Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei

Abstract.— Species of Anolis lizards that use broad substrates have long legs, which provide enhanced maximal sprint speed, whereas species that use narrow surfaces have short legs, which permit careful movements. We raised hatchling A. sagrei in terraria provided with only broad or only narrow surfaces. At the end of the experiment, lizards in the broad treatment had relatively longer hindlimbs than lizards in the narrow treatment. These results indicate that not only is hindlimb length a plastic trait in these lizards, but that this plasticity leads to the production of phenotypes appropriate to particular environments. Comparison to hindlimb lengths of other Anolis species indicates that the range of plasticity is limited compared to the diversity shown throughout the anole radiation. Nonetheless, this plasticity potentially could have played an important role in the early stages of the Caribbean anole radiation.     

Quantification of correlational selection on thermal physiology,thermoregulatory behavior,and energy metabolism in lizards

Phenotypic selection is widely accepted as the primary cause of adaptive evolution in natural populations, but selection on complex functional properties linking physiology, behavior, and morphology has been rarely quantified. In ectotherms, correlational selection on thermal physiology, thermoregulatory behavior, and energy metabolism is of special interest because of their potential coadaptation. We quantified phenotypic selection on thermal sensitivity of locomotor performance (sprint speed), thermal preferences, and resting metabolic rate in captive populations of an ectothermic vertebrate, the common lizard, Zootoca vivipara. No correlational selection between thermal sensitivity of performance, thermoregulatory behavior, and energy metabolism was found. A combination of high body mass and resting metabolic rate was positively correlated with survival and negatively correlated with fecundity. Thus, different mechanisms underlie selection on metabolism in lizards with small body mass than in lizards with high body mass. In addition, lizards that selected the near average preferred body temperature grew faster that their congeners. This is one of the few studies that quantifies significant correlational selection on a proxy of energy expenditure and stabilizing selection on thermoregulatory behavior.     

Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace

Caribbean Anolis lizards are often cited as a textbook example of adaptive radiation. Similar morphologies (ecomorphs) have originated in similar ecological settings on different large islands in the West Indies. However, relatively little is known about one of the morphologically most specialized and divergent ecomorphs: the twig anoles. Here, we investigate aspects of morphology, dewlap size, locomotor and bite performance, structural habitat and diet of the poorly known twig anole, Anolis sheplani from Hispaniola. Few observations have previously been made of this species in its natural habitat, and few quantitative data on its natural history are available. A. sheplani is an extreme twig anole with respect to its morphology, performance capacities, and ecological niche. Males and females of this species do not differ from each other in body dimensions, performance or habitat use, but males do have a bigger dewlap than females. We present data for 25 individuals and compare them with data for other Greater Antillean anoles. It becomes apparent that twig anoles constitute a large component of the morphological, functional, and ecological diversity of Anolis lizards. Small twig anoles such as A. sheplani appear to be pushing the boundaries of morphospace and are thus crucial in our understanding of the evolution of phenotypic diversity.     

An intraspecific analysis of trade-offs in sprinting performance in a West Indian lizard species (Anolis lineatopus)

We examined whether a trade-off exists in sprinting ability among individuals within the Caribbean lizard Anolis lineatopus. Specifically, we made the following predictions: Longer-legged (relative to body size) individual lizards should sprint faster than shorter-legged lizards on a broad (5.1 cm diameter) rod. However, longer-legged lizards should also decline in sprinting performance to a greater extent than shorter-legged lizards when sprinting on rods of different diameters. To test these predictions, we examined morphology and sprinting performance in adult male, adult female and juvenile A. lineatopus. As predicted, longer-legged lizards are faster sprinters than shorter-legged lizards on the broad substrate, but they also decline more in speed between the broad and narrow (0.7 cm diameter) dowel. However, despite statistically significant morphological differences among intraspecific classes, differences in morphology did not result in differences in sprinting performance among intraspecific classes, with the exception that larger lizards run faster than smaller lizards on each dowel size.     

Probing the adaptive landscape using experimental islands: density-dependent natural selection on lizard body size

Anolis lizards in the Greater Antilles are thought to have diversified through natural selection on body size and shape, presumably due to interspecific competition and variation in locomotor performance. Here we measure natural selection on body size over three years and across seven replicate populations of the brown anole, A. sagrei. We experimentally manipulated an important component of the environment (population density) on several small islands to test the role of density in driving natural selection. Results indicate that the strength of natural selection was proportional to population density (r2 = 0.81), and favored larger body sizes at higher density, presumably owing to the enhanced competitive ability afforded by large size. Changes in the distribution of body size by selective releases of lizards to islands show that this effect did not arise by pure density dependence, since smaller individuals were disproportionately selected against at higher densities. We measured significant broad sense heritability for body size in the laboratory (h2 = 0.55) indicating that selection in the wild could have an evolutionary response. Our results suggest an important effect of population density on natural selection in Anolis lizards.     

The quick and the fast: the evolution of acceleration capacity in Anolis lizards

Although of prime ecological relevance, acceleration capacity is a poorly understood locomotor performance trait in terrestrial vertebrates. No empirical data exist on which design characteristics determine acceleration capacity among species and whether these design traits influence other aspects of locomotor performance. In this study we explore how acceleration capacity and sprint speed have evolved in Anolis lizards. We investigate whether the same or different morphological traits (i.e., limb dimensions and muscle mass) correlate with both locomotor traits. Within our sample of Anolis lizards, relative sprint speed and acceleration capacity coevolved. However, whereas the variation in relative acceleration capacity is primarily explained by the variation in relative knee extensor muscle mass, the variation in relative sprint speed is correlated to the variation in relative femur, tibia, and metatarsus length as well as knee extensor muscle mass. The fact that the design features required to excel in either performance trait partly overlap might explain the positive correlation between the variation in relative sprint speed and acceleration capacity. Furthermore, our data show how similar levels of sprint performance can be achieved through different morphological traits (limb segment lengths and muscle mass) suggesting that redundant mapping has potentially played a role in mitigating trade-offs.     

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.     

Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a population-level analysis

Recent ecomorphological studies have shown that the predicted correlations between morphology and ecology on broad taxonomic levels are often obscured when comparing more closely related groups. Among species, comparisons of lizards often indicate very little support for adaptive radiations into novel habitats. As few population level studies have been performed, we compared body, head and limb shape between four populations of Urosaurus ornatus living in structurally distinct habitats (cliffs, rocks, trees and boulders). Surprisingly, clear correlations between habitat use and body shape among populations were found, most of which were in good accordance with a priori biomechanical predictions (e.g. flat body and head for extreme climbers; long distal hindlimb segments for jumpers and runners; narrow body and long tail for tree dwelling lizards). This indicates that populations of Urosaurus ornatus are seemingly 'adapted' to the habitat they live in. However, quantification of performance and behaviour are needed to determine the adaptive nature of these observations.     

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.     

An experimental test of the role of predators in the maintenance of a genetically based polymorphism

Polymorphisms provide one of the most useful tools for understanding the maintenance of genetic and phenotypic variation in nature. We have previously described a genetically based polymorphism in dorsal patterning that is expressed by female brown anole lizards, Anolis sagrei, which occur in Bar, Diamond and intermediate Diamond-Bar morphs. Previous studies of island populations in The Bahamas support a role for selection in maintaining the polymorphism, but the agents responsible for this selection remain unclear. We tested two main hypotheses regarding the importance of predation as a selective agent that maintains the polymorphism within populations. First, we tested whether correlational selection favours different combinations of morph, locomotor performance and escape behaviour by measuring morph-specific natural selection on sprint speed, running endurance and the propensity of females to either 'freeze' or 'run' in response to attempted capture. Morphs did not differ in any of these traits, nor did correlational selection consistently favour any particular combinations of morph and antipredator behaviour. Second, we experimentally excluded bird and snake predators from two entire island populations, allowed these predators access to two additional islands and then measured subsequent differences in natural selection on morphs in each population. Predators reduced the survival of Bar and Diamond females, but not of genetically intermediate Diamond-Bar females. These results provide limited evidence that predation may play a role in maintaining this polymorphism, although the functional traits that could account for differential susceptibility to predation remain unclear.     

EVOLUTION OF SPRINT SPEED IN LACERTID LIZARDS: MORPHOLOGICAL,PHYSIOLOGICAL, AND BEHAVIORAL COVARIATION

Organismal performance abilities occupy a central position in phenotypic evolution; they are determined by suites of interacting lower-level traits (e.g., morphology and physiology) and they are a primary focus of natural selection. The mechanisms by which higher levels of organismal performance are achieved during evolution are therefore fundamentally important for understanding correlated evolution in general and coadaptation in particular. Here we address correlated evolution of morphological, physiological, and behavioral characteristics that influence interspecific variation in sprint speed in a clade of lacertid lizards. Phylogenetic analyses using independent contrasts indicate that the evolution of high maximum sprinting abilities (measured on a photocell-timed racetrack) has occurred via the evolution of (1) longer hind limbs relative to body size, and (2) a higher physiologically optimum temperature for sprinting. For ectotherms, which experience variable body temperatures while active, sprinting abilities in nature depend on both maximum capacities and relative performance levels (i.e., percent of maximum) that can be attained. With respect to temperature effects, relative performance levels are determined by the interaction between thermal physiology and thermoregulatory behavior. Among the 13 species or subspecies of lizards in the present study, differences in the optimal temperature for sprinting (body temperature at which lizards run fastest) closely matched interspecific variation in median preferred body temperature (measured in a laboratory photothermal gradient), indicating correlated evolution of thermal physiology and thermal preferences. Variability of the preferred body temperatures maintained by each species is, across species, negatively correlated with the thermal-performance breadth (range of body temperatures over which lizards can run relatively fast). This pattern leads to interspecific differences in the levels of relative sprint speed that lizards are predicted to attain while active at their preferred temperatures. The highest levels of predicted relative performance are achieved by species that combine a narrow, precise distribution of preferred temperatures with the ability to sprint at near-maximum speeds over a wide range of body temperatures. The observed among-species differences in predicted relative speed were positively correlated with the interspecific variation in maximum sprinting capacities. Thus, species that attain the highest maximum speeds are (1) also able to run at near-maximum levels over a wide range of temperatures and (2) also maintain body temperatures within a narrow zone near the optimal temperature for sprinting. The observed pattern of correlated evolution therefore has involved traits at distinct levels of biological organization, that is, morphology, physiology, and behavior; and trade-offs are not evident. We hypothesize that this particular trait combination has evolved in response to coadaptational selection pressures. We also discuss our results in the context of possible evolutionary responses to global climatic change.     

Is Habitat Preference Associated with Locomotor Performance in Multiocellated Racerunners(Eremias multiocellata) from a Desert Steppe?

Locomotor performance in lizards is strongly affected by structural habitat. Understanding this relationship allows us to predict species distributions across habitat types. However, little information is available about the ecological role of the locomotion of multiocellated racerunner(Eremias multiocellata) in the desert steppe ecosystem of Inner Mongolia, China. Herein, we studied the effects of habitat structure on the locomotor performance of this lizard species in the field. We found that the sprint speed of this lizard declined significantly with increasing vegetation coverage. Manipulative experiments were further conducted to examine the effects of branch barriers and surface substrates on the sprint speed of the lizard. We found that the sprint speed was significantly influenced by the surface substrates and branch barriers, and there were no interactions between them. Branch barriers impeded sprint speed, and E. multiocellata showed better locomotor performance on sandy rather than loamy substrates. Our results indicate that E. multiocellata tends to occupy open areas with sandy substrates, but its locomotor performance is not closely associated with habitat preference.     

Experimentally replicated disruptive selection on performance traits in a Caribbean lizard

A central theme underlying studies of adaptive radiation is that ecologically mediated selection drives diversification. However, demonstrating the ecological basis of natural selection and linking this process to patterns of morphological diversity represents a formidable challenge. This is because selection experiments that test correlations between an organism's phenotype and its ecology are difficult to perform in the wild. Previous studies of Anolis lizards have shown that divergent morphologies are correlated with habitat use and have evolved repeatedly on islands throughout the Greater Antilles. Here, we show that the forms of selection acting within a species support an ecological mechanism for diversification. In natural populations, performance-related traits such as limb length are subject to correlational and disruptive selection driven by differences in habitat use. Experimental manipulations in the wild verify the same pattern of selection and indicate that both the targets and forms of selection are consistent through time. Elsewhere, we have demonstrated that these traits are heritable and should therefore evolve in response to selection. Our results provide evidence for the short-term repeatability of selection and its potency in the diversification of anoles.     

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.     

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.     

Effect of locomotor approach on feeding kinematics in the green anole (Anolis carolinensis)

Squamates are well-known models for studying to examine locomotor and feeding behaviors in tetrapods, but studies that integrate both behavioral activities remain scarce. Anolis lizards are a classical lineage to study the evolutionary relationships between locomotor behavior and complex structural features of the habitat. Here, we analyzed prey-capture behavior in one representative arboreal predator, Anolis carolinensis, to demonstrate the functional links between locomotor strategies and the kinematics of feeding. A. carolinensis uses two strategies to catch living insects on perches: Head-Up Capture and Jump Capture. In both cases, lizards use lingual prehension to capture the prey and the kinematic patterns of the trophic apparatus are not significantly influenced by the selected strategies. Therefore, to capture one prey type, movements of the trophic structures are highly fixed and A. carolinensis modulates the locomotor pattern to exploit the environment. Predation behavior in A. carolinensis integrates two different behavioral patterns: locomotor plasticity of prey-approach and biomechanical stereotypy of tongue prehension to successfully capture the prey.     

Cranial morphology and bite force in Chamaeleolis lizards--adaptations to molluscivory?

Anolis lizards have become a model system for the study of adaptive radiations as species with similar morphologies occupying similar habitats have arisen independently on all the larger islands in the Caribbean. However, on both, Cuba and Hispaniola unique forms have evolved that seemingly have no counterparts on any of the other Caribbean islands. Anoles of the genus Chamaeleolis comprise such a unique form and have been termed 'twig giants' because of their cryptic life style, slow locomotor mode, and short limbs. However, some of the most unusual features of these lizards are their large heads and molluscivorous diet. Here, we compare head shape, bite force, and muscle structure among sexes and age classes of Chamaeleolis lizards with Anolis crown giants. Our data show that Chamaeleolis lizards have a dramatically different head shape characterized by tall heads with a pronounced temporal ridge and long snouts. Analyses of bite force, surprisingly, show no differences between adult Chamaeleolis and Anolis crown giants. Juveniles of Chamaeleolis, however, have very tall heads for their size and bite harder than Anolis juveniles do. This can be related to the propensity of juveniles of this genus to eat snails, food items for which high bite forces are crucial. This observation is corroborated by the presence of well-developed jaw adductors in juveniles. Thus, our data suggest that the unusual phenotype of adults with large and tall heads may be due to selection on the juvenile life history stages.     

Locomotor compensation creates a mismatch between laboratory and field estimates of escape speed in lizards: a cautionary tale for performance-to-fitness studies

A key assumption in evolutionary studies of locomotor adaptation is that standard laboratory measures of performance accurately reflect what animals do under natural circumstances. One widely examined measure of performance is maximum sprint speed, which is believed to be important for eluding predators, capturing prey, and defending territories. Previous studies linking maximum sprint speed to fitness have focused on laboratory measurements, and we suggest that such analyses may be appropriate for some species and intraspecific classes, but not others. We provide evidence for a general inverse relationship between maximum laboratory sprint speed and the percentage of maximum capacity that animals use when escaping from a threat in the field (the model of locomotor compensation). Further, absolute values of field escape speed and maximum laboratory speed are not significantly related when comparing across a diverse group of Anolis and lacertid lizards. We show that this pattern of locomotor compensation holds both within (i.e., among intraspecific classes) and among lizard species (with some exceptions). We propose a simple method of plotting field escape speed (y-axis) versus maximum laboratory speed (x-axis) among species and/or intraspecific classes that allows researchers to determine whether their study organisms are good candidates for relating laboratory performance to fitness. We suggest that species that reside directly on, or near the "best fitness line" (field escape speed = maximum laboratory speed) are most likely to bear fruit for such studies.     

The relevance of morphology for habitat use and locomotion in two species of wall lizards

Understanding if morphological differences between organisms that occupy different environments are associated to differences in functional performance can suggest a functional link between environmental and morphological variation. In this study we examined three components of the ecomorphological paradigm – morphology, locomotor performance and habitat use – using two syntopic wall lizards endemic to the Iberian Peninsula as a case study to establish whether morphological variation is associated with habitat use and determine the potential relevance of locomotor performance for such an association. Differences in habitat use between both lizards matched patterns of morphological variation. Indeed, individuals of Podarcis guadarramae lusitanicus, which are more flattened, used more rocky environments, whereas Podarcis bocagei, which have higher heads, used more vegetation than rocks. These patterns translated into a significant association between morphology and habitat use. Nevertheless, the two species were only differentiated in some of the functional traits quantified, and locomotor performance did not exhibit an association with morphological traits. Our results suggest that the link between morphology and habitat use is mediated by refuge use, rather than locomotor performance, in this system, and advise caution when extrapolating morphology-performance-environment associations across organisms.     

Experimental analysis of retreat‐site selection by thick‐tailed geckos Nephrurus milii

Abstract Although animals use habitats non‐randomly in the wild, complex correlations among environmental features mean that proximate influences on habitat selection can be identified only by experimental manipulation of potential cues. Thick‐tailed geckos Nephrurus milii are large lizards that are widely distributed through southern Australia. These nocturnally active animals typically spend daylight hours under surface rocks. We presented captive geckos with alternative retreat‐sites (rock crevices) differing in attributes potentially relevant to habitat selection. The lizards showed strong preference for shelter‐sites that enhanced thermoregulation (warm rather than cool) and that reduced the animal's vulnerability to predators (narrow crevices with small openings and not containing the scent of a predatory snake). Horizontal rather than sloping crevices were also preferred. Overall crevice size and thickness of the overlying rock did not influence retreat‐site selection in the laboratory, but could be important in the field because of their influence on thermal regimes under rocks. The present study supports the idea that nocturnal reptiles base their selection of diurnal shelters on multiple aspects related to the fitness consequences of occupancy of alternative available retreat‐sites.