Department of Physics, Emory University, Atlanta, GA 30322;
School of Physics, Georgia Institute of Technology, Atlanta, GA 30332.
Proc Natl Acad Sci U S A. 2021 Feb 9;118(6). doi: 10.1073/pnas.2018264118.
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.
装饰生物表面的微小结构可以显著影响行为，但对于生存至关重要的动物-环境相互作用的多样性使得将结构的功能归因于结构具有挑战性。微观皮肤纹理可能对蛇和其他无肢运动者特别重要，因为基质相互作用仅通过身体接触来介导。虽然以前的研究已经描述了一些蛇类物种的腹侧表面特征，但这些纹理的功能后果还不完全清楚。在这里，我们进行了一项比较研究，将原子力显微镜测量与数学建模相结合，以生成将微观纹理与运动性能联系起来的预测。我们发现，栖息在沙质沙漠中的少数侧身蜿蜒蛇类的腹侧皮肤结构存在进化上的趋同，这种各向同性的纹理与在广泛的侧行蛇和来自不同栖息地和广泛地理范围的其他蛇的系统发育广泛采样中观察到的从头至尾定向、微米级的刺明显不同。一个将结构方向性与摩擦各向异性相关联的数学模型表明，各向同性增强了侧身蜿蜒时的运动，而各向异性通过身体的侧向波动改善了蜿蜒时的运动。我们的研究结果强调了综合方法如何为结构-功能关系提供定量预测，并深入了解生物系统中的行为和进化适应。
