Shared behavioral mechanisms underlie C. elegans aggregation and swarming

Abstract

In complex biological systems, simple individual-level behavioral rules can give rise to emergent group-level behavior. While collective behavior has been well studied in cells and larger organisms, the mesoscopic scale is less understood, as it is unclear which sensory inputs and physical processes matter a priori. Here, we investigate collective feeding in the roundworm C. elegans at this intermediate scale, using quantitative phenotyping and agent-based modeling to identify behavioral rules underlying both aggregation and swarming-a dynamic phenotype only observed at longer timescales. Using fluorescence multi-worm tracking, we quantify aggregation in terms of individual dynamics and population-level statistics. Then we use agent-based simulations and approximate Bayesian inference to identify three key behavioral rules for aggregation: cluster-edge reversals, a density-dependent switch between crawling speeds, and taxis towards neighboring worms. Our simulations suggest that swarming is simply driven by local food depletion but otherwise employs the same behavioral mechanisms as the initial aggregation.

Data availability

All data generated and analysed during this study is deposited on the Open Worm Movement Database community page (https://zenodo.org/communities/open-worm-movement-database/). As the full dataset is over 1TB, it is not possible to provide a single DOI for the full dataset. Instead, each recording has a separate DOI, which can be found in Supplementary Table 2. The code for model simulations is available at github.com/ljschumacher/sworm-model.

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

Article and author information

Author details

  1. Siyu Serena Ding

    Institute of Clinical Sciences, Imperial 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:" 0000-0002-8590-3908
  2. Linus J Schumacher

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Avelino E Javer

    Institute of Clinical Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Robert G Endres

    Department of Life Sciences, Imperial College London, London, United Kingdom
    For correspondence
    r.endres@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1379-659X
  5. André EX Brown

    Instititue of Clinical Sciences, Imperial College London, London, United Kingdom
    For correspondence
    andre.brown@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1324-8764

Funding

Biotechnology and Biological Sciences Research Council (BB/N00065X/1)

  • Robert G Endres
  • André EX Brown

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

Reviewing Editor

  1. Tâm Mignot, CNRS-Aix Marseille University, France

Version history

  1. Received: November 1, 2018
  2. Accepted: April 19, 2019
  3. Accepted Manuscript published: April 25, 2019 (version 1)
  4. Version of Record published: May 16, 2019 (version 2)

Copyright

© 2019, Ding 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. Siyu Serena Ding
  2. Linus J Schumacher
  3. Avelino E Javer
  4. Robert G Endres
  5. André EX Brown
(2019)
Shared behavioral mechanisms underlie C. elegans aggregation and swarming
eLife 8:e43318.
https://doi.org/10.7554/eLife.43318

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https://doi.org/10.7554/eLife.43318

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