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.

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.

Metrics

  • 2,923
    views
  • 329
    downloads
  • 41
    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. 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

Share this article

https://doi.org/10.7554/eLife.38675

Further reading

    1. Cell Biology
    2. Evolutionary Biology
    Paul Richard J Yulo, Nicolas Desprat ... Heather L Hendrickson
    Research Article

    Maintenance of rod-shape in bacterial cells depends on the actin-like protein MreB. Deletion of mreB from Pseudomonas fluorescens SBW25 results in viable spherical cells of variable volume and reduced fitness. Using a combination of time-resolved microscopy and biochemical assay of peptidoglycan synthesis, we show that reduced fitness is a consequence of perturbed cell size homeostasis that arises primarily from differential growth of daughter cells. A 1000-generation selection experiment resulted in rapid restoration of fitness with derived cells retaining spherical shape. Mutations in the peptidoglycan synthesis protein Pbp1A were identified as the main route for evolutionary rescue with genetic reconstructions demonstrating causality. Compensatory pbp1A mutations that targeted transpeptidase activity enhanced homogeneity of cell wall synthesis on lateral surfaces and restored cell size homeostasis. Mechanistic explanations require enhanced understanding of why deletion of mreB causes heterogeneity in cell wall synthesis. We conclude by presenting two testable hypotheses, one of which posits that heterogeneity stems from non-functional cell wall synthesis machinery, while the second posits that the machinery is functional, albeit stalled. Overall, our data provide support for the second hypothesis and draw attention to the importance of balance between transpeptidase and glycosyltransferase functions of peptidoglycan building enzymes for cell shape determination.

    1. Chromosomes and Gene Expression
    2. Evolutionary Biology
    Gülnihal Kavaklioglu, Alexandra Podhornik ... Christian Seiser
    Research Article

    Repression of retrotransposition is crucial for the successful fitness of a mammalian organism. The domesticated transposon protein L1TD1, derived from LINE-1 (L1) ORF1p, is an RNA-binding protein that is expressed only in some cancers and early embryogenesis. In human embryonic stem cells, it is found to be essential for maintaining pluripotency. In cancer, L1TD1 expression is highly correlative with malignancy progression and as such considered a potential prognostic factor for tumors. However, its molecular role in cancer remains largely unknown. Our findings reveal that DNA hypomethylation induces the expression of L1TD1 in HAP1 human tumor cells. L1TD1 depletion significantly modulates both the proteome and transcriptome and thereby reduces cell viability. Notably, L1TD1 associates with L1 transcripts and interacts with L1 ORF1p protein, thereby facilitating L1 retrotransposition. Our data suggest that L1TD1 collaborates with its ancestral L1 ORF1p as an RNA chaperone, ensuring the efficient retrotransposition of L1 retrotransposons, rather than directly impacting the abundance of L1TD1 targets. In this way, L1TD1 might have an important role not only during early development but also in tumorigenesis.