1. Genetics and Genomics
  2. Neuroscience
Download icon

fruitless mutant male mosquitoes gain attraction to human odor

Research Article
  • Cited 0
  • Views 1,524
  • Annotations
Cite this article as: eLife 2020;9:e63982 doi: 10.7554/eLife.63982

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.

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.

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.

Reviewing Editor

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

Publication 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.

Metrics

  • 1,524
    Page views
  • 278
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Genetics and Genomics
    2. Plant Biology
    Thierry Halter et al.
    Research Article

    Active DNA demethylation has emerged as an important regulatory process of plant and mammalian immunity. However, very little is known about the mechanisms by which active demethylation controls transcriptional immune reprogramming and disease resistance. Here, we first show that the Arabidopsis active demethylase ROS1 promotes basal resistance towards Pseudomonas syringae by antagonizing RNA-directed DNA methylation (RdDM). Furthermore, we find that ROS1 facilitates the flagellin-triggered induction of the disease resistance gene RMG1 by limiting RdDM at the 3' boundary of a remnant RC/Helitron transposable element (TE) embedded in its promoter. We further identify flagellin-responsive ROS1 putative primary targets, and show that at a subset of promoters, ROS1 erases methylation at discrete regions exhibiting WRKY transcription factors (TFs) binding. In particular, we demonstrate that ROS1 removes methylation at the orphan immune receptor RLP43 promoter, to ensure DNA binding of WRKY TFs. Finally, we show that ROS1-directed demethylation of the RMG1 and RLP43 promoters is causal for both flagellin responsiveness of these genes and for basal resistance. Overall, these findings significantly advance our understanding of how active demethylases shape transcriptional immune reprogramming to enable antibacterial resistance.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Iman Hamid et al.
    Research Article Updated

    Humans have undergone large migrations over the past hundreds to thousands of years, exposing ourselves to new environments and selective pressures. Yet, evidence of ongoing or recent selection in humans is difficult to detect. Many of these migrations also resulted in gene flow between previously separated populations. These recently admixed populations provide unique opportunities to study rapid evolution in humans. Developing methods based on distributions of local ancestry, we demonstrate that this sort of genetic exchange has facilitated detectable adaptation to a malaria parasite in the admixed population of Cabo Verde within the last ~20 generations. We estimate that the selection coefficient is approximately 0.08, one of the highest inferred in humans. Notably, we show that this strong selection at a single locus has likely affected patterns of ancestry genome-wide, potentially biasing demographic inference. Our study provides evidence of adaptation in a human population on historical timescales.