Morphology In Lizards Research Articles

Body size estimation from isolated fossil bones reveals deep time evolutionary trends in North American lizards.

Lizards play vital roles in extant ecosystems. However, their roles in extinct ecosystems are poorly understood because the fossil record of lizards consists mostly of isolated bones. This makes it difficult to document changes in lizard morphology and body size over time, which is essential for studies of lizard paleoecology and evolution. It is also difficult to compare available fossil lizard data with existing sources of extant lizard data because extant studies rarely measure individual bones. Furthermore, no previous study has regressed measurements of individual bones to body length across crown lizard groups, nor tested those regressions on fossil skeletons. An extensive dataset of individual bone measurements from extant lizards across crown taxonomic groups is here employed to develop novel methods for estimating lizard body size from isolated fossil elements. These methods were applied to a comparably large dataset of fossil lizard specimens from the robust Paleogene record (66-23 Ma) of the Western Interior of North America. This study tests the hypothesis that anatomical proportions have been conserved within higher-level crown lizard groups since the Paleogene and can therefore be used to reconstruct snout-vent length (SVL) and mass for fossil specimens referred to the same groups. Individual bones demonstrated strong correlation with SVL in extant as well as fossil lizard specimens (R2 ≥ 0.69). Equations for mass estimation from individual bones were derived from the SVL regressions using published equations for calculating lizard body mass from SVL. The resulting body size estimates from regression equations for the entire fossil dataset revealed that lizards reached greatest maximum body size in the middle Paleogene, with the largest size class dominated by anguid lizards that exceeded 1 meter in SVL and 1.5 kg in body mass. Maximum body size decreased to under 400 mm and below 1.5 kg in the late Paleogene. No association was found between changes in maximum lizard body size and marine isotope proxies of global temperature through the Paleogene. This is the first study to investigate body size evolution across lizard clades over a deep time interval and for a large geographic region. The proposed methods can be used to generate body size regressions and provide estimates of body size for isolated lizard bones referred to any crown group.

Climate aridity and habitat drive geographical variation in morphology and thermo-hydroregulation strategies of a widespread lizard species

Abstract Thermo-hydroregulation strategies involve concurrent changes in functional traits related to energy, water balance and thermoregulation and play a key role in determining life-history traits and population demography of terrestrial ectotherms. Local thermal and hydric conditions should be important drivers of the geographical variation of thermo-hydroregulation strategies, but we lack studies that examine these changes across climatic gradients in different habitat types. Here, we investigated intraspecific variation of morphology and thermo-hydroregulation traits in the widespread European common lizard (Zootoca vivipara louislantzi) across a multidimensional environmental gradient involving independent variation in air temperature and rainfall and differences in habitat features (access to free-standing water and forest cover). We sampled adult males for morphology, resting metabolic rate, total and cutaneous evaporative water loss and thermal preferences in 15 populations from the rear to the leading edge of the distribution across an elevational gradient ranging from sea level to 1750 m. Besides a decrease in adult body size with increasing environmental temperatures, we found little effect of thermal conditions on thermo-hydroregulation strategies. In particular, relict lowland populations from the warm rear edge showed no specific ecophysiological adaptations. Instead, body mass, body condition and resting metabolic rate were positively associated with a rainfall gradient, while forest cover and water access in the habitat throughout the season also influenced cutaneous evaporative water loss. Our study emphasizes the importance of rainfall and habitat features rather than thermal conditions for geographical variation in lizard morphology and physiology.

Machine learning accurately predicts the multivariate performance phenotype from morphology in lizards.

Completing the genotype-to-phenotype map requires rigorous measurement of the entire multivariate organismal phenotype. However, phenotyping on a large scale is not feasible for many kinds of traits, resulting in missing data that can also cause problems for comparative analyses and the assessment of evolutionary trends across species. Measuring the multivariate performance phenotype is especially logistically challenging, and our ability to predict several performance traits from a given morphology is consequently poor. We developed a machine learning model to accurately estimate multivariate performance data from morphology alone by training it on a dataset containing performance and morphology data from 68 lizard species. Our final, stacked model predicts missing performance data accurately at the level of the individual from simple morphological measures. This model performed exceptionally well, even for performance traits that were missing values for >90% of the sampled individuals. Furthermore, incorporating phylogeny did not improve model fit, indicating that the phenotypic data alone preserved sufficient information to predict the performance based on morphological information. This approach can both significantly increase our understanding of performance evolution and act as a bridge to incorporate performance into future work on phenomics.

Shrinking into the big city: influence of genetic and environmental factors on urban dragon lizard morphology and performance capacity

Urban wildlife faces a novel set of challenges resulting in selective pressure that can lead to population-level changes. We studied Australian water dragons (Intellagama lesueurii) from urban and natural populations to test if urban populations differed in body size, shape, and performance capacity. If urban-derived morphology has arisen through selection, we predicted distinct morphological differences between wild dragons from urban and natural areas in both adult and hatchling life-stages. Urban hatchlings were morphologically distinct (shorter body lengths and longer limbs) from natural populations, while urban adult males continued this trend but only for body size (shorter body lengths). We then experimentally reared hatchlings originating from urban and natural populations within urban- and natural-style enclosures (2 × 2 factorial design) for a year to determine if differences in morphology and performance capacity (sprint speed, endurance, and clinging ability) were related to either the individual’s origin population or developmental environment. Yearlings reared in urban-style enclosures, irrespective of population origin, had smaller body sizes compared to those from natural-style enclosures, suggesting developmental environment was affecting their morphology. Despite this difference in body size, yearling dragon performance capacity was not significantly different between treatments. Overall, this study provides evidence of a complex relationship driving urban-divergent morphology – whereby urban dragons emerge as smaller hatchlings with longer limbs (innate traits) and are then further influenced by the urban environments that they develop in (phenotypic plasticity); however, and potentially owing to behavioral, ecological, and demographical differences, these changes appear to be sex-specific.

Attenuated phenotypic responses of lizard morphology to logging and fire-related forest disturbance

Animals that face natural and human-mediated landscape disturbance processes can demonstrate different modalities of phenotypic variation to influence local population persistence. Differences in the frequency and pervasiveness of environmental variation can cause an individual’s phenotype to demonstrate either directional plasticity (i.e., environmental matching), canalization, or increased trait variance. Furthermore, how important a trait’s influence is on fitness can further mediate the nature of phenotypic outcomes to environmental variation. We explored the effects of multi-decadal chronosequences of logging and fire-related forest disturbance on morphological variation of the generalist lizard species, the Yellow-bellied water skink (Eulamprus heatwolei) in Southern Australia. There was evidence that both logging and fire-related disturbance could influence multiple elements of vegetation structure that would construe a major source of environmental variation for lizards. Nevertheless, neither logging nor fire-related disturbance effects resulted in significant differences in lizard morphological traits. However, there was evidence that years post-fire disturbance was associated with a modest but significant increase in a measure of lizard morphological variance. For the most part, we suggest that lizards exhibit canalization in their morphological responses to disturbance related environmental variation. In forests ecosystems with complex temporal and spatial regimes of environmental variation, canalization of lizard morphology could be expected to ensure phenotypic stability within or across generations to favor geometric, over arithmetic, fitness.

Lizards ran bipedally 110 million years ago

Four heteropod lizard trackways discovered in the Hasandong Formation (Aptian-early Albian), South Korea assigned to Sauripes hadongensis, n. ichnogen., n. ichnosp., which represents the oldest lizard tracks in the world. Most tracks are pes tracks (N = 25) that are very small, average 22.29 mm long and 12.46 mm wide. The pes tracks show “typical” lizard morphology as having curved digit imprints that progressively increase in length from digits I to IV, a smaller digit V that is separated from the other digits by a large interdigital angle. The manus track is 19.18 mm long and 19.23 mm wide, and shows a different morphology from the pes. The predominant pes tracks, the long stride length of pes, narrow trackway width, digitigrade manus and pes prints, and anteriorly oriented long axis of the fourth pedal digit indicate that these trackways were made by lizards running bipedally, suggesting that bipedality was possible early in lizard evolution.

Does the Morphology of the Forelimb Flexor Muscles Differ Between Lizards Using Different Habitats?

Lizards are an interesting group to study how habitat use impacts the morphology of the forelimb because they occupy a great diversity of ecological niches. In this study, we specifically investigated whether habitat use impacts the morphology of the forelimb flexor muscles in lizards. To do so, we performed dissections and quantified the physiological cross sectional area (PCSA), the fiber length, and the mass of four flexor muscles in 21 different species of lizards. Our results show that only the PCSA of the m. flexor carpi radialis is different among lizards with different ecologies (arboreal versus non-arboreal). This difference disappeared, however, when taking phylogeny into account. Arboreal species have a higher m. flexor carpi radialis cross sectional area likely allowing them to flex the wrist more forcefully which may allow them climb and hold on to branches better. In contrast, other muscles are not different between arboreal and non-arboreal species. Further studies focusing on additional anatomical features of the lizard forelimb as well as studies documenting how lizards use the arboreal niche are needed to fully understand how an arboreal life style may constrain limb morphology in lizards. Anat Rec, 301:424-433, 2018. © 2018 Wiley Periodicals, Inc.

Evolutionary morphology of the lizard chemosensory system

Foraging mode plays a pivotal role in traditional reconstructions of squamate evolution. Transitions between modes are said to spark concerted changes in the morphology, physiology, behaviour, and life history of lizards. With respect to their sensory systems, species that adopt a sit-and-wait strategy are thought to rely on visual cues primarily, while actively hunting species would predominantly use chemical information. The morphology of the tongue and the vomeronasal-organs is believed to mirror this dichotomy. Still, support for this idea of concerted evolution of the morphology of the lizard sensory system merely originates from studies comparing only a few, distantly related taxa that differ in many aspects of their biology besides foraging mode. Hence, we compared vomeronasal-lingual morphology among closely related lizard species (Lacertidae). Our findings show considerable interspecific variation indicating that the chemosensory system of lacertids has undergone substantial change over a short evolutionary time. Although our results imply independent evolution of tongue and vomeronasal-organ form, we find evidence for co-variation between sampler and sensor, hinting towards an ‘optimization’ for efficient chemoreception. Furthermore, our findings suggest species’ degree of investment in chemical signalling, and not foraging behaviour, as a leading factor driving the diversity in vomeronasal-lingual morphology among lacertid species.

Social context affects tail displays by Phrynocephalus vlangalii lizards from China.

Competition between animals for limited resources often involves signaling to establish ownership or dominance. In some species, the defended resource relates to suitable thermal conditions and refuge from predators. This is particularly true of burrow-dwelling lizards such as the Qinghai toad-headed agama (Phrynocephalus vlangalii), which are found on the Tibetan plateau of western China. Male and female lizards occupy separate burrows, which are vital for anti-predator behaviour during warmer months when lizards are active and, crucially, provide shelter from harsh winter conditions. These lizards are readily observed signaling by means of tail displays on the sand dunes they inhabit. Given the selective pressure to hold such a resource, both males and females should exhibit territorial behaviour and we considered this study system to examine in detail how social context influences motion based territorial signaling. We confirmed that territorial signaling was used by both sexes, and by adopting a novel strategy that permitted 3D reconstruction of tail displays, we identified significant variation due to social context. However, signal structure was not related to lizard morphology. Clearly, the burrow is a highly valued resource and we suggest that additional variation in signaling behaviour might be mediated by resource quality.

Do Adult Phenotypes Reflect Selection on Juvenile Performance? A Comparative Study on Performance and Morphology in Lizards.

When competing for food or other resources, or when confronted with predators, young animals may be at a disadvantage relative to adults because of their smaller size. Additionally, the ongoing differentiation and growth of tissues may constrain performance during early ontogenetic stages. However, juveniles must feed before they can become reproductively active adults and as such the adult phenotype may be the result of an ontogenetic filter imposing selection on juvenile phenotype and performance. Here we present ontogenetic data on head morphology and bite force for different lizard species. We test whether adults reflect selection on juveniles by comparing slopes of growth trajectories before and after sexual maturity in males and females and by examining the variance in head morphology and bite force in juveniles versus adults. Finally, we also present the first results of a selection study where animals were measured, marked and released, and recaptured the subsequent year to test whether head morphology and bite force impact survival.

Distribution pattern and number of ticks on lizards

The success of ectoparasites depends primarily on the site of attachment and body condition of their hosts. Ticks usually tend to aggregate on vertebrate hosts in specific areas, but the distribution pattern may depend on host body size and condition, sex, life stage or skin morphology. Here, we studied the distribution of ticks on lizards and tested the following hypothesis: occurrence or high abundance of ticks is confined with body parts with smaller scales and larger interscalar length because such sites should provide ticks with superior attachment conditions. This study was performed in field conditions in central Poland in 2008–2011. In total, 500 lizards (Lacerta agilis) were caught and 839 ticks (Ixodes ricinus, larvae and nymphs) were collected from them. Using generalised linear mixed models, we found that the ticks were most abundant on forelimbs and their axillae, with 90% of ticks attached there. This part of the lizard body and the region behind the hindlimb were covered by the smallest scales with relatively wide gaps between them. This does not fully support our hypothesis that ticks prefer locations with easy access to skin between scales, because it does not explain why so few ticks were in the hindlimb area. We found that the abundance of ticks was positively correlated with lizard body size index (snout-vent length). Tick abundance was also higher in male and mature lizards than in female and young individuals. Autotomy had no effect on tick abundance. We found no correlation between tick size and lizard morphology, sex, autotomy and body size index. The probability of occurrence of dead ticks was positively linked with the total number of ticks on the lizard but there was no relationship between dead tick presence and lizard size, sex or age. Thus lizard body size and sex are the major factors affecting the abundance of ticks, and these parasites are distributed nearly exclusively on the host's forelimbs and their axillae.

Repeated evolution of exaggerated dewlaps and other throat morphology in lizards.

The existence of elaborate ornamental structures in males is often assumed to reflect the outcome of female mate choice for showy males. However, female mate choice appears weak in many iguanian lizards, but males still exhibit an array of ornament-like structures around the throat. We performed a phylogenetic comparative study to assess whether these structures have originated in response to male-male competition or the need for improved signal efficiency in visually difficult environments. We found little evidence for the influence of male-male competition. Instead, forest species were more likely to exhibit colourful throat appendages than species living in open habitats, suggesting selection for signal efficiency. On at least three independent occasions, throat ornamentation has become further elaborated into a large, conspicuously coloured moving dewlap. Although the function of the dewlap is convergent, the underlying hyoid apparatus has evolved very differently, revealing the same adaptive outcome has been achieved through multiple evolutionary trajectories. More generally, our findings highlight that extravagant, ornament-like morphology can evolve in males without the direct influence of female mate choice and that failure to consider alternative hypotheses for the evolution of these structures can obscure the true origins of signal diversity among closely related taxa.

Homology of the Jaw Muscles in Lizards and Snakes—A Solution from a Comparative Gnathostome Approach

Homology or shared evolutionary origin of jaw adductor muscles in lizards and snakes has been difficult to establish, although snakes clearly arose within the lizard radiation. Lizards typically have temporal adductors layered lateral to medial, and in snakes the muscles are arranged in a rostral to caudal pattern. Recent work has suggested that the jaw adductor group in gnathostomes is arranged as a folded sheet; when this theory is applied to snakes, homology with lizard morphology can be seen. This conclusion revisits the work of S.B. McDowell, J Herpetol 1986; 20:353-407, who proposed that homology involves identity of m. levator anguli oris and the loss of m. adductor mandibulae externus profundus, at least in "advanced" (colubroid) snakes. Here I advance the folded sheet hypothesis across the whole snake tree using new and literature data, and provide a solution to this homology problem.

Anatomy of the Crus and Pes of Neotropical Iguanian Lizards in Relation to Habitat use and Digitally Based Grasping Capabilities

Ecomorphological studies of lizards have explored the role of various morphological traits and how these may be associated with, among other things, habitat use. We present an analysis of selected traits of internal morphology of the hind limbs of Neotropical iguanian lizards and their relationship to habitat use. Considering that one of the most widely-held hypotheses relating to the origin of grasping is associated with the exploitation of the narrow-branch arboreal habitat, we include subdivisions of this designation as two of our ecologically defined categories of habitat exploitation for analysis, and compare lizards assigned to these categories to the features displayed by terrestrial lizards. The influence of phylogeny in shaping the morphology of lizards was assessed by using the comparative method. K values were significant for several osteological traits. Most of the K values for the variables based upon muscle and tendon morphometric characters (13 out 21), by contrast, had values <1, suggesting that their variation cannot be explained by phylogeny alone. Results of our phylogenetic and conventional ANCOVA analyses reveal that the characters highlighted through the application of the comparative method are not absolutely related to habitat in terms of the categories considered here. It appears that the bauplan of the lizard pes incorporates a morphological configuration that is sufficiently versatile to enable exploitation of almost all of the available habitats. As unexpected as conservation of internal gross morphology appears, it represents a means of accommodating to environmental challenges by apparently permitting adequacy for all situations examined.

The birdlike raptor Sinornithosaurus was venomous

We suggest that some of the most avian dromaeosaurs, such as Sinornithosaurus, were venomous, and propose an ecological model for that taxon based on its unusual dentition and other cranial features including grooved teeth, a possible pocket for venom glands, and a groove leading from that pocket to the exposed bases of the teeth. These features are all analogous to the venomous morphology of lizards. Sinornithosaurus and related dromaeosaurs probably fed on the abundant birds of the Jehol forests during the Early Cretaceous in northeastern China.

Expression of breeding coloration in European Green Lizards (Lacerta viridis): variation with morphology and tick infestation

According to the hypothesis of parasite-mediated sexual selection, for a communication system to work reliably, parasites should reduce the showiness of sexual signals of their host. In this study, we examined whether the expression of breeding coloration in free-ranging adult European Green Lizards ( Lacerta viridis (Laurenti, 1768)) is linked with infestation by their common ectoparasite Ixodes ricinus (L., 1758) (Acari: Ixodidae). We found that tick infestation was higher in males than in females. Males showing relatively heavier body for their tail length (predominantly males with regenerated tails) and relatively thinner tail base experienced higher infestation rates. In turn, relatively heavier females for their snout–vent length were less tick infested. Although some components of throat and chest coloration varied significantly with relative tail length, tail-base thickness, body mass, and head size, a measure of male throat and female chest color saturation seemed independent of lizard morphology. After correcting for the effects of morphology on skin coloration and tick load, the saturation of blue throat color in male lizards decreased with increasing level of tick infestation. In contrast, yellow chest color saturation increased with residual tick numbers in females. Considering presumably different signaling functions of male and female lizard coloration, our work suggests that tick infestation might represent a handicap for Green Lizards.

Allometric prediction of locomotor performance: an example from Southeast Asian flying lizards.

Allometric scaling analysis is the standard paradigm for studies attempting to unravel the consequences of evolutionary size change (Huxley 1932; Gould 1966; SchmidtNielsen 1984). Although the value of this approach is clear, prediction of the allometry of performance is often hamstrung by the complexity of biological systems. This complexity derives from the heterogeneous interaction of physiological and morphological variables that together determine maximal performance. Despite this complication, allometric analysis is widely employed primarily because understanding the consequences of size evolution is so important to our field. Not only does size influence virtually every aspect of an organism’s biology (Calder 1984; Schmidt-Nielsen 1984), but it is also remarkably variable, even among closely related species. There is little consensus in the literature regarding the expected relationship between morphology and locomotor performance over a range of sizes. Despite a diversity of alternative models attempting to predict the allometry of performance (Thompson 1917; Hill 1950; Alexander 1968; McMahon 1973, 1975, 1984; Gunther 1975; Bennet-Clark 1977; Rubin and Lanyon 1984; Marsh 1988, 1994; Wakeling et al. 1999), empirical data often fail to conform to any extant model (e.g., Emerson 1978; Garland 1983, 1985; Chappell 1989; Katz and Gosline 1993; Bennett 2000; Wil-

Reproductive Cycle and Characteristics of the Widely-Foraging Lizard, Cnemidophorus communis, from Jalisco, Mexico

A 1993-1994 study of the reproductive biology of Cnemidophorus communis in the Chamela region, Jalisco, Mexico, revealed that males reached sexual maturity at a snout-vent length (SVL) of 59 mm, and females reached sexual maturity at a SVL of 68 mm. Males exhibited maximum testicular activity from May through October, decreasing in November, and females were reproductive, having vitellogenic follicles or oviductal eggs, from July through October. The mean number of vitellogenic follicles was 6.69 ′ 0.59 (2-10, n = 13) and mean clutch size of oviductal eggs was 4.8 ′ 0.44 (3-9, n = 17). Clutch size and egg mass were positively correlated with SVL but relative clutch mass remained constant among females and years. Proximal climatic factors influenced timing and intensity of reproduction in C. communis, but the historical effect of foraging mode on teiid lizard morphology constrains relative clutch mass.

Frillneck Lizard Morphology: Comparisons between Sexes and Sites

Frillneck Lizard Morphology: Comparisons between Sexes and Sites

Climate, Competition, and the Structure of Temperate Zone Lizard Communities

The roles of climate and competition in relation to the structure of temperate zone lizard communities were investigated. Lizard species richness was positively related to mean January temperature, but negatively related to warm—season precipitation and mean July temperature. Generic groups showed little overlap in morphological factor space but considerable overlap in habitat use. Species that were similar in either morphology or habitat use were dissimilar in the alternative factor space. A canonical correlation analysis revealed a significant relationship between lizard morphology and habitat use. In general, large bulky lizards were associated with extensive vegetative cover while small slenderbodied lizards were found in open desert or grassland conditions. No significant relationship was found between community size and measures of niche overlap or species packing in either morphological or ecological space. A comparison of species packing between the field communities and randomly generated null communities revealed no significant overdispersion of the natural communities in either habitat use or morphology, thus providing no evidence to support the limiting—similarity hypothesis.