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doi: 10.1371/journal.pone.0039429. Epub 2012 Jun 27.

Repeated origin and loss of adhesive toepads in geckos

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Repeated origin and loss of adhesive toepads in geckos

Tony Gamble et al. PLoS One.2012.

Abstract

Geckos are well known for their extraordinary clinging abilities and many species easily scale vertical or even inverted surfaces. This ability is enabled by a complex digital adhesive mechanism (adhesive toepads) that employs van der Waals based adhesion, augmented by frictional forces. Numerous morphological traits and behaviors have evolved to facilitate deployment of the adhesive mechanism, maximize adhesive force and enable release from the substrate. The complex digital morphologies that result allow geckos to interact with their environment in a novel fashion quite differently from most other lizards. Details of toepad morphology suggest multiple gains and losses of the adhesive mechanism, but lack of a comprehensive phylogeny has hindered efforts to determine how frequently adhesive toepads have been gained and lost. Here we present a multigene phylogeny of geckos, including 107 of 118 recognized genera, and determine that adhesive toepads have been gained and lost multiple times, and remarkably, with approximately equal frequency. The most likely hypothesis suggests that adhesive toepads evolved 11 times and were lost nine times. The overall external morphology of the toepad is strikingly similar in many lineages in which it is independently derived, but lineage-specific differences are evident, particularly regarding internal anatomy, with unique morphological patterns defining each independent derivation.

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Conflict of interest statement

Competing Interests:The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Gecko phylogeny and the evolution of adhesive toepads.
Maximum likelihood tree showing phylogenetic relationships among gecko genera. Toepad traits, including the presence of adhesive toepads, toepad shape and the presence of paraphalanges, are illustrated by colored squares on the tips of the branches (squares with two colors indicate polymorphism within the clade). Rectangles at internal nodes represent ancestral presence or absence probabilities of adhesive toepads inferred using the 6-parameter binary-state speciation and extinction (BiSSE) model. Details for lettered clades are presented in Table 1. Representative images illustrate a variety of gecko toepad morphologies. Single digits from representative gecko species illustrating the morphological diversity of paraphalangeal elements (in gray with stippling) are shown on the right. Clades enclosed in gray boxes are shown in greater detail in Figures 3 and 4.
Figure 2
Figure 2. Bayesian parameter estimates inferred using the 6-parameter binary-state speciation and extinction (BiSSE) model.
Estimates of: A. trait-specific speciation rates (lambda); B. trait-specific extinction rates (mu); C. transition rate parameters (q01 =  gain of adhesive toepads, q10 =  loss of adhesive toepads); D. net diversification rates calculated as the difference between speciation (lambda) and extinction (mu) rates for genera with and without adhesive toepads. The 95% credibility intervals for each parameter are shaded and indicated by bars along the x-axis.
Figure 3
Figure 3. An unambiguous gain of adhesive toepads in house geckos (Hemidactylus).
Maximum likelihood tree of includedHemidactylus species and their close relatives, the padless “naked-toed” geckos and theCyrtodactylus +Geckoella clade. Circles at nodes indicate bootstrap support. Bayesian posterior probabilities of the presence of toepads are shown for two key nodes. Selected morphological components that comprise the digital adhesive mechanism are illustrated for each major clade. All three clades share spinules on the subdigital epidermis although only inHemidactylus are they fully elaborated as setae. In theCyrtodactylus +Hemidactylus clade: the subdigital lamellae are broadened; the antepenultimate phalanx of the digit (in blue) is reduced and, together with the penultimate phalanx and the claw, forms a raised arc; and the dorsal (extensor) musculature is expanded distally along the digit. The transition to fully functional toepads occurs inHemidactylus, which incorporate the tendinous system that controls individual scansors, and possesses epdidermal spinules that are of increased length and that are multi-spatulate, enhancing functional adhesive surface area. These are recognizable as setae.
Figure 4
Figure 4. Two unambiguous losses of adhesive toepads in south African geckos.
Maximum likelihood tree illustrating two independent losses of the digital adhesive mechanism in the southern African geckosChondrodactylus angulifer andPachydactylus rangei (in shaded boxes). Circles at nodes indicate bootstrap support. Bayesian posterior probabilities of the presence of toepads are shown for the most recent common ancestor of the included lineages, clearly indicating that the ancestor of this group possessed toepads. Representative species and their associated digital morphologies are illustrated. (A) Rupicolous habitat where padded members of this clade typically occur. (B) Sand dune habitat where the padlessChondrodactylus angulifer and the web-footedPachydactylus rangei typically occur.
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