A persistent behavioral state enables sustained predation of humans by mosquitoes

  1. Trevor R Sorrells  Is a corresponding author
  2. Anjali Pandey
  3. Adriana Rosas-Villegas
  4. Leslie B Vosshall  Is a corresponding author
  1. The Rockefeller University, United States

Abstract

Predatory animals pursue prey in a noisy sensory landscape, deciding when to continue or abandon their chase. The mosquito Aedes aegypti is a micropredator that first detects humans at a distance through sensory cues such as carbon dioxide. As a mosquito nears its target it senses more proximal cues such as body heat that guide it to a meal of blood. How long the search for blood continues after initial detection of a human is not known. Here we show that a 5-second optogenetic pulse of fictive carbon dioxide induced a persistent behavioral state in female mosquitoes that lasted for more than 10 minutes. This state is highly specific to females searching for a blood meal and was not induced in recently blood-fed females or in males, who do not feed on blood. In males that lack the gene fruitless, which controls persistent social behaviors in other insects, fictive carbon dioxide induced a long-lasting behavior response resembling the predatory state of females. Finally, we show that the persistent state triggered by detection of fictive carbon dioxide enabled females to engorge on a blood meal mimic offered up to 14 minutes after the initial 5-second stimulus. Our results demonstrate that a persistent internal state allows female mosquitoes to integrate multiple human sensory cues over long timescales, an ability that is key to their success as an apex micropredator of humans.

Data availability

Data availabilityAll data generated or analyzed during this study are included in the manuscript and Source Data Files 1-4. Large datasets are available at https://github.com/trevorsorrells/Optothermocycler.Code availabilityAnalysis code used in this publication is available at https://github.com/trevorsorrells/Optothermocycler.

The following data sets were generated

Article and author information

Author details

  1. Trevor R Sorrells

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, San Francisco, United States
    For correspondence
    trevorsorrells@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3527-8622
  2. Anjali Pandey

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5521-635X
  3. Adriana Rosas-Villegas

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9114-0882
  4. Leslie B Vosshall

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United States
    For correspondence
    leslie@rockefeller.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6060-8099

Funding

Howard Hughes Medical Institute (Investigator Award)

  • Trevor R Sorrells
  • Leslie B Vosshall

Jane Coffin Childs Memorial Fund for Medical Research (Postdoctoral Fellowship)

  • Trevor R Sorrells

Kavli Neural Systems Institute, The Rockefeller University (Postdoctoral Fellowship)

  • Trevor R Sorrells

Kavli Neural Systems Institute, The Rockefeller University (Pilot Award)

  • Trevor R Sorrells

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

Ethics

Animal experimentation: Blood feeding of mosquitoes with live anesthetized mice was conducted according to approved institutional animal care and use committee (IACUC) protocol #17108 of The Rockefeller University.

Human subjects: Blood feeding of mosquitoes with human volunteers was conducted according to IRB protocol LV-0652. Human volunteers gave written informed consent to participate in the experiments.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Publication history

  1. Received: December 29, 2021
  2. Accepted: May 11, 2022
  3. Accepted Manuscript published: May 12, 2022 (version 1)

Copyright

© 2022, Sorrells 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. Trevor R Sorrells
  2. Anjali Pandey
  3. Adriana Rosas-Villegas
  4. Leslie B Vosshall
(2022)
A persistent behavioral state enables sustained predation of humans by mosquitoes
eLife 11:e76663.
https://doi.org/10.7554/eLife.76663

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