1. Genetics and Genomics
  2. Neuroscience
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fruitless mutant male mosquitoes gain attraction to human odor

Research Article
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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.

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.

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.

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  1. Further reading

Further reading

    1. Genetics and Genomics
    2. Medicine
    Emanuela Abiusi et al.
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    Background:

    Spinal muscular atrophy (SMA) is a neuromuscular disorder characterized by the degeneration of the second motor-neuron. The phenotype ranges from very severe to very mild forms. All patients have the homozygous loss of the SMN1 gene and a variable number of SMN2 (generally two-to-four copies), inversely related with the severity. The amazing results of the available treatments have made compelling the need of prognostic biomarkers to predict the progression trajectories of patients. Beside the SMN2 products, few other biomarkers have been evaluated so far, including some miRs.

    Methods:

    We performed whole miRNome analysis of muscle samples of patients and controls (14 biopsies and 9 cultures). The levels of muscle differentially expressed miRs were evaluated in serum samples (51 patients and 37 controls) and integrated with SMN2 copies, SMN2-full length transcript levels in blood and age (SMA-score).

    Results:

    Over 100 miRs were differentially expressed in SMA muscle; three of them (HSA-miR-181a-5p, -324-5p, -451a; SMA-miRs) were significantly up-regulated in serum of patients. The severity predicted by the SMA-score was related with that of the clinical classification at a correlation coefficient of 0.87 (p<10-5).

    Conclusions:

    miRNome analyses suggest the primary involvement of skeletal muscle in SMA pathogenesis; the SMA-miRs are likely actively released in the blood flow, even if their function and target cells require to be elucidated. The accuracy of the SMA-score needs to be verified in replicative studies: if confirmed, its use could be crucial for the routine prognostic assessment, also in pre-symptomatic patients.

    Funding:

    Telethon Italia (grant # GGP12116).

    1. Evolutionary Biology
    2. Genetics and Genomics
    Franziska Gruhl et al.
    Research Article

    Circular RNAs (circRNAs) are found across eukaryotes and can function in post-transcriptional gene regulation. Their biogenesis through a circle-forming backsplicing reaction is facilitated by reverse-complementary repetitive sequences promoting pre-mRNA folding. Orthologous genes from which circRNAs arise, overall contain more strongly conserved splice sites and exons than other genes, yet it remains unclear to what extent this conservation reflects purifying selection acting on the circRNAs themselves. Our analyses of circRNA repertoires from five species representing three mammalian lineages (marsupials, eutherians: rodents, primates) reveal that surprisingly few circRNAs arise from orthologous exonic loci across all species. Even the circRNAs from orthologous loci are associated with young, recently active and species-specific transposable elements, rather than with common, ancient transposon integration events. These observations suggest that many circRNAs emerged convergently during evolution - as a byproduct of splicing in orthologs prone to transposon insertion. Overall, our findings argue against widespread functional circRNA conservation.