Lizard Skull Research Articles

Dynamic evolutionary interplay between ontogenetic skull patterning and whole-head integration.

The arrangement and morphology of the vertebrate skull reflect functional and ecological demands, making it a highly adaptable structure. However, the fundamental developmental and macroevolutionary mechanisms leading to different vertebrate skull phenotypes remain unclear. Here we exploit the morphological diversity of squamate reptiles to assess the developmental and evolutionary patterns of skull variation and covariation in the whole head. Our geometric morphometric analysis of a complex squamate ontogenetic dataset (209 specimens, 169 embryos, 44 species), covering stages from craniofacial primordia to fully ossified bones, reveals that morphological differences between snake and lizard skulls arose gradually through changes in spatial relationships (heterotopy) followed by alterations in developmental timing or rate (heterochrony). Along with dynamic spatiotemporal changes in the integration pattern of skull bone shape and topology with surrounding brain tissues and sensory organs, we identify a relatively higher phenotypic integration of the developing snake head compared with lizards. The eye, nasal cavity and Jacobson's organ are pivotal in skull morphogenesis, highlighting the importance of sensory rearrangements in snake evolution. Furthermore, our findings demonstrate the importance of early embryonic, ontogenetic and tissue interactions in shaping craniofacial evolution and ecological diversification in squamates, with implications for the nature of cranio-cerebral relations across vertebrates.

Identification of Late Pleistocene and Holocene fossil lizards from Hall's Cave (Kerr County, Texas) and a primer on morphological variation in North American lizard skulls.

Fossil identification practices have a profound effect on our interpretation of the past because these identifications form the basis for downstream analyses. Therefore, well-supported fossil identifications are necessary for examining the impact of past environmental changes on populations and communities. Here we apply an apomorphic identification framework in a case study identifying fossil lizard remains from Hall's Cave, a late Quaternary fossil site located in Central Texas, USA. We present images and descriptions of a broad comparative sample of North American lizard cranial elements and compile new and previously reported apomorphic characters for identifying fossil lizards. Our fossil identifications from Hall's Cave resulted in a minimum of 11 lizard taxa, including five lizard taxa previously unknown from the site. Most of the identified fossil lizard taxa inhabit the area around Hall's Cave today, but we reinforce the presence of an extirpated species complex of horned lizard. A main goal of this work is to establish a procedure for making well-supported fossil lizard identifications across North America. The data from this study will assist researchers endeavoring to identify fossil lizards, increasing the potential for novel discoveries related to North American lizards and facilitating more holistic views of ancient faunal assemblages.

Anatomical network analyses reveal evolutionary integration and modularity in the lizards skull

The morphology of lizard skulls is highly diverse, and it is crucial to understand the factors that constrain and promote their evolution to understand how lizards thrive. The results of interactions between cranial bones reflecting these factors can be detected as integration and modularity, and the analysis of integration and modularity allows us to explore the underlying factors. In this study, the integration and modularity of the skulls of lizards and the outgroup tuatara are analyzed using a new method, Anatomical Network Analysis (AnNA), and the factors causing lizards morphological diversity are investigated by comparing them. The comparison of modular structures shows that lizard skulls have high integration and anisomerism, some differences but basically common modular patterns. In contrast, the tuatara shows a different modular pattern from lizards. In addition, the presence of the postorbital bar by jugal and postorbital (postorbitofrontal) also reflect various functional factors by maintaining low integration. The maintenance of basic structures due to basic functional requirements and changes in integration within the modules play a significant role in increasing the morphological diversity of the lizard skull and in the prosperity of the lizards.

Surface sculpturing in the skull of gecko lizards (Squamata: Gekkota)

Abstract It has previously been stated that geckos are characterized by smooth cranial bones bearing no sculpturing; however, there are many exceptions. Here we systematically characterize variation in sculpturing in cranial bones across all seven gekkotan families and examine patterns of evolutionary transitions in these traits on a multigene molecular gekkotan phylogeny to elucidate trends in phenotypic diversification in bone sculpturing. Over 195 species were reviewed using specimens where smooth, grooved, pitted and rugose sculpturing patterns were found. Of the 26 cranial bones, only seven (premaxilla, maxilla, nasal, prefrontal, frontal, parietal and postorbitofrontal) were found to bear sculpturing across more than three species. Sculpturing was found to extend beyond these seven bones onto either the dentary, surangular and/or quadrate within five species. Phylogenetic analysis showed that sculpturing evolved recently and repeatedly in several distinct lineages. The remaining 19 skull bones were smooth, except in the five species above, supporting the suggestion that smooth skull bones were ancestral in gekkotans. There is no apparent relationship between body size and the presence of bone sculpturing. The functional significance, if any, of sculpturing requires further investigation.

Tracing the developmental origin of a lizard skull: Chondrocranial architecture, heterochrony, and variation in lacertids.

The sand lizard, Lacerta agilis, is a classical model species in herpetology. Its adult skull anatomy and its embryonic development are well known. The description of its fully formed primordial skull by Ernst Gaupp, in 1900, was a key publication in vertebrate morphology and influenced many comparative embryologists. Based on recent methodological considerations, we restudied the early cranial development of this species starting as early as the formation of mesenchymal condensations up to the fully formed chondrocranium. We traced the formation of the complex chondrocranial architecture in detail, clarified specific homologies for the first time, and uncovered major differences to old textbook descriptions. Comparison with other lacertid lizards revealed a very similar genesis of the primordial skull. However, we detected shifts in the developmental timing of particular cartilaginous elements, mainly in the nasal region, which may correlate to specific ecological adaptation in the adults. Late timing of nasal elements might be an important innovation for the successful wide range distribution of the well-known sand lizard.

Ontogeny, But Not Sexual Dimorphism, Drives the Intraspecific Variation of Quadrate Morphology in Hemidactylus turcicus (Squamata: Gekkonidae)

Abstract The functional components of the lizard skull are divided into the chondrocranial braincase, protective dermatocranium, lower jaw, and hyobranchial apparatus. These regions are interconnected and become operational through the quadrate, a bone critical for cranial biomechanics and support of the peripheral auditory system. The quadrate is a complex and variable structure in squamates; however, neither the intraspecific nor interspecific variation of this element has been studied in detail. We investigated the intraspecific variation of quadrate morphology within Hemidactylus turcicus with the use of cleared and double-stained specimens and high-resolution x-ray microcomputed tomography. Our objectives were to quantify quadrate shape and the degree of intraspecific variation within this element with the use of 2-D and 3-D geometric morphometric analyses and investigate if this variation is driven by ontogeny and/or sexual dimorphism. Our results demonstrate that ontogeny, but not sexual shape dimo...

The relationship between cranial structure, biomechanical performance and ecological diversity in varanoid lizards.

Skull structure is intimately associated with feeding ability in vertebrates, both in terms of specific performance measures and general ecological characteristics. This study quantitatively assessed variation in the shape of the cranium and mandible in varanoid lizards, and its relationship to structural performance (von Mises strain) and interspecific differences in feeding ecology. Geometric morphometric and linear morphometric analyses were used to evaluate morphological differences, and finite element analysis was used to quantify variation in structural performance (strain during simulated biting, shaking and pulling). This data was then integrated with ecological classes compiled from relevant scientific literature on each species in order to establish structure-function relationships. Finite element modelling results showed that variation in cranial morphology resulted in large differences in the magnitudes and locations of strain in biting, shaking and pulling load cases. Gracile species such as Varanus salvadorii displayed high strain levels during shaking, especially in the areas between the orbits. All models exhibit less strain during pull back loading compared to shake loading, even though a larger force was applied (pull =30N, shake = 20N). Relationships were identified between the morphology, performance, and ecology. Species that did not feed on hard prey clustered in the gracile region of cranial morphospace and exhibited significantly higher levels of strain during biting (P = 0.0106). Species that fed on large prey clustered in the elongate area of mandible morphospace. This relationship differs from those that have been identified in other taxonomic groups such as crocodiles and mammals. This difference may be due to a combination of the open ‘space-frame’ structure of the varanoid lizard skull, and the ‘pull back’ behaviour that some species use for processing large prey.

Scaling of the sexual size and shape skull dimorphism in the sand lizard (Lacerta agilis L.)

Sand lizards (Lacerta agilis) exhibit a clear pattern of sexual dimorphism, both in coloration and body proportions, where males have larger heads and are longer-legged at a given snout-to-vent length (SVL). In this study we analyse allometry of skull growth with SVL and skull length (SL) as references. The sand lizard skull is basically sexually size dimorphic and there are only minor shape differences. When SVL is used as a reference point, it generates differences in all traits to be measured, presumably because SVL is subject to different and strong selection pressures in both sexes. When skull length is taken as a reference point, differences in skull shape are restricted only to the postorbital region, which is wider in males. This may reflect selection pressure on stronger bite force in males.

The importance of accurate muscle modelling for biomechanical analyses: a case study with a lizard skull

Computer-based simulation techniques such as multi-body dynamics analysis are becoming increasingly popular in the field of skull mechanics. Multi-body models can be used for studying the relationships between skull architecture, muscle morphology and feeding performance. However, to be confident in the modelling results, models need to be validated against experimental data, and the effects of uncertainties or inaccuracies in the chosen model attributes need to be assessed with sensitivity analyses. Here, we compare the bite forces predicted by a multi-body model of a lizard (Tupinambis merianae) with in vivo measurements, using anatomical data collected from the same specimen. This subject-specific model predicts bite forces that are very close to the in vivo measurements and also shows a consistent increase in bite force as the bite position is moved posteriorly on the jaw. However, the model is very sensitive to changes in muscle attributes such as fibre length, intrinsic muscle strength and force orientation, with bite force predictions varying considerably when these three variables are altered. We conclude that accurate muscle measurements are crucial to building realistic multi-body models and that subject-specific data should be used whenever possible.

A new lizard skull from the Purbeck Limestone Group (Lower Cretaceous) of England

Abstract The Purbeck Limestone Group of England has yielded a rich assemblage of Late Jurassic to Early Cretaceous (Berriasian) vertebrate fossils, including one of the most diverse Early Cretaceous lizard assemblages on record. Here we describe the first articulated lizard skull from Purbeck. The specimen was rediscovered in the collections of the British Geological Survey, having been excavated at least a century ago. Although originally assigned to the Purbeck genus Paramacellodus, with which it shares maxillary and some dental characters, the new Purbeck skull differs from other Purbeck genera, including Paramacellodus, in frontal, pterygoid and maxillary morphology. It is here assigned to a new genus and species. Cladistic analysis groups it with Lacertoidea, unlike Paramacellodus, Becklesius and Parasaurillus which group with scincids and cordyliforms.

Evolution of the third eye: a phylogenetic comparative study of parietal-eye size as an ecophysiological adaptation in Liolaemus lizards

The parietal, or third, eye is a photosensory organ situated in the middle of the skull of many lizards. Despite many hypotheses, its exact ecological functions are still unclear. Studies have compared the presence and absence of a functioning parietal eye, although there are no quantitative studies of parietal-eye traits in relation to ecology, physiology or behaviour. In the present study, we report the first comparative study of relative parietal-eye size in relation to climatic and thermophysiological variables. We studied thirty species of Liolaemus, a genus of South-American lizards inhabiting a range of climatic conditions, but found little evidence for adaptation to thermal environment, in that parietal-eye size did not vary meaningfully with latitude, altitude or any measures of environmental temperature. Neither did it relate to thermophysiology; there was a weak relation to thermal tolerance, although this was partially confounded with body size, which explained 23% of the among-species variance after controlling for within-species variation. The negative results obtained could not be explained by phylogenetic constraints because we found no evidence of phylogenetic inertia. We also observed high intraspecific variation indicating that parietal-eye size may not be under strong selection for accuracy. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 870–883.

The Relationship Between Cephalic Scales and Bones in Lizards: A Preliminary Microtomographic Survey on Three Lacertid Species

In the last two decades, there has been a great deal of interest in the morphology and anatomy of the lizard skull in an ecological and evolutionary perspective. However, the relationship between variations in many key anatomical features remains largely unknown. Using microtomography and geometric morphometrics, we examined the relationship between bones and scales associated with the parietal foramen in the three lizards species most common in the Italian peninsula: Podarcis muralis, P. sicula, and Lacerta bilineata. The imprints of the scales are clearly recognizable on the outer bone surface, and this may suggest a structural interaction between these elements. The temporal osteoderms are visible in the larger males and in the larger females of L. bilineata, but they are absent in the smaller specimens of L. bilineata and in all Podarcis specimens. Two parallel rows of pterygoid teeth are present in all the specimens of L. bilineata and are absent in the smaller male of L. bilineata and in both Podarcis species. Cheek osteoderms occurred only in the largest specimens of our sample (i.e., large L. bilineata), being possibly related to hyperostotic processes and densitometric thresholds more than to phylogeny. Minor differences may be also associated with the form of the parietal foramen. In absolute terms the parietal foramen tends to be largest in L. bilineata but in relation to skull length the foramen tends to be larger in P. muralis. In this latter species the foramen is also more elongated. In all three species the fronto-parietal suture occupies a similar location relatively to the scale spatial organization. A shared allometric pattern shows that the main vault enlargement can be localised at the areas anterior to the fronto-parietal suture, providing further information on the possible morphogenetic dynamics associated with the interaction between scales and bones around this structure.

The evolution of the lepidosaurian lower temporal bar: new perspectives from the Late Cretaceous of South China

Until recently, it was considered axiomatic that the skull of lizards and snakes arose from that of a diapsid ancestor by loss of the lower temporal bar. The presence of the bar in the living New Zealand Tuatara, Sphenodon, was thus considered primitive, corroborating its status as a ‘living fossil’. A combination of new fossils and rigorous phylogeny has demonstrated unequivocally that the absence of the bar is the primitive lepidosaurian condition, prompting questions as to its function. Here we describe new material of Tianyusaurus, a remarkable lizard from the Late Cretaceous of China that is paradoxical in having a complete lower temporal bar and a fixed quadrate. New material from Jiangxi Province is more complete and less distorted than the original holotype. Tianyusaurus is shown to be a member of the Boreoteiioidea, a successful clade of large herbivorous lizards that were dispersed through eastern Asia, Europe and North America in the Late Cretaceous, but disappeared in the end-Cretaceous extinction. A unique combination of characters suggests that Tianyusaurus took food items requiring a large gape.

Combined finite element and multibody dynamics analysis of biting in a Uromastyx hardwickii lizard skull.

Lizard skulls vary greatly in shape and construction, and radical changes in skull form during evolution have made this an intriguing subject of research. The mechanics of feeding have surely been affected by this change in skull form, but whether this is the driving force behind the change is the underlying question that we are aiming to address in a programme of research. Here we have implemented a combined finite element analysis (FEA) and multibody dynamics analysis (MDA) to assess skull biomechanics during biting. A skull of Uromastyx hardwickii was assessed in the present study, where loading data (such as muscle force, bite force and joint reaction) for a biting cycle were obtained from an MDA and applied to load a finite element model. Fifty load steps corresponding to bilateral biting towards the front, middle and back of the dentition were implemented. Our results show the importance of performing MDA as a preliminary step to FEA, and provide an insight into the variation of stress during biting. Our findings show that higher stress occurs in regions where cranial sutures are located in functioning skulls, and as such support the hypothesis that sutures may play a pivotal role in relieving stress and producing a more uniform pattern of stress distribution across the skull. Additionally, we demonstrate how varying bite point affects stress distributions and relate stress distributions to the evolution of metakinesis in the amniote skull.

Assessment of the role of sutures in a lizard skull: a computer modelling study

Sutures form an integral part of the functioning skull, but their role has long been debated among vertebrate morphologists and palaeontologists. Furthermore, the relationship between typical skull sutures, and those involved in cranial kinesis, is poorly understood. In a series of computational modelling studies, complex loading conditions obtained through multibody dynamics analysis were imposed on a finite element model of the skull of Uromastyx hardwickii, an akinetic herbivorous lizard. A finite element analysis (FEA) of a skull with no sutures revealed higher patterns of strain in regions where cranial sutures are located in the skull. From these findings, FEAs were performed on skulls with sutures (individual and groups of sutures) to investigate their role and function more thoroughly. Our results showed that individual sutures relieved strain locally, but only at the expense of elevated strain in other regions of the skull. These findings provide an insight into the behaviour of sutures and show how they are adapted to work together to distribute strain around the skull. Premature fusion of one suture could therefore lead to increased abnormal loading on other regions of the skull causing irregular bone growth and deformities. This detailed investigation also revealed that the frontal-parietal suture of the Uromastyx skull played a substantial role in relieving strain compared with the other sutures. This raises questions about the original role of mesokinesis in squamate evolution.

Cranial performance in the Komodo dragon (Varanus komodoensis) as revealed by high‐resolution 3‐D finite element analysis

The Komodo dragon (Varanus komodoensis) displays a unique hold and pull-feeding technique. Its delicate 'space-frame' skull morphology differs greatly from that apparent in most living large prey specialists and is suggestive of a high degree of optimization, wherein use of materials is minimized. Here, using high-resolution finite element modelling based on dissection and in vivo bite and pull data, we present results detailing the mechanical performance of the giant lizard's skull. Unlike most modern predators, V. komodoensis applies minimal input from the jaw muscles when butchering prey. Instead it uses series of actions controlled by postcranial muscles. A particularly interesting feature of the performance of the skull is that it reveals considerably lower overall stress when these additional extrinsic forces are added to those of the jaw adductors. This remarkable reduction in stress in response to additional force is facilitated by both internal and external bone anatomy. Functional correlations obtained from these analyses also provide a solid basis for the interpretation of feeding ecology in extinct species, including dinosaurs and sabre-tooth cats, with which V. komodoensis shares various cranial and dental characteristics.

Rigid-body analysis of a lizard skull: Modelling the skull of Uromastyx hardwickii

Lizard skulls vary greatly in their detailed morphology. Theoretical models and practical studies have posited a definite relationship between skull morphology and bite performance, but this can be difficult to demonstrate in vivo. Computer modelling provides an alternative approach, as long as hard and soft tissue components can be integrated and the model can be validated. An anatomically accurate three-dimensional computer model of an Uromastyx hardwickii skull was developed for rigid-body dynamic analysis. The Uromastyx jaw was first opened under motion control, and then muscle forces were applied to produce biting simulations where bite forces and joint forces were calculated. Bite forces comparable to those reported in the literature were predicted, and detailed muscular force information was produced along with additional information on the stabilizing role of temporal ligaments in late jaw closing.

TESTING HYPOTHESES OF CONVERGENCE WITH MULTIVARIATE DATA: MORPHOLOGICAL AND FUNCTIONAL CONVERGENCE AMONG HERBIVOROUS LIZARDS

Despite its importance to evolutionary theory, convergence remains an understudied phenomenon and is usually investigated using qualitative data. This paper advances a new, multidimensional view of convergence. Three patterns indicative of convergence are discussed, and techniques to discover and test convergent patterns in a quantitative framework are developed. These concepts and methods are applied to a dataset of digitized coordinates on 1554 lizard skulls and 1292 lower jaws to test hypotheses of convergence among herbivorous lizards. Encompassing seven independent acquisitions of herbivory, this lizard sample provides an ideal natural experiment for exploring ideas of convergence among different systems (here, morphological and functional). Three related questions are addressed: (1) Do herbivorous lizards show evidence of convergence in skull and lower jaw morphology? (2) What, if any, is the morphospace pattern associated with this convergence? (3) Is it possible to predict the direction of convergence using functional models? Relative warp analysis and permutation tests reveal that the skulls and lower jaws of herbivorous lizards do show evidence of convergence. Herbivore skulls deviate from their carnivorous or omnivorous sister groups toward the same area of morphospace. Without a phylogenetic perspective, this pattern would not be recognizable. Lower jaws of herbivores are not convergent in morphology but are convergent in function: herbivores deviate away from their carnivorous sister groups toward higher values of mechanical advantage. These results illustrate the desirability of quantitative methods, informed by phylogenetic information, in the study of convergence.

Morphological evolution of the lizard skull: A geometric morphometrics survey

Patterns of diversity among lizard skulls were studied from a morphological, phylogenetic, and functional perspective. A sample of 1,030 lizard skulls from 441 species in 17 families was used to create a lizard skull morphospace. This morphospace was combined with a phylogeny of lizard families to summarize general trends in the evolution of the lizard skull. A basal morphological split between the Iguania and Scleroglossa was observed. Iguanians are characterized by a short, high skull, with large areas of attachment for the external adductor musculature, relative to their sister group. The families of the Iguania appear to possess more intrafamilial morphological diversity than families of the Scleroglossa, but rarefaction of the data reveals this to be an artifact caused by the greater number of species represented in Iguanian families. Iguanian families also appear more dissimilar to one another than families of the Scleroglossa. Permutation tests indicate that this pattern is real and not due to the smaller number of families in the Iguanidae. Parallel and convergent evolution is observed among lizards with similar diets: ant and termite specialists, carnivores, and herbivores. However, these patterns are superimposed over the more general phylogenetic pattern of lizard skull diversity. This study has three central conclusions. Different clades of lizards show different patterns of disparity and divergence in patterns of morphospace occupation. Phylogeny imposes a primary signal upon which a secondary ecological signal is imprinted. Evolutionary patterns in skull metrics, taken with functional landmarks, allow testing of trends and the development of new hypotheses concerning both shape and biomechanics.

The origin of snake feeding

Snakes are renowned for their ability to engulf extremely large prey, and their highly flexible skulls and extremely wide gape are among the most striking adaptations found in vertebrates1,2,3,4,5. However, the evolutionary transition from the relatively inflexible lizard skull to the highly mobile snake skull remains poorly understood, as they appear to be fundamentally different and no obvious intermediate stages have been identified4,5. Here we present evidence that mosasaurs — large, extinct marine lizards related to snakes — represent a crucial intermediate stage. Mosasaurs, uniquely among lizards, possessed long, snake-like palatal teeth for holding prey. Also, although they retained the rigid upper jaws typical of lizards, they possessed highly flexible lower jaws that were not only morphologically similar to those of snakes, but also functionally similar. The highly flexible lower jaw is thus inferred to have evolved before the highly flexible upper jaw — in the macrophagous common ancestor of mosasaurs and snakes — for accommodating large prey. The mobile upper jaw evolved later — in snakes — for dragging prey into the oesophagus. Snakes also have more rigid braincases than lizards, and the partially fused meso- and metakinetic joints of mosasaurs are transitional between the loose joints of lizards and the rigid joints of snakes. Thus, intermediate morphologies in snake skull evolution should perhaps be sought not in small burrowing lizards, as commonly assumed, but in large marine forms.