Phylogenetic eigenvectors and nonstationarity in the evolution of theropod dinosaur skulls

Despite the long‐standing interest in nonstationarity of both phenotypic evolution and diversification rates, only recently have methods been developed to study this property. Here, we propose a methodological expansion of the phylogenetic signal‐representation (PSR) curve based on phylogenetic eigenvectors to test for nonstationarity. The PSR curve is built by plotting the coefficients of determination R² from phylogenetic eigenvector regression (PVR) models increasing the number of phylogenetic eigenvectors against the accumulated eigenvalues. The PSR curve is linear under a stationary model of trait evolution (i.e. the Brownian motion model). Here we describe the distribution of shifts in the models R² and used a randomization procedure to compare observed and simulated shifts along the PSR curve, which allowed detecting nonstationarity in trait evolution. As an applied example, we show that the main evolutionary pattern of variation in the theropod dinosaur skull was nonstationary, with a significant shift in evolutionary rates in derived oviraptorosaurs, an aberrant group of mostly toothless, crested, birdlike theropods. This result is also supported by a recently proposed Bayesian‐based method (AUTEUR). A significant deviation between Ceratosaurus and Limusaurus terminal branches was also detected. We purport that our new approach is a valuable tool for evolutionary biologists, owing to its simplicity, flexibility and comprehensiveness.     

Jaw biomechanics and the evolution of biting performance in theropod dinosaurs

Despite the great diversity in theropod craniomandibular morphology, the presence and distribution of biting function types across Theropoda has rarely been assessed. A novel method of biomechanical profiling using mechanical advantage computed for each biting position along the entirety of the tooth row was applied to 41 extinct theropod taxa. Multivariate ordination on the polynomial coefficients of the profiles reveals the distribution of theropod biting performance in function space. In particular, coelophysoids are found to occupy a unique region of function space, while tetanurans have a wide but continuous function space distribution. Further, the underlying phylogenetic structure and evolution of biting performance were investigated using phylogenetic comparative methods. There is a strong phylogenetic signal in theropod biomechanical profiles, indicating that evolution of biting performance does not depart from Brownian motion evolution. Reconstructions of ancestral function space occupation conform to this pattern, but phylogenetically unexpected major shifts in function space occupation can be observed at the origins of some clades. However, uncertainties surround ancestor estimates in some of these internal nodes, so inferences on the nature of these evolutionary changes must be viewed with caution.     

The utility of cranial ontogeny for phylogenetic inference: a case study in crocodylians using geometric morphometrics

The degree to which the ontogeny of organisms could facilitate our understanding of phylogenetic relationships has long been a subject of contention in evolutionary biology. The famed notion that ‘ontogeny recapitulates phylogeny’ has been largely discredited, but there remains an expectation that closely related organisms undergo similar morphological transformations throughout ontogeny. To test this assumption, we used three‐dimensional geometric morphometric methods to characterize the cranial morphology of 10 extant crocodylian species and construct allometric trajectories that model the post‐natal ontogenetic shape changes. Using time‐calibrated molecular and morphological trees, we employed a suite of comparative phylogenetic methods to assess the extent of phylogenetic signal in these trajectories. All analyses largely demonstrated a lack of significant phylogenetic signal, indicating that ontogenetic shape changes contain little phylogenetic information. Notably, some Mantel tests yielded marginally significant results when analysed with the morphological tree, which suggest that the underlying signal in these trajectories is correlated with similarities in the adult cranial morphology. However, despite these instances, all other analyses, including more powerful tests for phylogenetic signal, recovered statistical and visual evidence against the assumption that similarities in ontogenetic shape changes are commensurate with phylogenetic relatedness and thus bring into question the efficacy of using allometric trajectories for phylogenetic inference.     

The influence of size on body shape diversification across Indo‐Pacific shore fishes*

Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo‐Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3% to 50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage‐specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.     

Aspects of comparative cranial mechanics in the theropod dinosaurs Coelophysis, Allosaurus and Tyrannosaurus

The engineering analysis technique finite element analysis (FEA) is used here to investigate cranial stress and strain during biting and feeding in three phylogenetically disparate theropod taxa: Coelophysis bauri , Allosaurus fragilis and Tyrannosaurus rex . Stress patterns are generally similar in all taxa with the ventral region of the skull tensed whilst the dorsal aspect is compressed, although the skull is not purely behaving as a cantilever beam as there is no discernible neutral region of bending. Despite similarities, stress patterns are not wholly comparable: there are key differences in how certain regions of the skull contain stress, and it is possible to link such differences to cranial morphology. In particular, nasal morphology can be explained by the stress patterns revealed here. Tyrannosaurus models shear and compress mainly in the nasal region, in keeping with the indistinguishably fused and expanded morphology of the nasal bones. Conversely Allosaurus and Coelophysis models experience peak shear and compression in the fronto-parietal region (which is tightly interdigitated and thickened in the case of Allosaurus ) yet in contrast the nasal region is lightly stressed, corresponding to relatively gracile nasals and a frequently patent internasal suture evident in Allosaurus . Such differences represent alternate mechanical specializations between taxa that may be controlled by functional, phylogenetic or mechanical constraints. Creation of finite element models placed in a phylogenetic context permits the investigation of the role of such mechanical character complexes in the cranium of nonavian theropods and the lineage leading towards modern birds.  © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society , 2005, 144 , 309–316.     

The impact of digging on the evolution of the rodent mandible

There are two main (but not mutually exclusive) methods by which subterranean rodents construct burrows: chisel-tooth digging, where large incisors are used to dig through soil; and scratch digging, where forelimbs and claws are used to dig instead of incisors. A previous study by the authors showed that upper incisors of chisel-tooth diggers were better adapted to dig but the overall cranial morphology within the rodent sample was not significantly different. This study analyzed the lower incisors and mandibles of the specimens used in the previous study to show the impact of chisel-tooth digging on the rodent mandible. We compared lower incisors and mandibular shape of chisel-tooth digging rodents with nonchisel-tooth digging rodents to see if there were morphological differences between the two groups. The shape of incisors was quantified using incisor radius of curvature and second moment of area (SMA). Mandibular shape was quantified using landmark based geometric morphometrics. We found that lower incisor shape was strongly influenced by digging group using a Generalized Phylogenetic ancova (analysis of covariance). A phylogenetic Procrustes anova (analysis of variance) showed that mandibular shape of chisel-tooth digging rodents was also significantly different from nonchisel-tooth digging rodents. The phylogenetic signal of incisor radius of curvature was weak, whereas that of incisor SMA and mandibular shape was significant. This is despite the analyses revealing significant differences in the shape of both mandibles and incisors between digging groups. In conclusion, we showed that although the mandible and incisor of rodents are influenced by function, there is also a degree of phylogenetic affinity that shapes the rodent mandibular apparatus.     

Phylogeny of the superfamily Gelechioidea (Lepidoptera: Obtectomera), with an exploratory application on geometric morphometrics

The superfamily Gelechioidea (Lepidoptera: Obtectomera) has a high species diversity. It consists of more than 18,400 described species and has a global distribution. Among it, large numbers of species were reported to be economically important to people's production and life. However, relationships among families or subfamilies in Gelechioidea have been exceptionally difficult to resolve using morphology or single gene genealogies. Multiple gene genealogies had been used in the molecular phylogenetic studies on Gelechioidea during the past years, but their phylogenetic relationships remain to be controversial mainly due to their limited taxa sampling relative to such high species diversity. In this paper, 89 ingroup species representing 55 genera are sequenced and added to the data downloaded from GenBank, and six species representing four closely related superfamilies are chosen as outgroup. The molecular phylogeny of Gelechioidea is reconstructed based on the concatenated data set composed of one mitochondrial marker (COI) and seven nuclear markers (CAD, EF-1ɑ, GAPDH, IDH, MDH, RpS5, wingless). The phylogenetic results, taking into consideration of the comparative morphological study, show that the clade of Gelechioidea is strongly supported and separated from other superfamilies, which further proves its monophyly. Five families are newly defined: Autostichidae sensu nov., Depressariidae sensu nov., Peleopodidae sensu nov., Ashinagidae sensu nov. and Epimarptidae sensu nov. Meanwhile, a monophyletic “SSABM” clade considered to be closely related is proposed for the first time, consisting of Stathmopodidae, Scythrididae, Ashinagidae, Blastobasidae and Momphidae. Moreover, geometric morphometric analyses using merged landmark data set from fore and hind wings of 118 representative species are conducted. The phenetic tree shows that the monophyly and phylogenetic relationships correspond with the results of molecular phylogeny largely, which well proves its importance and potential application in both phylogenetic reconstruction and species identification.     

No evidence for directional evolution of body mass in herbivorous theropod dinosaurs

The correlation between large body size and digestive efficiency has been hypothesized to have driven trends of increasing mass in herbivorous clades by means of directional selection. Yet, to date, few studies have investigated this relationship from a phylogenetic perspective, and none, to our knowledge, with regard to trophic shifts. Here, we reconstruct body mass in the three major subclades of non-avian theropod dinosaurs whose ecomorphology is correlated with extrinsic evidence of at least facultative herbivory in the fossil record—all of which also achieve relative gigantism (more than 3000 kg). Ordinary least-squares regressions on natural log-transformed mean mass recover significant correlations between increasing mass and geological time. However, tests for directional evolution in body mass find no support for a phylogenetic trend, instead favouring passive models of trait evolution. Cross-correlation of sympatric taxa from five localities in Asia reveals that environmental influences such as differential habitat sampling and/or taphonomic filtering affect the preserved record of dinosaurian body mass in the Cretaceous. Our results are congruent with studies documenting that behavioural and/or ecological factors may mitigate the benefit of increasing mass in extant taxa, and suggest that the hypothesis can be extrapolated to herbivorous lineages across geological time scales.     

Morphological disparity in theropod jaws: comparing discrete characters and geometric morphometrics

Disparity, the diversity of form and function of organisms, can be assessed from cladistic or phenetic characters, and from discrete characters or continuous characters such as landmarks, outlines, or ratios. But do these different methods of assessing disparity provide comparable results? Here we provide evidence that all metrics correlate significantly with each other and capture similar patterns of morphological variation. We compare three methods of capturing morphological disparity (discrete characters, geometric morphometric outlines and geometric morphometric landmarks) in coelurosaurian dinosaurs. We standardize our study by focusing all our metrics on the mandible, so avoiding the risk of confounding disparity methods with anatomical coverage of the taxa. The correlation is strongest between the two geometric morphometric methods, and weaker between the morphometric methods and the discrete characters. By using phylogenetic simulations of discrete character and geometric morphometric data sets, we show that the strength of these correlations is significantly greater than expected from the evolution of random data under Brownian motion. All disparity metrics confirm that Maniraptoriformes had the highest disparity of all coelurosaurians, and omnivores and herbivores had higher disparity than carnivores.     

The skull evolution of oviraptorosaurian dinosaurs: the role of niche partitioning in diversification

Oviraptorosaurs are bird‐like theropod dinosaurs that thrived in the final pre‐extinction ecosystems during the latest Cretaceous, and the beaked, toothless skulls of derived species are regarded as some of the most peculiar among dinosaurs. Their aberrant morphologies are hypothesized to have been caused by rapid evolution triggered by an ecological/biological driver, but little is known about how their skull shapes and functional abilities diversified. Here, we use quantitative techniques to study oviraptorosaur skull form and mandibular function. We demonstrate that the snout is particularly variable, that mandibular form and upper/lower beak form are significantly correlated with phylogeny, and that there is a strong and significant correlation between mandibular function and mandible/lower beak shape, suggesting a form–function association. The form–function relationship and phylogenetic signals, along with a moderate allometric signal in lower beak form, indicate that similar mechanisms governed beak shape in oviraptorosaurs and extant birds. The two derived oviraptorosaur clades, oviraptorids and caenagnathids, are significantly separated in morphospace and functional space, indicating that they partitioned niches. Oviraptorids coexisting in the same ecosystem are also widely spread in morphological and functional space, suggesting that they finely partitioned feeding niches, whereas caenagnathids exhibit extreme disparity in beak size. The diversity of skull form and function was likely key to the diversification and evolutionary success of oviraptorosaurs in the latest Cretaceous.     

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.     

Discrete and morphometric traits reveal contrasting patterns and processes in the macroevolutionary history of a clade of scorpions

Many palaeontological studies have investigated the evolution of entire body plans, generally relying on discrete character‐taxon matrices. In contrast, macroevolutionary studies performed by neontologists have mostly focused on morphometric traits. Although these data types are very different, some studies have suggested that they capture common patterns. Nonetheless, the tests employed to support this claim have not explicitly incorporated a phylogenetic framework and may therefore be susceptible to confounding effects due to the presence of common phylogenetic structure. We address this question using the scorpion genus Brachistosternus Pocock 1893 as case study. We make use of a time‐calibrated multilocus molecular phylogeny, and compile discrete and traditional morphometric data sets, both capturing the overall morphology of the organisms. We find that morphospaces derived from these matrices are significantly different, and that the degree of discordance cannot be replicated by simulations of random character evolution. Moreover, we find strong support for contrasting modes of evolution, with discrete characters being congruent with an ‘early burst’ scenario whereas morphometric traits suggest species‐specific adaptations to have driven morphological evolution. The inferred macroevolutionary dynamics are therefore contingent on the choice of character type. Finally, we confirm that metrics of correlation fail to detect these profound differences given common phylogenetic structure in both data sets, and that methods incorporating a phylogenetic framework and accounting for expected covariance should be favoured.     

Air‐filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’–bird transition

Pneumatic (air‐filled) postcranial bones are unique to birds among extant tetrapods. Unambiguous skeletal correlates of postcranial pneumaticity first appeared in the Late Triassic (approximately 210 million years ago), when they evolved independently in several groups of bird‐line archosaurs (ornithodirans). These include the theropod dinosaurs (of which birds are extant representatives), the pterosaurs, and sauropodomorph dinosaurs. Postulated functions of skeletal pneumatisation include weight reduction in large‐bodied or flying taxa, and density reduction resulting in energetic savings during foraging and locomotion. However, the influence of these hypotheses on the early evolution of pneumaticity has not been studied in detail previously. We review recent work on the significance of pneumaticity for understanding the biology of extinct ornithodirans, and present detailed new data on the proportion of the skeleton that was pneumatised in 131 non‐avian theropods and Archaeopteryx. This includes all taxa known from significant postcranial remains. Pneumaticity of the cervical and anterior dorsal vertebrae occurred early in theropod evolution. This ‘common pattern’ was conserved on the line leading to birds, and is likely present in Archaeopteryx. Increases in skeletal pneumaticity occurred independently in as many as 12 lineages, highlighting a remarkably high number of parallel acquisitions of a bird‐like feature among non‐avian theropods. Using a quantitative comparative framework, we show that evolutionary increases in skeletal pneumaticity are significantly concentrated in lineages with large body size, suggesting that mass reduction in response to gravitational constraints at large body sizes influenced the early evolution of pneumaticity. However, the body size threshold for extensive pneumatisation is lower in theropod lineages more closely related to birds (maniraptorans). Thus, relaxation of the relationship between body size and pneumatisation preceded the origin of birds and cannot be explained as an adaptation for flight. We hypothesise that skeletal density modulation in small, non‐volant, maniraptorans resulted in energetic savings as part of a multi‐system response to increased metabolic demands. Acquisition of extensive postcranial pneumaticity in small‐bodied maniraptorans may indicate avian‐like high‐performance endothermy.     

Testing convergent and parallel adaptations in talpids humeral mechanical performance by means of geometric morphometrics and finite element analysis

The shape and mechanical performance in Talpidae humeri were studied by means of Geometric Morphometrics and Finite Element Analysis, including both extinct and extant taxa. The aim of this study was to test whether the ability to dig, quantified by humerus mechanical performance, was characterized by convergent or parallel adaptations in different clades of complex tunnel digger within Talpidae, that is, Talpinae+Condylura (monophyletic) and some complex tunnel diggers not belonging to this clade. Our results suggest that the pattern underlying Talpidae humerus evolution is evolutionary parallelism. However, this insight changed to true convergence when we tested an alternative phylogeny based on molecular data, with Condylura moved to a more basal phylogenetic position. Shape and performance analyses, as well as specific comparative methods, provided strong evidence that the ability to dig complex tunnels reached a functional optimum in distantly related taxa. This was also confirmed by the lower phenotypic variance in complex tunnel digger taxa, compared to non‐complex tunnel diggers. Evolutionary rates of phenotypic change showed a smooth deceleration in correspondence with the most recent common ancestor of the Talpinae+Condylura clade. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

The asymmetry of the carpal joint and the evolution of wing folding in maniraptoran theropod dinosaurs

In extant birds, the hand is permanently abducted towards the ulna, and the wrist joint can bend extensively in this direction to fold the wing when not in use. Anatomically, this asymmetric mobility of the wrist results from the wedge-like shape of one carpal bone, the radiale, and from the well-developed convexity of the trochlea at the proximal end of the carpometacarpus. Among the theropod precursors of birds, a strongly convex trochlea is characteristic of Coelurosauria, a clade including the highly derived Maniraptora in addition to tyrannosaurs and compsognathids. The shape of the radiale can be quantified using a ‘radiale angle’ between the proximal and distal articular surfaces. Measurement of the radiale angle and reconstruction of ancestral states using squared-change parsimony shows that the angle was small (15°) in primitive coelurosaurs but considerably larger (25°) in primitive maniraptorans, indicating that the radiale was more wedge-shaped and the carpal joint more asymmetric. The radiale angle progressively increased still further within Maniraptora, with concurrent elongation of the forelimb feathers and the forelimb itself. Carpal asymmetry would have permitted avian-like folding of the forelimb in order to protect the plumage, an early advantage of the flexible, asymmetric wrist inherited by birds.     

Testing different 3D techniques using geometric morphometrics: Implications for cranial fluctuating asymmetry in humans

This study aimed to test the performance of 3D digitizer, CT scanner, and surface scanner in detecting cranial fluctuating asymmetry. Sets of 32 landmarks (6 in the midline and 13 bilateral) were acquired from 14 archeological crania using a 3D digitizer, and from 3D models generated from a CT scanner and surface scanner using Viewbox 4. Levels of shape variation were analyzed in MorphoJ using Procrustes analysis of variance and Principal component analysis. Intra-observer error accounted for 1.7%, 1.8%, and 4.5% of total shape variation for 3D digitizer, CT scanner, and surface scanner respectively. Fluctuating asymmetry accounted for 15%–16% of total shape variation. Variation between techniques accounted for 18% of total shape variation. We found a higher level of missing landmarks in our surface scan data than for both 3D digitizer and CT scanner data, and both 3D model-based techniques sometimes obscured taphonomic damage. All three 3D techniques are appropriate for measuring cranial fluctuating asymmetry. We advise against combining data collected with different techniques.     

The dentary of hadrosauroid dinosaurs: evolution through heterochrony

The near-global distribution of hadrosaurid dinosaurs during the Cretaceous has been attributed to mastication, a behaviour commonly recognized as a mammalian adaptation. Its occurrence in a non-mammalian lineage should be accompanied by the evolution of several morphological modifications associated with food acquisition and processing. This study investigated morphological variation in the dentary, a major element of the hadrosauroid lower jaw. Eighty-four hadrosauroid dentaries were subjected to geometric morphometric and statistical analyses to investigate their taxonomic, ontogenetic, and individual variation. Results suggest increased food acquisition and processing efficiency in saurolophids through a complex pattern of evolutionary and growth-related changes. The edentulous region grew longer relative to dentary length, allowing for food acquisition specialization anteriorly and processing posteriorly, and became ventrally directed, possibly associated with foraging low-growing vegetation, especially in younger individuals. The saurolophid coronoid process became anteriorly directed and relatively more elongate, with an expanded apex, increasing moment arm length, with muscles pulling the jaw more posteriorly, increasing mechanical advantage. During growth, all hadrosauroids underwent anteroposterior dental battery elongation by the addition of teeth, and edentulous region ventralization decreased. The dental battery became deeper in saurolophids by increasing the number of teeth per tooth family. The increased coronoid process anterior inclination and relative edentulous region elongation in saurolophids are hypothesized to have evolved through hypermorphosis and/or acceleration, peramorphic heterochronic processes; the development of an anteroposteriorly shorter but dorsoventrally taller saurolophid dentary, is probably due to post-displacement in dental battery elongation and edentulous region decreased ventral orientation, a paedomorphic heterochronic process.     

The impact of digging on craniodental morphology and integration

The relationship between the form and function of the skull has been the subject of a great deal of research, much of which has concentrated on the impact of feeding on skull shape. However, there are a number of other behaviours that can influence craniodental morphology. Previous work has shown that subterranean rodents that use their incisors to dig (chisel‐tooth digging) have a constrained cranial shape, which is probably driven by a necessity to create high bite forces at wide gapes. Chisel‐tooth‐digging rodents also have an upper incisor root that is displaced further back into the cranium compared with other rodents. This study quantified cranial shape and upper incisors of a phylogenetically diverse sample of rodents to determine if chisel‐tooth‐digging rodents differ in craniodental morphology. The study showed that the crania of chisel‐tooth‐digging rodents shared a similar place in morphospace, but a strong phylogenetic signal within the sample meant that this grouping was nonsignificant. It was also found that the curvature of the upper incisor in chisel‐tooth diggers was significantly larger than in other rodents. Interestingly, most subterranean rodents in the sample (both chisel‐tooth and scratch diggers) had upper incisors that were better able to resist bending than those of terrestrial rodents, presumably due to their similar diets of tough plant materials. Finally, the incisor variables and cranial shape were not found to covary consistently in this sample, highlighting the complex relationship between a species’ evolutionary history and functional morphology.