Abstract

The Aedes aegypti mosquito shows extreme sexual dimorphism in feeding. Only females are attracted to and obtain a blood-meal from humans, which they use to stimulate egg production. The fruitless gene is sex-specifically spliced and encodes a BTB zinc-finger transcription factor proposed to be a master regulator of male courtship and mating behavior across insects. We generated fruitless mutant mosquitoes and showed that males failed to mate, confirming the ancestral function of this gene in male sexual behavior. Remarkably, fruitless males also gain strong attraction to a live human host, a behavior that wild-type males never display, suggesting that male mosquitoes possess the central or peripheral neural circuits required to host-seek and that removing fruitless reveals this latent behavior in males. Our results highlight an unexpected repurposing of a master regulator of male-specific sexual behavior to control one module of female-specific blood-feeding behavior in a deadly vector of infectious diseases.

Data availability

All raw data are provided in Data File 1. Plasmids are available at Addgene (#141099, #141100). RNA-seq data are available in the Short Read Archive at Genbank (Bioproject: PRJNA612100). Details of Quattroport fabrication and operation are available at Github: https://github.com/VosshallLab/Basrur_Vosshall2020

The following data sets were generated

Article and author information

Author details

  1. Nipun S Basrur

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United States
    For correspondence
    nbasrur@rockefeller.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7068-7798
  2. Maria Elena De Obaldia

    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:" 0000-0003-2488-3672
  3. Takeshi Morita

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Margaret Herre

    Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ricarda K von Heynitz

    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:" 0000-0002-3038-3036
  6. Yael N Tsitohay

    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:" 0000-0002-8716-9444
  7. 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 (Vosshall-Investigator)

  • Leslie B Vosshall

National Center for Advancing Translational Sciences (UL1 TR000043)

  • Leslie B Vosshall

Harvey L. Karp Discovery Award (postdoctoral fellowship)

  • Maria Elena De Obaldia
  • Takeshi Morita

Japan Society for Promotion of Science (JSPS Overseas Research Fellowship)

  • Takeshi Morita

Helen Hay Whitney Foundation (HHW Fellowship)

  • Maria Elena De Obaldia

National Center for Advancing Translational Sciences (UL1 TR001866)

  • Maria Elena De Obaldia

National Institute on Deafness and Other Communication Disorders (F30DC017658)

  • Margaret Herre

National Institute of General Medical Sciences (T32GM007739)

  • Margaret Herre

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

Reviewing Editor

  1. Kristin Scott, University of California, Berkeley, United States

Ethics

Animal experimentation: Blood-feeding procedures with live mice were approved and monitored by The Rockefeller University Institutional Animal Care and Use Committee (IACUC protocol 17018) .

Human subjects: Blood-feeding procedures and behavioral experiments with human volunteers were approved and monitored by The Rockefeller University Institutional Review Board (IRB protocol LV-0652). Human subjects gave their written informed consent to participate.

Version history

  1. Received: October 13, 2020
  2. Accepted: November 28, 2020
  3. Accepted Manuscript published: December 7, 2020 (version 1)
  4. Version of Record published: January 13, 2021 (version 2)
  5. Version of Record updated: January 18, 2021 (version 3)

Copyright

© 2020, Basrur 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. Nipun S Basrur
  2. Maria Elena De Obaldia
  3. Takeshi Morita
  4. Margaret Herre
  5. Ricarda K von Heynitz
  6. Yael N Tsitohay
  7. Leslie B Vosshall
(2020)
fruitless mutant male mosquitoes gain attraction to human odor
eLife 9:e63982.
https://doi.org/10.7554/eLife.63982

Share this article

https://doi.org/10.7554/eLife.63982

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