Avian tail ontogeny, pygostyle formation, and interpretation of juvenile Mesozoic specimens

The avian tail played a critical role in the evolutionary transition from long- to short-tailed birds, yet its ontogeny in extant birds has largely been ignored. This deficit has hampered efforts to effectively identify intermediate species during the Mesozoic transition to short tails. Here we show that fusion of distal vertebrae into the pygostyle structure does not occur in extant birds until near skeletal maturity, and mineralization of vertebral processes also occurs long after hatching. Evidence for post-hatching pygostyle formation is also demonstrated in two Cretaceous specimens, a juvenile enantiornithine and a subadult basal ornithuromorph. These findings call for reinterpretations of Zhongornis haoae, a Cretaceous bird hypothesized to be an intermediate in the long- to short-tailed bird transition, and of the recently discovered coelurosaur tail embedded in amber. Zhongornis, as a juvenile, may not yet have formed a pygostyle, and the amber-embedded tail specimen is reinterpreted as possibly avian. Analyses of relative pygostyle lengths in extant and Cretaceous birds suggests the number of vertebrae incorporated into the pygostyle has varied considerably, further complicating the interpretation of potential transitional species. In addition, this analysis of avian tail development reveals the generation and loss of intervertebral discs in the pygostyle, vertebral bodies derived from different kinds of cartilage, and alternative modes of caudal vertebral process morphogenesis in birds. These findings demonstrate that avian tail ontogeny is a crucial parameter specifically for the interpretation of Mesozoic specimens, and generally for insights into vertebrae formation

First Evidence of Dinosaurian Secondary Cartilage in the Post-Hatching Skull of Hypacrosaurus stebingeri (Dinosauria, Ornithischia)

Bone and calcified cartilage can be fossilized and preserved for hundreds of millions of years. While primary cartilage is fairly well studied in extant and fossilized organisms, nothing is known about secondary cartilage in fossils. In extant birds, secondary cartilage arises after bone formation during embryonic life at articulations, sutures and muscular attachments in order to accommodate mechanical stress. Considering the phylogenetic inclusion of birds within the Dinosauria, we hypothesized a dinosaurian origin for this “avian” tissue. Therefore, histological thin sectioning was used to investigate secondary chondrogenesis in disarticulated craniofacial elements of several post-hatching specimens of the non-avian dinosaur Hypacrosaurus stebingeri (Ornithischia, Lambeosaurinae). Secondary cartilage was found on three membrane bones directly involved with masticatory function: (1) as nodules on the dorso-caudal face of a surangular; and (2) on the bucco-caudal face of a maxilla; and (3) between teeth as islets in the alveolar processes of a dentary. Secondary chondrogenesis at these sites is consistent with the locations of secondary cartilage in extant birds and with the induction of the cartilage by different mechanical factors - stress generated by the articulation of the quadrate, stress of a ligamentous or muscular insertion, and stress of tooth formation. Thus, our study reveals the first evidence of “avian” secondary cartilage in a non-avian dinosaur. It pushes the origin of this “avian” tissue deep into dinosaurian ancestry, suggesting the creation of the more appropriate term “dinosaurian” secondary cartilage

Data from: Joint histology in Alligator mississippiensis challenges the identification of synovial joints in fossil archosaurs and inferences of cranial kinesis

Archosaurs, like all vertebrates, have different types of joints that allow or restrict cranial kinesis, such as synovial joints and fibrous joints. In general, synovial joints are more kinetic than fibrous joints, because the former possess a fluid-filled cavity and articular cartilage that facilitate movement. Even though there is a considerable lack of data on the microstructure and the structure–function relationships in the joints of extant archosaurs, many functional inferences of cranial kinesis in fossil archosaurs have hinged on the assumption that elongated condylar joints are (i) synovial and/or (ii) kinetic. Cranial joint microstructure was investigated in an ontogenetic series of American alligators, Alligator mississippiensis. All the presumably synovial, condylar joints found within the head of the American alligator (the jaw joint, otic joint and laterosphenoid–postorbital (LS–PO) joint) were studied by means of paraffin histology and undecalcified histology paired with micro-computed tomography data to better visualize three-dimensional morphology. Results show that among the three condylar joints of A. mississippiensis, the jaw joint was synovial as expected, but the otherwise immobile otic and LS–PO joints lacked a synovial cavity. Therefore, condylar morphology does not always imply the presence of a synovial articulation nor mobility. These findings reveal an undocumented diversity in the joint structure of alligators and show that crocodylians and birds build novel, kinetic cranial joints differently. This complicates accurate identification of synovial joints and functional inferences of cranial kinesis in fossil archosaurs and tetrapods in general

MUVC AL_623 DICOM

microCT data of a juvenile American alligator (Alligator mississippiensis) scanned on a Siemens Inveon MicroCT at 21µm

La métaplasie interprétée comme un processus de formation de certains tissus minéralisés de dinosaures : une évaluation préliminaire

Les biologistes évolutionnistes définissent la « métaplasie » comme la transformation permanente de l’identité d’une cellule, et il existe beaucoup d’exemples de ce type de transformation chez les vertébrés actuels (par exemple, des chondrocytes qui se transforment en ostéoblastes). Ces métaplasies ont été observées pendant la minéralisation des tendons « ossifiés » d’oiseaux actuels. Dans cette étude, nous avons examiné des tendons ossifiés de Bubo et Meleagris, et utilisé les caractéristiques de leurs tissus métaplastiques pour reconnaître ces derniers chez plusieurs dinosaures non aviens. Les éléments fossilisés qui composent notre échantillon sont variés et incluent des tendons et un os nasal d’hadrosaure, la base de la massue de la queue d’un ankylosaure, des épines neurales de sauropodes et des apophyses allongées de vertèbres caudales de dromaeosaures. Les tendons minéralisés aviens montrent un tissu primaire (analogue à celui de l’os primaire) et des reconstructions secondaires (RSs ; analogues aux ostéones secondaires). Ces deux tissus sont composés de faisceaux fibreux qui sont très compactés et séparés par des espaces en forme d’arcs en section transversale. Lorsqu’ils sont observés longitudinalement, ces faisceaux forment des stratifications en arêtes de poissons (herringbone). Il n’y a aucune évidence d’ostéocytes au niveau de ce tissu primaire, et les espaces précédemment interprétés comme des lacunes ostéocytaires sont en fait simplement des espaces vides entre les faisceaux fibreux. Le tissu qui entoure les espaces vasculaires est dense, non vascularisé et apparemment hyperminéralisé. La minéralisation des fibres se fait de façon centrifuge. Chez les dinosaures non aviens, les structures primaires et secondaires sont identiques à celles trouvées dans les tendons minéralisés aviens. En effet, (1) ils sont très fibreux ; (2) ils ont des faisceaux fibreux séparés par des espaces en forme d’arc en section transversale, et (3) ils sont disposés en arêtes de poisson (herringbone) en vue longitudinale. Les RSs sont différentes des systèmes haversiens typiques, car elles possèdent des bords irréguliers, ce qui suggère une destruction de la matrice fibreuse et la formation d’espaces vasculaires initiaux (peut-être due à une lyse enzymatique ou une phagocytose). Par la suite, des fibroblastes, fibrocytes ou autres cellules auraient pris part au remodelage. Des ostéocytes avec des canalicules ont été observés uniquement dans des RSs matures, localisées profondément dans les éléments (et non au niveau de leurs bordures extérieures). Comme les tissus primaires et secondaires des fossiles sont identiques à ceux trouvés dans les tendons minéralisés d’oiseaux actuels, il est probable que des processus similaires sont responsables de la formation de ces éléments fossiles. Leurs propriétés biomécaniques étaient aussi vraisemblablement similaires, présentant peut-être une résistance aux traumatismes, comme la fibre de carbone. Même si le tissu primaire de l’épine neurale du sauropode est différent des autres tissus et semble être formé de fibrocartilage hyperminéralisé, ces RSs sont similaires à celles observées chez les autres dinosaures. Puisqu’aucune lacune ostéocytaire n’a été observée dans ces tissus primaires de dinosaures, nous formons l’hypothèse que ces tissus fossilisés ont étés formés par transformations métaplastiques (peut-être à partir de fibroblastes), plutôt que par ossification périostique et intramembranaire. Cette étude suggère que des modes de minéralisation alternatifs auraient pu être plus abondants chez les dinosaures non aviens que ce qui est généralement accepté.Evolutionary biologists define “metaplasia” as the permanent transformation of a cell identity, and there are many examples of such transformations in living vertebrates (e.g., chondrocytes transforming directly into osteoblasts). These metaplasias have been observed during the mineralization of “ossified” tendons of living birds. In the present study, we examined “ossified” tendons in Bubo and Meleagris and used the characteristics of these metaplastic tissues to recognize them in several non-avian dinosaur taxa. The fossilized skeletal elements that form our sample are varied and include hadrosaurian tendons and a nasal bone, an ankylosaur tail club “handle”, sauropod neural spines, and some dromaeosaur tail rods. The extant avian mineralized tendons were formed of a primary tissue (analogous to primary bone) and secondary reconstructions (SRs; analogous to secondary osteons). Both were composed of fiber bundles (or fascicles) that were closely packed together and separated by arc-shaped spaces in cross-section. When viewed longitudinally, they were arranged in a herringbone pattern. There is no evidence of osteocytes within the primary tendon matrix; what was previously interpreted as osteocyte lacunae are instead arc-shaped spaces between fiber fascicles, and tissue immediately surrounding vascular spaces is dense, avascular and apparently hypermineralized. Mineralization of fibers began centrally and moved in a centrifugal direction. In the non-avian dinosaurs examined, primary and secondary tissue structures were virtually identical to those found within the avian mineralized tendons. Indeed, (1) they were densely fibrous; (2) they showed fiber fascicles separated by arcuate-shaped spaces when viewed transversally, and (3) they were arranged in a herringbone pattern longitudinally. SRs differ from typical Haversian systems in possessing highly irregular borders, suggesting destruction of the fibrous matrix and formation of initial vascular spaces was accomplished perhaps by phagocytosis or enzymatic lysis with subsequent remodeling by fibrocytes, fibroblasts, or an as of yet unknown cell type. Osteocytes with canaliculi were only observed in “mature” SRs, found deep within the elements (and never close to their external borders). Because fossilized primary and secondary tissue structures were identical to those found within the avian mineralized tendons examined, it is likely that identical processes are responsible for their formation. Biomechanical properties were also likely similar, potentially affording carbon fiber-like, trauma-resistant properties to the “ossified” tendons and nasal bones of hadrosaurs, the tail “handles” of ankylosaurs, and the tail rods of dromaeosaurs. In contrast, the primary tissue from a sauropod mineralized nuchal ligament appears to be made of hypermineralized fibrocartilage, but the SRs interdigitating with the hypermineralized fibrocartilage resemble the reconstructions observed in the other fossil skeletal elements and likely formed by the same processes. Since no osteocyte lacunae were observed in any of these dinosaurian primary tissues, we hypothesize that the fossilized cranial and skeletal elements examined here formed through metaplastic transformation (perhaps from fibroblasts) rather than by periosteal and intramembranous ossification. This study suggests that alternative modes of mineralization might be more abundant in non-avian dinosaurs than previously reported.</p

MUVC AL_721 DICOM

Medical CT data of adult Alligator mississippiensis scanned at 600µm slice thickness

Dinosaur paleohistology : Review, trends and new avenues of investigation

In the mid-19th century, the discovery that bone microstructure in fossils could be preserved with fidelity provided a new avenue for understanding the evolution, function, and physiology of long extinct organisms. This resulted in the establishment of paleohistology as a subdiscipline of vertebrate paleontology, which has contributed greatly to our current understanding of dinosaurs as living organisms. Dinosaurs are part of a larger group of reptiles, the Archosauria, of which there are only two surviving lineages, crocodilians and birds. The goal of this review is to document progress in the field of archosaur paleohistology, focusing in particular on the Dinosauria. We briefly review the "growth age" of dinosaur histology, which has encompassed new and varied directions since its emergence in the 1950s, resulting in a shift in the scientific perception of non-avian dinosaurs from "sluggish" reptiles to fast-growing animals with relatively high metabolic rates. However, fundamental changes in growth occurred within the sister clade Aves, and we discuss this major evolutionary transition as elucidated by histology. We then review recent innovations in the field, demonstrating how paleohistology has changed and expanded to address a diversity of non-growth related questions. For example, dinosaur skull histology has elucidated the formation of curious cranial tissues (e.g., "metaplastic" tissues), and helped to clarify the evolution and function of oral adaptations, such as the dental batteries of duck-billed dinosaurs. Lastly, we discuss the development of novel techniques with which to investigate not only the skeletal tissues of dinosaurs, but also less-studied soft-tissues, through molecular paleontology and paleohistochemistry-recently developed branches of paleohistology- and the future potential of these methods to further explore fossilized tissues. We suggest that the combination of histological and molecular methods holds great potential for examining the preserved tissues of dinosaurs, basal birds, and their extant relatives. This review demonstrates the importance of traditional bone paleohistology, but also highlights the need for innovation and new analytical directions to improve and broaden the utility of paleohistology, in the pursuit of more diverse, highly specific, and sensitive methods with which to further investigate important paleontological questions

Fusion Patterns in the Skulls of Modern Archosaurs Reveal That Sutures Are Ambiguous Maturity Indicators for the Dinosauria.

The sutures of the skulls of vertebrates are generally open early in life and slowly close as maturity is attained. The assumption that all vertebrates follow this pattern of progressive sutural closure has been used to assess maturity in the fossil remains of non-avian dinosaurs. Here, we test this assumption in two members of the Extant Phylogenetic Bracket of the Dinosauria, the emu, Dromaius novaehollandiae and the American alligator, Alligator mississippiensis, by investigating the sequence and timing of sutural fusion in their skulls. As expected, almost all the sutures in the emu skull progressively close (i.e., they get narrower) and then obliterate during ontogeny. However, in the American alligator, only two sutures out of 36 obliterate completely and they do so during embryonic development. Surprisingly, as maturity progresses, many sutures of alligators become wider in large individuals compared to younger, smaller individuals. Histological and histomorphometric analyses on two sutures and one synchondrosis in an ontogenetic series of American alligator confirmed our morphological observations. This pattern of sutural widening might reflect feeding biomechanics and dietary changes through ontogeny. Our findings show that progressive sutural closure is not always observed in extant archosaurs, and therefore suggest that cranial sutural fusion is an ambiguous proxy for assessing maturity in non-avian dinosaurs

Ontogeny reveals function and evolution of the hadrosaurid dinosaur dental battery

Abstract Background Hadrosaurid dinosaurs, dominant Late Cretaceous herbivores, possessed complex dental batteries with up to 300 teeth in each jaw ramus. Despite extensive interest in the adaptive significance of the dental battery, surprisingly little is known about how the battery evolved from the ancestral dinosaurian dentition, or how it functioned in the living organism. We undertook the first comprehensive, tissue-level study of dental ontogeny in hadrosaurids using several intact maxillary and dentary batteries and compared them to sections of other archosaurs and mammals. We used these comparisons to pinpoint shifts in the ancestral reptilian pattern of tooth ontogeny that allowed hadrosaurids to form complex dental batteries. Results Comparisons of hadrosaurid dental ontogeny with that of other amniotes reveals that the ability to halt normal tooth replacement and functionalize the tooth root into the occlusal surface was key to the evolution of dental batteries. The retention of older generations of teeth was driven by acceleration in the timing and rate of dental tissue formation. The hadrosaurid dental battery is a highly modified form of the typical dinosaurian gomphosis with a unique tooth-to-tooth attachment that permitted constant and perfectly timed tooth eruption along the whole battery. Conclusions We demonstrate that each battery was a highly dynamic, integrated matrix of living replacement and, remarkably, dead grinding teeth connected by a network of ligaments that permitted fine scale flexibility within the battery. The hadrosaurid dental battery, the most complex in vertebrate evolution, conforms to a surprisingly simple evolutionary model in which ancestral reptilian tissue types were redeployed in a unique manner. The hadrosaurid dental battery thus allows us to follow in great detail the development and extended life history of a particularly complex food processing system, providing novel insights into how tooth development can be altered to produce complex dentitions, the likes of which do not exist in any living vertebrate