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The small structures that decorate biological surfaces can significantly affect behavior, yet the diversity of animal–environment interactions essential for survival makes ascribing functions to structures challenging. Microscopic skin textures may be particularly important for snakes and other limbless locomotors, where substrate interactions are mediated solely through body contact. While previous studies have characterized ventral surface features of some snake species, the functional consequences of these textures are not fully understood. Here, we perform a comparative study, combining atomic force microscopy measurements with mathematical modeling to generate predictions that link microscopic textures to locomotor performance. We discover an evolutionary convergence in the ventral skin structures of a few sidewinding specialist vipers that inhabit sandy deserts—an isotropic texture that is distinct from the head-to-tail-oriented, micrometer-sized spikes observed on a phylogenetically broad sampling of nonsidewinding vipers and other snakes from diverse habitats and wide geographic range. A mathematical model that relates structural directionality to frictional anisotropy reveals that isotropy enhances movement during sidewinding, whereas anisotropy improves movement during slithering via lateral undulation of the body. Our results highlight how an integrated approach can provide quantitative predictions for structure–function relationships and insights into behavioral and evolutionary adaptations in biological systems. 

While terrestrial locomotors often contend with permanently deformable substrates like sand, soil, and mud, principles of motion on such materials are lacking. We study the desert-specialist shovel-nosed snake traversing a model sand and find body inertia is negligible despite rapid transit and speed dependent granular reaction forces. New surface resistive force theory (RFT) calculation reveals how wave shape in these snakes minimizes material memory effects and optimizes escape performance given physiological power limitations. RFT explains the morphology and waveform-dependent performance of a diversity of non-sand-specialist snakes but overestimates the capability of those snakes which suffer high lateral slipping of the body. Robophysical experiments recapitulate aspects of these failure-prone snakes and elucidate how re-encountering previously deformed material hinders performance. This study reveals how memory effects stymied the locomotion of a diversity of snakes in our previous studies (Marvi et al., 2014) and indicates avenues to improve all-terrain robots. 

Limbless animals like snakes inhabit most terrestrial environments, generating thrust to overcome drag on the elongate body via contacts with heterogeneities. The complex body postures of some snakes and the unknown physics of most terrestrial materials frustrates understanding of strategies for effective locomotion. As a result, little is known about how limbless animals contend with unplanned obstacle contacts. We studied a desert snake,Chionactis occipitalis, which uses a stereotyped head-to-tail traveling wave to move quickly on homogeneous sand. In laboratory experiments, we challenged snakes to move across a uniform substrate and through a regular array of force-sensitive posts. The snakes were reoriented by the array in a manner reminiscent of the matter-wave diffraction of subatomic particles. Force patterns indicated the animals did not change their self-deformation pattern to avoid or grab the posts. A model using open-loop control incorporating previously described snake muscle activation patterns and body-buckling dynamics reproduced the observed patterns, suggesting a similar control strategy may be used by the animals. Our results reveal how passive dynamics can benefit limbless locomotors by allowing robust transit in heterogeneous environments with minimal sensing.