9aa6ab2023-11-26T14:14:22ZengBMCBMC Biology1741-70072023-09-0121111610.1186/s12915-023-01693-0The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacityYijia Guo0Ke Hu1Jingni Zhou2Zhensheng XieYijie Zhao3Siyu Zhao4Jinbao Gu5Xiaohong Zhou6Guiyun Yan7Anthony A. James8Xiao-Guang Chen9Department of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityProgram in Public Health, University of CaliforniaDepartment of Microbiology & Molecular Genetics, University of CaliforniaDepartment of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical UniversityAbstract Background Worldwide invasion and expansion of Aedes albopictus, an important vector of dengue, chikungunya, and Zika viruses, has become a serious concern in global public health. Chemical insecticides are the primary means currently available to control the mosquito populations. However, long-term and large-scale use of insecticides has selected for resistance in the mosquito that is accompanied by a genetic load that impacts fitness. Results A number of laboratory strains representing different resistance mechanisms were isolated and identified from laboratory-derived, deltamethrin-resistant Ae. albopictus recovered in previous work. Resistance levels and fitness costs of the strains were evaluated and compared to characterize the evolution of the resistance genotypes and phenotypes. The heterozygous F1534S mutation (1534F/S) in the voltage gated sodium channel (vgsc) gene product (VGSC), first detected in early stages of resistance evolution, not only confers high-level resistance, but also produces no significant fitness costs, leading to the rapid spread of resistance in the population. This is followed by the increase in frequency of homozygous F1534S (1534S/S) mosquitoes that have significant fitness disadvantages, prompting the emergence of an unlinked I1532T mutation with fewer side effects and a mating advantage better adapted to the selection and reproductive pressures imposed in the experiments. Metabolic resistance with no significant fitness cost and mediating a high-tolerance resistance phenotype may play a dominant role in the subsequent evolution of resistance. The different resistant strains had similar vector competence for dengue virus type-2 (DENV-2). Furthermore, a comparative analysis of vectorial capacity revealed that increased survival due to deltamethrin resistance balanced the negative fitness cost effects and contributed to the risk of dengue virus (DENV) transmission by resistant populations. The progressive evolution of resistance results in mosquitoes with both target-site insensitivity and metabolic resistance with lower fitness costs, which further leads to resistant populations with both high resistance levels and vectorial capacity. Conclusions This study reveals a possible mechanism for the evolution of deltamethrin resistance in Aedes albopictus. These findings will help guide practical strategies for insecticide use, resistance management and the prevention and control of mosquito-borne disease.https://doi.org/10.1186/s12915-023-01693-0Target-site resistanceMetabolic resistanceSelectionPyrethroidVector competence |
| spellingShingle | Yijia Guo Ke Hu Jingni Zhou Zhensheng Xie Yijie Zhao Siyu Zhao Jinbao Gu Xiaohong Zhou Guiyun Yan Anthony A. James Xiao-Guang Chen The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity BMC Biology Target-site resistance Metabolic resistance Selection Pyrethroid Vector competence |
| title | The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity |
| title_full | The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity |
| title_fullStr | The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity |
| title_full_unstemmed | The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity |
| title_short | The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity |
| title_sort | dynamics of deltamethrin resistance evolution in aedes albopictus has an impact on fitness and dengue virus type 2 vectorial capacity |
| topic | Target-site resistance Metabolic resistance Selection Pyrethroid Vector competence |
| url | https://doi.org/10.1186/s12915-023-01693-0 |
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