Evolution of the Gekkotan Adhesive System: Does Digit Anatomy Point to One or More Origins?

Abstract

Recently-developed, molecularly-based phylogenies of geckos have provided the basis for reassessing the number of times adhesive toe-pads have arisen within the Gekkota. At present both a single origin and multiple origin hypotheses prevail, each of which has consequences that relate to explanations about digit form and evolutionary transitions underlying the enormous variation in adhesive toe pad structure among extant, limbed geckos (pygopods lack pertinent features). These competing hypotheses result from mapping the distribution of toe pads onto a phylogenetic framework employing the simple binary expedient of whether such toe pads are present or absent. It is evident, however, that adhesive toe pads are functional complexes that consist of a suite of integrated structural components that interact to bring about adhesive contact with the substratum and release from it. We evaluated the competing hypotheses about toe pad origins using 34 features associated with digit structure (drawn from the overall form of the digits; the presence and form of adhesive scansors; the proportions and structure of the phalanges; aspects of digital muscular and tendon morphology; presence and form of paraphalangeal elements; and the presence and form of substrate compliance-enhancing structures). We mapped these onto a well-supported phylogeny to reconstruct their evolution. Nineteen of these characters proved to be informative for all extant, limbed geckos, allowing us to assess which of them exhibit co-occurrence and/or clade-specificity. We found the absence of adhesive toe pads to be the ancestral state for the extant Gekkota as a whole, and our data to be consistent with independent origins of adhesive toe pads in the Diplodactylidae, Sphaerodactylidae, Phyllodactylidae, and Gekkonidae, with a strong likelihood of multiple origins in the latter three families. These findings are consistent with recently-published evidence of the presence of adhesively-competent digits in geckos generally regarded as lacking toe pads. Based upon morphology we identify other taxa at various locations within the gekkotan tree that are promising candidates for the expression of the early phases of adhesively-assisted locomotion. Investigation of functionally transitional forms will be valuable for enhancing our understanding of what is necessary and sufficient for the transition to adhesively-assisted locomotion, and for those whose objectives are to develop simulacra of the gekkotan adhesive system for biotechnological applications.

Nonlinear variation in clinging performance with surface roughness in geckos

“…Subdigital adhesive toe pads in geckos represent a classic example of the evolution of locomotory traits that have evolved independently, on multiple occasions (Gamble, Greenbaum, Jackman, Russell, & Bauer, 2012Irschick et al, 1996;Russell & Gamble, 2019), and enabled the exploitation of several habitat types. In geckos, subdigital pads consist of laterally expanded scales (called lamellae) covered with modified scale derivatives in the form of stalks termed setae (Maderson, 1964;Russell, 2002).…”

Evolution of pedal digit orientation and morphology in relation to acquisition and secondary loss of the adhesive system in geckos

“…The more recent ancestral state reconstruction analysis (Gamble et al, ) also indicates that Narudasia festiva , Ptenopus , and SE Asian Cnemaspis are secondarily padless. There does not, however, appear to be any morphological evidence that these purported “secondarily padless species” once had an adhesive system (Russell & Gamble, ). Therefore, all of these taxa can be alternatively interpreted as being either ancestrally or secondarily padless.…”

Skin hydrophobicity as an adaptation for self‐cleaning in geckos

“…Functional morphological units often consist of complex multitrait structures, and there are multiple ways for a functionally complex organ to evolve and be optimized for particular outcomes, which can be conceptualized with many‐to‐one mapping (Alfaro, Bolnick, & Wainwright, 2005; Wainwright, 2007). However, if complex traits are analyzed as single traits, results can be misleading or difficult to interpret, so evolutionary morphology studies should address the evolution of functional outcomes directly (Garland Jr & Losos, 1994; Hagey et al, 2017; Russell & Gamble, 2019; Tiatragul, Murali, & Stroud, 2017).…”