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      Population genomics of the Asian tiger mosquito, Aedes albopictus: insights into the recent worldwide invasion

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          Abstract

          Aedes albopictus, the “Asian tiger mosquito,” is an aggressive biting mosquito native to Asia that has colonized all continents except Antarctica during the last ~30–40 years. The species is of great public health concern as it can transmit at least 26 arboviruses, including dengue, chikungunya, and Zika viruses. In this study, using double‐digest Restriction site‐Associated DNA (dd RAD) sequencing, we developed a panel of ~58,000 single nucleotide polymorphisms ( SNPs) based on 20 worldwide Ae. albopictus populations representing both the invasive and the native range. We used this genomic‐based approach to study the genetic structure and the differentiation of Ae. albopictus populations and to understand origin(s) and dynamics of the recent invasions. Our analyses indicated the existence of two major genetically differentiated population clusters, each one including both native and invasive populations. The detection of additional genetic structure within each major cluster supports that these SNPs can detect differentiation at a global and local scale, while the similar levels of genomic diversity between native and invasive range populations support the scenario of multiple invasions or colonization by a large number of propagules. Finally, our results revealed the possible source(s) of the recent invasion in Americas, Europe, and Africa, a finding with important implications for vector‐control strategies.

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          Critical review of the vector status of Aedes albopictus.

          N G Gratz (2004)
          The mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), originally indigenous to South-east Asia, islands of the Western Pacific and Indian Ocean, has spread during recent decades to Africa, the mid-east, Europe and the Americas (north and south) after extending its range eastwards across Pacific islands during the early 20th century. The majority of introductions are apparently due to transportation of dormant eggs in tyres. Among public health authorities in the newly infested countries and those threatened with the introduction, there has been much concern that Ae. albopictus would lead to serious outbreaks of arbovirus diseases (Ae. albopictus is a competent vector for at least 22 arboviruses), notably dengue (all four serotypes) more commonly transmitted by Aedes (Stegomyia) aegypti (L.). Results of many laboratory studies have shown that many arboviruses are readily transmitted by Ae. albopictus to laboratory animals and birds, and have frequently been isolated from wild-caught mosquitoes of this species, particularly in the Americas. As Ae. albopictus continues to spread, displacing Ae. aegypti in some areas, and is anthropophilic throughout its range, it is important to review the literature and attempt to predict whether the medical risks are as great as have been expressed in scientific journals and the popular press. Examination of the extensive literature indicates that Ae. albopictus probably serves as a maintenance vector of dengue in rural areas of dengue-endemic countries of South-east Asia and Pacific islands. Also Ae. albopictus transmits dog heartworm Dirofilaria immitis (Leidy) (Spirurida: Onchocercidae) in South-east Asia, south-eastern U.S.A. and both D. immitis and Dirofilaria repens (Raillet & Henry) in Italy. Despite the frequent isolation of dengue viruses from wild-caught mosquitoes, there is no evidence that Ae. albopictus is an important urban vector of dengue, except in a limited number of countries where Ae. aegypti is absent, i.e. parts of China, the Seychelles, historically in Japan and most recently in Hawaii. Further research is needed on the dynamics of the interaction between Ae. albopictus and other Stegomyia species. Surveillance must also be maintained on the vectorial role of Ae. albopictus in countries endemic for dengue and other arboviruses (e.g. Chikungunya, EEE, Ross River, WNV, LaCrosse and other California group viruses), for which it would be competent and ecologically suited to serve as a bridge vector.
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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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              Differential Susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika Virus

              Background Since the major outbreak in 2007 in the Yap Island, Zika virus (ZIKV) causing dengue-like syndromes has affected multiple islands of the South Pacific region. In May 2015, the virus was detected in Brazil and then spread through South and Central America. In December 2015, ZIKV was detected in French Guiana and Martinique. The aim of the study was to evaluate the vector competence of the mosquito spp. Aedes aegypti and Aedes albopictus from the Caribbean (Martinique, Guadeloupe), North America (southern United States), South America (Brazil, French Guiana) for the currently circulating Asian genotype of ZIKV isolated from a patient in April 2014 in New Caledonia. Methodology/Principal Findings Mosquitoes were orally exposed to an Asian genotype of ZIKV (NC-2014-5132). Upon exposure, engorged mosquitoes were maintained at 28°±1°C, a 16h:8h light:dark cycle and 80% humidity. 25–30 mosquitoes were processed at 4, 7 and 14 days post-infection (dpi). Mosquito bodies (thorax and abdomen), heads and saliva were analyzed to measure infection, dissemination and transmission, respectively. High infection but lower disseminated infection and transmission rates were observed for both Ae. aegypti and Ae. albopictus. Ae. aegypti populations from Guadeloupe and French Guiana exhibited a higher dissemination of ZIKV than the other Ae. aegypti populations examined. Transmission of ZIKV was observed in both mosquito species at 14 dpi but at a low level. Conclusions/Significance This study suggests that although susceptible to infection, Ae. aegypti and Ae. albopictus were unexpectedly low competent vectors for ZIKV. This may suggest that other factors such as the large naïve population for ZIKV and the high densities of human-biting mosquitoes contribute to the rapid spread of ZIKV during the current outbreak.
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                Author and article information

                Contributors
                panagiota.kotsakiozi@yale.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                24 October 2017
                December 2017
                : 7
                : 23 ( doiID: 10.1002/ece3.2017.7.issue-23 )
                : 10143-10157
                Affiliations
                [ 1 ] Department of Ecology and Evolutionary Biology Yale UniversityNew Haven CT USA
                [ 2 ] Department of Public Health and Infectious Disease Sapienza University of Rome Rome Italy
                [ 3 ] School of Bioscience and Veterinary Medicine University of Camerino Camerino Italy
                [ 4 ] Laboratório de Fisiologia e Controle de Artrópodes Vetores IOC‐FIOCRUZ Rio de Janeiro Brazil
                [ 5 ] Department of Environmental Biology Sapienza University of Rome Rome Italy
                [ 6 ] Department of Biology Georgetown University Washington DC USA
                Author notes
                [*] [* ] Correspondence

                Panayiota Kotsakiozi, Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA.

                Email: panagiota.kotsakiozi@ 123456yale.edu

                Author information
                http://orcid.org/0000-0002-8007-5330
                Article
                ECE33514
                10.1002/ece3.3514
                5723592
                29238544
                a9c53535-77ef-43fc-8bd5-83cce5ce94e8
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 June 2017
                : 28 August 2017
                : 30 August 2017
                Page count
                Figures: 6, Tables: 2, Pages: 15, Words: 12350
                Funding
                Funded by: NIH
                Award ID: R15 AI111328
                Award ID: 5T32AI007404‐2
                Funded by: Institute for Biospheric Studies, Yale University
                Funded by: Bodossaki Foundation
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece33514
                December 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.2.8 mode:remove_FC converted:10.12.2017

                Evolutionary Biology
                arboviruses vector,ddrad,genetic structure,phylogeography,snps
                Evolutionary Biology
                arboviruses vector, ddrad, genetic structure, phylogeography, snps

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