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...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/83524 |
| _version_ | 1797853485173047296 |
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| author | Noah H Rose Athanase Badolo Massamba Sylla Jewelna Akorli Sampson Otoo Andrea Gloria-Soria Jeffrey R Powell Bradley J White Jacob E Crawford Carolyn S McBride |
| author_facet | Noah H Rose Athanase Badolo Massamba Sylla Jewelna Akorli Sampson Otoo Andrea Gloria-Soria Jeffrey R Powell Bradley J White Jacob E Crawford Carolyn S McBride |
| author_sort | Noah H Rose |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-09T19:50:19Z |
| format | Article |
| id | doaj.art-e09d40edc9304d659dbdd66768fc069b |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-09T19:50:19Z |
| publishDate | 2023-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e09d40edc9304d659dbdd66768fc069b2023-04-03T07:03:35ZengeLife Sciences Publications LtdeLife2050-084X2023-03-011210.7554/eLife.83524Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoesNoah H Rose0https://orcid.org/0000-0001-7129-4753Athanase Badolo1https://orcid.org/0000-0002-6652-4240Massamba Sylla2Jewelna Akorli3https://orcid.org/0000-0002-3972-0860Sampson Otoo4Andrea Gloria-Soria5https://orcid.org/0000-0002-5401-3988Jeffrey R Powell6Bradley J White7Jacob E Crawford8Carolyn S McBride9https://orcid.org/0000-0002-8898-1768Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States; Princeton Neuroscience Institute, Princeton University, Princeton, United StatesLaboratory of Fundamental and Applied Entomology, Université Joseph Ki-Zerbo, Ouagadougou, Burkina FasoDepartment of Livestock Sciences and Techniques, Sine Saloum University El Hadji Ibrahima NIASS, Kaffrine, SenegalDepartment of Parasitology, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, GhanaDepartment of Parasitology, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, GhanaDepartment of Entomology. Center for Vector Biology & Zoonotic Diseases. The Connecticut Agricultural Experiment Station, New Haven, United StatesYale University, New Haven, United StatesVerily Life Sciences, South San Francisco, United StatesVerily Life Sciences, South San Francisco, United StatesDepartment of Ecology and Evolutionary Biology, Princeton University, Princeton, United States; Princeton Neuroscience Institute, Princeton University, Princeton, United StatesThe 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.https://elifesciences.org/articles/83524Aedes aegypticoalescentclimate changeurban evolution |
| spellingShingle | Noah H Rose Athanase Badolo Massamba Sylla Jewelna Akorli Sampson Otoo Andrea Gloria-Soria Jeffrey R Powell Bradley J White Jacob E Crawford Carolyn S McBride Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes eLife Aedes aegypti coalescent climate change urban evolution |
| 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 | Aedes aegypti coalescent climate change urban evolution |
| url | https://elifesciences.org/articles/83524 |
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