Solutions to a Sticky Problem: Convergence of the Adhesive Systems of Geckos and Anoles (Reptilia: Squamata)

The modes and mechanisms of organismal attachment are numerous and diverse. Terrestrial vertebrates, however, achieve robust and releasable attachment to both abiotic and biotic substrata in three chief ways: hook-like anchors, such as claws, permit temporary attachment to surfaces via mechanical interlocking and/or frictional interactions with surface asperities; attachment organs releasing glandular secretions (e.g., the toe pads of hylid frogs, suction cups of disc-winged bats) achieve attachment via wet adhesion and/or suction; subdigital pads of some lineages of lizards possess filamentous outgrowths that induce friction and/or adhesion via molecular interactions. Lizards are the largest organisms to employ fibrillar-based attachment, but only the adhesive subdigital pads of geckos and anoles are sufficiently adhesively competent to support forces in excess of their body mass. The adhesive systems of geckos and anoles have long been considered convergent, but beyond general statements to this effect, convergence has not been rigorously assessed. Here we review what is known of the adhesive apparatus of both gekkotan and anoline lizards within the context of two hierarchically stratified domains: (1) adhesive attachment and the structure of setae and setal fields, and (2) the higher-order anatomical specializations that control the operation of the setae. We employ this information to identify the physical and organismic drivers of convergence of fibrillar adhesive systems, thereby enabling us to assess the particular, rather than superficially general, extent of convergence of the adhesive system of geckos and anoles. Our synopsis of gekkotan and anoline setae, setal fields, and their adhesive systems reveals numerous physical and organismic constraints, perceived as the drivers of convergent evolution, that have led to similar morphological and functional outcomes. We posit that the setae and setal fields of geckos and anoles are convergent structures that enhance effective attachment to diverse substrata. Setae exhibit deep homology, arising from the convergently evolved spinulate Oberhäutchen of the epidermis. Following the initial exaptation of spinules as van der Waals adhesion-promoting setae, those of geckos and anoles followed somewhat different evolutionary pathways as the setae became organized into integrated setal fields. These pathways are reflective of differences in how the biomechanical control of the setal fields, during their application and release from the substratum, is achieved. Although anoles seemingly exhibit only a single evolutionary origin of the adhesive system, that of geckos has arisen on multiple independent occasions, with a broad range of expression of anatomical configurations that characterize the functional system. A broad survey of such configurations among geckos reveals that some are morphologically (and probably behaviorally) more similar to those of anoles than are others. Our assessment of the extent of convergence of the adhesive apparatuses of geckos and anoles identifies gekkotan taxa with an adhesive apparatus that most closely resembles that of anoles and explores what is minimally necessary to promote reversible attachment via molecular interactions. Our findings should contribute not only to ongoing investigations of the functional morphology of these adhesive systems but also should be informative to those who design biomimetic fibrillar adhesives intended to operate similarly to their natural counterparts.