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Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes

The globally invasive mosquito subspecies Aedes aegypti aegypti is an effective vector of human arboviruses, in part because it specializes in biting humans and breeding in human habitats. Recent work suggests that specialization first arose as an adaptation to long, hot dry seasons in the West Afri...

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Autores principales: Rose, Noah H, Badolo, Athanase, Sylla, Massamba, Akorli, Jewelna, Otoo, Sampson, Gloria-Soria, Andrea, Powell, Jeffrey R, White, Bradley J, Crawford, Jacob E, McBride, Carolyn S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10038657/
https://www.ncbi.nlm.nih.gov/pubmed/36897062
http://dx.doi.org/10.7554/eLife.83524
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author Rose, Noah H
Badolo, Athanase
Sylla, Massamba
Akorli, Jewelna
Otoo, Sampson
Gloria-Soria, Andrea
Powell, Jeffrey R
White, Bradley J
Crawford, Jacob E
McBride, Carolyn S
author_facet Rose, Noah H
Badolo, Athanase
Sylla, Massamba
Akorli, Jewelna
Otoo, Sampson
Gloria-Soria, Andrea
Powell, Jeffrey R
White, Bradley J
Crawford, Jacob E
McBride, Carolyn S
author_sort Rose, Noah H
collection PubMed
description The globally invasive mosquito subspecies Aedes aegypti aegypti is an effective vector of human arboviruses, in part because it specializes in biting humans and breeding in human habitats. Recent work suggests that specialization first arose as an adaptation to long, hot dry seasons in the West African Sahel, where Ae. aegypti relies on human-stored water for breeding. Here, we use whole-genome cross-coalescent analysis to date the emergence of human-specialist populationsand thus further probe the climate hypothesis. Importantly, we take advantage of the known migration of specialists out of Africa during the Atlantic Slave Trade to calibrate the coalescent clock and thus obtain a more precise estimate of the older evolutionary event than would otherwise be possible. We find that human-specialist mosquitoes diverged rapidly from ecological generalists approximately 5000 years ago, at the end of the African Humid Period—a time when the Sahara dried and water stored by humans became a uniquely stable, aquatic niche in the Sahel. We also use population genomic analyses to date a previously observed influx of human-specialist alleles into major West African cities. The characteristic length of tracts of human-specialist ancestry present on a generalist genetic background in Kumasi and Ouagadougou suggests the change in behavior occurred during rapid urbanization over the last 20–40 years. Taken together, we show that the timing and ecological context of two previously observed shifts towards human biting in Ae. aegypti differ; climate was likely the original driver, but urbanization has become increasingly important in recent decades.
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spelling pubmed-100386572023-03-25 Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes Rose, Noah H Badolo, Athanase Sylla, Massamba Akorli, Jewelna Otoo, Sampson Gloria-Soria, Andrea Powell, Jeffrey R White, Bradley J Crawford, Jacob E McBride, Carolyn S eLife Evolutionary Biology The globally invasive mosquito subspecies Aedes aegypti aegypti is an effective vector of human arboviruses, in part because it specializes in biting humans and breeding in human habitats. Recent work suggests that specialization first arose as an adaptation to long, hot dry seasons in the West African Sahel, where Ae. aegypti relies on human-stored water for breeding. Here, we use whole-genome cross-coalescent analysis to date the emergence of human-specialist populationsand thus further probe the climate hypothesis. Importantly, we take advantage of the known migration of specialists out of Africa during the Atlantic Slave Trade to calibrate the coalescent clock and thus obtain a more precise estimate of the older evolutionary event than would otherwise be possible. We find that human-specialist mosquitoes diverged rapidly from ecological generalists approximately 5000 years ago, at the end of the African Humid Period—a time when the Sahara dried and water stored by humans became a uniquely stable, aquatic niche in the Sahel. We also use population genomic analyses to date a previously observed influx of human-specialist alleles into major West African cities. The characteristic length of tracts of human-specialist ancestry present on a generalist genetic background in Kumasi and Ouagadougou suggests the change in behavior occurred during rapid urbanization over the last 20–40 years. Taken together, we show that the timing and ecological context of two previously observed shifts towards human biting in Ae. aegypti differ; climate was likely the original driver, but urbanization has become increasingly important in recent decades. eLife Sciences Publications, Ltd 2023-03-10 /pmc/articles/PMC10038657/ /pubmed/36897062 http://dx.doi.org/10.7554/eLife.83524 Text en © 2023, Rose et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Rose, Noah H
Badolo, Athanase
Sylla, Massamba
Akorli, Jewelna
Otoo, Sampson
Gloria-Soria, Andrea
Powell, Jeffrey R
White, Bradley J
Crawford, Jacob E
McBride, Carolyn S
Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
title Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
title_full Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
title_fullStr Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
title_full_unstemmed Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
title_short Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
title_sort dating the origin and spread of specialization on human hosts in aedes aegypti mosquitoes
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10038657/
https://www.ncbi.nlm.nih.gov/pubmed/36897062
http://dx.doi.org/10.7554/eLife.83524
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