Terrestrial animals that venture into the water on a regular basis face a number of challenges not encountered by their strictly terrestrial counterparts. While submerged, they must deal with hydrodynamic drag forces hindering locomotion and with the risk of running out of air. Back on land, the film of water adhering to their body surface may interfere with locomotion and thermoregulation or may increase the risk of bio-fouling. Many semi-aquatic invertebrates (and plants) have developed complex surface microstructures with water-repellent properties to overcome these problems, but equivalent adaptations of the skin have not been reported for vertebrates that encounter similar environmental challenges.
The transition to a semi-aquatic lifestyle has independently occurred multiple times throughout the evolutionary history of Anolis (see Fig. 1A below). In anoles, the skin surface is covered with microscopic hair-like ornaments, and contingent upon its complexity, organization, and length dimensions, these hair-like microstructures may have the potential to generate extreme surface hydrophobicity. Indeed, similar skin surface microstructures have been found in geckos and are shown to be responsible for the highly hydrophobic surface of their skin. The water-resistant properties of anole skin, however, have remained unexamined, but very recent discoveries have provided valuable insight into this matter. Boccia et al. (2021) observed that semi-aquatic Anolis lizards are able to sustain long periods submerged underwater by iteratively expiring and re-inspiring narial air bubbles. As in semi-aquatic insects, a hydrophobic skin is a key requirement for the underwater formation of an air bubble, hence, functional respiration, so a hydrophobic skin in semi-aquatic anoles is implied. However, whether a hydrophobic structured skin surface in anoles has evolved in response to life at the water-land interface is still an open question. Answering this question was the primary goal of our study.
We studied the skin surface morphology of preserved anole specimens using scanning electron microscopy and tested the wettability of the skin surface using contact-angle goniometry (Fig. 1D). We found that the skin surface of semi-aquatic species of Anolis lizards is characterized by a more elaborate microstructural architecture (i.e. longer hair-like structures; Fig 1B,C) and a lower wettability (Fig. 1D,E) relative to closely related terrestrial species. In addition, phylogenetic comparative models revealed repeated independent evolution of enhanced skin hydrophobicity associated with the transition to a semi-aquatic lifestyle, providing evidence of adaptation.
We believe our findings bring an additional dimension to the recent biological phenomenon described by Boccia et al. (2021) namely that diving Anolis lizards not only repeatedly and independently evolved a specialized rebreathing behavior with the transitioning to a semi-aquatic lifestyle, but that its evolution presumably also coincided with, or was preceded by, the evolution of a hydrophobic structured skin to successfully do so.
Our study was published in Journal of Experimental Biology. And thanks to Day’s Edge Productions, we also got the issue cover!
Reference
S. Baeckens, M. Temmerman, S. Gorb, C. Neto, M. Whiting & R. Van Damme (2021) Convergent evolution of skin surface microarchitecture and increased skin hydrophobicity in semi-aquatic anole lizards. Journal of Experimental Biology 224(19): jeb242939 (doi: 10.1242/jeb.242939)
Kevin de Queiroz
Cool! I had once planned to do this very same study but never got around to it.