Chuanhui Zang, Xuejun Wang, Yan Liu, Haifang Wang, Qintong Sun, Peng Cheng, Ye Zhang, Maoqing Gong, Hongmei Liu
{"title":"Wolbachia and mosquitoes: Exploring transmission modes and coevolutionary dynamics in Shandong Province, China","authors":"Chuanhui Zang, Xuejun Wang, Yan Liu, Haifang Wang, Qintong Sun, Peng Cheng, Ye Zhang, Maoqing Gong, Hongmei Liu","doi":"10.1371/journal.pntd.0011944","DOIUrl":null,"url":null,"abstract":"Vector-borne diseases leave a large footprint on global health. Notable culprits include West Nile virus (WNV), St. Louis encephalitis virus (SLEV), and Japanese encephalitis virus (JEV), all transmitted by <jats:italic>Culex</jats:italic> mosquitoes. Chemical insecticides have been widely used to reduce the spread of mosquito-borne diseases. Still, mosquitoes are becoming more and more resistant to most chemical insecticides which cause particular harm to the ecology. <jats:italic>Wolbachia</jats:italic> belongs to the family Ehrlichiaceae in the order Rickettsiales and is a matrilineally inherited endosymbiont present in 60% of insects in nature. <jats:italic>Wolbachia</jats:italic> is capable of inducing a wide range of reproductive abnormalities in its hosts, such as cytoplasmic incompatibility, and can alter mosquito resistance to pathogen infection. <jats:italic>Wolbachia</jats:italic> has been proposed as a biological alternative to chemical vector control, and specific research progress and effectiveness have been achieved. Despite the importance of <jats:italic>Wolbachia</jats:italic>, this strategy has not been tested in <jats:italic>Culex pipiens pallens</jats:italic>, the most prevalent mosquito species in Shandong Province, China. Little is known about how the mass release of <jats:italic>Wolbachia</jats:italic>-infected mosquitoes may impact the genetic structure of <jats:italic>Culex pipiens pallens</jats:italic>, and how the symbiotic bacterium <jats:italic>Wolbachia</jats:italic> interacts with mitochondria during host mosquito transmission. Based on the population genetic structure of <jats:italic>Culex pipiens pallens</jats:italic> in Shandong Province, this study investigated the infection rate and infection type of <jats:italic>Wolbachia</jats:italic> in Shandong Province and jointly analysed the evolutionary relationship between the host mosquito and the symbiotic bacterium <jats:italic>Wolbachia</jats:italic>. Our study showed that <jats:italic>Wolbachia</jats:italic> naturally infected by <jats:italic>Culex pipiens pallens</jats:italic> in Shandong Province was less homologous to <jats:italic>Wolbachia</jats:italic> infected by <jats:italic>Aedes albopictus</jats:italic> released from mosquito factory in Guangzhou. Our results also show that <jats:italic>Culex pipiens pallens</jats:italic> is undergoing demographic expansion in Shandong Province. The overall <jats:italic>Wolbachia</jats:italic> infection rate of <jats:italic>Culex pipiens pallens</jats:italic> was 92.8%, and a total of 15 WSP haplotypes were detected. We found that the genetic diversity of <jats:italic>Wolbachia</jats:italic> was low in <jats:italic>Culex pipiens pallens</jats:italic> from Shandong Province, and the mosquitoes were infected only with type B <jats:italic>Wolbachia</jats:italic>. Visualizing the relationship between <jats:italic>Culex pipiens pallens</jats:italic> and <jats:italic>Wolbachia</jats:italic> using a tanglegram revealed patterns of widespread associations. A specific coevolutionary relationship exists between the host mosquito and <jats:italic>Wolbachia</jats:italic>. Knowledge of this mosquito–<jats:italic>Wolbachia</jats:italic> relationship will provide essential scientific information required for <jats:italic>Wolbachia</jats:italic>-based vector control approaches in Shandong Province and will lead to a better understanding of the diversity and evolution of <jats:italic>Wolbachia</jats:italic> for its utility as a biocontrol agent.","PeriodicalId":20260,"journal":{"name":"PLoS Neglected Tropical Diseases","volume":"7 1","pages":""},"PeriodicalIF":3.8000,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Neglected Tropical Diseases","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1371/journal.pntd.0011944","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Medicine","Score":null,"Total":0}
引用次数: 0
Abstract
Vector-borne diseases leave a large footprint on global health. Notable culprits include West Nile virus (WNV), St. Louis encephalitis virus (SLEV), and Japanese encephalitis virus (JEV), all transmitted by Culex mosquitoes. Chemical insecticides have been widely used to reduce the spread of mosquito-borne diseases. Still, mosquitoes are becoming more and more resistant to most chemical insecticides which cause particular harm to the ecology. Wolbachia belongs to the family Ehrlichiaceae in the order Rickettsiales and is a matrilineally inherited endosymbiont present in 60% of insects in nature. Wolbachia is capable of inducing a wide range of reproductive abnormalities in its hosts, such as cytoplasmic incompatibility, and can alter mosquito resistance to pathogen infection. Wolbachia has been proposed as a biological alternative to chemical vector control, and specific research progress and effectiveness have been achieved. Despite the importance of Wolbachia, this strategy has not been tested in Culex pipiens pallens, the most prevalent mosquito species in Shandong Province, China. Little is known about how the mass release of Wolbachia-infected mosquitoes may impact the genetic structure of Culex pipiens pallens, and how the symbiotic bacterium Wolbachia interacts with mitochondria during host mosquito transmission. Based on the population genetic structure of Culex pipiens pallens in Shandong Province, this study investigated the infection rate and infection type of Wolbachia in Shandong Province and jointly analysed the evolutionary relationship between the host mosquito and the symbiotic bacterium Wolbachia. Our study showed that Wolbachia naturally infected by Culex pipiens pallens in Shandong Province was less homologous to Wolbachia infected by Aedes albopictus released from mosquito factory in Guangzhou. Our results also show that Culex pipiens pallens is undergoing demographic expansion in Shandong Province. The overall Wolbachia infection rate of Culex pipiens pallens was 92.8%, and a total of 15 WSP haplotypes were detected. We found that the genetic diversity of Wolbachia was low in Culex pipiens pallens from Shandong Province, and the mosquitoes were infected only with type B Wolbachia. Visualizing the relationship between Culex pipiens pallens and Wolbachia using a tanglegram revealed patterns of widespread associations. A specific coevolutionary relationship exists between the host mosquito and Wolbachia. Knowledge of this mosquito–Wolbachia relationship will provide essential scientific information required for Wolbachia-based vector control approaches in Shandong Province and will lead to a better understanding of the diversity and evolution of Wolbachia for its utility as a biocontrol agent.
期刊介绍:
PLOS Neglected Tropical Diseases publishes research devoted to the pathology, epidemiology, prevention, treatment and control of the neglected tropical diseases (NTDs), as well as relevant public policy.
The NTDs are defined as a group of poverty-promoting chronic infectious diseases, which primarily occur in rural areas and poor urban areas of low-income and middle-income countries. Their impact on child health and development, pregnancy, and worker productivity, as well as their stigmatizing features limit economic stability.
All aspects of these diseases are considered, including:
Pathogenesis
Clinical features
Pharmacology and treatment
Diagnosis
Epidemiology
Vector biology
Vaccinology and prevention
Demographic, ecological and social determinants
Public health and policy aspects (including cost-effectiveness analyses).