Forward locomotion of the nematode C. elegans is achieved through modulation of a single gait

Abstract

The ability of an animal to locomote through its environment depends crucially on the interplay between its active endogenous control and the physics of its interactions with the environment. The nematode worm Caenorhabditis elegans serves as an ideal model system for studying the respective roles of neural control and biomechanics, as well as the interaction between them. With only 302 neurons in a hard-wired neural circuit, the worm's apparent anatomical simplicity belies its behavioural complexity. Indeed, C. elegans exhibits a rich repertoire of complex behaviors, the majority of which are mediated by its adaptive undulatory locomotion. The conventional wisdom is that two kinematically distinct C. elegans locomotion behaviors-swimming in liquids and crawling on dense gel-like media-correspond to distinct locomotory gaits. Here we analyze the worm's motion through a series of different media and reveal a smooth transition from swimming to crawling, marked by a linear relationship between key locomotion metrics. These results point to a single locomotory gait, governed by the same underlying control mechanism. We further show that environmental forces play only a small role in determining the shape of the worm, placing conditions on the minimal pattern of internal forces driving locomotion.

Figure 1. (a)–(c) Proportionality of key locomotion parameters in a variety of environments (a range of gelatin concentrations, deformable agar surface, non-deformable membrane surface, with n ⩾3 replicates per environment).

Lines show the best linear fits to the data. (d)–(f) frequency, wavelength, and amplitude of the locomotion wave all decay smoothly with K in the different media (gelatin and agar, with n⩾3 replicates per environment). Lines show the best power-law fits to the data. Note the doubly logarithmic scales. In all graphs, filled circles show gelatin data. Different colors represent different gelatin concentrations. Agar and membrane data are represented by black triangles and white squares respectively.

Figure 2. Sequences of four midlines extracted from movies of worms moving in/on different media.

(a)–(c) Worm midlines have been displaced vertically, rotated, and aligned for clarity, with the head to the left and time increasing from top to bottom in quarter-period steps. The scale bar corresponds to approximately 0.1 mm. Estimated K values are (a) 35, (b) 35, and (c) 1.9. (d) Same midlines as above (a)–(c), still rotated, with the head to the left, but without removing the center of mass motion.

Figure 3. Estimated power dissipation due to resistive drag (see Methods).

Agar data are represented by black triangles, while filled circles show gelatin data. Different colors represent different gelatin concentrations.