Perran A Ross, Ella Yeatman, Mel S Berran, Xinyue Gu, Ary A Hoffmann, Belinda van Heerwaarden
{"title":"<i>Wolbachia</i> strain <i>w</i>MelM disrupts egg retention by <i>Aedes aegypti</i> females prevented from ovipositing.","authors":"Perran A Ross, Ella Yeatman, Mel S Berran, Xinyue Gu, Ary A Hoffmann, Belinda van Heerwaarden","doi":"10.1128/aem.01491-24","DOIUrl":null,"url":null,"abstract":"<p><p><i>Aedes aegypti</i> mosquitoes are well adapted to dry climates and can retain their eggs for extended periods in the absence of suitable habitat. <i>Wolbachia</i> strains transferred from other insects to mosquitoes can be released to combat dengue transmission by blocking virus replication and spreading through populations, but host fitness costs imposed by <i>Wolbachia</i>, particularly under some environments, can impede spread. We, therefore, assessed the impact of two <i>Wolbachia</i> strains being released for dengue control (<i>w</i>AlbB and <i>w</i>MelM) on fecundity and egg viability following extended egg retention (up to 24 days) under laboratory conditions. Egg viability following retention decreased to a greater extent in females carrying <i>w</i>MelM compared to uninfected or <i>w</i>AlbB females. Fertility fully recovered in uninfected females following a second blood meal after laying retained eggs, while <i>w</i>MelM females experienced only partial recovery. Effects of <i>w</i>MelM on egg retention were similar regardless of whether females were crossed to uninfected or <i>w</i>MelM males, suggesting that fitness costs were triggered by <i>Wolbachia</i> presence in females. The fecundity and hatch proportions of eggs of <i>w</i>MelM females declined with age, regardless of whether females used stored sperm or were recently inseminated. Costs of some <i>Wolbachia</i> strains during egg retention may affect the invasion and persistence of <i>Wolbachia</i> in release sites where larval habitats are scarce and/or intermittent.IMPORTANCE<i>Wolbachia</i> mosquito releases are expanding around the world with substantial impacts on dengue transmission. Releases have succeeded in many locations, but the establishment of <i>Wolbachia</i> has been challenging in some environments, and the factors contributing to this outcome remain unresolved. Here, we explore the effects of <i>Wolbachia</i> on a novel trait, egg retention, which is likely to be important for the persistence of mosquito populations in locations with intermittent rainfall. We find substantial impacts of the <i>Wolbachia</i> strain <i>w</i>MelM on the quality of retained eggs but not the <i>w</i>AlbB strain. This cost is driven by the <i>Wolbachia</i> infection status of the female and can partially recover following a second blood meal. The results of our study may help to explain the difficulty in establishing <i>Wolbachia</i> strains at some field release sites and emphasize the need to characterize <i>Wolbachia</i> phenotypes across a variety of traits and strains.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":" ","pages":"e0149124"},"PeriodicalIF":3.9000,"publicationDate":"2024-12-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.01491-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Aedes aegypti mosquitoes are well adapted to dry climates and can retain their eggs for extended periods in the absence of suitable habitat. Wolbachia strains transferred from other insects to mosquitoes can be released to combat dengue transmission by blocking virus replication and spreading through populations, but host fitness costs imposed by Wolbachia, particularly under some environments, can impede spread. We, therefore, assessed the impact of two Wolbachia strains being released for dengue control (wAlbB and wMelM) on fecundity and egg viability following extended egg retention (up to 24 days) under laboratory conditions. Egg viability following retention decreased to a greater extent in females carrying wMelM compared to uninfected or wAlbB females. Fertility fully recovered in uninfected females following a second blood meal after laying retained eggs, while wMelM females experienced only partial recovery. Effects of wMelM on egg retention were similar regardless of whether females were crossed to uninfected or wMelM males, suggesting that fitness costs were triggered by Wolbachia presence in females. The fecundity and hatch proportions of eggs of wMelM females declined with age, regardless of whether females used stored sperm or were recently inseminated. Costs of some Wolbachia strains during egg retention may affect the invasion and persistence of Wolbachia in release sites where larval habitats are scarce and/or intermittent.IMPORTANCEWolbachia mosquito releases are expanding around the world with substantial impacts on dengue transmission. Releases have succeeded in many locations, but the establishment of Wolbachia has been challenging in some environments, and the factors contributing to this outcome remain unresolved. Here, we explore the effects of Wolbachia on a novel trait, egg retention, which is likely to be important for the persistence of mosquito populations in locations with intermittent rainfall. We find substantial impacts of the Wolbachia strain wMelM on the quality of retained eggs but not the wAlbB strain. This cost is driven by the Wolbachia infection status of the female and can partially recover following a second blood meal. The results of our study may help to explain the difficulty in establishing Wolbachia strains at some field release sites and emphasize the need to characterize Wolbachia phenotypes across a variety of traits and strains.
期刊介绍:
Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.