Abstract

BackgroundMany species of snakes exhibit epidermal surface nanostructures that form complex motifs conferring self-cleaning properties, and sometimes structural iridescence, to their skin.ResultsUsing 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.ConclusionsThese 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.

Highlights

  • Many species of snakes exhibit epidermal surface nanostructures that form complex motifs conferring self-cleaning properties, and sometimes structural iridescence, to their skin

  • 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

  • Confocal microscopy of oberhautchen cells To image the oberhautchen cells, located below the two to three thin layers of peridermal cells that cover snake embryos, we used confocal microscopy on biopsies of African House Snake (Boaedon fuliginosus) embryonic skin dyed with the Syto9 Green Fluorescent Nucleic Acid Stain [16] (Fig. 2a)

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Summary

Introduction

Many species of snakes exhibit epidermal surface nanostructures that form complex motifs conferring self-cleaning properties, and sometimes structural iridescence, to their skin. Many species of Squamates (lizards and snakes) exhibit submicron-sized surface gratings (periodic surface deformations) of their skin, i.e., at the apical surface of the oberhautchen cells (the outermost layer of cells in the stratum corneum [1]). These sub-cellular structures, termed ‘scale microstructures’, ‘micro-dermatoglyphics’, ‘nanostructures’, or ‘nanogratings’, exhibit a variety of forms that can be Arrigo et al BMC Evolutionary Biology (2019) 19:91 a b c d e larger spinules and irregular pits that cause the accumulation of dirt in the form of a protective caudal plug [12]. This study established characters such as cell shape, cell boundary, and cell surface morphology and enumerated hypotheses for potential links between specific structural features and ecological characters (e.g., the potential presence of longer digitations in arboreal species) but the authors did not find any conclusive correlation between scale nanomorphology and ecological characters

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