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Edited by Martin Chalfie, Columbia University, New York, NY, and approved April 1, 2014 (received for review January 29, 2014)
Significance
How independent agents interact to form collective behavior is of interest in diverse disciplines. Larger animals coordinate their motions via their nervous systems. However, little is known regarding the mechanisms by which microscopic animals coordinate their gaits. We observed that, when in a swarm, clusters of Caenorhabditis elegans synchronize their swimming gait. To identify the mechanism responsible for this behavior, we devised controlled experiments to examine the interactions between pairs of animals. Our studies indicate that steric hindrance is the dominant factor responsible for gait synchronization in C. elegans, and that hydrodynamic interactions and mechanosensation do not play a significant role. We infer that a similar mechanism may apply to other microscopic swimming organisms and self-propelled particles.
Abstract
Collective motion is observed in swarms of swimmers of various sizes, ranging from self-propelled nanoparticles to fish. The mechanisms that govern interactions among individuals are debated, and vary from one species to another. Although the interactions among relatively large animals, such as fish, are controlled by their nervous systems, the interactions among microorganisms, which lack nervous systems, are controlled through physical and chemical pathways. Little is known, however, regarding the mechanism of collective movements in microscopic organisms with nervous systems. To attempt to remedy this, we studied collective swimming behavior in the nematode Caenorhabditis elegans, a microorganism with a compact nervous system. We evaluated the contributions of hydrodynamic forces, contact forces, and mechanosensory input to the interactions among individuals. We devised an experiment to examine pair interactions as a function of the distance between the animals and observed that gait synchronization occurred only when the animals were in close proximity, independent of genes required for mechanosensation. Our measurements and simulations indicate that steric hindrance is the dominant factor responsible for motion synchronization in C. elegans, and that hydrodynamic interactions and genotype do not play a significant role. We infer that a similar mechanism may apply to other microscopic swimming organisms and self-propelled particles.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: bau{at}seas.upenn.edu.
Author contributions: J.Y., D.M.R., and H.H.B. designed research; J.Y. performed research; J.Y., D.M.R., and H.H.B. analyzed data; and J.Y., D.M.R., and H.H.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1401828111/-/DCSupplemental.
Gait synchronization in Caenorhabditis elegans
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