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.     

Beyond black and white: divergent behaviour and performance in three rapidly evolving lizard species at White Sands

Determining which traits enable organisms to colonize and persist in new environments is key to understanding adaptation and ecological speciation. New environments can present novel selective pressures on colonists' morphology, behaviour, and performance, collectively referred to as ecomorphology. To investigate ecomorphological change during adaptation and incipient ecological speciation, we measured differences in morphology (body shape and size), behaviour (startle response), and performance (sprint speed) in three New Mexican lizard species: Holbrookia maculata, Sceloporus undulatus, and Aspidoscelis inornata. Each species is represented by dark morphs, cryptic on the brown adobe soils of the Chihuahuan Desert, and white morphs, cryptic on the gypsum substrate of White Sands. For each species, we then determined the effects of morphology and startle response on sprint speed on matched and mismatched substrate. For two of the three species, white morphs had larger body size and longer limbs. However, we found no statistical evidence that these morphological differences affected sprint speed. Colour morphs also exhibited different escape responses on the two substrates: in all species, dark morphs were less likely to immediately sprint from a simulated predator on white sand. As a result, escape response had a significant effect on sprint speed for two of the three species. Not surprisingly, all lizards sprinted faster on dark soil, which was probably due to the lizards' more immediate escape response and the higher compaction of dark soil. The relationship between escape response and sprint performance across the dark soil and white sand habitats suggests that behavioural differences may be an important component of adaptation and speciation in new environments. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 169–182.     

The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini)

Phenotypic differences among species are known to have functional consequences that in turn allow species to use different habitats. However, the role of behaviour in this ecomorphological paradigm is not well defined. We investigated the relationship between morphology, ecology and escape behaviour among 25 species of the lizard clade Liolaemus in a phylogenetic framework. We demonstrate that the relationship between morphology and characteristics of habitat structure shows little or no association, consistent with a previous study on this group. However, a significant relationship was found between morphology and escape behaviour with the distance a lizard moved from a potential predator correlated with body width, axilla-groin length, and pelvis width. A significant relationship between escape behaviour and habitat structure occupation was found; lizards that occupied tree trunks and open ground ran longer distances from predators and were found greater distances from shelter. Behavioural strategies used by these lizards in open habitats appear to have made unnecessary the evolution of limb morphology that has occurred in other lizards from other clades that are found in open settings. Understanding differences in patterns of ecomorphological relationships among clades is an important component for studying adaptive diversification.     

The relationship between limb morphology, kinematics, and force during running: the evolution of locomotor dynamics in lizards

Terrestrial locomotion occurs via the hierarchical links between morphology, kinematics, force, and center-of-mass mechanics. In a phylogenetically broad sample of seven lizard species, we show that morphological variation drives kinematic variation, which, in turn, drives force variation. Species with short limbs use a short stride–high frequency strategy when running at steady-speed and to change speeds. This link between morphology and kinematics results in relatively small vertical forces during the support phase of the stride cycle. Conversely, species with long limbs use a long stride–low frequency strategy, resulting in large vertical forces during the support phase. In view of these findings, we suggest that limb length may predict locomotor energetics in lizards because energetics are largely determined by vertical forces and stride frequency. Additionally, we propose an energetic trade-off with both long- and short-limbed species paying the most energy to move, whereas intermediate-limbed species move using less energy. Finally, when these traits are mapped onto a lizard phylogeny, we show that locomotor functional morphology exhibits both deep phylogenetic effects and contemporary patterns of evolutionary convergence. Overall, the present study provides a foundation for testing hypotheses regarding the integration and evolution of functional traits in lizards and animals in general.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 634–651.     

The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.     

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.     

Effects of Limb Length,Body Mass,Gender, Gravidity,and Elevation on Escape Speed in the Lizard Psammodromus algirus

Most animals rely on their escape speed to flee from predators. Here, we test several hypotheses on the evolution of escape speed in the lizard Psammodromus algirus. We test that: (1) Longer limbs should improve speed sprint. (2) Heavier lizards should be impaired regarding their sprint speed ability, suggesting a trade-off between fat storage and escape capability. (3) Males should achieve faster speeds due to their higher exposure to predators. (4) Gravid females, with increased body mass, should perform lower speed than non-gravid females. And (5) there are inter-population differences in sprint speed across an elevational gradient. We measured lizards sprint speed in a lineal raceway in the laboratory, filming races in standardized conditions and then calculating their maximal speed. We found that hind limb length greatly determined maximal sprint speed, lizards with longer limbs being faster. In parallel, higher body masses reduced maximal speed, which points to a trade-off between fat storage and escaping capability. Sexual differences also arose, as males were faster than females, as a consequence of males having longer limbs. Regarding females, gravidity did not impair maximal sprint speed, suggesting adaptations which compensate for the increased body mass. Finally, we found no elevational trend in both limbs length and sprint speed. In any case, this study suggests that selection on escape capacity may cast morphological evolution, and affect other life-history traits, such as fat storage and reproduction.     

Camouflage versus running performance as strategies against predation in a lizard inhabiting different habitats

Running speed and camouflage are associated with the foraging and anti‐predator abilities of animals. The toad‐headed lizard, Phrynocephalus versicolor, has evolved a darker dorsal color in melanistic habitats and maintained a lighter color in adjacent, non‐melanistic habitats. We test the hypothesis that lizards have weaker running speed on well‐matching backgrounds than on less matching backgrounds. We used lizard models to compare the predation pressure, while the running speed of dark and light lizards were compared in field tunnels using a video recording method. Our results indicated that both the dark lizards in melanistic Heishankou (HSK) and the light lizards in non‐melanistic Guazhou (GZ) face lower predation pressure than potential color‐background unmatched lizards. The light lizards have a potentially higher running speed than darker lizards in melanistic habitats, which implies that substrate color matching populations with benefits of camouflage might have lower anti‐predation pressure, and the costs of investment in melanin production may reduce running capacity.     

Morphological divergence patterns among populations of Poecilia vivipara (Teleostei Poeciliidae): test of an ecomorphological paradigm

The structure of body size and shape divergence among populations of Poecilia vivipara inhabiting quaternary lagoons in South-eastern Brazil was studied. This species is abundant throughout an environmental gradient formed by water salinity differences. The salinity gradient influences the habitat structure (presence of macrophytes) and the fish community (presence of large predators). Size and shape variation within and among populations was quantified by geometric morphometrics and analysed by indirect and direct gradient ordinations, using salinity and geography as a framework. Morphological divergence was associated with the salinity gradient. The evolutionary allometries observed were independent of within-group static allometries. Sexually dimorphic patterns were observed in size variation and within-population allometries. Specimens from freshwater (higher predation) sites presented smaller sizes, relatively longer caudal regions, lower anterior regions and a ventrally displaced eye. These features are consistent with an ecomorphological paradigm for aquatic organisms from populations subject to intense predation. A process of directional selection is postulated as the most likely force driving diversification among P. vivipara populations.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 799–812.     

Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae)

Within populations, individual animals may vary considerably in morphology and ecology. The degree to which variation in morphology is related to ecological variation within a population remains largely unexplored. We investigated whether variation in body size and shape among sexes and age classes of the lizard Podarcis melisellensis translates in differential whole-animal performance (sprint speed, bite force), escape and prey attack behaviour in the field, microhabitat use and diet. Male and female adult lizards differed significantly in body size and head and limb proportions. These morphological differences were reflected in differences in bite strength, but not in sprint speed. Accordingly, field measurements of escape behaviour and prey attack speed did not differ between the sexes, but males ate larger, harder and faster prey than females. In addition to differences in body size, juveniles diverged from adults in relative limb and head dimensions. These shape differences may explain the relatively high sprint and bite capacities of juvenile lizards. Ontogenetic variation in morphology and performance is strongly reflected in the behaviour and ecology in the field, with juveniles differing from adults in aspects of their microhabitat use, escape behaviour and diet.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 251–264.     

Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards

Many of the classic examples of adaptive radiation, including Caribbean Anolis lizards, are found on islands. However, Anolis also exhibits substantial species richness and ecomorphological disparity on mainland Central and South America. We compared patterns and rates of morphological evolution to investigate whether, in fact, island Anolis are exceptionally diverse relative to their mainland counterparts. Quite the contrary, we found that rates and extent of diversification were comparable--Anolis adaptive radiation is not an island phenomenon. However, mainland and Caribbean anoles occupy different parts of morphological space; in independent colonizations of both island and mainland habitats, island anoles have evolved shorter limbs and better-developed toe pads. These patterns suggest that the two areas are on different evolutionary trajectories. The ecological causes of these differences are unknown, but may relate to differences in predation or competition among mainland and island communities.     

Relations between microhabitat use and limb shape in phrynosomatid lizards

With the exception of the well-documented case for anoline lizards, recent studies have found few evolutionary relationships between morphology and habitat use in lizards despite clear-cut biomechanical predictions. One of the factors typically hampering these analyses is the clustering of habitat use within evolutionary lineages. In the present study, body shape was quantified for male and female lizards of 30 species of phrynosomatid lizards. This group was selected as little clustering of ecological variables seemed to be present. The results of traditional analyses indicate that evolutionary correlates of habitat use were prominent in the hindlimbs of both sexes. Species living in open habitats are characterized by longer femurs, and longer hindlimbs relative to the forelimb. Moreover, males from ground-dwelling species utilizing open habitats have longer toes on the hind foot than males from climbing species. Phylogenetic analyses indicated strong evolutionary associations between habitat use and the relative length of front and hindlimbs, with species from open terrestrial habitats having significantly shorter frontlimbs relative to their hindlimb than rock or tree climbing species. Evolutionary associations between morphology and habitat use were generally stronger for male lizards, indicating a potentially important contribution of sexual selection to the evolution of differences in limb proportions.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 149–163.     

Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure

We investigated the possible role of variation in predation pressure in the phenotypic divergence of two island populations of the Italian wall lizard, Podarcis sicula . In 1971, ten adult specimens from the island of Pod Kopište (Adriatic Sea, Croatia) were transported to the island of Pod Mrčaru, 3.5 km east, where they founded a new population. Although the two islands resemble each other in general physiognomy (size, elevation, microclimate) and in the absence of terrestrial predators, lizards from the newly established population are now on average larger and have shorter hind limbs. They also exhibit lower maximal sprint speed as measured on a racetrack, and fatigue faster when chased in a torus track. In the field, lizards from the original population of Pod Kopište respond to a simulated predatory attack by fleeing at larger approach distances and by running further from the predator than lizards from Pod Mrčaru. These changes in morphology, behaviour and performance may result from the relaxed predation intensity on the latter island. Our analysis of the structural features of the microhabitats suggests that the vegetation on Pod Mrčaru offers more protection to lizards. Also, plasticine models of lizards, laid out on the islands, less often exhibited signs of being attacked by birds on Pod Mrčaru than on Pod Kopište. Our findings provide an example of how changes in (possibly a single) environmental factor may simultaneously produce responses in behaviour, morphology and whole-animal physiology, and this on a surprisingly small spatial and temporal scale.     

Frequency of tail loss reflects variation in predation levels,predator efficiency,and the behaviour of three populations of brown anoles

We investigated two predictions regarding the incidence of tail regeneration in lizards for three populations of brown anoles exposed to varying predation levels from the same predator (cats). Firstly although inefficient predators are likely to increase the incidence of regenerated tails (i.e. lizards can escape through tail autotomy), highly efficient predators will kill and eat the lizard and thus leave no evidence of autotomy. At the site with no cats, only 4% of anoles demonstrated signs of tail regeneration. This value was not significantly different from the site where feral cats (i.e. ‘efficient’ predators that would capture prey to eat, as supported by behavioural observation) were present (7%). By contrast, 25% of anoles present at the site with pet cats (well‐fed domesticated cats that caught and played with anoles, i.e. were ‘inefficient’ predators) exhibited regenerated tails. Secondly, more obvious lizards are more susceptible to predation attempts. Supporting this hypothesis, our data indicate a higher incidence of regenerated tails (28%) was recorded amongst adult males (which are territorial, occupying exposed positions) compared to females and subadult males (17%) or juveniles (1%). In conclusion, the behaviour of both the predator and the lizard influences the frequency of regenerated tails in brown anoles. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 648–656.     

EVOLUTIONARY PATTERNS OF THE THERMAL SENSITIVITY OF SPRINT SPEED IN ANOLIS LIZARDS

I present evidence that the thermal sensitivity of sprint speed of Anolis lizards has evolved to match the activity body temperatures (T_b) experienced by local populations in nature. Anolis lizards from a range of altitudes in Costa Rica have limited thermoregulatory abilities and consequently have field T_b that differ substantially in median and interquartile distance (a measure of variability). Experimentally determined maximal sprint temperatures (T_b at which lizards run fastest) were positively correlated with median field T_b, and performance breadths (ranges of T_b over which lizards run well) were correlated with the variability (interquartile distance) of field T_b in the species I examined. Such correlations would be expected if the thermal sensitivity of sprint speed and field T_b had evolved together to improve the sprint performance of lizards in nature. Integration of laboratory and field studies indicates that several species of Anolis regularly experience impaired sprint speeds in the field, despite apparent evolutionary modification of their thermal physiologies. However, this impairment would have been more severe if the thermal sensitivities of sprint speed had not evolved. Data from other groups of lizards indicate that the thermal sensitivity of sprint speed has not evolved to match T_b of local populations (Hertz et al., 1983; Crowley, 1985). These lizards experience less variable T_b and less impairment of sprint speeds in the field than do the anoles. Thus, selection for modification of the thermal sensitivity of sprint speed might have been stronger for anoles than for other groups of lizards.     

Does relaxed predation drive phenotypic divergence among insular populations?

The evolution of striking phenotypes on islands is a well‐known phenomenon, and there has been a long‐standing debate on the patterns of body size evolution on islands. The ecological causes driving divergence in insular populations are, however, poorly understood. Reduced predator fauna is expected to lower escape propensity, increase body size and relax selection for crypsis in small‐bodied, insular prey species. Here, we investigated whether escape behaviour, body size and dorsal coloration have diverged as predicted under predation release in spatially replicated islet and mainland populations of the lizard species Podarcis gaigeae. We show that islet lizards escape approaching observers at shorter distances and are larger than mainland lizards. Additionally, we found evidence for larger between‐population variation in body size among the islet populations than mainland populations. Moreover, islet populations are significantly more divergent in dorsal coloration and match their respective habitats poorer than mainland lizards. These results strongly suggest that predation release on islets has driven population divergence in phenotypic and behavioural traits and that selective release has affected both trait means and variances. Relaxed predation pressure is therefore likely to be one of the major ecological factors driving body size divergence on these islands.     

Colonization of novel White Sands habitat is associated with changes in lizard anti‐predator behaviour

Colonization of novel habitats is often associated with differences in ecological community composition. For small diurnal animals, differences in predator diversity and abundance can lead to behavioural shifts in the novel habitat. The eastern fence lizard Sceloporus undulatus (Bosc and Daudin, 1801) recently colonized the gypsum dunes of White Sands, a predator‐poor community relative to the predator‐rich community of the surrounding Chihuahuan dark‐soil habitat. We used field experiments to assess S. undulatus anti‐predator behaviour in white‐sand versus dark‐soil habitats, and used laboratory assays to determine whether behavioural differences could be mediated by hormonal regulation. Overall, we found that white‐sand lizards were less vigilant but more wary than their dark‐soil counterparts; it took them longer to detect a simulated predator, but once detected they were more likely to retreat from their perches than dark‐soil lizards. At the proximate level, differences in anti‐predator behaviour could not be explained by differences in plasma hormone levels (corticosterone and testosterone); we detected elevated corticosterone for lizards in our stress treatment relative to control treatment, but found no differences between habitats in baseline or acute corticosterone levels. At the evolutionary level, we suggest that differences in anti‐predator behaviour may be explained by differences across habitats in predation environment, habituation, and/or the cost of retreating. Our study implicates changes in predator community composition in mediating ecological divergence in behaviour. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 657–667.     

Ecomorphology of Anolis lizards of the Choco' region in Colombia and comparisons with Greater Antillean ecomorphs

We analysed the ecomorphological relationships in four species of Anolis lizard that occur in the Choco' region in Colombia. The region is one of the most diverse of the Neotropical lowlands. The species were assigned to traditionally recognized Greater Antillean ecomorph categories based on habitat use data. Principal component analyses were carried out to examine correlations between the morphological traits, body size, and habitat use. We found that species are separated in morphological space principally by body size and lamella number. Upon removal of the effect of body size, correlations between morphology and habitat use became apparent. However, when compared with Greater Antillean ecomorphs, we found little evidence of morphological convergence in species occupying similar habitats. The species of the Choco' region are, however, clearly separated in the multidimensional morphological space from the Antillean taxa, and appear to form a separate cluster differentiating principally in body size and the number of lamellae. Mainland species clearly constitute an ecomorphological radiation but apparently this is independent of that of the West Indian fauna. More studies are needed to understand the causes for the independence of evolutionary trajectories on the mainland and the Greater Antilles, and to obtain a better understanding of the ecological and evolutionary processes underlying the radiation of these faunas.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 29–39.     

A phylogenetic test for adaptive convergence in rock-dwelling lizards

Phenotypic similarity of species occupying similar habitats has long been taken as strong evidence of adaptation, but this approach implicitly assumes that similarity is evolutionarily derived. However, even derived similarities may not represent convergent adaptation if the similarities did not evolve as a result of the same selection pressures; an alternative possibility is that the similar features evolved for different reasons, but subsequently allowed the species to occupy the same habitat, in which case the convergent evolution of the same feature by species occupying similar habitats would be the result of exaptation. Many lizard lineages have evolved to occupy vertical rock surfaces, a habitat that places strong functional and ecological demands on lizards. We examined four clades in which species that use vertical rock surfaces exhibit long hindlimbs and flattened bodies. Morphological change on the phylogenetic branches leading to the rock-dwelling species in the four clades differed from change on other branches of the phylogeny; evolutionary transitions to rock-dwelling generally were associated with increases in limb length and decreases in head depth. Examination of particular characters revealed several different patterns of evolutionary change. Rock-dwelling lizards exhibited similarities in head depth as a result of both adaptation and exaptation. Moreover, even though rock-dwelling species generally had longer limbs than their close relatives, clade-level differences in limb length led to an overall lack of difference between rock- and non-rock-dwelling lizards. These results indicate that evolutionary change in the same direction in independent lineages does not necessarily produce convergence, and that the existence of similar advantageous structures among species independently occupying the same environment may not indicate adaptation.     

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.