Physical confinement regulates transition in nematode motility

How do worms navigate their complex natural surroundings? Undulatory microswimmers such as nematodes typically inhabit environments such as soil, vegetable matter, and host tissues. While the natural habitats of nematodes are often three-dimensional granular niches with spatiotemporally varying visco-elasto-plastic material properties that impose physical constraints on their motion, current knowledge about nematode motility patterns broadly comes from investigating model organisms such as Caenorhabditis elegans either inside liquid cultures or the surface of soft agar pads. How nematodes move through 3D granular niches across different degrees of physical confinement remains poorly understood due to a lack of optically transparent 3D granular matrices. We bridge this gap by engineering an optically transparent granular matrix to directly visualise and quantitatively analyse nematode motion. Importantly, nematodes can freely move through this matrix by generating a minimal yield stress; once the nematode moves away, the matrix self-heals to ensure the material properties remain invariant. Using these platforms, we observe that the propulsive speed of nematodes shows a non-monotonic relation with the yield stress of their microenvironment. This non-monotonicity emerges as nematodes optimize for efficient navigation at higher yield stress, wherein, their forward propulsive speed matches the wave speed along their body. This regulation of locomotory behaviour is purely dictated by the physical interaction of the nematode with its environment without involving soft-touch sensory neurons. Remarkably, predictions from a slender body theory of undulatory motion exactly capture the scaling behaviour for both efficiency and mode of motion as obtained from the experimental data. Finally, in a phase space described by non-dimensional propulsive efficiency and a non-dimensional time scale of motility, we capture a gait transition from poorly efficient thrashing under low confinement to more efficient crawling under high confinement. Thus, our work establishes a new regulatory paradigm describing how distinct modes of undulatory motion emerge under different degrees of physical confinement.