Physical Confinement Regulates Transitions in Nematode Motility

How do worms navigate their complex natural surroundings? Laboratory studies using nematodes such as interrogate motility patterns as an indicator of their behavioral responses using liquid cultures or two-dimensional (2D) agar pads. However, typically inhabit three-dimensional granular niches—such as soft soil and decomposed biological matter—with spatiotemporally varying viscoelastoplastic material properties that impose physical constraints on their motion. Here, by directly visualizing worm motility in transparent 3D granular matrices with tunable mechanical properties, we find that the propulsive speed of nematodes shows a nonmonotonic dependence on the yield stress of their microenvironment. Biophysical measurements reveal that this nonmonotonicity emerges as nematodes optimize for efficient navigation under higher confinement by matching their forward propulsive speed to the wave speed along their body. This regulation of locomotory behavior is purely dictated by the physical interaction of the nematode with its environment without involving soft-touch sensory neurons. Remarkably, our predictions from a slender body theory of undulatory motion in yield stress environments exactly capture the scaling behavior for both efficiency and mode of motion as obtained from the experimental data. Further, in a nondimensionalized phase space defined by propulsive efficiency and timescale of motility, we show that increasing confinement leads to a sharp gait transition from poorly efficient thrashing to highly efficient crawling. Our work thus establishes a biophysical paradigm wherein the physical interaction of worms with their mechanical microenvironment leads to a transition between distinct modes of undulatory motion, entirely as a consequence of 3D physical confinement.