Adaptive simplification and the evolution of gecko locomotion: Morphological and biomechanical consequences of losing adhesion

Abstract

Innovations permit the diversification of lineages, but they may also impose functional constraints on behaviors such as locomotion. Thus, it is not surprising that secondary simplification of novel locomotory traits has occurred several times among vertebrates and could potentially lead to exceptional divergence when constraints are relaxed. For example, the gecko adhesive system is a remarkable innovation that permits locomotion on surfaces unavailable to other animals, but has been lost or simplified in species that have reverted to a terrestrial lifestyle. We examined the functional and morphological consequences of this adaptive simplification in the Pachydactylus radiation of geckos, which exhibits multiple unambiguous losses or bouts of simplification of the adhesive system. We found that the rates of morphological and 3D locomotor kinematic evolution are elevated in those species that have simplified or lost adhesive capabilities. This finding suggests that the constraints associated with adhesion have been circumvented, permitting these species to either run faster or burrow. The association between a terrestrial lifestyle and the loss/reduction of adhesion suggests a direct link between morphology, biomechanics, and ecology.biomechanics | toepads | Pachydactylus | adaptation | Namibia S tructural innovations involving coordinated changes in multiple anatomical systems [Frazzetta's "complex adaptations" (1)] are associated with the diversification of many groups of vertebrates. Many such innovations often occur repeatedly within, as well as between, clades. One example is the evolution of the prehensile tail, which has arisen in primates, nonprimate mammals, seahorses, amphibians, and several groups of lizard, allowing its possessors to move through the environment in novel ways (2-6). Although the acquisition of such innovations is often implicated in both diversification and ecological specialization, much less is known about the causes and consequences of their secondary reduction and loss. If such novelties promote organismal diversity, then the evolutionary simplification of such innovations might commonly occur only when their diminution becomes even more advantageous. Generally, across the tree of life, we might expect that many of the most extraordinary examples of adaptive divergence should coincide not only with the origin and retention of innovations but also with their simplification, and ultimately their loss, in association with adaptation to new situations.Much of what is known about the secondary simplification of locomotor structures relates to limb loss/reduction in tetrapods (7-11), such as in snakes and lizards. The increase in the rate of evolutionary change in these situations suggests that the origin of an elongate body likely led not only to relaxed selection for the retention of limbs, but also to rapid adaptive selection, favoring both their loss and other associated morphological changes. In these cases, it is expected that both the rate of morphological evolution and the area...

Extreme positive allometry of animal adhesive pads and the size limits of adhesion-based climbing

“…Adhesive pads allow access to arboreal habitats (19)(20)(21), but they may come at the cost of reduced locomotor performance in situations where no adhesion is required (22,23). Thus, the multiple independent losses, gains, and reductions of adhesive pads in amphibians, insects, lizards, and spiders (24)(25)(26)(27) likely reflect the ecological, behavioral, and taxonomic diversity within these groups (28,29).…”

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

“…The morphological variation of pedal form among padbearing lineages is likely impacted by the function of the gecko adhesive system (Higham et al, ). When examined on a broad scale, however, there appear to be multiple outcomes to the acquisition of an adhesive system.…”

“…This might explain the large region of morphospace occupied by padbearing lineages (Figure ) and the lack of difference in the rates of morphological change between padbearing and padless lineages, in contrast to our prediction. Within the Pachydactylus radiation (as represented here by the clade bracketed by Pachydactylus rangei and Rhoptropus afer , Figure ), the rate of morphological and kinematic evolution increases following the secondary loss of adhesion and reversion to a cursorial lifestyle (Higham et al, ). Perhaps, the ability to detect a rate shift relates to the relative age of the group and the fact that all species are relatively closely related.…”

“…We combine data of Russell et al () and those collected by us from museum specimens to test the predictions of Russell et al () about the differences between padbearing and padless geckos, namely that interdigital angles are greater, digits are shorter, and the pes is more symmetrical in padbearing geckos. We also predict that the occupation of morphospace will be less extensive, and that the rates of morphological change will be slower in padbearing geckos due to functional constraints imposed by the adhesive apparatus (Higham et al, ). We use a geometric morphometric framework to capture shape evolution so as to better assess the aforementioned aspects of the evolution of pedal symmetry, including the incorporation of data from the tarsals that is seldom considered in the analysis of foot form.…”

Sticking to the story: outstanding challenges in gecko-inspired adhesives

“…In general, such studies have not simultaneously considered questions relating to the functional morphology of adhesive toe pads. Specific studies that reconstruct the evolutionary history of a radiation driven by a major innovation (Harmon et al, 2008) or that link morphological variation to the optimization of ecological performance and design principles for biologically inspired mimics would be highly informative (Russell and Higham, 2009;Higham and Russell, 2010;Russell and Johnson, 2014;Collins et al, 2015;Higham et al, 2015). We predict that when ecologists who are interested in basic biology and autecology of geckos increase their collaborations with researchers working on gecko adhesion in laboratory settings, there will be a new wave of findings that advance our understanding of gecko ecology and evolution as well as of gecko-inspired synthetic adhesives.…”