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      Wolbachia strain wAu efficiently blocks arbovirus transmission in Aedes albopictus

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          Abstract

          The global incidence of arboviral diseases transmitted by Aedes mosquitoes, including dengue, chikungunya, yellow fever, and Zika, has increased dramatically in recent decades. The release of Aedes aegypti carrying the maternally inherited symbiont Wolbachia as an intervention to control arboviruses is being trialled in several countries. However, these efforts are compromised in many endemic regions due to the co-localization of the secondary vector Aedes albopictus, the Asian tiger mosquito. Ae. albopictus has an expanding global distribution following incursions into a number of new territories. To date, only the wMel and wPip strains of Wolbachia have been reported to be transferred into and characterized in this vector. A Wolbachia strain naturally infecting Drosophila simulans, wAu, was selected for transfer into a Malaysian Ae. albopictus line to create a novel triple-strain infection. The newly generated line showed self-compatibility, moderate fitness cost and complete resistance to Zika and dengue infections.

          Author summary

          Aedes albopictus, the invasive Asian tiger mosquito, is responsible for numerous outbreaks of important viruses such as dengue and Zika in various regions of the world. The need for alterative control interventions propelled the development of a novel approach that exploits a natural insect symbiont, Wolbachia; when transferred into non-native hosts, these maternally-inherited bacteria are able to interfere with the transmission of mosquito-borne viruses, and also provide reproductive advantages to the host, offering a promising tool for self-sustaining field applications. Currently, several field trials are ongoing for the primary vector of dengue and several other arboviruses, Aedes aegypti, providing encouraging results. In this study, Ae. albopictus has been targeted for a similar approach: this mosquito species naturally carries two strains of Wolbachia. The introduction of a third, non-native strain made this line less able to transmit dengue and Zika viruses and had an impact on its fitness.

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          Most cited references25

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus.

            Aedes albopictus, commonly known as the Asian tiger mosquito, is currently the most invasive mosquito in the world. It is of medical importance due to its aggressive daytime human-biting behavior and ability to vector many viruses, including dengue, LaCrosse, and West Nile. Invasions into new areas of its potential range are often initiated through the transportation of eggs via the international trade in used tires. We use a genetic algorithm, Genetic Algorithm for Rule Set Production (GARP), to determine the ecological niche of Ae. albopictus and predict a global ecological risk map for the continued spread of the species. We combine this analysis with risk due to importation of tires from infested countries and their proximity to countries that have already been invaded to develop a list of countries most at risk for future introductions and establishments. Methods used here have potential for predicting risks of future invasions of vectors or pathogens.
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              Incompatible and sterile insect techniques combined eliminate mosquitoes

              The radiation-based sterile insect technique (SIT) has successfully suppressed field populations of several insect pest species, but its effect on mosquito vector control has been limited. The related incompatible insect technique (IIT)-which uses sterilization caused by the maternally inherited endosymbiotic bacteria Wolbachia-is a promising alternative, but can be undermined by accidental release of females infected with the same Wolbachia strain as the released males. Here we show that combining incompatible and sterile insect techniques (IIT-SIT) enables near elimination of field populations of the world's most invasive mosquito species, Aedes albopictus. Millions of factory-reared adult males with an artificial triple-Wolbachia infection were released, with prior pupal irradiation of the released mosquitoes to prevent unintentionally released triply infected females from successfully reproducing in the field. This successful field trial demonstrates the feasibility of area-wide application of combined IIT-SIT for mosquito vector control.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: Writing – original draft
                Role: Methodology
                Role: MethodologyRole: Writing – review & editing
                Role: Methodology
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – original draft
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                10 March 2020
                March 2020
                : 14
                : 3
                : e0007926
                Affiliations
                [001]MRC- University of Glasgow- Centre for Virus Research, Glasgow, United Kingdom
                Faculty of Science, Ain Shams University (ASU), EGYPT
                Author notes

                The authors have declared that no competing interests exist.

                [¤]

                Current address: Dept. of Veterinary Pathobiology, University of Missouri, Columbia, Missouri, United States of America

                Author information
                http://orcid.org/0000-0002-2678-1832
                Article
                PNTD-D-19-01910
                10.1371/journal.pntd.0007926
                7083328
                32155143
                f4fafd28-32e0-4392-aea2-dda48de59eec
                © 2020 Mancini et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 November 2019
                : 17 January 2020
                Page count
                Figures: 4, Tables: 1, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 108508/Z/15/Z
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 202888/Z/16/Z
                Award Recipient :
                This work was supported by the Wellcome Trust grants 108508/Z/15/Z and 202888/Z/16/Z to SPS ( https://wellcome.ac.uk). The funders played no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Bacteria
                Wolbachia
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Flaviviruses
                Dengue Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Flaviviruses
                Dengue Virus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Viral Pathogens
                Flaviviruses
                Dengue Virus
                Biology and Life Sciences
                Organisms
                Viruses
                Viral Pathogens
                Flaviviruses
                Dengue Virus
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Flaviviruses
                Zika Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Flaviviruses
                Zika Virus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Viral Pathogens
                Flaviviruses
                Zika Virus
                Biology and Life Sciences
                Organisms
                Viruses
                Viral Pathogens
                Flaviviruses
                Zika Virus
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Organisms
                Viruses
                Arboviruses
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Biology and Life Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Aedes Aegypti
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-03-20
                The data underlying the results presented in the study are available from http://dx.doi.org/10.5525/gla.researchdata.961.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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