How to Make a Bird Skull: Major Transitions in the Evolution of the Avian Cranium, Paedomorphosis, and the Beak as a Surrogate Hand.

The avian skull is distinctive in its construction and in its function. Much of bird anatomical variety is expressed in the beak; but the beak itself, largely formed of the premaxillary bone, is set upon a shortened face and a bulbous, enlarged braincase. Here, we use original anatomical observations and reconstructions to describe the overall form of the avian skull in a larger context and to provide a general account of the evolutionary transformation from the early dinosaur skull-the skull of an archosaurian macropredator-to that of modern birds. Facial shortening, the enlargement of the braincase around an enlarged brain (with consequential reduction of circumorbital elements and the adductor chamber), and general thinning and looser articulation of bones are trends. Many of these owe to juvenilization or paedomorphosis, something that is abundantly evident from comparison of a juvenile early theropod (Coelophysis) to early avialans like Archaeopteryx Near the avian crown, the premaxilla becomes dramatically enlarged and integrated into the characteristic mobile kinetic system of birds. We posit that this addition of a large element onto the skull may be biomechanically feasible only because of the paedomorphic shortening of the face; and kinesis of the beak only because of the paedomorphic thinning of the bones and loosening of articulations, as played out in reverse during the maturation of Coelophysis Finally, the beak itself becomes elaborated as the hands are integrated into the wing. There are structural, kinematic, and neurological similarities between avian pecking and primate grasping. The ability to precision-select high-quality food against a complex but depauperate background may have permitted crown birds to survive the end-Cretaceous cataclysm by feeding on insects, seeds, and other detritus after the collapse of higher trophic levels in the food web.

Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell.

The turtle shell represents a unique modification of the ancestral tetrapod body plan. The homologies of its approximately 50 bones have been the subject of debate for more than 200 years. Although most of those homologies are now firmly established, the evolutionary origin of the dorsal median nuchal bone of the carapace remains unresolved. We propose a novel hypothesis in which the nuchal is derived from the paired, laterally positioned cleithra-dorsal elements of the ancestral tetrapod pectoral girdle that are otherwise retained among extant tetrapods only in frogs. This hypothesis is supported by origin of the nuchal as paired, mesenchymal condensations likely derived from the neural crest followed by a unique two-stage pattern of ossification. Further support is drawn from the establishment of the nuchal as part of a highly conserved "muscle scaffold" wherein the cleithrum (and its evolutionary derivatives) serves as the origin of the Musculus trapezius. Identification of the nuchal as fused cleithra is congruent with its general spatial relationships to other elements of the shoulder girdle in the adult morphology of extant turtles, and it is further supported by patterns of connectivity and transformations documented by critical fossils from the turtle stem group. The cleithral derivation of the nuchal implies an anatomical reorganization of the pectoral girdle in which the dermal portion of the girdle was transformed from a continuous lateral-ventral arc into separate dorsal and ventral components. This transformation involved the reduction and eventual loss of the scapular rami of the clavicles along with the dorsal and superficial migration of the cleithra, which then fused with one another and became incorporated into the carapace.

Evolutionary origins of the avian brain.

Features that were once considered exclusive to modern birds, such as feathers and a furcula, are now known to have first appeared in non-avian dinosaurs. However, relatively little is known of the early evolutionary history of the hyperinflated brain that distinguishes birds from other living reptiles and provides the important neurological capablities required by flight. Here we use high-resolution computed tomography to estimate and compare cranial volumes of extant birds, the early avialan Archaeopteryx lithographica, and a number of non-avian maniraptoran dinosaurs that are phylogenetically close to the origins of both Avialae and avian flight. Previous work established that avian cerebral expansion began early in theropod history and that the cranial cavity of Archaeopteryx was volumetrically intermediate between these early forms and modern birds. Our new data indicate that the relative size of the cranial cavity of Archaeopteryx is reflective of a more generalized maniraptoran volumetric signature and in several instances is actually smaller than that of other non-avian dinosaurs. Thus, bird-like encephalization indices evolved multiple times, supporting the conclusion that if Archaeopteryx had the neurological capabilities required of flight, so did at least some other non-avian maniraptorans. This is congruent with recent findings that avialans were not unique among maniraptorans in their ability to fly in some form.

Evolutionary origin of the turtle shell.

The origin of the turtle shell has perplexed biologists for more than two centuries. It was not until Odontochelys semitestacea was discovered, however, that the fossil and developmental data could be synthesized into a model of shell assembly that makes predictions for the as-yet unestablished history of the turtle stem group. We build on this model by integrating novel data for Eunotosaurus africanus-a Late Guadalupian (∼260 mya) Permian reptile inferred to be an early stem turtle. Eunotosaurus expresses a number of relevant characters, including a reduced number of elongate trunk vertebrae (nine), nine pairs of T-shaped ribs, inferred loss of intercostal muscles, reorganization of respiratory muscles to the ventral side of the ribs, (sub)dermal outgrowth of bone from the developing perichondral collar of the ribs, and paired gastralia that lack both lateral and median elements. These features conform to the predicted sequence of character acquisition and provide further support that E. africanus, O. semitestacea, and Proganochelys quenstedti represent successive divergences from the turtle stem lineage. The initial transformations of the model thus occurred by the Middle Permian, which is congruent with molecular-based divergence estimates for the lineage, and remain viable whether turtles originated inside or outside crown Diapsida.

Birds have paedomorphic dinosaur skulls.

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony­change in the timing or rate of developmental events­has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.

Variation, variability, and the origin of the avian endocranium: insights from the anatomy of Alioramus altai (Theropoda: Tyrannosauroidea).

The internal braincase anatomy of the holotype of Alioramus altai, a relatively small-bodied tyrannosauroid from the Late Cretaceous of Mongolia, was studied using high-resolution computed tomography. A number of derived characters strengthen the diagnosis of this taxon as both a tyrannosauroid and a unique, new species (e.g., endocranial position of the gasserian ganglion, internal ramification of the facial nerve). Also present are features intermediate between the basal theropod and avialan conditions that optimize as the ancestral condition for Coelurosauria--a diverse group of derived theropods that includes modern birds. The expression of several primitive theropod features as derived character states within Tyrannosauroidea establishes previously unrecognized evolutionary complexity and morphological plasticity at the base of Coelurosauria. It also demonstrates the critical role heterochrony may have played in driving patterns of endocranial variability within the group and potentially reveals stages in the evolution of neuroanatomical development that could not be inferred based solely on developmental observations of the major archosaurian crown clades. We discuss the integration of paleontology with variability studies, especially as applied to the nature of morphological transformations along the phylogenetically long branches that tend to separate the crown clades of major vertebrate groups.

Finding the frame shift: digit loss, developmental variability, and the origin of the avian hand.

The origin of the tridactyl hand of crown birds from the pentadactyl hand of those early theropod dinosaurs lying along the avian stem has become a classic, but at times seemingly intractable, historical problem. The point in question is whether the fingers of crown birds represent digits 1-3 as predicted by generalized trends in the fossil record; or digits 2-4, as evidenced by the topology of the embryonic mesenchymal condensations from which the digits develop. The frame shift hypothesis attempted to resolve this paradox by making these signals congruent by means of a homeotic transformation in digital identity, but recently the paleontological support for this hypothesis was questioned. Here, we reassess the frame shift from a paleontological perspective by addressing what predictions a frame shift makes for skeletal morphology, whether the frame shift remains a viable explanation of the known fossil data, and where on the theropod tree the frame shift most likely occurred. Our results indicate that the frame shift remains viable, and based on the inferred pattern of digit loss, the frame shift likely occurred at a deeper position in theropod phylogeny than previously proposed. A new evolutionary model of the frame shift is described in which the early history of the frame-shifted hand is marked by an extended zone of developmental polymorphism. This model provides a new conceptual framework for the role of developmental variability in communicating broad evolutionary patterns on a taxonomically inclusive phylogenetic tree.

Identity of the avian wing digits: problems resolved and unsolved.

Controversy over bird wing digit identity has been a touchstone for various ideas in the phylogeny of birds, homology, and developmental evolution. This review summarizes the past 10 years of progress toward understanding avian digit identity. We conclude that the sum of evidence supports the Frame Shift Hypothesis, indicating that the avian wing digits have changed anatomical location. Briefly, the derivation of birds from theropod dinosaurs and the positional identities of the avian wing digits as 2, 3, and 4¹ are no longer in question. Additionally, increasing evidence indicates that the developmental programs for identity of the wing digits are of digits I, II, and III. Therefore, the attention moves from whether the digit identity frame shift occurred, to what the mechanisms of the frame shift were, and when in evolution it happened. There is considerable uncertainty about these issues and we identify exciting new research directions to resolve them.

Tyrannosaur paleobiology: new research on ancient exemplar organisms.

Tyrannosaurs, the group of dinosaurian carnivores that includes Tyrannosaurus rex and its closest relatives, are icons of prehistory. They are also the most intensively studied extinct dinosaurs, and thanks to large sample sizes and an influx of new discoveries, have become ancient exemplar organisms used to study many themes in vertebrate paleontology. A phylogeny that includes recently described species shows that tyrannosaurs originated by the Middle Jurassic but remained mostly small and ecologically marginal until the latest Cretaceous. Anatomical, biomechanical, and histological studies of T. rex and other derived tyrannosaurs show that large tyrannosaurs could not run rapidly, were capable of crushing bite forces, had accelerated growth rates and keen senses, and underwent pronounced changes during ontogeny. The biology and evolutionary history of tyrannosaurs provide a foundation for comparison with other dinosaurs and living organisms.

Transitional fossils and the origin of turtles.

The origin of turtles is one of the most contentious issues in systematics with three currently viable hypotheses: turtles as the extant sister to (i) the crocodile-bird clade, (ii) the lizard-tuatara clade, or (iii) Diapsida (a clade composed of (i) and (ii)). We reanalysed a recent dataset that allied turtles with the lizard-tuatara clade and found that the inclusion of the stem turtle Proganochelys quenstedti and the 'parareptile' Eunotosaurus africanus results in a single overriding morphological signal, with turtles outside Diapsida. This result reflects the importance of transitional fossils when long branches separate crown clades, and highlights unexplored issues such as the role of topological congruence when using fossils to calibrate molecular clocks.

A long-snouted, multihorned tyrannosaurid from the Late Cretaceous of Mongolia.

Tyrannosaurid theropods are characterized by a generalized body plan, and all well-known taxa possess deep and robust skulls that are optimized for exerting powerful bite forces. The fragmentary Late Cretaceous Alioramus appears to deviate from this trend, but its holotype and only known specimen is incomplete and poorly described. A remarkable new tyrannosaurid specimen from the Maastrichtian (Late Cretaceous) of Mongolia, including a nearly complete and well-preserved skull and an extensive postcranium, represents a new species of Alioramus, Alioramus altai. This specimen conclusively demonstrates that Alioramus is a small, gracile, long-snouted carnivore that deviates from other tyrannosaurids in its body plan and presumably its ecological habits. As such, it increases the range of morphological diversity in one of the most familiar extinct clades. Phylogenetic analysis places Alioramus deep within the megapredatory Tyrannosauridae, and within the tyrannosaurine subclade that also includes Tarbosaurus and Tyrannosaurus. Both pneumatization and ornamentation are extreme compared with other tyrannosaurids, and the skull contains eight discrete horns. The new specimen is histologically aged at nine years old but is smaller than other tyrannosaurids of similar age. Despite its divergent cranial form, Alioramus is characterized by a similar sequence of ontogenetic changes as the megapredatory Tyrannosaurus and Albertosaurus, indicating that ontogenetic change is conservative in tyrannosaurids.

The postnatal skull of the extant North American turtle Pseudemys texana (Cryptodira: Emydidae), with comments on the study of discrete intraspecific variation.

This study describes the postnatal morphology of the skull in the extant testudinoid turtle Pseudemys texana. The material basis of this study is drawn from a single population and therefore provides the opportunity to document cranial variation expressed at multiple levels of inference (e.g., ontogeny, sexual dimorphism, individual) within a taxonomically restricted sample. Such descriptions are exceedingly rare for reptiles but are important for evaluating the inherent biological information that skeletal morphology provides to more inclusive biological questions. Results indicate that postnatal variation in Pseudemys texana for discrete cranial characters is considerable, especially when recognizing the taxonomically conservative nature of the sample and the fact that most of the examined characters were drawn from published phylogenetic analyses. Results demonstrate a complex relationship between size, skeletal maturity, and the expression of discrete skeletal characters in this sexually dimorphic reptile. Such complexity potentially could affect our interpretation of evolutionary history based on discrete characters. This study emphasizes the need for increasing the numbers and taxonomic breadth of morphological descriptions based on expanded samples so that a better understanding of the phylogenetic distribution and modular expression of anatomical variability can be achieved. The available empirical data lag seriously behind recent theoretical advances that broaden the application of intraspecific variation data for discrete characters to phylogenetic and evolutionary questions.