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.     

Correlations between lizard cranial shape and diet: a quantitative, phylogenetically informed analysis

Although the relationship between dietary and phenotypic specialization has been well documented for many vertebrate groups, it has been stated that few such general trends can be established for lizards. This is often thought to be due to the lack of dietary specialization in many lizards. For example, many species that are reported to be insectivorous may also consume a variety of plant materials, and the reverse is often true as well. In this study, we investigate whether a correlation exists between general cranial form and dietary niche in lizards. Additionally, we test previously proposed hypotheses suggesting that herbivorous lizards should be larger bodied than lizards with other diets. Our data indicate that lizards specializing in food items imposing different mechanical demands on the feeding system show clear patterns of morphological specialization in their cranial morphology. True herbivores (diet of fibrous and tough foliage) are clearly distinguished from omnivorous and carnivorous lizards by having taller skulls and shorter snouts, likely related to the need for high bite forces. This allows herbivores to mechanically reduce relatively less digestible foliage. Carnivores have relatively longer snouts and retroarticular processes, which may result in more efficient capture and processing of elusive prey. When analysed in an explicit phylogenetic context, only snout length and skull mass remained significantly different between dietary groups. The small number of differences in the phylogenetic analyses is likely the result of shared evolutionary history and the relative paucity of independent origins of herbivory and omnivory in our sample. Analyses of the relationship between diet and body size show that on average herbivores have a larger body size than carnivores, with omnivores intermediate between the two other dietary groups. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 433–466.     

Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: an approach based on geometric morphometrics

Relative warp analyses of landmarks describing cranial and mandibular shape are used for investigating patterns of morphological variation among extant bears (Mammalia, Carnivora, Ursidae) indicative of diet and feeding behavior. These patterns are used for deriving inferences about the autecology of two extinct species previously assumed to have had different dietary preferences, the North American giant, short-faced bear Arctodus simus and the Eurasian cave bear Ursus spelaeus . Results reveal a set of shared craniodental traits among the herbivorous bears, including short and vaulted skulls with well-developed zygomatic arches, lateralized orbits and small canines, concave jaws with a highly positioned condyle, large moment arms for the temporalis and masseter muscles, and long cheek teeth. In contrast, those bears that consume animal resources have long skulls with small zygomatic arches, frontalized orbits and well-developed canines, and long jaws with a deep mandibular symphysis, low muscle leverages, a condyle situated at the level of the tooth row and reduced cheek teeth. The craniodental morphology of omnivorous bears is intermediate between those of faunivores and herbivores. This is also the case of the short-faced bear and the cave bear, which suggests that previous reconstructions of the feeding ecology of these extinct species (highly carnivorous for A. simus and herbivorous for U. spelaeus ) should be revised.     

Functional cranial analysis of large animalivorous bats (Microchiroptera)

Large animalivorous bats include carnivorous, piscivorous and insectivorous microchiropterans. Skull proportions and tooth morphology are examined and interpreted functionally. Four wide- faced bats from four families are convergent in having wide skulls, large masseter muscle volumes and stout jaws, indicating a powerful bite. Three of the four also have long canine teeth relative to their maxillary toothrows. Carnivorous bats have more elongate skulls, larger brain volumes and larger pinnae. The wide-faced bats are all dral emitters and have heads positively tilted relative to the basicranial axis. The carnivorous species are nasal-emitting bats and have negatively tilted heads. The orientation of the head relative to the basicranial axis affects several characters of the skull and jaws and is not correlated with size. The speculation that the type of echolocation may be more of a determinant of evolutionary change than the feeding mechanism is addressed. Wide-faced bats are thought to be capable of eating hard prey items (durophagus) and are probably non- discriminating, aurally less sophisticated insect generalists while the carnivorous and non- durophagus insectivorous bats may be more discriminating and aurally more sophisticated in what they eat.     

Giant lizards occupied herbivorous mammalian ecospace during the Paleogene greenhouse in Southeast Asia

Mammals dominate modern terrestrial herbivore ecosystems, whereas extant herbivorous reptiles are limited in diversity and body size. The evolution of reptile herbivory and its relationship to mammalian diversification is poorly understood with respect to climate and the roles of predation pressure and competition for food resources. Here, we describe a giant fossil acrodontan lizard recovered with a diverse mammal assemblage from the late middle Eocene Pondaung Formation of Myanmar, which provides a historical test of factors controlling body size in herbivorous squamates. We infer a predominately herbivorous feeding ecology for the new acrodontan based on dental anatomy, phylogenetic relationships and body size. Ranking body masses for Pondaung Formation vertebrates indicates that the lizard occupied a size niche among the larger herbivores and was larger than most carnivorous mammals. Paleotemperature estimates of Pondaung Formation environments based on the body size of the new lizard are approximately 2–5°C higher than modern. These results indicate that competitive exclusion and predation by mammals did not restrict body size evolution in these herbivorous squamates, and elevated temperatures relative to modern climates during the Paleogene greenhouse may have resulted in the evolution of gigantism through elevated poikilothermic metabolic rates and in response to increases in floral productivity.     

Shape at the cross‐roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory

Patterns of skull shape in Carnivora provide examples of parallel and convergent evolution for similar ecomorphological adaptations. However, although most researchers report on skull homoplasies among hypercarnivorous taxa, evolutionary trends towards herbivory remain largely unexplored. In this study, we analyse the skull of the living herbivorous carnivorans to evaluate the importance of natural selection and phylogenetic legacy in shaping the skulls of these peculiar species. We quantitatively estimated shape variability using geometric morphometrics. A principal components analysis of skull shape incorporating all families of arctoid carnivorans recognized several common adaptations towards herbivory. Ancestral state reconstructions of skull shape and the reconstructed phylogenetic history of morphospace occupation more explicitly reveal the true patterns of homoplasy among the herbivorous carnivorans. Our results indicate that both historical constraints and adaptation have interplayed in the evolution towards herbivory of the carnivoran skull, which has resulted in repeated patterns of biomechanical homoplasy.     

The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics

Theropod dinosaurs, an iconic clade of fossil species including Tyrannosaurus and Velociraptor, developed a great diversity of body size, skull form and feeding habits over their 160+ million year evolutionary history. Here, we utilize geometric morphometrics to study broad patterns in theropod skull shape variation and compare the distribution of taxa in cranial morphospace (form) to both phylogeny and quantitative metrics of biting behaviour (function). We find that theropod skulls primarily differ in relative anteroposterior length and snout depth and to a lesser extent in orbit size and depth of the cheek region, and oviraptorosaurs deviate most strongly from the "typical" and ancestral theropod morphologies. Noncarnivorous taxa generally fall out in distinct regions of morphospace and exhibit greater overall disparity than carnivorous taxa, whereas large-bodied carnivores independently converge on the same region of morphospace. The distribution of taxa in morphospace is strongly correlated with phylogeny but only weakly correlated with functional biting behaviour. These results imply that phylogeny, not biting function, was the major determinant of theropod skull shape.     

Intercontinental community convergence of ecology and morphology in desert lizards

Evolutionary ecologists have long debated the extent to which communities in similar environments but different geographic regions exhibit convergence. On the one hand, if species' adaptations and community structure are determined by environmental features, convergence would be expected. However, if historical contingencies have long-lasting effects convergence would be unlikely. Most studies to date have emphasized the differences between communities in similar environments and little quantitative evidence for convergence exists. The application of comparative phylogenetic methods to ecological studies provides an opportunity to further investigate hypotheses of convergence. We compared the evolutionary patterns of structural ecology and morphology of 42 species of iguanian lizards from deserts of Australia and North America. Using a comparative approach, we found that evolutionary convergence of ecology and morphology occurs both in overall, community-wide patterns and in terms of pairs of highly similar intercontinental pairs of species. This result indicates that in these desert lizards, deterministic adaptive evolution shapes community patterns and overrides the historical contingencies unique to particular lineages.     

Trophic convergence drives morphological convergence in marine tetrapods

Marine tetrapod clades (e.g. seals, whales) independently adapted to marine life through the Mesozoic and Caenozoic, and provide iconic examples of convergent evolution. Apparent morphological convergence is often explained as the result of adaptation to similar ecological niches. However, quantitative tests of this hypothesis are uncommon. We use dietary data to classify the feeding ecology of extant marine tetrapods and identify patterns in skull and tooth morphology that discriminate trophic groups across clades. Mapping these patterns onto phylogeny reveals coordinated evolutionary shifts in diet and morphology in different marine tetrapod lineages. Similarities in morphology between species with similar diets—even across large phylogenetic distances—are consistent with previous hypotheses that shared functional constraints drive convergent evolution in marine tetrapods.     

Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen.     

Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach

Understanding how and why certain clades diversify greatly in morphology whereas others do not remains a major theme in evolutionary biology. Projecting families of phylogenies into multivariate morphospaces can distinguish two scenarios potentially leading to unequal morphological diversification: unequal magnitude of change per phylogenetic branch, and unequal efficiency in morphological innovation. This approach is demonstrated using a case study of skulls in sister clades within the South American fish superfamily Anostomoidea. Unequal morphological diversification in this system resulted not from the morphologically diverse clade changing more on each phylogenetic branch, but from that clade distributing an equal amount of change more widely through morphospace and innovating continually. Although substantial morphological evolution occurred throughout the less diverse clade's history, most of that clade's expansion in morphospace occurred in the most basal branches, and more derived portions of that radiation oscillated within previously explored limits. Because simulations revealed that there is a maximum 2.7% probability of generating two clades that differ so greatly in the density of lineages within morphospace under a null Brownian model, the observed difference in pattern likely reflects a difference in the underlying evolutionary process. Clade-specific factors that may have promoted or arrested morphological diversification are discussed.     

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.     

Morphological correlates of ant eating in horned lizards (Phrynosoma)

The North American horned lizards ( Phrynosoma ) represent a morphologically specialized group of ant-eating lizards. Although variation in dietary fidelity is observed among the species, all appear to possess morphological specializations thought to be related to their ant-eating diets. Previous studies have examined morphological specialization in Phrynosoma , but they have not taken into account the phylogenetic relationships of its member species. In the present study, the morphological characteristics of the head, jaws and teeth that are thought to be important in prey capture and prey processing were examined to test whether variation in cranial morphology is associated with diet in lizards of the genus Phrynosoma . It is suggested that lizards of the genus Phrynosoma are indeed morphologically specialized and that ant-eating is associated with reduced dentition and an overall reduction in the robustness of morphological structures important in prey processing. Although this trend holds for the highly myrmecophagous species of Phrynosoma , a robust cranial morphology is apparent in the short-horned lizard clade ( Phrynosoma ditmarsi , Phrynosoma douglasii , Phrynosoma hernandesi , Phrynosoma orbiculare ), implying the ability to process a variety of dietary items. The present study suggests that additional feeding specializations exist within an already specialized clade (i.e. the short-horned lizard clade) and highlights the need for more detailed dietary and behavioural studies of feeding behaviour in this uniquely specialized group of lizards.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 13–24.     

Incomplete convergence of gliding mammal skeletons*

Ecology and biomechanics play central roles in the generation of phenotypic diversity. When unrelated taxa invade a similar ecological niche, biomechanical demands can drive convergent morphological transformations. Thus, examining convergence helps to elucidate the key catalysts of phenotypic change. Gliding mammals are often presented as a classic case of convergent evolution because they independently evolved in numerous clades, each possessing patagia (“wing” membranes) that generate lift during gliding. We use phylogenetic comparative methods to test whether the skeletal morphologies of the six clades of extant gliding mammals demonstrate convergence. Our results indicate that glider skeletons are convergent, with glider groups consistently evolving proportionally longer, more gracile limbs than arborealists, likely to increase patagial surface area. Nonetheless, we interpret gliders to represent incomplete convergence because (1) evolutionary model-fitting analyses do not indicate strong selective pressures for glider trait optima, (2) the three marsupial glider groups diverge rather than converge, and (3) the gliding groups remain separated in morphospace (rather than converging on a single morphotype), which is reflected by an unexpectedly high level of morphological disparity. That glider skeletons are morphologically diverse is further demonstrated by fossil gliders from the Mesozoic Era, which possess unique skeletal characteristics that are absent in extant gliders. Glider morphologies may be strongly influenced by factors such as body size and attachment location of patagia on the forelimb, which can vary among clades. Thus, convergence in gliders appears to be driven by a simple lengthening of the limbs, whereas additional skeletal traits reflect nuances of the gliding apparatus that are distinct among different evolutionary lineages. Our unexpected results add to growing evidence that incomplete convergence is prevalent in vertebrate clades, even among classic cases of convergence, and they highlight the importance of examining form-function relationships in light of phylogeny, biomechanics, and the fossil record.     

Digest: How many ways to make a snake? Evidence for historical contingency of the convergence of squamate reptiles*

Do convergent phenotypes arise from the same evolutionary pathways, or might different pathways produce convergent morphology? Bergmann and Morinaga (2019) found different evolutionary pathways underlie morphology among six clades of lizards and snakes. Their findings provide evidence for the role of historical contingency in evolution.     

Size evolution in island lizards

Aim  The island rule, small animal gigantism and large animal dwarfism on islands, is a topic of much recent debate. While size evolution of insular lizards has been widely studied, whether or not they follow the island rule has never been investigated. I examined whether lizards show patterns consistent with the island rule.
Location  Islands worldwide.
Methods  I used literature data on the sizes of island–mainland population pairs in 59 species of lizards, spanning the entire size range of the group, and tested whether small insular lizards are larger than their mainland conspecifics and large insular lizards are smaller. I examined the influence of island area, island isolation, and dietary preferences on lizard size evolution.
Results  Using mean snout–vent length as an index of body size, I found that small lizards on islands become smaller than their mainland conspecifics, while large ones become larger still, opposite to predictions of the island rule. This was especially strong in carnivorous lizards; omnivorous and herbivorous species showed a pattern consistent with the island rule but this result was not statistically significant. No trends consistent with the island rule were found when maximum snout–vent length was used. Island area had, at best, a weak effect on body size. Using maximum snout–vent length as an index of body size resulted in most lizard populations appearing to be dwarfed on islands, but no such pattern was revealed when mean snout–vent length was used as a size index.
Main conclusions  I suggest that lizard body size is mostly influenced by resource availability, with large size allowing some lizard populations to exploit resources that are unavailable on the mainland. Lizards do not follow the island rule. Maximum snout–vent length may be biased by sampling effort, which should be taken into account when one uses this size index.     

How do food passage rate and assimilation differ between herbivorous lizards and nonruminant mammals?

Summary What digestive adaptations permit herbivorous nonruminant mammals to sustain much higher metabolic rates than herbivorous lizards, despite gross similarity in digestive anatomy and physiology? We approached this question by comparing four herbivorous species eating the same diet of alfalfa pellets: two lizards (chuckwalla and desert iugana) and two mammals (desert woodrat and laboratory mouse). The mammals had longer small and large intestines, greater intestinal surface area, much higher (by an order of magnitude) food intake normalized to metabolic live mass, and much faster food passage times (a few hours instead of a few days). Among both reptiles and mammals, passage times increase with body size and are longer for herbivores than for carnivores. The herbivorous lizards, despite these much slower passage times, had slightly lower apparent digestive efficiencies than the mammals. At least for chuckwallas, this difference from mammals was not due to differences in body temperature regime. Comparisons of chuckwallas and woodrats in their assimilation of various dietary components showed that the woodrat's main advantage lay in greater assimilation of the dietary fiber fraction. Woodrats achieved greater fiber digestion despite shorter residence time, but possibly because of a larger fermentation chamber, coprophagy, and/or different conditions for microbial fermentation. We conclude with a comparative overview of digestive function in herbivorous lizards and mammals, and with a list of four major unsolved questions.     

Digestive enzyme activities in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat

Three digestive enzymes in four species of closely related prickleback fishes (family Stichaeidae: Cebidichthys violaceus, Xiphister mucosus , Xiphister atropurpureus and Anoplarchus purpurescens ) were analysed to assess whether diet or phylogeny played a larger role in influencing digestive enzyme activity. Cebidichthys violaceus and X. mucosus are primarily herbivorous, whereas X. atropurpureus and A. purpurescens are mainly carnivorous. The two Xiphister species are sister taxa, and A. purpurescens is in a clade adjacent to that of the three other species. Pepsin and trypsin specific activities did not differ significantly among the four species, but α‐amylase activity was significantly higher in the two Xiphister species, followed by C. violaceus , and then A. purpurescens . The wide disparity between the two carnivores, the striking similarity between the two sister taxa, and the significant difference between the two herbivores indicate that activity of α‐amylase follows a pattern influenced more by phylogeny than by diet in these fishes.     

Cranial morphology and dietary habits of rodents

Rodents are important components of nearly every terrestrial ecosystem and display considerable ecological diversity. Nevertheless, a lack of data on the ecomorphology of rodents has led to them being largely overlooked in palaeoecological reconstructions. Here, geometric and linear morphometrics are used to examine how cranial and dental shapes reflect the diets of living rodent species. Although most rodents are omnivores or generalist herbivores, some species have evolved highly specialized carnivorous, insectivorous, and herbivorous diets. Results show that living rodents with similar diets display convergent morphology, despite their independent evolutionary histories. Carnivores have relatively elongate incisors, elongate and narrow incisor blades, orthodont incisor angles, reduced cheek tooth areas, and enlarged temporal fossae. Insectivores display relatively degenerate dentition, elongate rostra, narrow and thin zygomatic arches, and smaller temporal fossae. Herbivores are characterized by relatively broader incisor blades, longer molar tooth rows, larger cheek tooth areas, wider skull and rostrum, thicker and broader zygomatic arches, and larger temporal fossae. These results suggest that cranial and dental morphology can be used to accurately infer extinct rodent diets regardless of ancestry. Application to extinct beavers suggests that most had highly specialized herbivorous diets.     

部分蜥蜴类牙齿特征补充

The characteristics of modern lizard teeth have often been overlooked as an aid to classification. In order to i-dentify isolated teeth or rows of teeth on the jaws of Quaternary lizard fossils, we observed many modern lizard skulls with complete tooth rows, and thereby discovered that there are different patterns of tooth arrangement which are a significant aid to classification and also valuable in distinguishing lizard tooth fragments or isolated teeth. Our observations suggest that lizard teeth can be divided into three major types: 1 ) Homodont, pleurodont with single-cusp. This kind of teeth is usually slender and closely spaced. Teeth number 20 - 30 or more. The smaller-sized lizards, such as Gekkos gecko, G.Japonicus, Eumeces chinensis (Fig. 1 :A, a), E. xanthi, Leiolopisma tsinlingensis (Fig. 1 :B, b), L. reevesii, Ly-gosoma indicum, Platyurus platyurus and Hemidactylus frenatus, have this kind of arrangement. 2) Heterodont, sub-acrodont or pleurodont, with single-conical cusp teeth at the anterior of the tooth row and with flat-conical bicuspid teeth posteriorly. There are about 18 - 19 check teeth. Eremias argus (Fig. 1:C,c), E. multiocellata and E. brenchltyi have this kind of arrangement. 3 ) Heterodont, with single-conical cusp teeth in the anterior part of the tooth row and with tricuspid, subacrodont teeth posteriorly. There are vertical grooves between the teeth on the external side of the low-er jaw. The fourth tooth in most species is canine-like. There are 16 or less check teeth. The larger-sized lizards, such as Phrynocephalus przewalski, P. frontalis (Fig. 1:D,d), Japalura splendida, J. flaviceos (Fig. 1 : E, e), Calotes versicolor and Leioleps belliana etc. possess this kind of arrangement. Evolutionary trends in lizard teeth are briefly dis-cussed.