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Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases.

ABSTRACT: 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.

SUBMITTER: Brown JE

PROVIDER: S-EPMC3125627 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases.

Brown Julia E JE McBride Carolyn S CS Johnson Petrina P Ritchie Scott S Paupy Christophe C Bossin Hervé H Lutomiah Joel J Fernandez-Salas Ildefonso I Ponlawat Alongkot A Cornel Anthony J AJ Black William C WC Gorrochotegui-Escalante Norma N Urdaneta-Marquez Ludmel L Sylla Massamba M Slotman Michel M Murray Kristy O KO Walker Christopher C Powell Jeffrey R JR

Proceedings. Biological sciences 20110112 1717

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 ...[more]

PMID: 21227970

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Project description:OBJECTIVES:The objective of this study was to map the global risk of the major arboviral diseases transmitted by Aedes aegypti and Aedes albopictus by identifying areas where the diseases are reported, either through active transmission or travel-related outbreaks, as well as areas where the diseases are not currently reported but are nonetheless suitable for the vector. METHODS:Data relating to five arboviral diseases (Zika, dengue fever, chikungunya, yellow fever, and Rift Valley fever (RVF)) were extracted from some of the largest contemporary databases and paired with data on the known distribution of their vectors, A. aegypti and A. albopictus. The disease occurrence data for the selected diseases were compiled from literature dating as far back as 1952 to as recent as 2017. The resulting datasets were aggregated at the country level, except in the case of the USA, where state-level data were used. Spatial analysis was used to process the data and to develop risk maps. RESULTS:Out of the 250 countries/territories considered, 215 (86%) are potentially suitable for the survival and establishment of A. aegypti and/or A. albopictus. A. albopictus has suitability foci in 197 countries/territories, while there are 188 that are suitable for A. aegypti. There is considerable variation in the suitability range among countries/territories, but many of the tropical regions of the world provide high suitability over extensive areas. Globally, 146 (58.4%) countries/territories reported at least one arboviral disease, while 123 (49.2%) reported more than one of the above diseases. The overall numbers of countries/territories reporting autochthonous vector-borne occurrences of Zika, dengue, chikungunya, yellow fever, and RVF, were 85, 111, 106, 43, and 39, respectively. CONCLUSIONS:With 215 countries/territories potentially suitable for the most important arboviral disease vectors and more than half of these reporting cases, arboviral diseases are indeed a global public health threat. The increasing proportion of reports that include multiple arboviral diseases highlights the expanding range of their common transmission vectors. The shared features of these arboviral diseases should motivate efforts to combine interventions against these diseases.

Project description:BACKGROUND:Genetic markers are widely used to understand the biology and population dynamics of disease vectors, but often markers are limited in the resolution they provide. In particular, the delineation of population structure, fine scale movement and patterns of relatedness are often obscured unless numerous markers are available. To address this issue in the major arbovirus vector, the yellow fever mosquito (Aedes aegypti), we used double digest Restriction-site Associated DNA (ddRAD) sequencing for the discovery of genome-wide single nucleotide polymorphisms (SNPs). We aimed to characterize the new SNP set and to test the resolution against previously described microsatellite markers in detecting broad and fine-scale genetic patterns in Ae. aegypti. RESULTS:We developed bioinformatics tools that support the customization of restriction enzyme-based protocols for SNP discovery. We showed that our approach for RAD library construction achieves unbiased genome representation that reflects true evolutionary processes. In Ae. aegypti samples from three continents we identified more than 18,000 putative SNPs. They were widely distributed across the three Ae. aegypti chromosomes, with 47.9% found in intergenic regions and 17.8% in exons of over 2,300 genes. Pattern of their imputed effects in ORFs and UTRs were consistent with those found in a recent transcriptome study. We demonstrated that individual mosquitoes from Indonesia, Australia, Vietnam and Brazil can be assigned with a very high degree of confidence to their region of origin using a large SNP panel. We also showed that familial relatedness of samples from a 0.4 km2 area could be confidently established with a subset of SNPs. CONCLUSIONS:Using a cost-effective customized RAD sequencing approach supported by our bioinformatics tools, we characterized over 18,000 SNPs in field samples of the dengue fever mosquito Ae. aegypti. The variants were annotated and positioned onto the three Ae. aegypti chromosomes. The new SNP set provided much greater resolution in detecting population structure and estimating fine-scale relatedness than a set of polymorphic microsatellites. RAD-based markers demonstrate great potential to advance our understanding of mosquito population processes, critical for implementing new control measures against this major disease vector.

Dataset Information

Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases.

Publications

Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases.

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