Ontogeny of the paraphalanges and derived phalanges of Hemidactylus turcicus (Squamata: Gekkonidae).

Gekkotan lizards of the genus Hemidactylus exhibit derived digital morphologies. These include heavily reduced antepenultimate phalanges of digits III and IV of the manus and digits III-V of the pes, as well as enigmatic cartilaginous structures called paraphalanges. Despite this well-known morphological derivation, no studies have investigated the development of these structures. We aimed to determine if heterochrony underlies the derived antepenultimate phalanges of Hemidactylus. Furthermore, we aimed to determine if convergently evolved paraphalanges exhibit similar or divergent developmental patterns. Herein we describe embryonic skeletal development in the hands and feet of four gekkonid species, exhibiting a range of digital morphologies. We determined that the derived antepenultimate phalanges of Hemidactylus are the products of paedomorphosis. Furthermore, we found divergent developmental patterns between convergently evolved paraphalanges.

Ankle structure of the Tokay gecko (Gekko gecko) and its role in the deployment of the subdigital adhesive system.

The remarkable ability of geckos to adhere to smooth surfaces is often thought of in terms of external structures, including the branching setae that make contact with the surface producing van der Waals forces. Some geckos also exhibit unique movements of the distal segments of the limbs during locomotion and static clinging, including active digital hyperextension and considerable pedal rotation. During static clinging, geckos can exhibit considerable adduction/abduction of the pes while the crus and thigh remain firmly adpressed to the substratum. This decoupling of pedal adduction/abduction from ankle flexion/extension and pedal long-axis rotation is a significant departure from pedal displacements of a typical lizard lacking adhesive ability. The structure of the ankle is likely key to this decoupling, although no detailed comparison of this complex joint between pad-bearing geckos and other lizards is available. Here we compare the configuration of the mesotarsal joint of nongekkotan lizards (Iguana and Pristidactylus) with that of the Tokay gecko (Gekko gecko) using prepared skeletons, scanning electron microscopy, and micro-computed tomographic (µCT) scans. We focus on the structure of the astragalocalcaneum and the fourth distal tarsal. The mesotarsal joint exhibits a suite of modifications that are likely associated with the secondarily symmetrical pes of pad-bearing geckos. For example, the lateral process of the astragalocalcaneum is much more extensive in G. gecko compared with other lizards. The mesotarsal joint exhibits several other differences permitting dissociation of long-axis rotation of the pes from flexion-extension movement, including a reduced ventral peg on the fourth distal tarsal, an articulatory pattern dominated by a well-defined, expansive distomesial notch of the astragalocalcaneum, and an associated broad proximodorsal articulatory facet of the fourth distal tarsal. Pad-bearing geckos are capable of effectively deploying their intricate adhesive system across a broad array of body angles because of this highly modified ankle. Future research should determine whether the differences encountered in G. gecko (and their extent) apply to the Gekkota as a whole and should examine how the elements of the ankle move dynamically during locomotion across a range of taxa.

The same but different: setal arrays of anoles and geckos indicate alternative approaches to achieving similar adhesive effectiveness.

The functional morphology of squamate fibrillar adhesive systems has been extensively investigated and has indirectly and directly influenced the design of synthetic counterparts. Not surprisingly, the structure and geometry of exemplar fibrils (setae) have been the subject of the bulk of the attention in such research, although variation in setal morphology along the length of subdigital adhesive pads has been implicated to be important in the effective functioning of these systems. Adhesive setal field configuration has been described for several geckos, but that of the convergent Anolis lizards, comprised of morphologically simpler fibrils, remains largely unexplored. Here, we examine setal morphology along the proximodistal axis of the digits of Anolis equestris and compare our findings to those for a model gecko, Gekko gecko. Consistent with previous work, we found that the setae of A. equestris are generally thinner, shorter, and present at higher densities than those of G. gecko and terminate in a single spatulate tip. Contrastingly, the setae of G. gecko are hierarchically branched in structure and carry hundreds of spatulate tips. Although the splitting of contacts into multiple smaller tips is predicted to increase the adhesive performance of a fiber compared to an unbranched one, we posited that the adhesive performance of G. gecko and A. equestris would be relatively similar when the configuration of the setal fields of each was accounted for. We found that, as in geckos, setal morphology of A. equestris follows a predictable pattern along the proximodistal axis of the pad, although there are several critical differences in the configuration of the setal fields of these two groups. Most notably, the pattern of variation in setal length of A. equestris is effectively opposite to that exhibited by G. gecko. This difference in clinal variation mirrors the difference in the direction in which the setal fields of anoles and geckos are peeled from the substrate, consistent with the hypothesis that biomechanical factors are the chief determinants of these patterns of variation. Future empirical work, however, is needed to validate this. Our findings set the stage for future comparative studies investigating the functional morphology of these convergent adhesive apparatuses. Such investigations will lead to an enhanced understanding of the interactions between form, function, and environment of fibril-based biological adhesive systems.

Population genetic structure and species delimitation of a widespread, Neotropical dwarf gecko.

Amazonia harbors the greatest biological diversity on Earth. One trend that spans Amazonian taxa is that most taxonomic groups either exhibit broad geographic ranges or small restricted ranges. This is likely because many traits that determine a species range size, such as dispersal ability or body size, are autocorrelated. As such, it is rare to find groups that exhibit both large and small ranges. Once identified, however, these groups provide a powerful system for isolating specific traits that influence species distributions. One group of terrestrial vertebrates, gecko lizards, tends to exhibit small geographic ranges. Despite one exception, this applies to the Neotropical dwarf geckos of the genus Gonatodes. This exception, Gonatodes humeralis, has a geographic distribution almost 1,000,000 km2 larger than the combined ranges of its 30 congeners. As the smallest member of its genus and a gecko lizard more generally, G. humeralis is an unlikely candidate to be a wide-ranged Amazonian taxon. To test whether or not G. humeralis is one or more species, we generated molecular genetic data using restriction-site associated sequencing (RADseq) and traditional Sanger methods for samples from across its range and conducted a phylogeographic study. We conclude that G. humeralis is, in fact, a single species across its contiguous range in South America. Thus, Gonatodes is a unique clade among Neotropical taxa, containing both wide-ranged and range-restricted taxa, which provides empiricists with a powerful model system to correlate complex species traits and distributions. Additionally, we provide evidence to support species-level divergence of the allopatric population from Trinidad and we resurrect the name Gonatodes ferrugineus from synonymy for this population.

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

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.

Experimental evidence for friction-enhancing integumentary modifications of chameleons and associated functional and evolutionary implications.

The striking morphological convergence of hair-like integumentary derivatives of lizards and arthropods (spiders and insects) demonstrates the importance of such features for enhancing purchase on the locomotor substrate. These pilose structures are responsible for the unique tractive abilities of these groups of animals, enabling them to move with seeming ease on overhanging and inverted surfaces, and to traverse inclined smooth substrates. Three groups of lizards are well known for bearing adhesion-promoting setae on their digits: geckos, anoles and skinks. Similar features are also found on the ventral subdigital and distal caudal skin of chameleons. These have only recently been described in any detail, and structurally and functionally are much less well understood than are the setae of geckos and anoles. The seta-like structures of chameleons are not branched (a characteristic of many geckos), nor do they terminate in spatulate tips (which is characteristic of geckos, anoles and skinks). They are densely packed and have attenuated blunt, globose tips or broad, blade-like shafts that are flattened for much of their length. Using a force transducer, we tested the hypothesis that these structures enhance friction and demonstrate that the pilose skin has a greater frictional coefficient than does the smooth skin of these animals. Our results are consistent with friction being generated as a result of side contact of the integumentary filaments. We discuss the evolutionary and functional implications of these seta-like structures in comparison with those typical of other lizard groups and with the properties of seta-mimicking synthetic structures.

Tail autotomy and subsequent regeneration alter the mechanics of locomotion in lizards.

Animals can undergo significant weight change for a variety of reasons. Autotomy, the voluntary shedding of an appendage in response to a predator stimulus, provides an effective model for measuring the effects of rapid weight change on locomotor behavior and the responses to more gradual weight gain, particularly in lizards capable of both autotomizing and regenerating their tail. Although the general effects of autotomy on locomotor performance are commonly explored, we investigated changes in locomotor mechanics associated with tail loss and long-term regeneration for the first time by measuring morphology, 3D kinematics and ground reaction forces (GRFs) in the leopard gecko Eublepharis macularius. Tail autotomy resulted in a 13% anterior shift in the center of mass (CoM), which only partially recovered after full regeneration of the tail. Although no changes in body or forelimb kinematics were evident, decreases in hindlimb joint angles signify a more sprawled posture following autotomy. Changes in hindlimb GRFs resulted in an increase in weight-specific propulsive force, without a corresponding change in locomotor speed. Hindlimb kinematics and GRFs following autotomy recovered to pre-autotomy values as the tail regenerated. These results suggest an active locomotor response to tail loss that demonstrates the causal relationships between variations in morphology, kinematics and force.

Get to the point: Claw morphology impacts frictional interactions on rough substrates.

Claws are a common anatomical feature among limbed amniotes and contribute to a variety of functions including prey capture, locomotion, and attachment. Previous studies of both avian and non-avian reptiles have found correlations between habitat use and claw morphology, suggesting that variation in claw shape permits effective functioning in different microhabitats. How, or if, claw morphology influences attachment performance, particularly in isolation from the rest of the digit, has received little attention. To examine the effects of claw shape on frictional interactions, we isolated the claws of preserved specimens of Cuban knight anoles (Anolis equestris), quantified variation in claw morphology via geometric morphometrics, and measured friction on four different substrates that varied in surface roughness. We found that multiple aspects of claw shape influence frictional interactions, but only on substrates for which asperities are large enough to permit mechanical interlocking with the claw. On such substrates, the diameter of the claw's tip is the most important predictor of friction, with narrower claw tips inducing greater frictional interactions than wider ones. We also found that claw curvature, length, and depth influence friction, but that these relationships depend on the substrate's surface roughness. Our findings suggest that although claw shape plays a critical role in the effective clinging ability of lizards, its relative importance is dependent upon the substrate. Description of mechanical function, as well as ecological function, is critical for a holistic understanding of claw shape variation.

Time-varying motor control of autotomized leopard gecko tails: multiple inputs and behavioral modulation.

Autotomy (voluntary loss of an appendage) is common among diverse groups of vertebrates and invertebrates, and much attention has been given to ecological and developmental aspects of tail autotomy in lizards. Although most studies have focused on the ramifications for the lizard (behavior, biomechanics, energetics, etc.), the tail itself can exhibit interesting behaviors once segregated from the body. For example, recent work highlighted the ability of leopard gecko tails to jump and flip, in addition to being able to swing back and forth. Little is known, however, about the control mechanisms underlying these movements. Using electromyography, we examined the time-varying in vivo motor patterns at four sites (two proximal and two distal) in the tail of the leopard gecko, Eublepharis macularius, following autotomy. Using these data we tested the hypothesis that the disparity in movements results simply from overlapping pattern generators within the tail. We found that burst duration, but not cycle duration, of the rhythmic swings reached a plateau at approximately 150 s following autotomy. This is likely because of physiological changes related to muscle fatigue and ischemia. For flips and jumps, burst and cycle duration exhibited no regular pattern. The coefficient of variation in motor patterns was significantly greater for jumps and flips than for rhythmic swings. This supports the conclusion that the different tail behaviors do not stem from overlapping pattern generators, but that they rely upon independent neural circuits. The signal controlling jumps and flips may be modified by sensory information from the environment. Finally, we found that jumps and flips are initiated using relatively synchronous activity between the two sides of the tail. In contrast, alternating activation of the right and left sides of the tail result in rhythmic swings. The mechanism underlying this change in tail behavior is comparable to locomotor gait changes in vertebrates.

Revisiting the classification of squamate adhesive setae: historical, morphological and functional perspectives.

Research on gecko-based adhesion has become a truly interdisciplinary endeavour, encompassing many disciplines within the natural and physical sciences. Gecko adhesion occurs by the induction of van der Waals intermolecular (and possibly other) forces between substrata and integumentary filaments (setae) terminating in at least one spatulate tip. Gecko setae have increasingly been idealized as structures with uniform dimensions and a particular branching pattern. Approaches to developing synthetic simulacra have largely adopted such an idealized form as a foundational template. Observations of entire setal fields of geckos and anoles have, however, revealed extensive, predictable variation in setal form. Some filaments of these fields do not fulfil the morphological criteria that characterize setae and, problematically, recent authors have applied the term 'seta' to structurally simpler and likely non-adhesively competent fibrils. Herein we briefly review the history of the definition of squamate setae and propose a standardized classificatory scheme for epidermal outgrowths based on a combination of whole animal performance and morphology. Our review is by no means comprehensive of the literature regarding the form, function, and development of the adhesive setae of squamates and we do not address significant advances that have been made in many areas (e.g. cell biology of setae) that are largely tangential to their classification and identification. We contend that those who aspire to simulate the form and function of squamate setae will benefit from a fuller appreciation of the diversity of these structures, thereby assisting in the identification of features most relevant to their objectives.

Vocalization by extant nonavian reptiles: A synthetic overview of phonation and the vocal apparatus.

Among amniote vertebrates, nonavian reptiles (chelonians, crocodilians, and lepidosaurs) are regarded as using vocal signals rarely (compared to birds and mammals). In all three reptilian clades, however, certain taxa emit distress calls and advertisement calls using modifications of regions of the upper respiratory tract. There is no central tendency in either acoustic mechanisms or the structure of the vocal apparatus, and many taxa that vocalize emit only relatively simple sounds. Available evidence indicates multiple origins of true vocal abilities within these lineages. Reptiles thus provide opportunities for studying the early evolutionary stages of vocalization. The early literature on the diversity of form of the laryngotracheal apparatus of reptiles boded well for the study of form-function relationships, but this potential was not extensively explored. Emphasis shifted away from anatomy, however, and centered instead on acoustic analysis of the sounds that are produced. New investigative techniques have provided novel ways of studying the form-function aspects of the structures involved in phonation and have brought anatomical investigation to the forefront again. In this review we summarize what is known about hearing in reptiles in order to contextualize the vocal signals they generate and the sound-producing mechanisms responsible for them. The diversity of form of the sound producing apparatus and the increasing evidence that reptiles are more dependent upon vocalization as a communication medium than previously thought indicates that they have a significant role to play in the understanding of the evolution of vocalization in amniotes.

Flip, flop and fly: modulated motor control and highly variable movement patterns of autotomized gecko tails.

Many animals lose and regenerate appendages, and tail autotomy in lizards is an extremely well-studied example of this. Whereas the energetic, ecological and functional ramifications of tail loss for many lizards have been extensively documented, little is known about the behaviour and neuromuscular control of the autotomized tail. We used electromyography and high-speed video to quantify the motor control and movement patterns of autotomized tails of leopard geckos (Eublepharis macularius). In addition to rhythmic swinging, we show that they exhibit extremely complex movement patterns for up to 30 min following autotomy, including acrobatic flips up to 3 cm in height. Unlike the output of most central pattern generators (CPGs), muscular control of the tail is variable and can be arrhythmic. We suggest that the gecko tail is well suited for studies involving CPGs, given that this spinal preparation is naturally occurring, requires no surgery and exhibits complex modulation.

Ecomorphological associations of scapulocoracoid form in Greater Antillean Anolis lizards.

External morphological metrics have featured prominently in comparative studies examining the morphological convergence that characterizes anoline ecomorphs. To what degree the appendicular-skeletal morphology of Greater Antillean island Anolis lizards tracks their diversity and ecological adaptation, however, remains relatively unexplored. Here we employ computed tomographic scanning techniques to visualize in situ the scapulocoracoid of ecomorph representatives (trunk-ground, trunk-crown, crown-giant, twig) from three islands (Jamaica, Hispaniola, and Puerto Rico), and compare its three-dimensional geometry using qualitative-descriptive and quantitative-morphometric techniques. In contrast to our previous, similarly-conducted study of the pelvic girdle of these same species, the form of the scapulocoracoid varies markedly both within and between species, with much of the variation relating to phylogenetic relationship, specimen size, and assigned ecomorph category. Morphometric variation that correlates with size and/or phylogenetic signal varies between species and cannot be eliminated from the data set without markedly reducing its overall variability. The discovered patterns of skeletal variation are consistent with the demands of locomotor mechanics imposed by the structural configuration of the microhabitat of these ecomorphs. Most pertinently the ecomorphs differ in the anteroposterior length of the coracoid, the dorsoventral height of the scapulocoracoid, the dorsoventral height of the scapula in relation to the height of the suprascapula, and the relative positioning of the borders of the scapulocoracoid fenestra. In the examined ecomorph categories these skeletal differences likely relate to microhabitat usage by permitting different degrees of tilting and displacement of the scapulocoracoid in the parasagittal plane and influencing the sizes of muscle origins and the vectors of their actions. These differences relate to the amount of humeral adduction applied during its protraction, and to the structural stability of the shoulder girdle during acrobatic maneuvers, thus influencing the perch diameter that can be effectively negotiated, a critical factor in the microhabitat structure of Anolis ecomorphs.

A new angle on clinging in geckos: incline, not substrate, triggers the deployment of the adhesive system.

Lizards commonly climb in complex three-dimensional habitats, and gekkotans are particularly adept at doing this by using an intricate adhesive system involving setae on the ventral surface of their digits. However, it is not clear whether geckos always deploy their adhesive system, given that doing so may result in decreased (i.e. reduction in speed) locomotor performance. Here, we investigate circumstances under which the adhesive apparatus of clinging geckos becomes operative, and examine the potential trade-offs between speed and clinging. We quantify locomotor kinematics of a gecko with adhesive capabilities (Tarentola mauritanica) and one without (Eublepharis macularius). Whereas, somewhat unusually, E. macularius did not suffer a decrease in locomotor performance with an increase in incline, T. mauritanica exhibited a significant decrease in speed between the level and a 10 degrees incline. We demonstrate that this results from the combined influence of slope and the deployment of the adhesive system. All individuals kept their digits hyperextended on the level, but three of the six individuals deployed their adhesive system on the 10 degrees incline, and they exhibited the greatest decrease in velocity. The deployment of the adhesive system was dependent on incline, not surface texture (600 grit sandpaper and Plexiglas), despite slippage occurring on the level Plexiglas substrate. Our results highlight the type of sensory feedback (gravity) necessary for deployment of the adhesive system, and the trade-offs associated with adhesion.

Configuration of the setal fields of Rhoptropus (Gekkota: Gekkonidae): functional, evolutionary, ecological and phylogenetic implications of observed pattern.

Many gekkotans possess seta-bearing adhesive subdigital pads. Details of setal structure, however, are largely based upon putatively exemplary fibrils deemed typical of the species. Little is known of the pattern of configuration of the setae across the subdigital pads and how great, if any, the variance in structure and dimensions is. To understand setal fields as functional entities, as opposed to individual setae, it is necessary to consider this pattern. Additionally, gekkotans within individual radiations occupy different environments and potentially are substrate-specific in terms of the locomotor surface exploited. To investigate these issues, we herein examine the configuration and dimensions of seven species of the gekkotan genus Rhoptropus, and an outgroup taxon, Chondrodactylus bibronii. All of these taxa are rupicolous and the array of rock surfaces exploited by this cluster of taxa is extensive. Our results show that setal field configuration follows a predictable pattern, both from one digit to another within a species, and between homologous digits and anatomical locations between species. One species, Rhoptropus afer, a more terrestrial taxon, exhibits significantly shorter setae and a smaller subdigital pad area than do its congeners, but exhibits the same overall pattern of setal arrangement. Our findings have implications for the understanding of the evolution of adhesive structures, and for the principles used for generating and manufacturing biomimetic artificial microfibrillar arrays.

The anatomy and development of the claws of Xenopus laevis (Lissamphibia: Anura) reveal alternate pathways of structural evolution in the integument of tetrapods.

Digital end organs composed of hard, modified epidermis, generally referred to as claws, are present in mammals and reptiles as well as in several non-amniote taxa such as clawed salamanders and frogs, including Xenopus laevis. So far, only the claws and nails of mammals have been characterized extensively and the question of whether claws were present in the common ancestor of all extant tetrapods is as yet unresolved. To provide a basis for comparisons between amniote and non-amniote claws, we investigated the development, growth and ultrastructure of the epidermal component of the claws of X. laevis. Histological examination of developing claws of X. laevis shows that claw formation is initiated at the tip of the toe by the appearance of superficial cornified cells that are dark brown. Subsequent accumulation of new, proximally extended claw sheath corneocyte layers increases the length of the claw. Histological studies of adult claws show that proliferation of cornifying claw sheath cells occurs along the entire length of the claw-forming epidermis. Living epidermal cells that are converting into the cornified claw sheath corneocytes undergo a form of programmed cell death that is accompanied by degradation of nuclear DNA. Subsequently, the cytoplasm and the nuclear remnants acquire a brown colour by an as-yet unknown mechanism that is likely homologous to the colouration mechanism that occurs in other hard, cornified structures of amphibians such as nuptial pads and tadpole beaks. Transmission electron microscopy revealed that the cornified claw sheath consists of parallel layers of corneocytes with interdigitations being confined to intra-layer contacts and a cementing substance filling the intercorneocyte spaces. Together with recent reports that showed the main molecular components of amniote claws are absent in Xenopus, our data support the hypothesis that claws of amphibians likely represent clade-specific innovations, non-homologous to amniote claws.

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

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.

The Integrative Biology of Gecko Adhesion: Historical Review, Current Understanding, and Grand Challenges.

Geckos are remarkable in their ability to reversibly adhere to smooth vertical, and even inverted surfaces. However, unraveling the precise mechanisms by which geckos do this has been a long process, involving various approaches over the last two centuries. Our understanding of the principles by which gecko adhesion operates has advanced rapidly over the past 20 years and, with this knowledge, material scientists have attempted to mimic the system to create artificial adhesives. From a biological perspective, recent studies have examined the diversity in morphology, performance, and real-world use of the adhesive apparatus. However, the lack of multidisciplinarity is likely a key roadblock to gaining new insights. Our goals in this paper are to 1) present a historical review of gecko adhesion research, 2) discuss the mechanisms and morphology of the adhesive apparatus, 3) discuss the origin and performance of the system in real-world contexts, 4) discuss advancement in bio-inspired design, and 5) present grand challenges in gecko adhesion research. To continue to improve our understanding, and to more effectively employ the principles of gecko adhesion for human applications, greater intensity and scope of interdisciplinary research are necessary.

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

Among geckos, the acquisition of the adhesive system is associated with several morphological changes of the feet that are involved in the operation of the adhesive apparatus. However, analyses using a comparative framework are lacking. We applied traditional morphometrics and geometric morphometric analysis with phylogenetic comparative methods to morphological data, collected from X-ray scans, to examine patterns of morphological evolution of the pes in association with the gain and loss of adhesive capabilities, and with habitat occupancy among 102 species of gecko. Padbearing gecko lineages tend to have shorter digits and greater inter-digital angles than padless ones. Arboreal and saxicolous species have shorter digits than terrestrial species. Our results suggest repeated shifts that converge upon a similar padbearing morphology, with some modifications being associated with the habitat occupied. We demonstrate that functional innovation and habitat can operate on, and influence, different components of foot morphology.

Going Out on a Limb: How Investigation of the Anoline Adhesive System Can Enhance Our Understanding of Fibrillar Adhesion.

The remarkable ability of geckos to adhere to a wide-variety of surfaces has served as an inspiration for hundreds of studies spanning the disciplines of biomechanics, functional morphology, ecology, evolution, materials science, chemistry, and physics. The multifunctional properties (e.g., self-cleaning, controlled releasability, reversibility) and adhesive performance of the gekkotan adhesive system have motivated researchers to design and fabricate gecko-inspired synthetic adhesives of various materials and properties. However, many challenges remain in our attempts to replicate the properties and performance of this complex, hierarchical fibrillar adhesive system, stemming from fundamental, but unanswered, questions about how fibrillar adhesion operates. Such questions involve the role of fibril morphology in adhesive performance and how the gekkotan adhesive apparatus is utilized in nature. Similar fibrillar adhesive systems have, however, evolved independently in two other lineages of lizards (anoles and skinks) and potentially provide alternate avenues for addressing these fundamental questions. Anoles are the most promising group because they have been the subject of intensive ecological and evolutionary study for several decades, are highly speciose, and indeed are advocated as squamate model organisms. Surprisingly, however, comparatively little is known about the morphology, performance, and properties of their convergently-evolved adhesive arrays. Although many researchers consider the performance of the adhesive system of Anolis lizards to be less accomplished than its gekkotan counterpart, we argue here that Anolis lizards are prime candidates for exploring the fundamentals of fibrillar adhesion. Studying the less complex morphology of the anoline adhesive system has the potential to enhance our understanding of fibril morphology and its relationship to the multifunctional performance of fibrillar adhesive systems. Furthermore, the abundance of existing data on the ecology and evolution of anoles provides an excellent framework for testing hypotheses about the influence of habitat microstructure on the performance, behavior, and evolution of lizards with subdigital adhesive pads.