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      Combining the Sterile Insect Technique with the Incompatible Insect Technique: III-Robust Mating Competitiveness of Irradiated Triple Wolbachia-Infected Aedes albopictus Males under Semi-Field Conditions

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          Abstract

          Combination of the sterile insect technique with the incompatible insect technique is considered to be a safe approach to control Aedes albopictus populations in the absence of an accurate and scalable sex separation system or genetic sexing strain. Our previous study has shown that the triple Wolbachia-infected Ae. albopictus strain ( wAlbA, wAlbB and wPip) was suitable for mass rearing and females could be completely sterilized as pupae with a radiation dose of at least 28 Gy. However, whether this radiation dose can influence the mating competitiveness of the triple infected males was still unknown. In this study we aimed to evaluate the effects of irradiation on the male mating competitiveness of the triple infected strain under laboratory and semi-field conditions. The results herein indicate that irradiation with a lower, female-sterilizing dose has no negative impact on the longevity of triple infected males while a reduced lifespan was observed in the wild type males ( wAlbA and wAlbB) irradiated with a higher male-sterilizing dose, in small cages. At different sterile: fertile release ratios in small cages, triple-infected males induced 39.8, 81.6 and 87.8% sterility in a wild type female population at 1:1, 5:1 and 10:1 release ratios, respectively, relative to a fertile control population. Similarly, irradiated triple infected males induced 31.3, 70.5 and 89.3% sterility at 1:1, 5:1 and 10:1 release ratios, respectively, again relative to the fertile control. Under semi-field conditions at a 5:1 release ratio, relative to wild type males, the mean male mating competitiveness index of 28 Gy irradiated triple-infected males was significantly higher than 35 Gy irradiated wild type males, while triple infected males showed no difference in mean mating competitiveness to either irradiated triple-infected or irradiated wild type males. An unexpected difference was also observed in the relative male mating competitiveness of the triple infected strain after irradiation at 28 Gy dose in small vs large cages, with a higher male mating competitiveness index calculated from results of experiments in the large cages. Based on these results, we consider that the male mating performance of the triple infected strain after irradiation at 28 Gy, a dose required for complete female sterility and the avoidance of population replacement, is approximately equal to that of the wild type males under semi-field conditions. Though field evaluation is required, this suggests that the triple infected strain is suitable for irradiation and release as part of a combined SIT-IIT approach to Ae. albopictus control.

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          Most cited references39

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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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            Eradication of Culex pipiens fatigans through cytoplasmic incompatibility.

            H Laven (1967)
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 March 2016
                2016
                : 11
                : 3
                : e0151864
                Affiliations
                [1 ]Sun Yat-sen University - Michigan State University Joint Center of Vector Control for Tropical Diseases, Zhongshan School of Medicine, Guangzhou, Guangdong Province, China
                [2 ]Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Vienna, Austria
                [3 ]Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America
                University of Camerino, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: KB ZX JG. Performed the experiments: DZ. Analyzed the data: DZ RSL ZX KB JG. Contributed reagents/materials/analysis tools: JG KB ZX. Wrote the paper: DZ RSL ZX KB JG.

                Article
                PONE-D-15-44838
                10.1371/journal.pone.0151864
                4798476
                26990981
                034f6393-dabb-4ca5-85db-d31df11daaa6
                © 2016 Zhang 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
                : 12 October 2015
                : 4 March 2016
                Page count
                Figures: 3, Tables: 2, Pages: 15
                Funding
                Research in Prof. Zhiyong Xi’s laboratory was supported by the National Institutes of Health/National Institute of Allergy and Infectious Disease R01AI080597, the Key Project of Chinese Ministry of Education (No. 311030), Guangdong Innovative Research Team Program (No. 2011S009), Scientific and Technological Leading Talents of Guangzhou Development District (No. 2013L-P116) and a grant from the Foundation for the NIH through the Grand Challenges in Global Health Initiative of the Bill and Melinda Gates Foundation.
                Categories
                Research Article
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Bacteria
                Wolbachia
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Evolutionary Emergence
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Metamorphosis
                Pupae
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Insect Metamorphosis
                Pupae
                People and Places
                Demography
                Fertility Rates
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Copulation
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Copulation
                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Analysis of Variance
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Statistical Methods
                Analysis of Variance
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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