Phylogenetic mapping of scale nanostructure diversity in snakes

Abstract

Background Many species of snakes exhibit epidermal surface nanostructures that form complex motifs conferring self-cleaning properties, and sometimes structural iridescence, to their skin. Results Using confocal microscopy, we show that these specialised cells can be greatly elongated along their left-right axis and that different types of nanostructures are generated by cell borders and cell surface. To characterise the complexity and diversity of these surface gratings, we analysed scanning electron microscopy images of skin sheds from 353 species spanning 19 of the 26 families of snakes and characterised the observed nanostructures with four characters. The full character matrix, as well as one representative SEM image of each of the corresponding species, is available as a MySQL relational database at https://snake-nanogratings.lanevol.org . We then performed continuous-time Markov phylogenetic mapping on the snake phylogeny, providing an evolutionary dynamical estimate for the different types of nanostructures. These analyses suggest that the presence of cell border digitations is the ancestral state for snake skin nanostructures which was subsequently and independently lost in multiple lineages. Our analyses also indicate that cell shape and cell border shape are co-dependent characters whereas we did not find correlation between a simple life habit classification and any specific nanomorphological character. Conclusions These results, compatible with the fact that multiple types of nanostructures can generate hydrophobicity, suggest that the diversity and complexity of snake skin surface nano-morphology are dominated by phylogenetic rather than habitat-specific functional constraints. The present descriptive study opens the perspective of investigating the cellular self-organisational cytoskeletal processes controlling the patterning of different skin surface nanostructures in snakes and lizards. Electronic supplementary material The online version of this article (10.1186/s12862-019-1411-6) contains supplementary material, which is available to authorized users.

Functional consequences of convergently evolved microscopic skin features on snake locomotion

“…occipitalis (Fig. 2C) revealed a structurally anisotropic texture in which the epidermal skin cells have caudally directed, elevated, regular, micrometersized spikes we refer to as microspicules; previous literature has inconsistently used other terms for these structures (e.g., microfibrils, denticles, or digits) that we feel offer poor or misleading anatomical characterizations (19)(20)(21). The anatomy seen in Ch.…”

Role of Scale Wettability on Rain-Harvesting Behavior in a Desert-Dwelling Rattlesnake

“…On nano- to microscale, the surface topology of the dorsal scales of the snakes can range from nearly smooth to highly complex. 16 Specifically, the scanning electron microscope (SEM) images of the scales of L. splendida (Figure 4a,b) reveal a nearly smooth surface without any discernible nanopattern. The scales of P. catenifer have a more distinct nanoscale pattern of parallel, shallow, and 5–10 μm long nanochannels, whose consecutive layers appear to stack on each other (Figure 4c,d).…”

“…15 Rattlesnakes, like many other snakes, are known to have an elaborate nanotexture on their dorsal scales. 16 However, the potential role these textures have on the interaction with water during the phenomenon of rain harvesting has not been explored. Accordingly, we systematically characterized surface nano-to-macroscale texture and its effect on surface wettability and water droplet impact dynamics on the dorsal skin (scales) of adult Western Diamond-backed Rattlesnakes ( C. atrox ), a New World viperid (Viperidae: Crotalinae).…”

Quantifying surface topography of biological systems from 3D scans

“…Recently, the micro‐ and nano‐structures that cover the skin surface of snakes have also been examined in an evolutionary framework (e.g. Arrigo et al., 2019). In contrast, the 3D surface characteristics of reptilian skin and its potential diversity among species occupying different environments has received limited attention.…”