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      Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa

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          Abstract

          Aedes aegypti, the major vector of dengue, yellow fever, chikungunya, and Zika viruses, remains of great medical and public health concern. There is little doubt that the ancestral home of the species is Africa. This mosquito invaded the New World 400‐500 years ago and later, Asia. However, little is known about the genetic structure and history of Ae. aegypti across Africa, as well as the possible origin(s) of the New World invasion. Here, we use ~17,000 genome‐wide single nucleotide polymorphisms ( SNPs) to characterize a heretofore undocumented complex picture of this mosquito across its ancestral range in Africa. We find signatures of human‐assisted migrations, connectivity across long distances in sylvan populations, and of local admixture between domestic and sylvan populations. Finally, through a phylogenetic analysis combined with the genetic structure analyses, we suggest West Africa and especially Angola as the source of the New World's invasion, a scenario that fits well with the historic record of 16th‐century slave trade between Africa and Americas.

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          Evolution of mosquito preference for humans linked to an odorant receptor

          Female mosquitoes are major vectors of human disease and the most dangerous are those that preferentially bite humans. A ‘domestic’ form of the mosquito Aedes aegypti has evolved to specialize in biting humans and is the major worldwide vector of dengue, yellow fever, and Chikungunya viruses. The domestic form coexists with an ancestral, animal-biting ‘forest’ form along the coast of Kenya. We collected the two forms, established laboratory colonies, and document striking divergence in preference for human versus animal odour. We further show that the evolution of preference for human odour in domestic mosquitoes is tightly linked to increases in the expression and ligand-sensitivity of the odorant receptor AaegOr4, which we found recognises a compound present at high levels in human odour. Our results provide a rare example of a gene contributing to behavioural evolution and provide insight into how disease-vectoring mosquitoes came to specialise on humans.
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            Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases.

            Understanding the processes by which species colonize and adapt to human habitats is particularly important in the case of disease-vectoring arthropods. The mosquito species Aedes aegypti, a major vector of dengue and yellow fever viruses, probably originated as a wild, zoophilic species in sub-Saharan Africa, where some populations still breed in tree holes in forested habitats. Many populations of the species, however, have evolved to thrive in human habitats and to bite humans. This includes some populations within Africa as well as almost all those outside Africa. It is not clear whether all domestic populations are genetically related and represent a single 'domestication' event, or whether association with human habitats has developed multiple times independently within the species. To test the hypotheses above, we screened 24 worldwide population samples of Ae. aegypti at 12 polymorphic microsatellite loci. We identified two distinct genetic clusters: one included all domestic populations outside of Africa and the other included both domestic and forest populations within Africa. This suggests that human association in Africa occurred independently from that in domestic populations across the rest of the world. Additionally, measures of genetic diversity support Ae. aegypti in Africa as the ancestral form of the species. Individuals from domestic populations outside Africa can reliably be assigned back to their population of origin, which will help determine the origins of new introductions of Ae. aegypti.
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              Human impacts have shaped historical and recent evolution in Aedes aegypti, the dengue and yellow fever mosquito.

              Although anthropogenic impacts are often considered harmful to species, human modifications to the landscape can actually create novel niches to which other species can adapt. These "domestication" processes are especially important in the context of arthropod disease vectors, where ecological overlap of vector and human populations may lead to epidemics. Here, we present results of a global genetic study of one such species, the dengue and yellow fever mosquito, Aedes aegypti, whose evolutionary history and current distribution have been profoundly shaped by humans. We used DNA sequences of four nuclear genes and 1504 single nucleotide polymorphism (SNP) markers developed with restriction-site associated DNA (RAD) sequencing to test the hypothesis that Ae. aegypti originated in Africa, where a domestic form arose and spread throughout the tropical and subtropical world with human trade and movement. Results confirmed African ancestry of the species, and supported a single subspeciation event leading to the pantropical domestic form. In addition, genetic data strongly supported the hypothesis that human trade routes first moved domestic Ae. aegypti out of Africa into the New World, followed by a later invasion from the New World into Southeast Asia and the Pacific. These patterns of domestication and invasion are relevant to many species worldwide, as anthropogenic forces increasingly impact evolutionary processes. © 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.
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                Author and article information

                Contributors
                jeffrey.powell@yale.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                13 July 2018
                August 2018
                : 8
                : 16 ( doiID: 10.1002/ece3.2018.8.issue-16 )
                : 7835-7848
                Affiliations
                [ 1 ] Yale University New Haven Connecticut
                [ 2 ] Centre for Research in Infectious Diseases P.O. Box 13591 Yaoundé Cameroon
                [ 3 ] Uganda Virus Research Institute Entebbe Uganda
                [ 4 ] MIVEGEC Laboratory (UMR IRD 224‐5290 CNRS‐UM) Institut de Recherche pour le développement (IRD) Montpellier France
                [ 5 ] IRD La Réunion‐GIP CYROI La Réunion France
                [ 6 ] Centre International de Recherches Médicales de Franceville (CIRMF) Franceville Gabon
                [ 7 ] Laboratoire d'Entomologie Fondamentale et Appliquée Université Ouaga 1 Pr Joseph KI‐ZERBO 03 BP 7021 Ouagadougou 03 Burkina Faso
                [ 8 ] Global Health and Tropical Medicine, GHTM Instituto de Higiene e Medicina Tropical, IHMT Universidade Nova de Lisboa, UNL Lisbon Portugal
                [ 9 ] Programa Nacional de Controle da Malária Direcção Nacional de Saúde Pública Ministério da Saúde Luanda Angola
                [ 10 ]Present address: The Connecticut Agricultural Experiment Station New Haven Connecticut
                Author notes
                [*] [* ] Correspondence

                Jeffrey R Powell, Yale University, New Haven, Connecticut.

                Email: jeffrey.powell@ 123456yale.edu

                Author information
                http://orcid.org/0000-0002-5401-3988
                http://orcid.org/0000-0002-7122-2079
                http://orcid.org/0000-0002-7651-5153
                Article
                ECE34278
                10.1002/ece3.4278
                6145026
                30250667
                92bbecec-5663-4f86-87e5-fd4cfdc0cbd0
                © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 29 May 2017
                : 22 May 2018
                : 29 May 2018
                Page count
                Figures: 7, Tables: 3, Pages: 14, Words: 9062
                Funding
                Funded by: National Institute of Allergy and Infectious Diseases
                Award ID: RO1 AI101112
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece34278
                August 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.9 mode:remove_FC converted:19.09.2018

                Evolutionary Biology
                aedes aegypti,africa,genetics,migration,population structure,snp‐chip
                Evolutionary Biology
                aedes aegypti, africa, genetics, migration, population structure, snp‐chip

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