Decelerated dinosaur skull evolution with the origin of birds.
ABSTRACT: The evolutionary radiation of birds has produced incredible morphological variation, including a huge range of skull form and function. Investigating how this variation arose with respect to non-avian dinosaurs is key to understanding how birds achieved their remarkable success after the Cretaceous-Paleogene extinction event. Using a high-dimensional geometric morphometric approach, we quantified the shape of the skull in unprecedented detail across 354 extant and 37 extinct avian and non-avian dinosaurs. Comparative analyses reveal fundamental differences in how skull shape evolved in birds and non-avian dinosaurs. We find that the overall skull shape evolved faster in non-avian dinosaurs than in birds across all regions of the cranium. In birds, the anterior rostrum is the most rapidly evolving skull region, whereas more posterior regions-such as the parietal, squamosal, and quadrate-exhibited high rates in non-avian dinosaurs. These fast-evolving elements in dinosaurs are strongly associated with feeding biomechanics, forming the jaw joint and supporting the jaw adductor muscles. Rapid pulses of skull evolution coincide with changes to food acquisition strategies and diets, as well as the proliferation of bony skull ornaments. In contrast to the appendicular skeleton, which has been shown to evolve more rapidly in birds, avian cranial morphology is characterised by a striking deceleration in morphological evolution relative to non-avian dinosaurs. These results may be due to the reorganisation of skull structure in birds-including loss of a separate postorbital bone in adults and the emergence of new trade-offs with development and neurosensory demands. Taken together, the remarkable cranial shape diversity in birds was not a product of accelerated evolution from their non-avian relatives, despite their frequent portrayal as an icon of adaptive radiations.
Project description:Comparative anatomy studies of the skull of archosaurs provide insights on the mechanisms of evolution for the morphologically and functionally diverse species of crocodiles and birds. One of the key attributes of skull evolution is the anatomical changes associated with the physical arrangement of cranial bones. Here, we compare the changes in anatomical organization and modularity of the skull of extinct and extant archosaurs using an Anatomical Network Analysis approach. We show that the number of bones, their topological arrangement, and modular organization can discriminate birds from non-avian dinosaurs, and crurotarsans. We could also discriminate extant taxa from extinct species when adult birds were included. By comparing within the same framework, juveniles and adults for crown birds and alligator (Alligator mississippiensis), we find that adult and juvenile alligator skulls are topologically similar, whereas juvenile bird skulls have a morphological complexity and anisomerism more similar to those of non-avian dinosaurs and crurotarsans than of their own adult forms. Clade-specific ontogenetic differences in skull organization, such as extensive postnatal fusion of cranial bones in crown birds, can explain this pattern. The fact that juvenile and adult skulls in birds do share a similar anatomical integration suggests the presence of a specific constraint to their ontogenetic growth.
Project description:Cranial morphology in birds is thought to be shaped by adaptive evolution for foraging performance. This understanding of ecomorphological evolution is supported by observations of avian island radiations, such as Darwin's finches, which display rapid evolution of skull shape in response to food resource availability and a strong fit between cranial phenotype and trophic ecology. However, a recent analysis of larger clades has suggested that diet is not necessarily a primary driver of cranial shape and that phylogeny and allometry are more significant factors in skull evolution. We use phenome-scale morphometric data across the breadth of extant bird diversity to test the influence of diet and foraging behaviour in shaping cranial evolution. We demonstrate that these trophic characters are significant but very weak predictors of cranial form at this scale. However, dietary groups exhibit significantly different rates of morphological evolution across multiple cranial regions. Granivores and nectarivores exhibit the highest rates of evolution in the face and cranial vault, whereas terrestrial carnivores evolve the slowest. The basisphenoid, occipital, and jaw joint regions have less extreme differences among dietary groups. These patterns demonstrate that dietary niche shapes the tempo and mode of phenotypic evolution in deep time, despite a weaker than expected form-function relationship across large clades.
Project description:Mosaic evolution, which results from multiple influences shaping morphological traits and can lead to the presence of a mixture of ancestral and derived characteristics, has been frequently invoked in describing evolutionary patterns in birds. Mosaicism implies the hierarchical organization of organismal traits into semiautonomous subsets, or modules, which reflect differential genetic and developmental origins. Here, we analyze mosaic evolution in the avian skull using high-dimensional 3D surface morphometric data across a broad phylogenetic sample encompassing nearly all extant families. We find that the avian cranium is highly modular, consisting of seven independently evolving anatomical regions. The face and cranial vault evolve faster than other regions, showing several bursts of rapid evolution. Other modules evolve more slowly following an early burst. Both the evolutionary rate and disparity of skull modules are associated with their developmental origin, with regions derived from the anterior mandibular-stream cranial neural crest or from multiple embryonic cell populations evolving most quickly and into a greater variety of forms. Strong integration of traits is also associated with low evolutionary rate and low disparity. Individual clades are characterized by disparate evolutionary rates among cranial regions. For example, Psittaciformes (parrots) exhibit high evolutionary rates throughout the skull, but their close relatives, Falconiformes, exhibit rapid evolution in only the rostrum. Our dense sampling of cranial shape variation demonstrates that the bird skull has evolved in a mosaic fashion reflecting the developmental origins of cranial regions, with a semi-independent tempo and mode of evolution across phenotypic modules facilitating this hyperdiverse evolutionary radiation.
Project description:Non-avian saurischian skulls underwent at least 165 million years of evolution and shapes varied from elongated skulls, such as in the theropod Coelophysis, to short and box-shaped skulls, such as in the sauropod Camarasaurus. A number of factors have long been considered to drive skull shape, including phylogeny, dietary preferences and functional constraints. However, heterochrony is increasingly being recognized as an important factor in dinosaur evolution. In order to quantitatively analyse the impact of heterochrony on saurischian skull shape, we analysed five ontogenetic trajectories using two-dimensional geometric morphometrics in a phylogenetic framework. This allowed for the comparative investigation of main ontogenetic shape changes and the evaluation of how heterochrony affected skull shape through both ontogenetic and phylogenetic trajectories. Using principal component analyses and multivariate regressions, it was possible to quantify different ontogenetic trajectories and evaluate them for evidence of heterochronic events allowing testing of previous hypotheses on cranial heterochrony in saurischians. We found that the skull shape of the hypothetical ancestor of Saurischia likely led to basal Sauropodomorpha through paedomorphosis, and to basal Theropoda mainly through peramorphosis. Paedomorphosis then led from Orionides to Avetheropoda, indicating that the paedomorphic trend found by previous authors in advanced coelurosaurs may extend back into the early evolution of Avetheropoda. Not only are changes in saurischian skull shape complex due to the large number of factors that affected it, but heterochrony itself is complex, with a number of possible reversals throughout non-avian saurischian evolution. In general, the sampling of complete ontogenetic trajectories including early juveniles is considerably lower than the sampling of single adult or subadult individuals, which is a major impediment to the study of heterochrony on non-avian dinosaurs. Thus, the current work represents an exploratory analysis. To better understand the cranial ontogeny and the impact of heterochrony on skull evolution in saurischians, the data set that we present here must be expanded and complemented with further sampling from future fossil discoveries, especially of juvenile individuals.
Project description:Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric analysis of the skull across 181 modern and extinct species to identify the primary drivers of their cranial evolution within a unified, quantitative framework. Diet and habitat preferences, but not reproductive mode, are major influences on skull-shape evolution across squamates, with fossorial and aquatic taxa exhibiting convergent and rapid changes in skull shape. In lizards, diet is associated with the shape of the rostrum, reflecting its use in grasping prey, whereas snakes show a correlation between diet and the shape of posterior skull bones important for gape widening. Similarly, we observe the highest rates of evolution and greatest disparity in regions associated with jaw musculature in lizards, whereas those forming the jaw articulation evolve faster in snakes. In addition, high-resolution ancestral cranial reconstructions from these data support a terrestrial, nonfossorial origin for snakes. Despite their disparate evolutionary trends, lizards and snakes unexpectedly share a common pattern of trait integration, with the highest correlations in the occiput, jaw articulation, and palate. We thus demonstrate that highly diverse phenotypes, exemplified by lizards and snakes, can and do arise from differential selection acting on conserved patterns of phenotypic integration.
Project description:BACKGROUND:The Psittaciformes (parrots and cockatoos) are characterised by their large beaks, and are renowned for their ability to produce high bite forces. These birds also possess a suite of modifications to their cranial architecture interpreted to be adaptations for feeding on mechanically resistant foods, yet the relationship between cranial morphology and diet has never been explicitly tested. Here, we provide a three-dimensional geometric morphometric analysis of the developmental and biomechanical factors that may be influencing the evolution of psittaciformes' distinctive cranial morphologies. RESULTS:Contrary to our own predictions, we find that dietary preferences for more- or less- mechanically resistant foods have very little influence on beak and skull shape, and that diet predicts only 2.4% of the shape variation in psittaciform beaks and skulls. Conversely, evolutionary allometry and integration together predict almost half the observed shape variation, with phylogeny remaining an important factor in shape identity throughout our analyses, particularly in separating cockatoos (Cacatuoidea) from the true parrots (Psittacoidea). CONCLUSIONS:Our results are similar to recent findings about the evolutionary trajectories of skull and beak shape in other avian families. We therefore propose that allometry and integration are important factors causing canalization of the avian head, and while diet clearly has an influence on beak shape between families, this may not be as important at driving evolvability within families as is commonly assumed.
Project description:Like other diapsids, Tyrannosaurus rex has two openings in the temporal skull region. In addition, like in other dinosaurs, its snout and lower jaw show large cranial fenestrae. In T. rex, they are thought to decrease skull weight, because, unlike most other amniotes, the skull proportion is immense compared to the body. Understanding morphofunctional complexity of this impressive skull architecture requires a broad scale phylogenetic comparison with skull types different to that of dinosaurs with fundamentally diverging cranial regionalization. Extant fully terrestrial vertebrates (amniotes) provide the best opportunities in that regard, as their skull performance is known from life. We apply for the first time anatomical network analysis to study skull bone integration and modular constructions in tyrannosaur and compare it with five representatives of the major amniote groups in order to get an understanding of the general patterns of amniote skull modularity. Our results reveal that the tyrannosaur has the most modular skull organization among the amniotes included in our study, with an unexpected separation of the snout in upper and lower sub-modules and the presence of a lower adductor chamber module. Independent pathways of bone reduction in opossum and chicken resulted in different degrees of cranial complexity with chicken having a typical sauropsidian pattern. The akinetic skull of opossum, alligator, and leatherback turtle evolved in independent ways mirrored in different patterns of skull modularity. Kinetic forms also show great diversity in modularity. The complex tyrannosaur skull modularity likely represents a refined mosaic of phylogenetic and ecological factors with food processing being probably most important for shaping its skull architecture. Mode of food processing primarily shaped skull integration among amniotes, however, phylogenetic patterns of skull integration are low in our sampling. Our general conclusions on amniote skull integrity are obviously preliminary and should be tested in subsequent studies. As such, this study provides a framework for future research focusing on the evolution of modularity on lower taxonomic levels.
Project description:The tongue, with fleshy, muscular, and bony components, is an innovation of the earliest land-dwelling vertebrates with key functions in both feeding and respiration. Here, we bring together evidence from preserved hyoid elements from dinosaurs and outgroup archosaurs, including pterosaurs, with enhanced contrast x-ray computed tomography data from extant taxa. Midline ossification is a key component of the origin of an avian hyoid. The elaboration of the avian tongue includes the evolution of multiple novel midline hyoid bones and a larynx suspended caudal to these midline elements. While variable in dentition and skull shape, most bird-line archosaurs show a simple hyoid structure. Bony, or well-mineralized, hyoid structures in dinosaurs show limited modification in response to dietary shifts and across significant changes in body-size. In Dinosauria, at least one such narrow, midline element is variably mineralized in some basal paravian theropods. Only in derived ornithischians, pterosaurs and birds is further significant hyoid elaboration recorded. Furthermore, only in the latter two taxa does the bony tongue structure include elongation of paired hyobranchial elements that have been associated in functional studies with hyolingual mobility. Pterosaurs and enantiornithine birds achieve similar elongation and inferred mobility via elongation of ceratobranchial elements while within ornithurine birds, including living Aves, ossified and separate paired epibranchial elements (caudal to the ceratobranchials) confer an increase in hyobranchial length. The mobile tongues seen in living birds may be present in other flighted archosaurs showing a similar elongation. Shifts from hypercarnivory to more diverse feeding ecologies and diets, with the evolution of novel locomotor strategies like flight, may explain the evolution of more complex tongue function.
Project description:In contrast to the vast majority of reptiles, the skulls of adult crown birds are characterized by a high degree of integration due to bone fusion, e.g., an ontogenetic event generating a net reduction in the number of bones. To understand this process in an evolutionary context, we investigate postnatal ontogenetic changes in the skulls of crown bird and non-avian theropods using anatomical network analysis (AnNA). Due to the greater number of bones and bone contacts, early juvenile crown birds have less integrated skulls, resembling their non-avian theropod ancestors, including Archaeopteryx lithographica and Ichthyornis dispars. Phylogenetic comparisons indicate that skull bone fusion and the resulting modular integration represent a peramorphosis (developmental exaggeration of the ancestral adult trait) that evolved late during avialan evolution, at the origin of crown-birds. Succeeding the general paedomorphic shape trend, the occurrence of an additional peramorphosis reflects the mosaic complexity of the avian skull evolution.
Project description:Feathers are remarkable evolutionary innovations that are associated with complex adaptations of the skin in modern birds. Fossilised feathers in non-avian dinosaurs and basal birds provide insights into feather evolution, but how associated integumentary adaptations evolved is unclear. Here we report the discovery of fossil skin, preserved with remarkable nanoscale fidelity, in three non-avian maniraptoran dinosaurs and a basal bird from the Cretaceous Jehol biota (China). The skin comprises patches of desquamating epidermal corneocytes that preserve a cytoskeletal array of helically coiled ?-keratin tonofibrils. This structure confirms that basal birds and non-avian dinosaurs shed small epidermal flakes as in modern mammals and birds, but structural differences imply that these Cretaceous taxa had lower body heat production than modern birds. Feathered epidermis acquired many, but not all, anatomically modern attributes close to the base of the Maniraptora by the Middle Jurassic.