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.     

Rock-dwelling lizards exhibit less sensitivity of sprint speed to increases in substrate rugosity

Effectively moving across variable substrates is important to all terrestrial animals. The effects of substrates on lizard performance have ecological ramifications including the partitioning of habitat according to sprinting ability on different surfaces. This phenomenon is known as sprint sensitivity, or the decrease in sprint speed due to change in substrate. However, sprint sensitivity has been characterized only in arboreal Anolis lizards. Our study measured sensitivity to substrate rugosity among six lizard species that occupy rocky, sandy, and/or arboreal habitats. Lizards that use rocky habitats are less sensitive to changes in substrate rugosity, followed by arboreal lizards, and then by lizards that use sandy habitats. We infer from comparative phylogenetic analysis that forelimb, chest, and tail dimensions are important external morphological features related to sensitivity to changes in substrate rugosity.     

The evolution of armament strength: evidence for a constraint on the biting performance of claws of durophagous decapods

Performance data for the claws of six sympatric species of Cancer crabs confirmed a puzzling pattern reported previously for two other decapod crustaceans (stone crabs, Menippe mercenaria, and lobsters, Homarus americanus): Although biting forces increased, maximum muscle stresses (force per unit area) declined with increasing claw size. The negative allometry of muscle stress and the stress at a given claw size were fairly consistent within and among Cancer species despite significant differences in adult body size and relative claw size, but were not consistent among decapod genera. Therefore, claw height can be used as a reliable predictor of maximum biting force for the genus Cancer, but must be used with caution as a predictor of maximum biting force in wider evolutionary and biogeographical comparisons of decapods. The decline in maximum muscle stress with increasing claw size in Cancer crabs contrasts with the pattern in several other claw traits. Significantly, three traits that affect maximal biting force increased intraspecifically with increasing claw size: relative claw size, mechanical advantage, and sarcomere length of the closer muscle. Closer apodeme area and angle of pinnation of the closer muscle fibers varied isometrically with claw size. The concordant behavior of these traits suggests selection for higher biting forces in larger crabs. The contrast between the size dependence of muscle stress (negative allometry) and the remaining claw traits (isometry or positive allometry) strongly suggests that an as yet unidentified constraint impairs muscle performance in larger claws. The negative allometry of muscle stress in two distantly related taxa (stone crabs and lobsters) further suggests this constraint may be widespread in decapod crustaceans. The implications of this performance constraint for the evolution of claw size and the "arms-race" between decapod predators and their hard-shelled prey is discussed.     

SPEED AND STAMINA TRADE-OFF IN LACERTID LIZARDS

Abstract.— Morphological and physiological considerations suggest that sprinting ability and endurance capacity put conflicting demands on the design of an animal's locomotor apparatus and therefore cannot be maximized simultaneously. To test this hypothesis, we correlated size‐corrected maximal sprint speed and stamina of 12 species of lacertid lizards. Phylogenetically independent contrasts of sprint speed and stamina showed a significant negative relationship, giving support to the idea of an evolutionary trade‐off between the two performance measures. To test the hypothesis that the trade‐off is mediated by a conflict in morphological requirements, we correlated both performance traits with snout‐vent length, size‐corrected estimates of body mass and limb length, and relative hindlimb length (the residuals of the relationship between hind‐ and forelimb length). Fast‐running species had hindlimbs that were long compared to their forelimbs. None of the other size or shape variables showed a significant relationship with speed or endurance. We conclude that the evolution of sprint capacity may be constrained by the need for endurance capacity and vice versa, but the design conflict underlying this trade‐off has yet to be identified.     

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.     

The comparative evolution of lizard claw and toe morphology and clinging performance

In this study, I utilize the expected functional relationships between claw and toe morphology and clinging performance as a basis for examining evolutionary trends across 85 lizard taxa from 13 families. After controlling for body size and phylogeny, multivariate comparisons indicate that several aspects of claw and toe morphology are correlated with clinging performance. Specifically, evolutionary increases in claw curvature, toe width and adhesive lamella number are correlated with increases in clinging performance on smooth substrates. Furthermore, evolutionary increases in claw height and decreases in toe length are correlated with increases in clinging performance on rough substrates. Sensitivity analyses revealed that changes in both branch lengths and procedural order of correction for body size and phylogeny do not generally have an effect on phylogenetic comparisons. These results demonstrate that the evolution of claw and toe morphology is correlated with the evolution of clinging performance across a wide range lizard taxa.     

THE EVOLUTION OF FORM AND FUNCTION: MORPHOLOGY AND LOCOMOTOR PERFORMANCE IN WEST INDIAN ANOLIS LIZARDS

I tested biomechanical predictions that morphological proportions (snout–vent length, forelimb length, hindlimb length, tail length, and mass) and maximal sprinting and jumping ability have evolved concordantly among 15 species of Anolis lizards from Jamaica and Puerto Rico. Based on a phylogenetic hypothesis for these species, the ancestor reconstruction and contrast approaches were used to test hypotheses that variables coevolved. Evolutionary change in all morphological and performance variables scales positively with evolution of body size (represented by snout–vent length); size evolution accounts for greater than 50% of the variance in sprinting and jumping evolution. With the effect of the evolution of body size removed, increases in hindlimb length are associated with increases in sprinting and jumping capability. When further variables are removed, evolution in forelimb and tail length exhibits a negative relationship with evolution of both performance measures. The success of the biomechanical predictions indicates that the assumption that evolution in other variables (e.g., muscle mass and composition) did not affect performance evolution is probably correct; evolution of the morphological variables accounts for approximately 80% of the evolutionary change in performance ability. In this case, however, such assumptions are clade-specific; extrapolation to taxa outside the clade is thus unwarranted. The results have implications concerning ecomorphological evolution. The observed relationship between forelimb and tail length and ecology probably is a spurious result of the correlation between these variables and hindlimb length. Further, because the evolution of jumping and sprinting ability are closely linked, the ability to adapt to certain microhabitats may be limited.     

Running in cold weather: morphology, thermal biology, and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatus section: Liolaemini: Iguania)

The integration or coadaptation of morphological, physiological, and behavioral traits is represented by whole-organism performance traits such as locomotion or bite force. Additionally, maximum sprint speed is a good indicator of whole-organism performance capacity as variation in sprinting ability can affect survival. We studied thermal biology, morphology, and locomotor performance in a clade of Liolaemus lizards that occurs in the Patagonian steppe and plateaus, a type of habitat characterized by its harsh cold climate. Liolaemus of the lineomaculatus section display a complex mixture of conservative and flexible traits. The phylogenetically informed analyses of these ten Liolaemus species show little coevolution of their thermal traits (only preferred and optimum temperatures were correlated). With regard to performance, maximum speed was positively correlated with optimum temperature. Body size and morphology influenced locomotor performance. Hindlimbs are key for maximal speed, but forelimb length was a better predictor for sustained speed (i.e. average speed over a total distance of 1.2?m). Finally, sustained speed differed among species with different diets, with herbivores running on average faster over a long distance than omnivores.     

Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer)

Many mammals dig, either during foraging to access subsurface food resources, or in creating burrows for shelter. Digging requires large forces produced by muscles and transmitted to the soil via the skeletal system; thus fossorial mammals tend to have characteristic modifications of the musculoskeletal system that reflect their digging ability. Bandicoots (Marsupialia: Peramelidae) scratch-dig mainly to source food, searching for subterranean food items including invertebrates, seeds, and fungi. They have musculoskeletal features for digging, including shortened, robust forelimb bones, large muscles, and enlarged muscle attachment areas. Here, we compared changes in the ontogenetic development of muscles associated with digging in the Quenda (Isoodon fusciventer). We measured muscle mass (m _m), pennation angle, and fiber length (FL) to calculate physiological cross-sectional area (PCSA; a proxy of maximum isometric force) as well as estimate the maximum isometric force (Fmax) for 34 individuals ranging in body size from 124 to 2,390 g. Males grow larger than females in this bandicoot species, however, we found negligible sex differences in mass-specific m _m, PCSA or FL for our sample. Majority of the forelimb muscles PCSA showed a positive allometric relationship with total body mass, while m _m and FL in the majority of forelimb muscles showed isometry. Mechanical similarity was tested, and two thirds of forelimb muscles maximum isometric forces (Fmax) scaled with isometry; therefore the forelimb is primarily mechanical similar throughout ontogeny. PCSA showed a significant difference between scaling slopes between main movers in the power stroke, and main movers of the recovery stroke of scratch-digging. This suggests that some forelimb muscles grow with positive allometry, specially these associated with the power stroke of digging. Intraspecific variation in PCSA is rarely considered in the literature, and thus this is an important study quantifying changes in muscle architectural properties with growth in a mammalian model of scratch-digging.     

青藏高原褐背拟地鸦表型特征的性别差异与地理变异

将数值分类用于鸟类分类学研究时,对于雌雄的形态特征差异没有被重视,尤其是对于雌雄同形的鸟类。本文以雌雄同形的褐背拟地鸦Pseudopodoces humilis为材料,运用SPSSl0．0FORwINDOwS统计分析软件对108号褐背拟地鸦标本(51♀♀,57♂♂)的数量性状(体长、跗跖长、翅长、尾长、嘴宽、嘴高、上喙长、下喙长、嘴裂、第3趾爪长、第1趾爪长)的原始数据进行分析,结果表明雌、雄性状在翅长(n＝51,P＝0．012)和嘴高(n＝57,P＝0．043)上有明显差异,但在体长、跗跖长、尾长、嘴宽、上喙长、下喙长、嘴裂、第3趾爪长、第1趾爪长等数值特征上却没有明显的差异。所以在以后对于褐背拟地鸦的地理种群变异和亚种分化的研究中,翅长和嘴高两特征应该根据雌雄分别讨论。通过对不同性状量度和纬度的相关回归分析,发现在测量标本所涉及的采集地范围内,即主要在青藏高原东南部地区,褐背拟地鸦体长和雄乌的翅长在地理分布上随纬度的增加而变小,而其它性状特征没有明显的地理分布纬度上的变化。     

Ontogenetic scaling of bite force in lizards and turtles

Because selection on juvenile life-history stages is likely strong, disproportionately high levels of performance (e.g., sprint speed, endurance, etc.) might be expected. Whereas this phenomenon has been demonstrated with respect to locomotor performance, data for feeding are scarce. Here, we investigate the relationships among body dimensions, head dimensions, and bite force during growth in lizards and turtles. We also investigate whether ontogenetic changes in bite performance are related to changes in diet. Our analyses show that, for turtles, head dimensions generally increase with negative allometry. For lizards, heads scale as expected for geometrically growing systems. Bite force generally increased isometrically with carapace length in turtles but showed significant positive allometry relative to body dimensions in lizards. However, both lizards and turtles display positive allometric scaling of bite force relative to some measures of head size throughout ontogeny, suggesting (1) strong selection for increased relative bite performance with increasing head size and (2) intrinsic changes in the geometry and/or mass of the jaw adductors during growth. Whereas our data generally do not provide strong evidence of compensation for lower absolute levels of performance, they do show strong links among morphology, bite force, and diet during growth.     

Self-Drying: A Gecko's Innate Ability to Remove Water from Wet Toe Pads

When the adhesive toe pads of geckos become wet, they become ineffective in enabling geckos to stick to substrates. This result is puzzling given that many species of gecko are endemic to tropical environments where water covered surfaces are ubiquitous. We hypothesized that geckos can recover adhesive capabilities following exposure of their toe pads to water by walking on a dry surface, similar to the active self-cleaning of dirt particles. We measured the time it took to recover maximum shear adhesion after toe pads had become wet in two groups, those that were allowed to actively walk and those that were not. Keeping in mind the importance of substrate wettability to adhesion on wet surfaces, we also tested geckos on hydrophilic glass and an intermediately wetting substrate (polymethylmethacrylate; PMMA). We found that time to maximum shear adhesion recovery did not differ in the walking groups based on substrate wettability (22.7±5.1 min on glass and 15.4±0.3 min on PMMA) but did have a significant effect in the non-walking groups (54.3±3.9 min on glass and 27.8±2.5 min on PMMA). Overall, we found that by actively walking, geckos were able to self-dry their wet toe pads and regain maximum shear adhesion significantly faster than those that did not walk. Our results highlight a unexpected property of the gecko adhesive system, the ability to actively self-dry and recover adhesive performance after being rendered dysfunctional by water.     

Morphological Variation of the Forelimb and Claw in Neotropical Sigmodontine Rodents (Rodentia: Cricetidae)

The limbs of mammals exhibit a variety of morphologies that reflect the diversity of their habitats and their functional needs, including subtle structural differences in their distal limb integumentary appendages (hooks, claws, adhesive pads). Little is known about structure and function of claws of sigmodontine rodents. Here, we analyze claw shape and forelimb skeleton morphology of 25 species of sigmodontine rodents with different locomotory types (ambulatory, fossorial, natatorial, quadrupedal saltatorial, and scansorial), taking into account their phylogenetic affinities. Qualitative differences in claw shape were examined using digital photographs, and quantitative measurements were made for length, height, and curvature of the claws of all digits, and dimensions of other forelimb skeletal elements. Our results show that both phylogeny and ecological categories explain substantial components of the morphological variation in sigmodontine rodents. Qualitative analysis reveals that non-specialized forms (ambulatory, quadrupedal saltatorial, and scansorial) tend to have high and strongly curved claws, whereas highly specialized forms (fossorial and natatorial) tend to have elongate and smoothly curved claws. However, the quantitative analysis differentiated the fossorial and scansorial by variables related to claw, and natatorial by variables related to bones of the forelimb. No variables that could differentiate ambulatory or quadrupedal saltatorial forms were found, demonstrating that these forms show a generalized morphological pattern. This study indicates that both historical and ecological factors contribute to the evolution of claw length in these groups.     

Size,but not sex,predicts pinch force and exoskeleton mechanical properties in crayfish of the genus Faxonius

Studies of animal weaponry and defensive structures rarely take into consideration their underlying mechanical properties. We measured the compressive strength and thickness of the exoskeleton of the claw (chela) in two North American crayfish species, Faxonius virilis and F. limosus. We performed similar measures on the carapace, a body region not directly involved in agonistic contests. Males of both species generated significantly stronger maximum pinch forces than females. However, these differences can be attributed to differences in claw size between the sexes. The thickness (ultrastructure) of the claw exoskeleton was a significant predictor of its compressive strength and likely explained the difference in compressive strength we observed between the two species. Neither claw thickness nor claw compressive strength was correlated with maximum pinch force. Additionally, we found that crayfish body size was a strong predictor of carapace compressive strength and thickness, whereas sex was not. The claw had greater compressive strength and thickness than the corresponding values for the carapace. Our study shows that the mechanical properties of the crayfish exoskeleton are largely a function of size and highlights the need to integrate mechanical properties into studies of animal morphology and performance.     

Limb and tail lengths in relation to substrate usage in Tropidurus lizards

A close relationship between morphology and habitat is well documented for anoline lizards. To test the generality of this relationship in lizards, snout-vent, tail, and limb lengths of 18 species of Tropidurus (Tropiduridae) were measured and comparisons made between body proportions and substrate usage. Phylogenetic analysis of covariance by computer simulation suggests that the three species inhabiting sandy soils have relatively longer feet than do other species. Phylogenetic ANCOVA also demonstrates that the three species inhabiting tree canopies and locomoting on small branches have short tails and hind limbs. These three species constitute a single subclade within the overall Tropidurus phylogeny and analyses with independent contrasts indicate that divergence in relative tail and hind limb length has been rapid since they split from their sister clade. Being restricted to a single subclade, the difference in body proportions could logically be interpreted as either an adaptation to the clade's lifestyle or simply a nonadaptive synapomorphy for this lineage. Nevertheless, previous comparative studies of another clade of lizards (Anolis) as well as experimental studies of Sceloporus lizards sprinting on rods of different diameters support the adaptive interpretation.     

Metabolic rate and endurance capacity in Australian varanid lizards (Squamata: Varanidae: Varanus)

In ecomorphological and ecophysiological studies, locomotor performance is often considered to be an intermediate step between the form of an organism and its environment. We examined this premise by measuring morphology, physiology and circular track endurance in the closely related group of Australian varanid lizards. Body size, body mass and relative body proportions were poor indicators of endurance. Body mass was not correlated with endurance and size-free lower forelimb length had only a weak relationship with endurance. Instead, maximal metabolic rate was positively correlated with endurance capacity in varanids. A comparison of varanids with other groups of lizards supported this result as varanids showed both elevated maximal metabolic rate and elevated endurance scores when compared with similar sized non-varanid lizards. There was support for a strong association between endurance with foraging mode and climate. Varanid species with higher endurance tended to be widely foraging and from xeric climates, while sit-and-wait and mesic species showed reduced endurance.   © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 664–676.     

Curvature facilitates prey fixation in predatory insect claws

Insects show a large variety in prey capture strategies, with a correspondingly large diversity in predatory adaptations. We studied a specific type of predatory claws, these can for example be found in praying mantis species. The claw is closeable over its entire length and the prey is fixed between the femur (upper arm) and the tibia (lower arm) of the insect leg. The morphology of these predatory claws is diverse. Some species have straight claws covered with spines, while other species have smooth, curved claws. We have studied the mechanics of this femur-tibia type of predatory insect claws, by making a physical model, eventually trying to explain why in some insect species the claws are curved instead of straight. The main results are (1) when comparing curved claws to straight claws, curvature leads to a strong reduction of forces driving the prey away from the pivoting point, thereby reducing the need for friction generating structures. (2) In the curved claw model a position exists where the resulting force on the prey is exactly zero. This is because the normal forces on the femur and tibia are opposed, and in line. At this position the prey is perfectly clamped and not driven out of the claw. This feature does not exist in straight claws. (3) In the curved claw, the prey cannot be placed at a position further than a certain maximum distance from the pivoting point. Near this maximum position, the resulting force on the prey reaches high values because moment arms are near zero. (4) Between the zero position and the maximum position the resulting force is directed toward the pivoting point, which stabilizes prey fixation.     

Is dietary niche breadth linked to morphology and performance in Sandveld lizards Nucras (Sauria: Lacertidae)?

The functional characteristics of prey items (such as hardness and evasiveness) have been linked with cranial morphology and performance in vertebrates. In lizards particularly, species with more robust crania generally feed on harder prey items and possess a greater bite force, whereas those that prey on evasive prey typically have longer snouts. However, the link between dietary niche breadth, morphology, and performance has not been explicitly investigated in lizards. The southern African genus Nucras was used to investigate this link because the species exhibit differing niche breadth values and dietary compositions. A phylogeny for the genus was established using mitochondrial and nuclear markers, and morphological clusters were identified. Dietary data of five Nucras species, as reported previously, were used in correlation analyses between cranial shape (quantified using geometric morphometrics) and dietary niche breadth, and the proportion of hard prey taken and bite force capacity. Dietary niche breadth and the proportion of hard prey eaten were significantly related to cranial shape, although not once phylogeny was accounted for using a phylogenetic generalized least squares regression. The proportion of evasive prey eaten was a significant predictor of forelimb length when phylogeny was taken into account. We conclude that, in Nucras, the percentage of evasive prey taken co‐evolves with forelimb morphology, and dietary niche breadth co‐evolves with cranial shape. However, although head width is correlated with the proportion of hard prey eaten, this appears to be the result of shared ancestry rather than adaptive evolution. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 674–688.     

Evolutionary approaches for studying functional morphology: examples from studies of performance capacity

Performance studies have long been a cornerstone of evolutionarystudies of adaptation because of their purported importancefor fitness. Nevertheless, for most systems, the mechanisticlink among habitat use, morphology and performance is poorlyunderstood. Further, few studies consider how behavior affectsthe relationship between morphology and performance. Here, Ihighlight the utility of considering both of these neglectedareas by discussing studies in two systems: (1) the evolutionof habitat use in Caribbean Anolis lizards, and (2) the evolutionof limb function in desert lizards. Caribbean Anolis lizardspartition the habitat via selection of different perch diameters,and surface diameter also exerts a strong effect on locomotorperformance. Phylogenetic analyses show that Anolis speciestend to avoid using perches in which their performance is submaximal,and also show that species with large performance breadths usea greater range of habitats. The underlying basis of this performanceto habitat use link is a trade-off between the ability to sprintquickly on broad surfaces and the ability to move effectivelyon narrow surfaces. Studies of the kinematics of high-speedlocomotion in five morphologically distinct lizard species revealthat some species exhibited behaviors that greatly enhancedtheir performance abilities relative to other species, suggestingthat behavior can play a key role in the link between morphologyand performance. Overall, these findings underscore the valueof using a mechanistic approach for studying the links betweenhabitat use, morphology and behavior.