Specific sensory neurons and insulin-like peptides modulate food type-dependent oogenesis and fertilization in Caenorhabditis elegans

Abstract

An animal's responses to environmental cues are critical for its reproductive program. Thus, a mechanism that allows the animal to sense and adjust to its environment should make for a more efficient reproductive physiology. Here we demonstrate that in Caenorhabditis elegans specific sensory neurons influence onset of oogenesis through insulin signaling in response to food-derived cues. The chemosensory neurons ASJ modulate oogenesis onset through the insulin-like peptide (ILP) INS‑6. In contrast, other sensory neurons, the olfactory neurons AWA, regulate food type-dependent differences in C. elegans fertilization rates, but not onset of oogenesis. AWA modulates fertilization rates at least partly in parallel to insulin receptor signaling, since the insulin receptor DAF‑2 regulates fertilization independently of food type, which requires ILPs other than INS-6. Together our findings suggest that optimal reproduction requires the integration of diverse food-derived inputs through multiple neuronal signals acting on the C. elegans germline.

Data availability

All data generated or analyzed during this study are included in the manuscript and supplemental files: Supplementary File 1 for the strain list used in the study and supplemental files to Figures 1 through 8.

Article and author information

Author details

  1. Shashwat Mishra

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Mohamed Dabaja

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Asra Akhlaq

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Bianca Pereira

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Kelsey Marbach

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mediha Rovcanin

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Rashmi Chandra

    Department of Biological Sciences, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Antonio Caballero

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Diana Fernandes de Abreu

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. QueeLim Ch'ng

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1941-3828
  11. Joy Alcedo

    Department of Biological Sciences, Wayne State University, Detroit, United States
    For correspondence
    joy.alcedo@wayne.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5279-6640

Funding

Wayne State University (Graduate Research Assistantship)

  • Shashwat Mishra

European Research Council (NeuroAge 242666)

  • QueeLim Ch'ng

Research Councils UK

  • QueeLim Ch'ng

National Institute of General Medical Sciences (R01 GM108962)

  • Joy Alcedo

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

Copyright

© 2023, Mishra 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. Shashwat Mishra
  2. Mohamed Dabaja
  3. Asra Akhlaq
  4. Bianca Pereira
  5. Kelsey Marbach
  6. Mediha Rovcanin
  7. Rashmi Chandra
  8. Antonio Caballero
  9. Diana Fernandes de Abreu
  10. QueeLim Ch'ng
  11. Joy Alcedo
(2023)
Specific sensory neurons and insulin-like peptides modulate food type-dependent oogenesis and fertilization in Caenorhabditis elegans
eLife 12:e83224.
https://doi.org/10.7554/eLife.83224

Share this article

https://doi.org/10.7554/eLife.83224

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