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.

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.

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

  • 6,535
    views
  • 716
    downloads
  • 43
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  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

Further reading

    1. Cell Biology
    2. Genetics and Genomics
    Showkat Ahmad Dar, Sulochan Malla ... Manolis Maragkakis
    Research Article

    Cells react to stress by triggering response pathways, leading to extensive alterations in the transcriptome to restore cellular homeostasis. The role of RNA metabolism in shaping the cellular response to stress is vital, yet the global changes in RNA stability under these conditions remain unclear. In this work, we employ direct RNA sequencing with nanopores, enhanced by 5ʹ end adapter ligation, to comprehensively interrogate the human transcriptome at single-molecule and -nucleotide resolution. By developing a statistical framework to identify robust RNA length variations in nanopore data, we find that cellular stress induces prevalent 5ʹ end RNA decay that is coupled to translation and ribosome occupancy. Unlike typical RNA decay models in normal conditions, we show that stress-induced RNA decay is dependent on XRN1 but does not depend on deadenylation or decapping. We observed that RNAs undergoing decay are predominantly enriched in the stress granule transcriptome while inhibition of stress granule formation via genetic ablation of G3BP1 and G3BP2 rescues RNA length. Our findings reveal RNA decay as a key component of RNA metabolism upon cellular stress that is dependent on stress granule formation.

    1. Chromosomes and Gene Expression
    2. Genetics and Genomics
    Arkadiy K Golov, Alexey A Gavrilov ... Sergey V Razin
    Research Article

    The enhancer-promoter looping model, in which enhancers activate their target genes via physical contact, has long dominated the field of gene regulation. However, the ubiquity of this model has been questioned due to evidence of alternative mechanisms and the lack of its systematic validation, primarily owing to the absence of suitable experimental techniques. In this study, we present a new MNase-based proximity ligation method called MChIP-C, allowing for the measurement of protein-mediated chromatin interactions at single-nucleosome resolution on a genome-wide scale. By applying MChIP-C to study H3K4me3 promoter-centered interactions in K562 cells, we found that it had greatly improved resolution and sensitivity compared to restriction endonuclease-based C-methods. This allowed us to identify EP300 histone acetyltransferase and the SWI/SNF remodeling complex as potential candidates for establishing and/or maintaining enhancer-promoter interactions. Finally, leveraging data from published CRISPRi screens, we found that most functionally verified enhancers do physically interact with their cognate promoters, supporting the enhancer-promoter looping model.