Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Edited by Neil H. Shubin, University of Chicago, Chicago, IL, and approved December 17, 2020 (received for review August 28, 2020)
Significance
Animal skins are complex, highly specialized surfaces that are decorated with a variety of small structural features, whose functional benefits are often unknown. We investigate the microscopic features present on snake skins—which serve as the only interface between these animals and their environments—and we discover that distantly related sidewinding vipers have a unique structure that is distinct from other snakes. We develop a mathematical model that links structure to function and provides insight into evolutionary and behavioral adaptation in limbless 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.
Footnotes
↵1J.M.R. and T.-D.L. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: jennifer.rieser{at}emory.edu.
Author contributions: D.I.G. and J.R.M. designed research; J.M.R. and T.-D.L. performed research; J.M.R., T.-D.L., J.L.T., and J.R.M. analyzed data; and J.M.R., T.-D.L., J.L.T., D.I.G., and J.R.M. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2018264118/-/DCSupplemental.
Data Availability.
Matlab files data have been deposited in the Open Science Framework (https://doi.org/10.17605/OSF.IO/KJ9TV; ref. 50).
Published under the PNAS license.
References
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Functional consequences of convergently evolved microscopic skin features on snake locomotion
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- Biological Sciences
- Evolution
- Physical Sciences
- Biophysics and Computational Biology
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