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      Influence of Urban Landscapes on Population Dynamics in a Short-Distance Migrant Mosquito: Evidence for the Dengue Vector Aedes aegypti

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          Abstract

          Background

          Dengue viruses are endemic across most tropical and subtropical regions. Because no proven vaccines are available, dengue prevention is primarily accomplished through controlling the mosquito vector Aedes aegypti. While dispersal distance is generally believed to be ∼100 m, patterns of dispersion may vary in urban areas due to landscape features acting as barriers or corridors to dispersal. Anthropogenic features ultimately affect the flow of genes affecting vector competence and insecticide resistance. Therefore, a thorough understanding of what parameters impact dispersal is essential for efficient implementation of any mosquito population suppression program. Population replacement and genetic control strategies currently under consideration are also dependent upon a thorough understanding of mosquito dispersal in urban settings.

          Methodology and Principal Findings

          We examined the effect of a major highway on dispersal patterns over a 2 year period. A. aegypti larvae were collected on the east and west sides of Uriah Butler Highway (UBH) to examine any effect UBH may have on the observed population structure in the Charlieville neighborhood in Trinidad, West Indies. A panel of nine microsatellites, two SNPs and a 710 bp sequence of mtDNA cytochrome oxidase subunit 1 ( CO1) were used for the molecular analyses of the samples. Three CO1 haplotypes were identified, one of which was only found on the east side of the road in 2006 and 2007. AMOVA using mtCO1 and nuclear markers revealed significant differentiation between the east- and west-side collections.

          Conclusion and Significance

          Our results indicate that anthropogenic barriers to A. aegypti dispersal exist in urban environments and should be considered when implementing control programs during dengue outbreaks and population suppression or replacement programs.

          Author Summary

          Worldwide, 2.5 billion people are at risk for dengue infection, with no vaccine or treatment available. Thus dengue prevention is largely focused on controlling its mosquito vector, Aedes aegypti. Traditional mosquito control approaches typically include insecticide applications and breeding site source reduction. Presently, novel dengue control measures including the sterile insect technique and population replacement with dengue-incompetent transgenic mosquitoes are also being considered. Success of all population control programs is in part dependent upon understanding mosquito population ecology, including how anthropogenic effects on the urban landscape influence dispersal and expansion. We conducted a two year population genetic study examining how a major metropolitan highway impacts mosquito dispersal in Trinidad, West Indies. As evidenced by significant differentiation using both nuclear and mitochondrial DNA sequences, the highway acted as a significant barrier to dispersal. Our results suggest that anthropogenic landscape features can be used effectively to enhance population suppression/replacement measures by defining mosquito control zones along recognized landscape barriers that limit population dispersal.

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          Most cited references42

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          The global emergence/resurgence of arboviral diseases as public health problems.

          During the past 20 years there has been a dramatic resurgence or emergence of epidemic arboviral diseases affecting both humans and domestic animals. These epidemics have been caused primarily by viruses thought to be under control such as dengue, Japanese encephalitis, yellow fever, and Venezuelan equine encephalitis, or viruses that have expanded their geographic distribution such as West Nile and Rift Valley fever. Several of these viruses are presented as case studies to illustrate the changing epidemiology. The factors responsible for the dramatic resurgence of arboviral diseases in the waning years of the 20th century are discussed, as is the need for rebuilding the public health infrastructure to deal with epidemic vector-borne diseases in the 21st century.
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            Invasions by insect vectors of human disease.

            Nonindigenous vectors that arrive, establish, and spread in new areas have fomented throughout recorded history epidemics of human diseases such as malaria, yellow fever, typhus, and plague. Although some vagile vectors, such as adults of black flies, biting midges, and tsetse flies, have dispersed into new habitats by flight or wind, human-aided transport is responsible for the arrival and spread of most invasive vectors, such as anthropophilic fleas, lice, kissing bugs, and mosquitoes. From the fifteenth century to the present, successive waves of invasion of the vector mosquitoes Aedes aegypti, the Culex pipiens Complex, and, most recently, Aedes albopictus have been facilitated by worldwide ship transport. Aircraft have been comparatively unimportant for the transport of mosquito invaders. Mosquito species that occupy transportable container habitats, such as water-holding automobile tires, have been especially successful as recent invaders. Propagule pressure, previous success, and adaptations to human habits appear to favor successful invasions by vectors.
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              Dispersal of the dengue vector Aedes aegypti within and between rural communities.

              Knowledge of mosquito dispersal is critical for vector-borne disease control and prevention strategies and for understanding population structure and pathogen dissemination. We determined Aedes aegypti flight range and dispersal patterns from 21 mark-release-recapture experiments conducted over 11 years (1991-2002) in Puerto Rico and Thailand. Dispersal was compared by release location, sex, age, season, and village. For all experiments, the majority of mosquitoes were collected from their release house or adjacent house. Inter-village movement was detected rarely, with a few mosquitoes moving a maximum of 512 meters from one Thai village to the next. Average dispersal distances were similar for males and females and females released indoors versus outdoors. The movement of Ae. aegypti was not influenced by season or age, but differed by village. Results demonstrate that adult Ae. aegypti disperse relatively short distances, suggesting that people rather than mosquitoes are the primary mode of dengue virus dissemination within and among communities.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                March 2010
                16 March 2010
                : 4
                : 3
                : e634
                Affiliations
                [1 ]Department of Biological Sciences, Eck Institute for Global Health, University of Notre Dame, Notre Dame, Indiana, United States of America
                [2 ]Department of Life Sciences, University of the West Indies, St. Augustine, Trinidad and Tobago, West Indies
                Duke University-National University of Singapore, Singapore
                Author notes

                Conceived and designed the experiments: RRH DDC DWS. Performed the experiments: RRH CLT DDC DWS. Analyzed the data: RRH. Wrote the paper: RRH DDC DWS.

                Article
                09-PNTD-RA-0469R2
                10.1371/journal.pntd.0000634
                2838782
                20300516
                2b0bf870-560e-45f0-ab93-00bf3eade933
                Hemme 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
                : 8 September 2009
                : 28 January 2010
                Page count
                Pages: 9
                Categories
                Research Article
                Ecology/Behavioral Ecology
                Ecology/Population Ecology
                Ecology/Spatial and Landscape Ecology
                Genetics and Genomics/Population Genetics
                Infectious Diseases/Viral Infections
                Public Health and Epidemiology/Infectious Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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