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      Genetic Diversity of Brazilian Aedes aegypti: Patterns following an Eradication Program

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          Abstract

          Background

          Aedes aegypti is the most important vector of dengue fever in Brazil, where severe epidemics have recently taken place. Ae. aegypti in Brazil was the subject of an intense eradication program in the 1940s and 50s to control yellow fever. Brazil was the largest country declared free of this mosquito by the Pan-American Health Organization in 1958. Soon after relaxation of this program, Ae. aegypti reappeared in this country, and by the early 1980s dengue fever had been reported. The aim of this study is to analyze the present-day genetic patterns of Ae. aegypti populations in Brazil.

          Methodology/Principal Findings

          We studied the genetic variation in samples of 11 widely spread populations of Ae. aegypti in Brazil based on 12 well-established microsatellite loci. Our principal finding is that present-day Brazilian Ae. aegypti populations form two distinct groups, one in the northwest and one in the southeast of the country. These two groups have genetic affinities to northern South American countries and the Caribbean, respectively. This is consistent with what has been reported for other genetic markers such as mitochondrial DNA and allele frequencies at the insecticide resistance gene, kdr.

          Conclusions/Significance

          We conclude that the genetic patterns in present day populations of Ae. aegypti in Brazil are more consistent with a complete eradication of the species in the recent past followed by re-colonization, rather than the alternative possibility of expansion from residual pockets of refugia. At least two colonizations are likely to have taken place, one from northern South American countries (e.g., Venezuela) that founded the northwestern group, and one from the Caribbean that founded the southeastern group. The proposed source areas were never declared free of Ae. aegypti.

          Author Summary

          The mosquito, Aedes aegypti, was historically very important as the major vector of yellow fever, whereas today it is most notorious for being the major transmitter of dengue fever. In the 1940s and 50s, the Pan-American Health Organization organized a campaign to eradicate Ae. aegypti from the New World. They were partly successful, with Brazil being the largest country to be declared free of Ae. aegypti. Within ten years of relaxation of control efforts, Ae. aegypti reappeared in Brazil and today is the vector of the most intense dengue epidemics in the New World. Here, we present population genetic data that are most consistent with the species having truly been eradicated from Brazil rather than simply pushed into small refugia as a consequence of the eradication campaign. The re-infestation most likely resulted from two sources: 1) from northern S. American countries like Venezuela into northwest Brazil and 2) from the Caribbean into the southeast of the country.

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          Most cited references30

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          Arlequin (version 3.0): An integrated software package for population genetics data analysis

          Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multi-locus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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            Isolation by distance, web service

            Background The population genetic pattern known as "isolation by distance" results from spatially limited gene flow and is a commonly observed phenomenon in natural populations. However, few software programs exist for estimating the degree of isolation by distance among populations, and they tend not to be user-friendly. Results We have created Isolation by Distance Web Service (IBDWS) a user-friendly web interface for determining patterns of isolation by distance. Using this site, population geneticists can perform a variety of powerful statistical tests including Mantel tests, Reduced Major Axis (RMA) regression analysis, as well as calculate F ST between all pairs of populations and perform basic summary statistics (e.g., heterozygosity). All statistical results, including publication-quality scatter plots in Postscript format, are returned rapidly to the user and can be easily downloaded. Conclusion IBDWS population genetics analysis software is hosted at and documentation is available at . The source code has been made available on Source Forge at .
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              The history of dengue outbreaks in the Americas.

              Dengue is a viral disease usually transmitted by Aedes aegypti mosquitoes. Dengue outbreaks in the Americas reported in medical literature and to the Pan American Health Organization are described. The outbreak history from 1600 to 2010 was categorized into four phases: Introduction of dengue in the Americas (1600-1946); Continental plan for the eradication of the Ae. aegypti (1947-1970) marked by a successful eradication of the mosquito in 18 continental countries by 1962; Ae. aegypti reinfestation (1971-1999) caused by the failure of the mosquito eradication program; Increased dispersion of Ae. aegypti and dengue virus circulation (2000-2010) characterized by a marked increase in the number of outbreaks. During 2010 > 1.7 million dengue cases were reported, with 50,235 severe cases and 1,185 deaths. A dramatic increase in the number of outbreaks has been reported in recent years. Urgent global action is needed to avoid further disease spread.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                September 2014
                18 September 2014
                : 8
                : 9
                : e3167
                Affiliations
                [1 ]Laboratorio de Epidemiologia e Sistematica Molecular, Instituto Oswald Cruz—Fiocruz, Rio de Janeiro, Brazil
                [2 ]Laboratório de Biologia Computacional e Sistemas, IOC – Fiocruz, Rio de Janeiro, Brazil
                [3 ]Laboratório de Fisiologia e Controle de Artrópodes Vetores, IOC – Fiocruz, Rio de Janeiro, Brazil
                [4 ]Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United States of America
                Makerere University, Uganda
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: FAM JRP. Performed the experiments: FAM AGS JEB. Analyzed the data: FAM RS AGS AJM JRP. Contributed reagents/materials/analysis tools: JRP FAM RS AJM. Contributed to the writing of the manuscript: FAM AGS RS AJM JRP.

                Article
                PNTD-D-14-00711
                10.1371/journal.pntd.0003167
                4169244
                25233218
                4f3401fd-90c3-40ac-b6f2-b76a8ddb49f4
                Copyright @ 2014

                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
                : 28 April 2014
                : 5 August 2014
                Page count
                Pages: 10
                Funding
                This work was supported by the Brazilian Dengue Control Program, Brazilian Ministry of Health and the US NIH grant RO1 AI101112. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biogeography
                Evolutionary Biology
                Genetics
                Population Biology
                Ecology and Environmental Sciences
                Species Colonization
                Medicine and Health Sciences
                Epidemiology
                Infectious Diseases
                Public and Occupational Health
                Tropical Diseases
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper, main text and Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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