Functional consequences of convergently evolved microscopic skin features on snake locomotion

Abstract

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.

Locomotor energetics in the Indonesian blue‐tongued skink (Tiliqua gigas) with implications for the cost of belly‐dragging in early tetrapods

“…Similarly, in an ichnological study comparing the tracks of Tiliqua to putative belly‐dragging trackways, Curth et al (2014) suggest that friction, or even adhesion, between the belly and the substrate may impose limitations upon movement speed during locomotion. This hypothesis is substantiated by experimental studies of snake and sandfish locomotion that highlight the substantial resistant forces of friction, which require powerful muscular forces to be overcome (Goldman & Hu, 2010; Hu et al, 2009; Rieser et al, 2021). Indeed, these frictional costs are sufficiently high as to cancel the energetic gains associated with their streamlined morphology and the lower inertial losses associated with limblessness (Hu & Shelley, 2012; Walton et al, 1990).…”

“…This hypothesis is substantiated by experimental studies of snake and sandfish locomotion that highlight the substantial resistant forces of friction, which require powerful muscular forces to be overcome (Goldman & Hu, 2010;Hu et al, 2009;Rieser et al, 2021). Indeed, these frictional costs are sufficiently high as to cancel the energetic gains associated with their streamlined morphology and the lower inertial losses associated with limblessness (Hu & Shelley, 2012;Walton et al, 1990).…”

Friction modulation in limbless, three-dimensional gaits and heterogeneous terrains

“…in terms of locomotory performance. This perspective recently received notable experimental support with evidence of evolutionary convergence in the ventral skin of sidewinding vipers across world deserts [30]. Their skin indeed evolved from well-documented anisotropic textures in non-sidewinders, to isotropic ones.…”

“…Despite these challenges, a recent convergence between zoologists, physicists, mathematicians, and roboticists has provided new impetus towards understanding the organization of out-of-plane behaviors [14,22,[27][28][29][30]. Among these, particular attention has been devoted to sidewinding (Fig.…”

Decoupling and Reprogramming the Wiggling Motion of Midge Larvae Using a Soft Robotic Platform

“…[ 4–10 ] However, given the complexity of biological behaviors, emulating and investigating these natural modes of locomotion with engineered systems has been challenging. [ 11–13 ] In this respect, burgeoning effort has been devoted to developing new simulation tools, physical models, and experimental platforms. Among these engineering tools, soft robotic systems are promising in light of their biologically relevant mechanical compliance, deformability, and modes of locomotion.…”