Changes to social feeding behaviors are not sufficient for the fitness gains of the C. elegans N2 reference strain

  1. Yuehui Zhao
  2. Lijiang Long
  3. Wen Xu
  4. Richard F Campbell
  5. Edward E Large
  6. Joshua S Greene
  7. Patrick T McGrath  Is a corresponding author
  1. Georgia Institute of Technology, United States
  2. The Rockefeller University, United States

Abstract

The standard reference Caenorhabditis elegans strain, N2, has evolved marked behavioral changes in social feeding behavior since its isolation from the wild. We show that the causal, laboratory-derived mutations in two genes, npr-1 and glb-5, confer large fitness advantages in standard laboratory conditions. Using environmental manipulations that suppress social/solitary behavior differences, we show the fitness advantages of the derived alleles remained unchanged, suggesting selection on these alleles acted through pleiotropic traits. Transcriptomics, developmental timing, and food consumption assays showed that N2 animals mature faster, produce more sperm, and consume more food than a strain containing ancestral alleles of these genes regardless of behavioral strategies. Our data suggest that the pleiotropic effects of glb-5 and npr-1 are a consequence of changes to O2 -sensing neurons that regulate both aerotaxis and energy homeostasis. Our results demonstrate how pleiotropy can lead to profound behavioral changes in a popular laboratory model.

Data availability

Sequencing data have been deposited in SRA under PRJNA437304.Source data file have been provided for all figures.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Yuehui Zhao

    Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9496-0023
  2. Lijiang Long

    Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Wen Xu

    Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2085-7223
  4. Richard F Campbell

    Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Edward E Large

    Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Joshua S Greene

    Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Patrick T McGrath

    Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    For correspondence
    patrick.mcgrath@biology.gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1598-3746

Funding

National Institute of General Medical Sciences (R01GM114170)

  • Yuehui Zhao
  • Lijiang Long
  • Wen Xu
  • Richard F Campbell
  • Edward E Large
  • Patrick T McGrath

National Institute on Aging (R21AG050304)

  • Patrick T McGrath

Ellison Medical Foundation (New Scholars in Aging)

  • Lijiang Long
  • Wen Xu
  • Patrick T McGrath

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

Reviewing Editor

  1. Yuichi Iino, University of Tokyo, Japan

Publication history

  1. Received: May 25, 2018
  2. Accepted: October 15, 2018
  3. Accepted Manuscript published: October 17, 2018 (version 1)
  4. Version of Record published: November 8, 2018 (version 2)

Copyright

© 2018, Zhao 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. Yuehui Zhao
  2. Lijiang Long
  3. Wen Xu
  4. Richard F Campbell
  5. Edward E Large
  6. Joshua S Greene
  7. Patrick T McGrath
(2018)
Changes to social feeding behaviors are not sufficient for the fitness gains of the C. elegans N2 reference strain
eLife 7:e38675.
https://doi.org/10.7554/eLife.38675

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