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.     

Divergent in shape and convergent in function: Adaptive evolution of the mandible in Sub‐Antarctic mice

Convergent evolution in similar environments constitutes strong evidence of adaptive evolution. Transported with people around the world, house mice colonized even remote areas, such as Sub‐Antarctic islands. There, they returned to a feral way of life, shifting towards a diet enriched in terrestrial macroinvertebrates. Here, we test the hypothesis that this triggered convergent evolution of the mandible, a morphological character involved in food consumption. Mandible shape from four Sub‐Antarctic islands was compared to phylogeny, tracing the history of colonization, and climatic conditions. Mandible shape was primarily influenced by phylogenetic history, thus discarding the hypothesis of convergent evolution. The biomechanical properties of the jaw were then investigated. Incisor in‐lever and temporalis out‐lever suggested an increase in the velocity of incisor biting, in agreement with observations on various carnivorous and insectivorous rodents. The mechanical advantage related to incisor biting also revealed an increased functional performance in Sub‐Antarctic populations, and appears to be an adaptation to catch prey more efficiently. The amount of change involved was larger than expected for a plastic response, suggesting microevolutionary processes were evolved. This study thus denotes some degree of adaptive convergent evolution related to changes in habitat‐related changes in dietary items in Sub‐Antarctic mice, but only regarding simple, functionally relevant aspects of mandible morphology.     

The geometry of taking flight: Limb morphometrics in Mesozoic theropods

Theropoda was one of the most successful dinosaurian clades during the Mesozoic and has remained a dominant component of faunas throughout the Cenozoic, with nearly 10,000 extant representatives. The discovery of Archaeopteryx provides evidence that avian theropods evolved at least 155 million years ago and that more than half of the tenure of avian theropods on Earth was during the Mesozoic. Considering the major changes in niche occupation for theropods resulting from the evolution of arboreal and flight capabilities, we have analyzed forelimb and hindlimb proportions among nonmaniraptoriform theropods, nonavian maniraptoriforms, and basal avialans using reduced major axis regressions, principal components analysis, canonical variates analysis, and discriminant function analysis. Our study is the first analysis on theropod limb proportions to apply phylogenetic independent contrasts and size corrections to the data to ensure that all the data are statistically independent and amenable to statistical analyses. The three ordination analyses we performed did not show any significant groupings or deviations between nonavian theropods and Mesozoic avian forms when including all limb elements. However, the bivariate regression analyses did show some significant trends between individual elements that suggested evolutionary trends of increased forelimb length relative to hindlimb length from nonmaniraptoriform theropods to nonavian maniraptoriforms to basal avialans. The increase in disparity and divergence away from the nonavian theropod body plan is well documented within Cenozoic forms. The lack of significant groupings among Mesozoic forms when examining the entire theropod body plan concurrently suggests that nonavian theropods and avian theropods did not substantially diverge in limb proportions until the Cenozoic. J. Morphol. 276:152–166, 2015. © 2014 Wiley Periodicals, Inc.     

Theropod forelimb design and evolution

We examined the relationship between forelimb design and function across the 230-million-year history of theropod evolution. Forelimb disparity was assessed by plotting the relative contributions of the three main limb elements on a ternary diagram. Theropods were divided into five functional groups: predatory, reduced, flying, wing-propelled diving, and flighdess. Forelimbs which maintained their primitive function, predation, are similarly proportioned, but non-avian theropods with highly reduced forelimbs have relatively longer humeri. Despite the dramatically different forces imparted by the evolution of flight, forelimb proportions of basal birds are only slighdy different from those of their non-avian relatives. An increase in disparity accompanied the subsequent radiation of birds. Each transition to flightlessness has been accompanied by an increase in relative humeral length, which results from relatively short distal limb elements. We introduce theoretical predictions based on five biomechanical and developmental factors that may have influenced the evolution of theropod limb proportions.     

Small Theropod Teeth from the Late Cretaceous of the San Juan Basin,Northwestern New Mexico and Their Implications for Understanding Latest Cretaceous Dinosaur Evolution

Studying the evolution and biogeographic distribution of dinosaurs during the latest Cretaceous is critical for better understanding the end-Cretaceous extinction event that killed off all non-avian dinosaurs. Western North America contains among the best records of Late Cretaceous terrestrial vertebrates in the world, but is biased against small-bodied dinosaurs. Isolated teeth are the primary evidence for understanding the diversity and evolution of small-bodied theropod dinosaurs during the Late Cretaceous, but few such specimens have been well documented from outside of the northern Rockies, making it difficult to assess Late Cretaceous dinosaur diversity and biogeographic patterns. We describe small theropod teeth from the San Juan Basin of northwestern New Mexico. These specimens were collected from strata spanning Santonian – Maastrichtian. We grouped isolated theropod teeth into several morphotypes, which we assigned to higher-level theropod clades based on possession of phylogenetic synapomorphies. We then used principal components analysis and discriminant function analyses to gauge whether the San Juan Basin teeth overlap with, or are quantitatively distinct from, similar tooth morphotypes from other geographic areas. The San Juan Basin contains a diverse record of small theropods. Late Campanian assemblages differ from approximately co-eval assemblages of the northern Rockies in being less diverse with only rare representatives of troodontids and a Dromaeosaurus-like taxon. We also provide evidence that erect and recurved morphs of a Richardoestesia-like taxon represent a single heterodont species. A late Maastrichtian assemblage is dominated by a distinct troodontid. The differences between northern and southern faunas based on isolated theropod teeth provide evidence for provinciality in the late Campanian and the late Maastrichtian of North America. However, there is no indication that major components of small-bodied theropod diversity were lost during the Maastrichtian in New Mexico. The same pattern seen in northern faunas, which may provide evidence for an abrupt dinosaur extinction.     

Phylogenetic convergence and multiple shell shape optima for gliding scallops (Bivalvia: Pectinidae)

An important question in evolutionary biology is how often, and to what extent, do similar ecologies elicit distantly related taxa to evolve towards the same phenotype? In some scenarios, the repeated evolution of particular phenotypes may be expected, for instance when species are exposed to common selective forces that result from strong functional demands. In bivalved scallops (Pectinidae), some species exhibit a distinct swimming behaviour (gliding), which requires specific biomechanical attributes to generate lift and reduce drag during locomotive events. Further, a phylogenetic analysis revealed that gliding behaviour has independently evolved at least four times, which raises the question as to whether these independent lineages have also converged on a similar phenotype. Here, we test the hypothesis that gliding scallops display shell shape convergence using a combination of geometric morphometrics and phylogenetic comparative methods that evaluate patterns of multivariate trait evolution. Our findings reveal that the gliding species display less morphological disparity and significant evolutionary convergence in morphospace, relative to expectations under a neutral model of Brownian motion for evolutionary phenotypic change. Intriguingly, the phylomorphospace patterns indicate that gliding lineages follow similar evolutionary trajectories to not one, but two regions of morphological space, and subsequent analyses identified significant differences in their biomechanical parameters, suggesting that these two groups of scallops accomplish gliding in different ways. Thus, whereas there is a clear gliding morphotype that has evolved convergently across the phylogeny, functionally distinct morphological subforms are apparent, suggesting that there may be two optima for the gliding phenotype in the Pectinidae.     

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.     

An integrative phylogenetic and extrapolatory approach to the reconstruction of dromaeosaur (Theropoda: Eumaniraptora) shoulder musculature

Dromaeosauridae is the sister taxon of the Avialae; thus, an investigation of dromaeosaur shoulder girdle musculature and forelimb function provides substantial information regarding changes in the size and performance of the theropod shoulder girdle musculature leading to avian powered flight. Twenty-two shoulder girdle muscles were reconstructed for the dromaeosaurid shoulder apparatus, based on phylogenetic inference, which involves the comparison of lepidosaurian, crocodilian and avian musculature, and extrapolatory inference, which involves a secondary comparison with functional analogues of theropods. In addition to these comparative methodologies, osteological correlates of shoulder musculature preserved in eumaniraptorans are identified, and comparisons with those of extant archosaurs allow these muscles to be definitively inferred in dromaeosaurids. This muscle reconstruction provides a foundation for subsequent investigation of differences in muscular attachment and function, based on scapulocoracoid morphology, across the theropod lineage leading to birds.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 146 , 301–344.     

Morphological and functional diversity in therizinosaur claws and the implications for theropod claw evolution

Therizinosaurs are a group of herbivorous theropod dinosaurs from the Cretaceous of North America and Asia, best known for their iconically large and elongate manual claws. However, among Therizinosauria, ungual morphology is highly variable, reflecting a general trend found in derived theropod dinosaurs (Maniraptoriformes). A combined approach of shape analysis to characterize changes in manual ungual morphology across theropods and finite-element analysis to assess the biomechanical properties of different ungual shapes in therizinosaurs reveals a functional diversity related to ungual morphology. While some therizinosaur taxa used their claws in a generalist fashion, other taxa were functionally adapted to use the claws as grasping hooks during foraging. Results further indicate that maniraptoriform dinosaurs deviated from the plesiomorphic theropod ungual morphology resulting in increased functional diversity. This trend parallels modifications of the cranial skeleton in derived theropods in response to dietary adaptation, suggesting that dietary diversification was a major driver for morphological and functional disparity in theropod evolution.     

Macroevolutionary dynamics in environmental space and the latitudinal diversity gradient in New World birds

Correlations between species richness and climate suggest non-random occupation of environmental space and niche evolution through time. However, the evolutionary mechanisms involved remain unresolved. Here, we partition the occupation of environmental space into intra- and inter-clade components to differentiate a model based on pure conservation of ancestral niches with higher diversification rates in the tropics, and an adaptive radiation model based on shifts in adaptive peaks at the family level allowing occupation of temperate regions. We examined these mechanisms using within- and among-family skewness components based on centroids of 3560 New World bird species across four environmental variables. We found that the accumulation of species in the tropics is a result of both processes. The components of adaptive radiation have family level skewness of species' distributions strongly structured in space, but not phylogenetically, according to the integrated analyses of spatial filters and phylogenetic eigenvectors. Moreover, stronger radiation components were found for energy variables, which are often used to argue for direct climatic effects on diversity. Thus, the correspondence between diversity and climate may be due to the conservation of ancestral tropical niches coupled with repeated broad shifts in adaptive peaks during birds' evolutionary history more than by higher diversification rates driven by more energy in the tropics.     

Phylogenetically structured variance in felid bite force: the role of phylogeny in the evolution of biting performance

A key question in evolution is the degree to which morphofunctional complexes are constrained by phylogeny. We investigated the role of phylogeny in the evolution of biting performance, quantified as bite forces, using phylogenetic eigenvector regression. Results indicate that there are strong phylogenetic signals in both absolute and size‐adjusted bite forces, although it is weaker in the latter. This indicates that elimination of size influences reduces the level of phylogenetic inertia and that the majority of the phylogenetic constraint is a result of size. Tracing the evolution of bite force through phylogeny by character optimization also supports this notion, in that relative bite force is randomly distributed across phylogeny whereas absolute bite force diverges according to clade. The nonphylogenetically structured variance in bite force could not be sufficiently explained by species‐unique morphology or by ecology. This study demonstrates the difficulties in identifying causes of nonphylogenetically structured variance in morphofunctional character complexes.     

Journeys through discrete‐character morphospace: synthesizing phylogeny,tempo, and disparity

Palaeontologists have long employed discrete categorical data to capture morphological variation in fossil species, using the resulting character–taxon matrices to measure evolutionary tempo, infer phylogenies and capture morphological disparity. However, to date these have been seen as separate approaches despite a common goal of understanding morphological evolution over deep time. Here I argue that there are clear advantages to considering these three lines of enquiry in a single space: the phylomorphospace. Conceptually these high‐dimensional spaces capture how a phylogenetic tree explores morphospace and allow us to consider important process questions around evolutionary rates, constraints, convergence and directional trends. Currently the literature contains fundamentally different approaches used to generate such spaces, with no direct comparison between them, despite the differing evolutionary histories they imply. Here I directly compare five different phylomorphospace approaches, three with direct literature equivalents and two that are novel. I use a single empirical case study of coelurosaurian theropod dinosaurs (152 taxa, 853 characters) to show that under many analyses the literature‐derived approaches tend to reflect introduced phylogenetic (rather than the intended morphological) signal. The two novel approaches, which produce limited ancestral state estimates prior to ordination, are able to minimize this phylogenetic signal and thus exhibit more realistic amounts of phylogenetic signal, rate heterogeneity, and convergent evolution.     

Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation

Background

Crocodilians have dominated predatory niches at the water-land interface for over 85 million years. Like their ancestors, living species show substantial variation in their jaw proportions, dental form and body size. These differences are often assumed to reflect anatomical specialization related to feeding and niche occupation, but quantified data are scant. How these factors relate to biomechanical performance during feeding and their relevance to crocodilian evolutionary success are not known.

Methodology/Principal Findings

We measured adult bite forces and tooth pressures in all 23 extant crocodilian species and analyzed the results in ecological and phylogenetic contexts. We demonstrate that these reptiles generate the highest bite forces and tooth pressures known for any living animals. Bite forces strongly correlate with body size, and size changes are a major mechanism of feeding evolution in this group. Jaw shape demonstrates surprisingly little correlation to bite force and pressures. Bite forces can now be predicted in fossil crocodilians using the regression equations generated in this research.

Conclusions/Significance

Critical to crocodilian long-term success was the evolution of a high bite-force generating musculo-skeletal architecture. Once achieved, the relative force capacities of this system went essentially unmodified throughout subsequent diversification. Rampant changes in body size and concurrent changes in bite force served as a mechanism to allow access to differing prey types and sizes. Further access to the diversity of near-shore prey was gained primarily through changes in tooth pressure via the evolution of dental form and distributions of the teeth within the jaws. Rostral proportions changed substantially throughout crocodilian evolution, but not in correspondence with bite forces. The biomechanical and ecological ramifications of such changes need further examination.     

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.     

The relationship between skull morphology, biting performance and foraging mode in Kalahari lacertid lizards

Lizards are a diverse clade in which one radiation consists entirely of sit-and-wait foragers and another consists of wide foragers. Lizards utilizing these two foraging modes are known to differ in diet, but little is known about how feeding morphology relates to diet and/or foraging mode. This study tested the hypothesis that skull morphology and biting performance are related to diet preference, and consequently, coevolve with foraging mode. Four species of lacertid lizard were studied because they vary in foraging mode, their phylogenetic relationships are known and they are well studied ecologically. Using an 'ecomorphological' approach, skull morphology and biting performance were quantified and mapped on to the phylogeny for the species. The results indicate that sit-and-wait species have shorter, wider skulls than the wide foraging species, and that all are significantly different in overall head shape. The sit-and-wait species had similar values for biting performance; however, clear phylogenetic patterns of covariation were not present between sit-and-wait and wide foraging species for either biting performance or skull morphology. Thus, skull morphology and performance have little influence on diet and foraging mode in these species. Instead it is likely that other factors such as seasonal prey availability and/or life history strategy shape foraging mode decisions.  © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 140 , 403–416.     

Skeletal completeness of the non‐avian theropod dinosaur fossil record

Non‐avian theropods were a highly successful clade of bipedal, predominantly carnivorous, dinosaurs. Their diversity and macroevolutionary patterns have been the subject of many studies. Changes in fossil specimen completeness through time and space can bias our understanding of macroevolution. Here, we quantify the completeness of 455 non‐avian theropod species using the skeletal completeness metric (SCM), which calculates the proportion of a complete skeleton preserved for a specimen. Temporal patterns of theropod skeletal completeness show peaks in the Carnian, Oxfordian–Kimmeridgian and Barremian–Aptian, and lows in the Berriasian and Hauterivian. Lagerstätten primarily drive the peaks in completeness and observed taxonomic diversity in the Oxfordian–Kimmeridgian and the Barremian–Aptian. Theropods have a significantly lower distribution of completeness scores than contemporary sauropodomorph dinosaurs but change in completeness through time for the two groups shows a significant correlation when conservation Lagerstätten are excluded, possibly indicating that both records are primarily driven by geology and sampling availability. Our results reveal relatively weak temporal sampling biases acting on the theropod record but relatively strong spatial and environmental biases. Asia has a significantly more complete record than any other continent, the mid northern latitudes have the highest abundance of finds, and most complete theropod skeletons come from lacustrine and aeolian environments. We suggest that these patterns result from historical research focus, modern climate dynamics, and depositional transportation energy plus association with conservation Lagerstätten, respectively. Furthermore, we find possible ecological biases acting on different theropod subgroups, but body size does not influence theropod completeness on a global scale.     

Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective

Secondary metabolites, at least the major ones present in a plant, apparently function as defence (against herbivores, microbes, viruses or competing plants) and signal compounds (to attract pollinating or seed dispersing animals). They are thus important for the plant's survival and reproductive fitness. Secondary metabolites therefore represent adaptive characters that have been subjected to natural selection during evolution. Molecular phylogenies of the Fabaceae, Solanaceae and Lamiaceae were reconstructed and employed as a framework to map and to interpret the distribution of some major defence compounds that are typical for the respective plant families; quinolizidine alkaloids and non-protein amino acids for legumes; tropane and steroidal alkaloids for Solanaceae, and iridoids and essential oils for labiates. The distribution of the respective compounds appears to be almost mutually exclusive in the families studied, implying a strong phylogenetic and ecological component. However, on a closer look, remarkable exceptions can be observed, in that certain metabolites are absent (or present) in a given taxon, although all the neighbouring and ancestral taxa express (or do not express, respectively) the particular trait. It is argued that these patterns might reflect differential expression of the corresponding genes that have evolved earlier in plant evolution. The inconsistent secondary metabolite profiles mean that the systematic value of chemical characters becomes a matter of interpretation in the same way as traditional morphological markers. Thus, the distribution of secondary metabolites has some value for taxonomy but their occurrence apparently reflects adaptations and particular life strategies embedded in a given phylogenetic framework.     

MODULARITY AND RATES OF EVOLUTIONARY CHANGE IN A POWER‐AMPLIFIED PREY CAPTURE SYSTEM

The dynamic interplay among structure, function, and phylogeny form a classic triad of influences on the patterns and processes of biological diversification. Although these dynamics are widely recognized as important, quantitative analyses of their interactions have infrequently been applied to biomechanical systems. Here we analyze these factors using a fundamental biomechanical mechanism: power amplification. Power‐amplified systems use springs and latches to generate extremely fast and powerful movements. This study focuses specifically on the power amplification mechanism in the fast raptorial appendages of mantis shrimp (Crustacea: Stomatopoda). Using geometric morphometric and phylogenetic comparative analyses, we measured evolutionary modularity and rates of morphological evolution of the raptorial appendage's biomechanical components. We found that “smashers” (hammer‐shaped raptorial appendages) exhibit lower modularity and 10‐fold slower rates of morphological change when compared to non‐smashers (spear‐shaped or undifferentiated appendages). The morphological and biomechanical integration of this system at a macroevolutionary scale and the presence of variable rates of evolution reveal a balance between structural constraints, functional variation, and the “roles of development and genetics” in evolutionary diversification.