Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems

Understanding the evolution of complex functional traits is a challenge for evolutionary physiology. Here we investigate the evolution of subdigital toepads in lizards, which have arisen independently at least three times, although with subtle anatomical differences. Some designs (anole, gecko) appear functionally equivalent, whereas other designs (skink) are inferior. The functional equivalence of geckos and anoles highlights the creative aspect of the evolutionary process in that these two groups have arrived at the same functional endpoint along very different trajectories. However, this functional equivalence does not result in equivalence for performance at whole-organism tasks (e.g., running uphill), as the evolution of behavior (e.g., toe-furling) has enabled geckos to be superior climbers than anoles. We also show that adaptive increases in the toepad size within a closely related lizard genus (Anolis) has resulted in concomitant evolution of enhanced clinging ability and increased perch heights. A third insight is that pad-bearing geckos are capable of carrying tremendous loads (up to 250% of body weight) up smooth surfaces, and that the toepad itself does not appear limiting. This comparative and whole-organism approach to lizard toepads underscores how organisms can evolve multiple solutions to evolutionary problems.     

Repeated origin and loss of adhesive toepads in geckos

Geckos are well known for their extraordinary clinging abilities and many species easily scale vertical or even inverted surfaces. This ability is enabled by a complex digital adhesive mechanism (adhesive toepads) that employs van der Waals based adhesion, augmented by frictional forces. Numerous morphological traits and behaviors have evolved to facilitate deployment of the adhesive mechanism, maximize adhesive force and enable release from the substrate. The complex digital morphologies that result allow geckos to interact with their environment in a novel fashion quite differently from most other lizards. Details of toepad morphology suggest multiple gains and losses of the adhesive mechanism, but lack of a comprehensive phylogeny has hindered efforts to determine how frequently adhesive toepads have been gained and lost. Here we present a multigene phylogeny of geckos, including 107 of 118 recognized genera, and determine that adhesive toepads have been gained and lost multiple times, and remarkably, with approximately equal frequency. The most likely hypothesis suggests that adhesive toepads evolved 11 times and were lost nine times. The overall external morphology of the toepad is strikingly similar in many lineages in which it is independently derived, but lineage-specific differences are evident, particularly regarding internal anatomy, with unique morphological patterns defining each independent derivation.     

A comparison of habitat use, morphology, clinging performance and escape behaviour among two divergent green anole lizard (Anolis carolinensis) populations

We measured available and actual habitat use, morphology, escape behaviour and clinging ability in a large sample ( N  = 242) of green anoles, Anolis carolinensis , in a habitat consisting primarily of segregated dense clumps of broad leaves, Aspidistra elatior (Tulane University campus, LA) to compare against similar data collected previously from a more typical habitat c. 30 km away, consisting of continuous strands of bushes and trees (Good Hope Field, St. Charles Parish, LA). At Tulane the anoles perched primarily on the broad, smooth leaves of broad leaves, whereas in Good Hope Field (GHF) they predominantly perched on branches and tree trunks. The two populations differed significantly in morphology. In Tulane, the anoles tended to have shorter distal hindlimb elements, longer forelimb elements, and were more 'slender' than those at GHF. A comparison of escape behaviour showed population and sex differences. In both populations, females had significantly longer approach distances (i.e. were more 'wary') than males. These distances were, in addition, significantly longer at GHF than at Tulane for both sexes; this may be due to the potentially higher diversity and abundance of predators at GHF, although habituation to humans may also play a role. Anoles at Tulane had significantly larger toepads and higher clinging abilities than those at GHF. The enhanced clinging abilities of anoles at Tulane may have arisen due to their propensity to use smooth leaves as their primary substrate. Overall, our data reveal substantial ecological, behavioural, morphological, and functional differences among populations, some of which may be adaptive.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 223–234.     

Character displacement in the midst of background evolution in island populations of Anolis lizards: A spatiotemporal perspective

Negative interactions between species can generate divergent selection that causes character displacement. However, other processes cause similar divergence. We use spatial and temporal replication across island populations of Anolis lizards to assess the importance of negative interactions in driving trait shifts. Previous work showed that the establishment of Anolis sagrei on islands drove resident Anolis carolinensis to perch higher and evolve larger toepads. To further test the interaction's causality and predictability, we resurveyed a subset of islands nine years later. Anolis sagrei had established on one island between surveys. We found that A. carolinensis on this island now perch higher and have larger toepads. However, toepad morphology change on this island was not distinct from shifts on six other islands whose Anolis community composition had not changed. Thus, the presence of A. sagrei only partly explains A. carolinensis trait variation across space and time. We also found that A. carolinensis on islands with previously established A. sagrei now perch higher than a decade ago, and that current A. carolinensis perch height is correlated with A. sagrei density. Our results suggest that character displacement likely interacts with other evolutionary processes in this system, and that temporal data are key to detecting such interactions.     

The effects of fire on the frillneck lizard (Chlamydosaurus kingii) in northern Australia

Abstract A population of frillneck lizards, Chlamydosaurus kingii, was monitored by radio telemetry and mark-recapture techniques between April 1991 and April 1994, as part of a landscape-scale fire experiment, in Kakadu National Park, Northern Territory. The study aimed to investigate both the short- and longer-term effects of fire on a lizard species in a tropical savanna where fires are frequent and often annual. Frillneck lizards are able to survive fires that occur in the first few months of the dry season by remaining perched in trees. A high level of mortality (29%) occurred during late dry-season fires, along with changes in their behavioural response to fire: sheltering in either larger trees or hollow termite mounds. Food is more accessible after fires due to the removal of ground vegetation. This is reflected in greater volume and diversity of prey in stomach contents after fires. This increase is more pronounced after late dry-season fires, possibly due to increased accessibility of prey caused by more complete vegetation removal. Frillneck lizards show an overall preference for trees with a dense canopy cover located in an area with a low density of grass. Fire has an effect on this relationship. Frillneck lizards in habitat unburnt for a number of years tend to perch in trees with a smaller canopy, whereas lizards in annually burnt habitat perch in trees with a dense canopy. Volume and composition of lizard stomach contents was broadly similar among fire treatments over a 2 year period, although termites were more predominant in stomach contents of lizards in unburnt habitat. Wet-season body condition is lower in lizards from unburnt habitat, although the reason for this is unclear. These results demonstrate the importance of different fire intensities and regimes on the ecology of a lizard species in a tropical savanna.     

Escape tactics and effects of perch height and habituation on flight initiation distance in two Jamaican anoles (Squamata: polychrotidae)

Escape by Anolis lizards is influenced by microhabitats and fight initiation distance increases with predation risk. Differences in microhabitat use among ecomorphs affect escape behavior, but only two studies have reported ecomorphological differences in flight initiation distance among Greater Antillean species. I studied effects of predation risk and microhabitats on escape behavior by conducting field experiments using two species of anoles, Anolis lineatopus and A. grahami, on the campus of the University of the West Indies at Mona, Jamaica. Because ecomorphological variation of anoles has evolved independently within each island of the Greater Antilles, but relationships between ecomorphs and escape behaviors are poorly known, I characterized microhabitat use and escape tactics, and determined relationships between flight initiation distance and two risk factors, habituation to human presence and perch height, in Anolis lineatopus, a trunk-ground anole and A. grahami, a trunk-crown anole. Sample sizes for A. lineatopus and A. grahami were 214 and 93, for microhabitat use and escape destinations, 74 and 34 for human presence and 125 and 34 for perch height. The two species occurred in similar microhabitats and exhibited similar escape tactics, but exhibited key differences expected for their ecomorphs. Both species were sighted frequently on the ground and on trees, but A. lineatopus were more frequently on ground and were perched lower than A. grahami. Both species escaped from ground to trees and when on trees hid on far sides and escaped without changing climbing direction with equal frequency. The frequency of fleeing upward was greater for A. grahami than A. lineatopus. Both species exhibited habituation by having shorter flight initiation distances in areas with more frequent exposure to people. In both species flight initiation distance increased as perch height decreased because, lizards had to climb farther to be out of reach when perched lower. The relationship between flight initiation distance and perch height may apply to other anole ecomorphs that flee upward when low perched on trees.     

A comparative analysis of clinging ability among pad-bearing lizards

We examined clinging ability, subdigital pad area and body mass in 14 pad-bearing lizard species from three families to test three predictions: (1) clinging ability and pad area should be tightly correlated among species; (2) pad area and clinging ability should scale similarly to body mass among 14 species; and (3) functional similarity in clinging capabilities should exist among species despite differences in body mass. Our results confirm two predictions; clinging ability is tightly correlated with pad area, even when the effects of body size are removed, and the lizards examined are approximately functionally similar in their clinging capabilities. Nevertheless, despite the tight correlation between pad area and clinging ability, pad area scales with body mass by a lower slope than clinging ability. Overall, these results indicate that although pad area is a strong determinant of clinging ability, other factors enable these lizards to maintain functional similarity.     

Intraspecific correlations among morphology, performance and habitat use within a green anole lizard (Anolis carolinensis) population

We examined habitat use, morphology, jumping and clinging ability for 403 juvenile, female and male green anole lizards, Anolis carolinensis, in a population in south‐eastern Louisiana. We sought to answer three questions: (1) Do age/sex classes differ in habitat use, morphology and performance ability? (2) Do habitat use, morphology and performance correlate among all individuals across three age/sex classes (juveniles, females and males)? (3) Do juveniles compensate for their poor absolute performance capacities by being better performers on a relative scale? The three age/sex classes were found to differ significantly in size‐adjusted morphology, habitat use and size‐adjusted performance capacity. Juveniles tended to occupy perches which were closer together than those of adult males and females. The distal elements of the hindlimb (femur, tibia) were significantly longer in males than in females and juveniles, while females were more stocky than males and juveniles. The only significant overall ecomorphological relationship detected was between the lengths of the distal hindlimb elements and maximum jump acceleration. Our hypothesis that juveniles should be better performers (relative to size) compared to adults was disproved, as adult females were always the best performers relative to size. Our analysis of a mainland anole population presents a different view of population structure compared to similar studies involving Caribbean Anolis lizards, which show more ecological differentiation among age/sex classes, and also show that juveniles are relatively good performers. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 211–221.     

Intraspecific variation in Anolis sagrei mirrors the adaptive radiation of Greater Antillean anoles

Anolis lizards of the Greater Antilles represent one of the classic examples of vertebrate adaptive radiation. The same morphological types ('ecomorphs') have evolved repeatedly in response to similar ecological pressures on different islands. We tested whether patterns of within species diversification were congruent with between species patterns and the processes leading to the adaptive radiation of Greater Antillean anoles by measuring variation in performance-related morphological characters in the brown anole, Anolis sagrei . We measured morphological and genetic variation in two different habitat types on each of five islands in the Bahamas. We estimated population structure and rates of gene flow within and among islands using eight microsatellite markers. Intraspecific variation in performance-related morphological characters was similar to the pattern of interspecific variation that characterizes the adaptive radiation of this group in the Greater Antilles. For example, limb length was correlated with perch diameter within A. sagrei as has also been shown among species of anole. Morphological divergence in traits has occurred despite relatively high levels of gene flow both within and among islands. These results are discussed in the context of the divergence-with-gene-flow model of speciation. The results provide important intraspecific evidence that the diversification of anoles has been shaped by natural selection and show how ecologically-based selection pressures explain diversification at both the population and species levels.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 189–199.     

Keratin intermediate filament chains in the European common wall lizard (Podarcis muralis) and a potential keratin filament crosslinker

On the basis of sequence homology with mammalian α-keratins, and on the criteria that the coiled-coil segments and central linker in the rod domain of these molecules must have conserved lengths if they are to assemble into viable intermediate filaments, a total of 28 Type I and Type II keratin intermediate filament chains (KIF) have been identified from the genome of the European common wall lizard (Podarcis muralis). Using the same criteria this number may be compared to 33 found here in the green anole lizard (Anole carolinensis) and 25 in the tuatara (Sphenodon punctatus). The Type I and Type II KIF genes in the wall lizard fall in clusters on chromosomes 13 and 2 respectively. Although some differences occur in the terminal domains in the KIF chains of the two lizards and tuatara, the similarities between key indicator residues – cysteine, glycine and proline – are significant. The terminal domains of the KIF chains in the wall lizard also contain sequence repeats commonly based on glycine and large apolar residues and would permit the fine tuning of physical properties when incorporated within the intermediate filaments. The H1 domain in the Type II chain is conserved across the lizards, tuatara and mammals, and has been related to its role in assembly at the 2–4 molecule level. A KIF-like chain (K80) with an extensive tail domain comprised of multiple tandem repeats has been identified as having a potential filament-crosslinking role.     

Divergent morphologies, performance, and escape behaviour in two tropical rock-using lizards (Reptilia: Scincidae)

The present study quantified microhabitat use, morphology, performance (sprinting, climbing, clinging, and jumping), and escape behaviour of two closely related tropical rock-using lizards. Specifically, the study tested whether: (1) a flatter body and longer limbs enhance performance in rocky habitats; (2) escape behaviour supports predictions based on habitat openness; and (3) there is a trade-off between sprinting and climbing performance. Despite the occupation of generally similar rocky habitats, the habitat of Carlia scirtetis was more open and composed of larger boulders with more regular surfaces, whereas the habitat of Carlia mundivensis was composed of more undergrowth and leaf litter, consisting of smaller boulders with irregular surfaces. The longer legs, flatter body, and greater sprinting and climbing ability of C. scirtetis, supports ecomorphological predictions. By contrast to predictions based on habitat openness, C. scirtetis allowed a potential threat to approach closer and ran further to a refuge than C. mundivensis , suggesting that escape behaviour as determined by performance may be species-specific or decoupled in these two species. The increased sprint speed of C. scirtetis highlighted a performance trade-off, with climbing speed lagging behind that of sprint speed. These results suggest that subtle differences in the structural microhabitat and the degree of habitat openness may ultimately result in substantial differences in morphology, performance, and threat behaviour in closely-related lizard species.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 85–98.     

Phenotypic integration between claw and toepad traits promotes microhabitat specialization in the Anolis adaptive radiation

The performance of an organism in its environment frequently depends more on its composite phenotype than on individual phenotypic traits. Thus, understanding environmental adaptation requires investigating patterns of covariation across functionally related traits. The replicated adaptive radiations of Greater Antillean Anolis lizards are characterized by ecological and morphological convergence, thus, providing an opportunity to examine the role of multiple phenotypes in microhabitat adaptation. Here, we examine integrated claw and toepad morphological evolution in relation to habitat partitioning across the adaptive radiations of Greater Antillean anoles. Based on analysis of 428 specimens from 57 species, we found that different aspects of claw morphology were associated with different perch dimensions, with claw height positively associated with perch diameter and claw curvature positively associated with perch height. Patterns of integration also varied across claw and toepad traits, likely driven by correlative selection for performance on smoother and rougher substrates. Finally, rates of evolution differed between claw and toepad traits, with claw length evolving faster than all other traits despite having no predicted functional importance. Our results highlight the multivariate nature of phenotypic adaptation and suggest that phenotypic integration across Greater Antillean anoles is driven by fine‐scale correlative selection based on structural habitat specialization.     

Perch selection by singing chaffinches: a better view of surroundings and the risk of predation

Predation risk varies among perches, and the vulnerability ofsinging chaffinches (Fringilla coelebs) might differ dependingon where they perch in a tree. To find out how singing of thechaffinch is associated with antipredatory behavior, I studiedperch selection in mature pine forest and in pine saplings,two habitats differing in the amount of cover for protection from predators. My results show that male chaffinches preferto sing below the canopy of mature pines and in the uppermostparts of sapling pines. Although these are the canopy partsmost exposed to sparrowhawk (Accipiter nisus) attacks, stayingin open sites may be a beneficial strategy for singing chaffinchesbecause it makes it possible to improve antipredatory vigilance.This assumption was supported by the hawk experiments. Afterbeing exposed to the sparrowhawk model, all of the singingbirds selected the conspicuous perch below the canopy of maturepines. The males that perched higher in the canopy before theexperiment moved to the lower canopy, whereas those males thatsang below the canopy did not change their singing perch.     

Sexual dimorphism of heads and abdomens: Different approaches to ‘being large’ in female and male lizards

Sexual‐size dimorphism (SSD) is widespread in animals. Body length is the most common trait used in the study of SSD in reptiles. However, body length combines lengths of different body parts, notably heads and abdomens. Focusing on body length ignores possible differential selection pressures on such body parts. We collected the head and abdomen lengths of 610 lizard species (Reptilia: Squamata: Sauria). Across species, males have relatively larger heads, whereas females have relatively larger abdomens. This consistent difference points to body length being an imperfect measure of lizard SSD because it comprises both abdomen and head lengths, which often differ between the sexes. We infer that female lizards of many species are under fecundity selection to increase abdomen size, consequently enhancing their reproductive output (enlarging either clutch or offspring size). In support of this, abdomens of lizards laying large clutches are longer than those of lizards with small clutches. In some analyses, viviparous lizards have longer abdomens than oviparous lizards with similar head lengths. Our data also suggest that male lizards are under sexual selection to increase head size, which is positively related to winning male–male combats and to faster grasping of females. Thus, larger heads could translate into higher probability to mate. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 665–673.     

Vertical clinging and leaping revisited: vertical support use as the ancestral condition of strepsirrhine primates

A re-examination of primate foot and knee anatomy suggests that strepsirrhine primates (adapiforms and lemuriforms) possess a unique and derived hindlimb related to their use of vertical supports. In contrast, leaping adaptations are older and shared by both major euprimate clades, Strepsirrhini and Haplorhini. Combining this derived hindlimb anatomy with leaping suggests that ancestral strepsirrhines were at least frequent vertical support users and leapers, and perhaps vertical clingers and leapers. These initial strepsirrhine adaptations were preadaptive for later lemuriform vertical clingers and leapers. In contrast, haplorhine vertical clingers and leapers require additional foot and leg modifications to accommodate a vertical clinging and leaping lifestyle. The movement pattern called vertical clinging and leaping evolved independently among different primate lineages throughout primate evolutionary history for several different ecological reasons.     

Comparative and behavioral analyses of preferred speed: Anolis lizards as a model system

I quantified the movement patterns of eight morphologically and ecologically diverse Caribbean Anolis lizard species in the field to address the following questions: (1) Do these eight species move at preferred speeds, and if so, what are these speeds? (2) What proportion of their maximum sprinting capacities do the anole species use when moving undisturbed? (3) What percentage of the time do lizards spend moving, and how far do they typically travel on a daily basis? (4) Have the preferred speeds of anoles coevolved with structural habitat use? Most of the distributions of speeds were highly skewed, with a preponderance of slow-speed locomotion (<20% of maximum capacity). Median speeds varied almost eightfold among species, from a low of 4.9 cm/s (3.0% of maximum) to a high of 38.0 cm/s (22.4% of maximum). For all eight species, at least 75% of their locomotor movements took place between 0% and 40% of maximum capacity. The eight species varied almost 15-fold in the percentage of time they spent moving, indicating that not all anole species are equally sedentary. Through usage of modern comparative methods, I showed that Anolis species that move slowly through their environments also tend to use narrow perch diameters and have large habitat breadths. These findings show how evolutionary approaches can be profitably integrated with physiological data to understand how species use their habitats.     

Stick or grip? Co-evolution of adhesive toepads and claws in Anolis lizards

Exploring the relationship between phenotype and performance in an ecological and evolutionary context is crucial to understanding the adaptive nature of phenotypic traits. Despite their ubiquity in vertebrates, few studies have examined the functional and ecological significance of claw morphologies. Here we examine the adhesive toepad and claw system of Anolis lizards. Claw characters are significantly different between lizards classified as arboreal (perch height ≥ 1 m) and non-arboreal (perch height < 1 m). Arboreal species possess significantly higher and longer claws, and show trends toward decreased claw curvature and wider claw tip angles. Toepad size and claw length and height are tightly correlated with each other and with perch height, suggesting that the adhesive toepad and gripping claw have co-evolved to accommodate different habitats. The functional morphology and evolution of claws are ripe areas for future investigation.     

Effects of substrate structure on speed and acceleration capacity in climbing geckos

We studied the effects of substrate structure on locomotor performance in a climbing gecko, Hemidactylus garnoti . We quantified three performance traits (acceleration capacity, instantaneous speed, and final speed) on three substrates: (i) smooth wood, (ii) a cloth surface, and (iii) a wire mesh. While acceleration capacity and instantaneous speed were highest on the wooden surface, final speed did not differ significantly among substrates. Using scanning electron microscopy (SEM) pictures, we estimated that 98% of the wooden surface is available for adhesion by the setae on the toepads, while this percentage is much lower for the mesh and cloth (41 and 37%, respectively). We suggest that when a gecko climbs up a gap-filled substrate, such as the wire mesh or cloth, adhesion will only happen between part of the toepad and the substrate, resulting in a diminished acceleration capacity. The higher acceleration capacity on the wooden substrate and the fact that the geckos tend to slip less often on this particular surface, may explain the difference in instantaneous speed. As for final speed, geckos might achieve similar final speeds on all three substrates by employing different locomotor strategies. Our results suggest that microhabitat use in nature might have a profound effect on locomotor performance and survival for climbing lizards such as geckos.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 385–393.     

Geckos as Springs: Mechanics Explain Across-Species Scaling of Adhesion

One of the central controversies regarding the evolution of adhesion concerns how adhesive force scales as animals change in size, either among or within species. A widely held view is that as animals become larger, the primary mechanism that enables them to climb is increasing pad area. However, prior studies show that much of the variation in maximum adhesive force remains unexplained, even when area is accounted for. We tested the hypothesis that maximum adhesive force among pad-bearing gecko species is not solely dictated by toepad area, but also depends on the ratio of toepad area to gecko adhesive system compliance in the loading direction, where compliance (C) is the change in extension (Δ) relative to a change in force (F) while loading a gecko’s adhesive system (C = dΔ/dF). Geckos are well-known for their ability to climb on a range of vertical and overhanging surfaces, and range in mass from several grams to over 300 grams, yet little is understood of the factors that enable adhesion to scale with body size. We examined the maximum adhesive force of six gecko species that vary in body size (~2–100 g). We also examined changes between juveniles and adults within a single species (Phelsuma grandis). We found that maximum adhesive force and toepad area increased with increasing gecko size, and that as gecko species become larger, their adhesive systems become significantly less compliant. Additionally, our hypothesis was supported, as the best predictor of maximum adhesive force was not toepad area or compliance alone, but the ratio of toepad area to compliance. We verified this result using a synthetic “model gecko” system comprised of synthetic adhesive pads attached to a glass substrate and a synthetic tendon (mechanical spring) of finite stiffness. Our data indicate that increases in toepad area as geckos become larger cannot fully account for increased adhesive abilities, and decreased compliance must be included to explain the scaling of adhesion in animals with dry adhesion systems.