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

  1. Noah H Rose  Is a corresponding author
  2. Athanase Badolo
  3. Massamba Sylla
  4. Jewelna Akorli
  5. Sampson Otoo
  6. Andrea Gloria-Soria
  7. Jeffrey R Powell
  8. Bradley J White
  9. Jacob E Crawford
  10. Carolyn S McBride  Is a corresponding author
  1. Princeton University, United States
  2. Université Joseph Ki-Zerbo, Burkina Faso
  3. Université du Sine Saloum El-Hâdj Ibrahima NIASS, Senegal
  4. University of Ghana, Ghana
  5. Connecticut Agricultural Experiment Station, United States
  6. Yale University, United States
  7. Verily Life Sciences, United States

Abstract

The globally invasive mosquito subspecies Aedes aegypti aegypti is a highly 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 is forced to rely on human-stored water for breeding. However, rainfall patterns in this region have changed dramatically over the past 10-20 thousand years, and we do not yet know exactly when specialization occurred. Here we use whole-genome cross-coalescent analysis to date the emergence of human specialist populations in the Sahel and thus further probe the climate hypothesis. Importantly, we take advantage of the known migration of human-specialist populations 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 5,000 years ago, which corresponds to 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, where mosquitoes tend to be more attracted to humans than in nearby rural populations regardless of climate. In this case, the characteristic length of tracts of human-specialist ancestry present on a generalist genetic background in Kumasi, Ghana and Ouagadougou, Burkina Faso 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. Understanding the changing relationship between mosquitoes and humans over time is critical for predicting and managing burdens of mosquito-borne disease.

Data availability

Scripts and processed data are available at github.com/noahrose/aaeg-evol-hist. Raw genomic data are available in the NCBI SRA at accession PRJNA602495. Phasing reference panel is available at doi:10.5061/dryad.2bvq83btk.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Noah H Rose

    Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    For correspondence
    noahr@princeton.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7129-4753
  2. Athanase Badolo

    Laboratory of Fundamental and Applied Entomology, Université Joseph Ki-Zerbo, Ouagadougou, Burkina Faso
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6652-4240
  3. Massamba Sylla

    Department of Livestock Sciences and Techniques, Université du Sine Saloum El-Hâdj Ibrahima NIASS, Kaffrine, Senegal
    Competing interests
    No competing interests declared.
  4. Jewelna Akorli

    Department of Parasitology, University of Ghana, Accra, Ghana
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3972-0860
  5. Sampson Otoo

    Department of Parasitology, University of Ghana, Accra, Ghana
    Competing interests
    No competing interests declared.
  6. Andrea Gloria-Soria

    Department of Entomology, Connecticut Agricultural Experiment Station, New Haven, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5401-3988
  7. Jeffrey R Powell

    Yale University, New Haven, United States
    Competing interests
    No competing interests declared.
  8. Bradley J White

    Verily Life Sciences, South San Francisco, United States
    Competing interests
    Bradley J White, is affiliated with Verily Life Sciences. The author has no financial interests to declare..
  9. Jacob E Crawford

    Verily Life Sciences, South San Francisco, United States
    Competing interests
    Jacob E Crawford, is affiliated with Verily Life Sciences. The author has no financial interests to declare..
  10. Carolyn S McBride

    Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    For correspondence
    csm7@princeton.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8898-1768

Funding

Helen Hay Whitney Foundation

  • Noah H Rose

New York Stem Cell Foundation

  • Carolyn S McBride

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Preprint posted: September 13, 2022 (view preprint)
  2. Received: September 16, 2022
  3. Accepted: March 10, 2023
  4. Accepted Manuscript published: March 10, 2023 (version 1)
  5. Version of Record published: March 24, 2023 (version 2)

Copyright

© 2023, Rose et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Noah H Rose
  2. Athanase Badolo
  3. Massamba Sylla
  4. Jewelna Akorli
  5. Sampson Otoo
  6. Andrea Gloria-Soria
  7. Jeffrey R Powell
  8. Bradley J White
  9. Jacob E Crawford
  10. Carolyn S McBride
(2023)
Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes
eLife 12:e83524.
https://doi.org/10.7554/eLife.83524

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https://doi.org/10.7554/eLife.83524

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