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      Quality control methods for Aedes albopictus sterile male production

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          Abstract

          The capacity of the released sterile males to survive, disperse, compete with wild males and inseminate wild females is an essential prerequisite to be evaluated in any area-wide integrated pest management (AW-IPM) programs including a sterile insect release method. Adequate quality control tests supported by standardized procedures need to be developed to measure these parameters and to identify and correct potential inappropriate rearing or handling methods affecting the overall male quality. In this study, we report results on the creation and validation of the first quality control devices designed to infer the survival and mating capacity of radio-sterilized Aedes albopictus males through the observation of their flight capacity under restricted conditions (flight organ device) and after stress treatment (aspirator device). Results obtained consistently indicate comparable flight capacity and quality parameters between untreated and 35 Gy irradiated males while a negative impact was observed with higher radiation doses at all observation time performed. The male flight capacity registered with the proposed quality control devices can be successfully employed, with different predictive capacities and response time, to infer the adult male quality. These simple and cost-effective tools provide a valuable method to detect and amend potentially sub-standard procedures in the sterile male production line and hence contribute to maintaining optimal quality and field performance of the mosquitoes being released.

          Author summary

          The absence of effective therapeutics and vaccines for emerging and re-emerging vector-borne diseases and the limited effectiveness of conventional vector control methods renovated the interest for the implementation and integration of the SIT and genetic control methods for successful area-wide integrated mosquito management strategies. These methods involve the release of mass reared insects genetically sterile, incompatible or resistant to pathogen amplification and transmission which need to effectively introduce in the wild target population adequate sterility or the desired genetically selected traits. The availability of easy and standardized quality control tests could facilitate the adoption of international procedures for mosquito strains evaluation and comparison and to assess strain suitability for effective mosquito genetic control applications.

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          Field performance of engineered male mosquitoes.

          Dengue is the most medically important arthropod-borne viral disease, with 50-100 million cases reported annually worldwide. As no licensed vaccine or dedicated therapy exists for dengue, the most promising strategies to control the disease involve targeting the predominant mosquito vector, Aedes aegypti. However, the current methods to do this are inadequate. Various approaches involving genetically engineered mosquitoes have been proposed, including the release of transgenic sterile males. However, the ability of laboratory-reared, engineered male mosquitoes to effectively compete with wild males in terms of finding and mating with wild females, which is critical to the success of these strategies, has remained untested. We report data from the first open-field trial involving a strain of engineered mosquito. We demonstrated that genetically modified male mosquitoes, released across 10 hectares for a 4-week period, mated successfully with wild females and fertilized their eggs. These findings suggest the feasibility of this technology to control dengue by suppressing field populations of A. aegypti.
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            The first releases of transgenic mosquitoes: an argument for the sterile insect technique

            Potential applications for reducing transmission of mosquito-borne diseases by releasing genetically modified mosquitoes have been proposed, and mosquitoes are being created with such an application in mind in several laboratories. The use of the sterile insect technique (SIT) provides a safe programme in which production, release and mating competitiveness questions related to mass-reared genetically modified mosquitoes could be answered. It also provides a reversible effect that would be difficult to accomplish with gene introgression approaches. Could new technologies, including recombinant DNA techniques, have improved the success of previous mosquito releases? Criteria for an acceptable transgenic sterile mosquito are described, and the characteristics of radiation-induced sterility are compared with that of current transgenic approaches. We argue that SIT using transgenic material would provide an essentially safe and efficacious foundation for other possible approaches that are more ambitious.
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              Historical applications of induced sterilisation in field populations of mosquitoes

              Research on sterile mosquito technology from 1955 to the 1980s provided a substantial body of knowledge on propagation and release of sterile mosquitoes. Radiation sterilisation and chemosterilisation have been used effectively to induce dominant lethality and thereby sterilise important mosquito vectors in the laboratory. Experimental releases of chemosterilised males provided complete control of Anopheles albimanus in a small breeding population (14-15 sq km) in El Salvador. Releases of radiation sterilised males failed to control either Aedes aegypti or Anopheles quadrimaculatus in the USA. Releases of radiation-sterilised and chemosterilised male Culex quinquefasciatus in the USA and India were successful in some instances. Development of genetic sexing systems for Anopheles and improved physical separation methods for Culex have made it possible to rear and release males almost exclusively (> 99%) minimizing the release of potential vectors, the females. Factors that affected efficacy in some field programmes included reduction of competitiveness by radiation, immigration of fertilized females from outside the release zones, and inability of laboratory-bred males to perform in the wild. Despite significant progress, institutional commitments to carry the process further were generally lacking in the late 1970s and until recently. Now, with renewed interest and support for further assessment of this technology, this paper summarizes the current knowledge base, prioritizes some areas of investigation, and challenges scientists and administrators to maintain an awareness of progress, remain realistic about the interpretation of new findings, and make decisions about the sterile insect technique on the basis of informed scientific documentation. Areas recommended for priority research status include the establishment of genetic sexing mechanisms that can be transferred to other mosquito species, re-examination of radiation sterilisation, aerial release technology and mass rearing.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                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
                11 September 2017
                September 2017
                : 11
                : 9
                : e0005881
                Affiliations
                [1 ] Insect Pest Control Laboratory, NAFA Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, FAO/IAEA Agriculture and Biotechnology Laboratories, Seibersdorf, Austria
                [2 ] Medical and Veterinary Entomology Department, Centro Agricoltura Ambiente CAA "G. Nicoli”, Crevalcore, Italy
                Liverpool School of Tropical Medicine, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2558-3954
                Article
                PNTD-D-17-00487
                10.1371/journal.pntd.0005881
                5608434
                28892483
                78dcd73a-53a2-4bea-b393-f56fe6f4fb8e
                © 2017 Balestrino 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
                : 3 April 2017
                : 18 August 2017
                Page count
                Figures: 8, Tables: 1, Pages: 18
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Biological Locomotion
                Flight (Biology)
                Insect Flight
                Medicine and Health Sciences
                Physiology
                Biological Locomotion
                Flight (Biology)
                Insect Flight
                Engineering and Technology
                Industrial Engineering
                Quality Control
                Biology and Life Sciences
                Physiology
                Biological Locomotion
                Flight (Biology)
                Medicine and Health Sciences
                Physiology
                Biological Locomotion
                Flight (Biology)
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Pupae
                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
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and Life Sciences
                Developmental Biology
                Fertilization
                Insemination
                Engineering and Technology
                Aerospace Engineering
                Flight Testing
                People and Places
                Demography
                Fertility Rates
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-09-21
                All relevant data are within the paper.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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