On the origin of frictional adhesion in geckos: small morphological changes lead to a major biomechanical transition in the genusGonatodes

Abstract

The evolutionary history of vertebrate locomotion is punctuated by innovations that have permitted expansion into novel ecological niches. Frictional adhesion of geckos is an innovation renowned for enabling locomotion on vertical and inverted smooth surfaces. Much is known about the microstructure and function of the fully-expressed gekkotan adhesive apparatus, although how it originated is poorly understood. Therefore, identifying species that exhibit the earliest stages of expression of frictional adhesion will provide significant insights into the evolution of this trait. Our previous investigation of digital proportions, shape, scalation, skeletal form, and subdigital epidermal micro-ornamentation in the genus Gonatodes led us to hypothesize that Gonatodes humeralis expresses incipient frictional adhesion. To test this, we first conducted a phylogenetic analysis of Gonatodes and related sphaerodactyl genera to clarify the historical context of the evolution of frictional adhesive capability in the genus. We then measured the ability of G. humeralis and its close relatives to generate frictional adhesive force, examined their locomotor capabilities on low-friction surfaces, and observed animals in their natural habitat. After accounting for body mass and phylogenetic relationships, we found that G. humeralis generates frictional adhesive force essentially equivalent to that of Anolis, and can scale vertical smooth surfaces. Gonatodes vittatus, a species that lacks elaborated epidermal setae, generates negligible frictional adhesive force and can only ascend smooth inclined surfaces with a pitch of ≤ 40°. We conclude that the ostensibly padless G. humeralis, with feet lacking the musculoskeletal, tendinous, and vascular modifications typical of pad-bearing geckos, nevertheless can employ frictional adhesive contact to assist locomotion. As in Anolis, the release of frictional adhesive contact occurs when the foot is plantar flexed after the heel has lifted from the surface. Our findings indicate that the origin of frictional adhesion was likely gradual but that, ultimately, this led to major shifts in ecology and function.