Sticky Toes: A tale of many convergences
All carnivorous species on earth strive to be better at two things: predator avoidance and prey capture. In reptiles and amphibians, these driving forces have led to the evolution of some truly magnificent life forms, such as flying frogs, lizards and snakes, and incredible tongue convergences in salamanders and chameleons. While these adaptations are wonderful subjects about which I could happily write until my fingers were bloody, I want to focus on another adaptation that has arisen countless times in different lineages: sticky toes.
Having adhesive toes in fact serves both of these functions: they allow you to better escape predators by seeking out locations that they cannot access, and they allow you to chase prey, particularly airborne prey, in a way that would not otherwise be possible, giving a competitive edge. Both of these functions have one important evolutionary outcome: a greater propensity to survive and therefore pass on genes.
It is perhaps unsurprising then that sticky toes have evolved numerous times, and in numerous ways. In this article, I want to talk about the two main adhesive structures that have arisen in herps: enlarged suction pads in amphibians, and adhesive lamellae in lizards. I would love to write about salamander adhesion as well, but for the sake of your attention span, I’ll control myself.
Frog toes: Simple suction or something more?
The simplest mechanical method for adhering to any surface is to create a vacuum between the surface and the digits. This is the dominant mode employed in treefrogs. Their natural moistness allows a fluid-filled joint to form between the surface and the toe. But it is not as simple as you might think.
In 2006, for the first time it was shown that simple capillary and viscous forces that create the toe suction used by Litoria caerulea, a tree frog from Australia, are not the only forces at play in the adhesion of its toes (Federle et al. 2006).
Federle et al. (2006) showed that the cell surface of the many hexagonal cells that compose the adhesive pad, between which mucus is secreted, is covered in peg-like projections. These, they posited, form more than just a surface-tension-based connection with a substrate, but also add boundary friction and close contact forces, giving enhanced adhesion.
But this is just one example. Numerous other Scanning Electron Microscope studies have been carried out in a wide variety of frogs, and have shown that a number of different cellular structures have emerged that address this problem (Ba-Omar et al. 2000). For anyone familiar with the evolution of frogs, this will come as no surprise. For those who are not, I invite you to read this normally pay-walled article by Pyron and Wiens (2011) that is offered for free from Pyron’s website. But let me summarise the important point I want you to take away from this paper, to save you having to read that 43-page article before proceeding: the possession of enlarged adhesive toe pads has evolved dozens of times independently. Indeed, if you look at just a small group of frogs, such as the microhylid subfamily Cophylinae of Madagascar, you find that there have been numerous swaps between terrestriality (associated with unenlarged toe pads) and arboreality (associated with enlarged toe pads) (Wollenberg et al. 2008). It is hard to imagine that toe pads that have emerged independently in so many lineages would all have exactly the same structure, and so the diversity is as expected.
Thus, while we may think frog adhesion to be a fairly simplistic mode mechanically, it has been achieved in a diverse variety of ways, and really represents an astounding case of repeated convergent evolution.
Lizard Toes: Super sticky surface structures!
Perhaps the most famous adhesive structures in all of the animal kingdom are gecko toes. Anyone who has been near the equator and southern hemisphere on a warm night has doubtless seen many Hemidactylus geckos crowded around lights, hunting on vertical and often inverted surfaces with apparent ease. This incredible ability has received a great deal of research attention, and in the last few years, bioengineers have begun on tapes and other structures that are able to emulate it. It is, in my opinion, one of the greatest evolutionary feats of all (pun intended).
For the sake of brevity, I will not go into great detail about how gecko toes work, but instead just summarise them briefly, and then talk about their evolution - it is more complicated and amazing than you would expect.
On the underside of the toe of a lizard with sticky toes are a series of small horizontal lines, together called a scansor. Each line is called a lamella, and is composed of thousands of setae, each of which ends in a few little spatulas, each of which ends in a broadened terminal pad a mere fraction of a micrometer across.
[x] These spatulae are so small that they create molecular adhesive forces between the toes of the animals and their substrate called Van der Waals forces (Autumn et al. 2002; Tian et al. 2006).
With such incredible specialisation, you might expect that these structures have arisen only once, and were perhaps lost several times, such as in the pygopodid geckos about which I am constantly talking. But this is not at all what is seen!
Gamble et al. (2012) looked at the phylogenetic relationships of geckos based on genetic data in the context of their adhesive toe structures. Their reconstruction of gecko evolution suggests no fewer than eleven independent gains of adhesive toe structures, and nine independent losses. That these incredibly complex features have come about independently so many times is astounding.
But wait, it gets better:
Americans, especially those living in the south eastern United States, will be familiar with anoles. These lizards are often mistaken for geckos (as anyone who watches the #geckos tag will know), because they share with them that special ability to run up and down vertical surfaces. But they are in fact much closer related to iguanas than to geckos. They have independently evolved scansorial adhesive systems, which have allowed them to diversify immensely in Central America and on the nearby islands. While their adhesive structures are not as complex as many gecko structures (they are not multi-branched), they are nonetheless extremely similar, and function in the very same way: through Van der Waals forces.
And if you thought that was as good as it gets, you are in for a treat!
[x] The green-blooded tree skink, Prasinohaema virens, has also independently evolved adhesive toe structures analogous to those of geckos and anoles (Williams & Peterson 1982). It is likely that the other members of the genus Prasinohaema have the same feature, but it is not known from any other skink genera. This, then, represents a third major group of lizards (Gekkota, Iguania, and Scincomorpha) to have members possessing highly specialised toe structures which facilitate their arboreal lifestyles.
Thus, it appears that subdigital lamellae have evolved independently at least thirteen times: eleven in geckos, once in anoles, and once in skinks. It is not, therefore, a natural propensity just of geckos to evolve these specialised structures, but rather of arboreal lizards to find this same pattern upon which to converge. This is evidenced by the number of independent losses of these structures in species that have adopted terrestrial lifestyles (e.g. Namib-Kalahari burrowing geckos, see Lamb & Bauer 2006 and Gamble et al. 2012).
This extent of convergence - with a minimum of thirteen independent evolutions of very similar, highly specialised structures for climbing in lizards, and countless instances of digital expansion in frogs - is almost unprecedented. It epitomises the concept of ‘limited forms most beautiful’ that is often used in the context of convergent evolution: evolution favours similar solutions to similar problems faced by different, often unrelated organisms. The pattern of adhesive structure loss is equally fascinating: nine losses of adhesion in geckos were inferred by Gamble et al. (2012), and the loss of terminally enlarged toes in frogs has been so frequent that it does not bear counting.
Thus, the pattern of loss and gain and convergence that can be seen in the reptiles and amphibians of the world really brings home the topic of this week’s blogging carnival with RAmBlN: herps really do adapt in some incredible ways, and they provide a magnificent system in which to study convergence and adaptive radiation on an ecological and global scale.
This has been a RAmBlN blog post: part of a series on herpetological adaptations, in celebration of Darwin Day 2014. Check out the other posts here! Like us on Facebook! Or follow us on twitter!
Autumn, K., M. Sitti, Y.A. Liang, A.M. Peattie, W.R. Hansen†, S. Sponberg, T.W. Kenny, R. Fearing, J.N. Israelachvili & R.J. Full. (2002) Evidence for van der Waals adhesion in gecko setae. PNAS, 99(19):12252–12256 (title photo)
Ba-Omar, T.A., J.R. Downie, W.J.P. Barnes. (2000) Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems. Journal of Zoology, 250:267-282
Federle, W., W.J.P. Barnes, W. Baumgartner, P. Drechsler & J.M. Smith. (2006) Wet but not slippery: boundary friction in tree frog adhesive toe pads. Journal of the Royal Society Interface, 3:689-697
Gamble, T., E. Greenbaum, T.R. Jackman, A.P. Russell & A.M. Bauer. (2012) Repeated Origin and Loss of Adhesive Toepads in Geckos. PLoS One, 7(6):e39429
Lamb, T. & A.M. Bauer. (2006) Footprints in the sand: independent reduction of subdigital lamellae in the Namib–Kalahari burrowing geckos. Proceedings of the Royal Society B, 273:855-864.
Pyron, R.A. & J.J. Wiens. (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61:543-583
Williamson, E.E. & J.A. Peterson. (1987) Convergent and Alternative Designs in the Digital Adhesive Pads of Scincid Lizards. Science, 215:1509-1511
Wollenberg, K.C., D.R. Vieites, A. van der Meijden, F. Glaw, D.C. Cannatella & M. Vences. (2008) Patterns of endemism and species richness in Malagasy cophyline frogs support a key role of mountainous areas for speciation. Evolution, 62(8):1890-1907
Tian, Y., N. Pesika, H. Zeng, K. Rosenberg, B. Zhao, P. McGuiggan, K. Autumn & J. Israelachvili. (2006) Adhesion and friction in gecko toe attachment and detachment. PNAS, 103(51):19320-19325