Evolution of dinosaur epidermal structures

Spectacularly preserved non-avian dinosaurs with integumentary filaments/feathers have revolutionized dinosaur studies and fostered the suggestion that the dinosaur common ancestor possessed complex integumentary structures homologous to feathers. This hypothesis has major implications for interpreting dinosaur biology, but has not been tested rigorously. Using a comprehensive database of dinosaur skin traces, we apply maximum-likelihood methods to reconstruct the phylogenetic distribution of epidermal structures and interpret their evolutionary history. Most of these analyses find no compelling evidence for the appearance of protofeathers in the dinosaur common ancestor and scales are usually recovered as the plesiomorphic state, but results are sensitive to the outgroup condition in pterosaurs. Rare occurrences of ornithischian filamentous integument might represent independent acquisitions of novel epidermal structures that are not homologous with theropod feathers.     

Studies of the fossil dinosaur bone in the scanning electron microscope.

A fossil dinosaur bone, 80 million years old, was subjected to investigation in the scanning microscope. The bone surfaces to be examined were prepared with appropritely modified methods used in the technique of replication in transmission electron microscopy. In the scanning microscope pictures of vascular canals were obtained. The walls of these canals were shown to be formed of collagen fibrils. Moreover, it was demonstrated that the internal surface of the canal wall is made up of bundles of collagen fibrils which run obliquely, corkscrewwise, and in the form of plexus to the long axis of tke canal; Besides, osteocytes of the dinosaur bone were isolated and pictures of their spatial structure together with characteristic points of departure of processes from the cell body were obtained.     

The first record of a dinosaur from Bulgaria

Mateus, O., Dyke, G.J., Motchurova-Dekova, N., Kamenov, G.D. & Ivanov, P. 2010: The first record of a dinosaur from Bulgaria. Lethaia, Vol. 43, pp. 88–94.
A portion of a left humerus from the Upper Maastrichtian of Vratsa district (NW Bulgaria) is shown to be from a non-avian theropod dinosaur: this is the first record of a dinosaur from Bulgaria. We describe this bone, suggest that it most likely pertains to an ornithomimosaur, and discuss the fossil record of other similar taxa of Late Cretaceous age that have been reported from Europe. To investigate the taphonomy of this fossil, rare earth element (REE) analysis is combined with strontium (Sr) isotope data to confirm that this Bulgarian dinosaur bone was initially fossilized in a terrestrial environment, then later re-worked into late Maastrichtian marine sediments. □ Bulgaria , Dinosauria , Late Cretaceous , Ornithomimosauria , rare earth elements , Sr isotopes , taphonomy , Theropoda .     

Was Dinosaurian Physiology Inherited by Birds? Reconciling Slow Growth in Archaeopteryx

Background

Archaeopteryx is the oldest and most primitive known bird (Avialae). It is believed that the growth and energetic physiology of basalmost birds such as Archaeopteryx were inherited in their entirety from non-avialan dinosaurs. This hypothesis predicts that the long bones in these birds formed using rapidly growing, well-vascularized woven tissue typical of non-avialan dinosaurs.

Methodology/Principal Findings

We report that Archaeopteryx long bones are composed of nearly avascular parallel-fibered bone. This is among the slowest growing osseous tissues and is common in ectothermic reptiles. These findings dispute the hypothesis that non-avialan dinosaur growth and physiology were inherited in totality by the first birds. Examining these findings in a phylogenetic context required intensive sampling of outgroup dinosaurs and basalmost birds. Our results demonstrate the presence of a scale-dependent maniraptoran histological continuum that Archaeopteryx and other basalmost birds follow. Growth analysis for Archaeopteryx suggests that these animals showed exponential growth rates like non-avialan dinosaurs, three times slower than living precocial birds, but still within the lowermost range for all endothermic vertebrates.

Conclusions/Significance

The unexpected histology of Archaeopteryx and other basalmost birds is actually consistent with retention of the phylogenetically earlier paravian dinosaur condition when size is considered. The first birds were simply feathered dinosaurs with respect to growth and energetic physiology. The evolution of the novel pattern in modern forms occurred later in the group''s history.     

Dinosaur peptides suggest mechanisms of protein survival

Eleven collagen peptide sequences recovered from chemical extracts of dinosaur bones were mapped onto molecular models of the vertebrate collagen fibril derived from extant taxa. The dinosaur peptides localized to fibril regions protected by the close packing of collagen molecules, and contained few acidic amino acids. Four peptides mapped to collagen regions crucial for cell-collagen interactions and tissue development. Dinosaur peptides were not represented in more exposed parts of the collagen fibril or regions mediating intermolecular cross-linking. Thus functionally significant regions of collagen fibrils that are physically shielded within the fibril may be preferentially preserved in fossils. These results show empirically that structure-function relationships at the molecular level could contribute to selective preservation in fossilized vertebrate remains across geological time, suggest a 'preservation motif', and bolster current concepts linking collagen structure to biological function. This non-random distribution supports the hypothesis that the peptides are produced by the extinct organisms and suggests a chemical mechanism for survival.     

Dinosaurian soft tissues interpreted as bacterial biofilms

A scanning electron microscope survey was initiated to determine if the previously reported findings of "dinosaurian soft tissues" could be identified in situ within the bones. The results obtained allowed a reinterpretation of the formation and preservation of several types of these "tissues" and their content. Mineralized and non-mineralized coatings were found extensively in the porous trabecular bone of a variety of dinosaur and mammal species across time. They represent bacterial biofilms common throughout nature. Biofilms form endocasts and once dissolved out of the bone, mimic real blood vessels and osteocytes. Bridged trails observed in biofilms indicate that a previously viscous film was populated with swimming bacteria. Carbon dating of the film points to its relatively modern origin. A comparison of infrared spectra of modern biofilms with modern collagen and fossil bone coatings suggests that modern biofilms share a closer molecular make-up than modern collagen to the coatings from fossil bones. Blood cell size iron-oxygen spheres found in the vessels were identified as an oxidized form of formerly pyritic framboids. Our observations appeal to a more conservative explanation for the structures found preserved in fossil bone.     

Analysis of fossil bone organic matrix by transmission electron microscopy

A transmission electron microscope (TEM) study was initiated on samples of geological ages ranging from Devonian to Jurassic to analyse the ultrastructure of the organic matrix in fossil bones that have preserved a histological structure after demineralisation. All samples show a network of variably well-preserved fibrils. Within the sampling, the best results were obtained in two specimens: the scales of the Devonian sarcopterygian tetrapodomorph Eustenopteron foordi, and the humerus of Jurassic dinosaur Lappentosaurus madagascariensis. Despite an extended time difference between both specimens, their fossil bone is composed of a plywood-like structure in which the fibrils are very closely packed. These observations support the hypothesis that dense initial packing of collagen fibrils favours the preservation of the fossil bone.     

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.     

The turnover of mineralized growth plate cartilage into bone may be regulated by osteocytes

During endochondral ossification, growth plate cartilage is replaced with bone. Mineralized cartilage matrix is resorbed by osteoclasts, and new bone tissue is formed by osteoblasts. As mineralized cartilage does not contain any cells, it is unclear how this process is regulated. We hypothesize that, in analogy with bone remodeling, osteoclast and osteoblast activity are regulated by osteocytes, in response to mechanical loading. Since the cartilage does not contain osteocytes, this means that cartilage turnover during endochondral ossification would be regulated by the adjacent bone tissue. We investigated this hypothesis with an established computational bone adaptation model. In this model, osteocytes stimulate osteoblastic bone formation in response to the mechanical bone tissue loading. Osteoclasts resorb bone near randomly occurring microcracks that are assumed to block osteocyte signals. We used finite element modeling to evaluate our hypothesis in a 2D-domain representing part of the growth plate and adjacent bone. Cartilage was added at a constant physiological rate to simulate growth. Simulations showed that osteocyte signals from neighboring bone were sufficient for successful cartilage turnover, since equilibrium between cartilage remodeling and growth was obtained. Furthermore, there was good agreement between simulated bone structures and rat tibia histology, and the development of the trabecular architecture resembled that of infant long bones. Additionally, prohibiting osteoclast invasion resulted in thickened mineralized cartilage, similar to observations in a knock-out mouse model. We therefore conclude that it is well possible that osteocytes regulate the turnover of mineralized growth plate cartilage.     

Dinosaurs and the Cretaceous Terrestrial Revolution

The observed diversity of dinosaurs reached its highest peak during the mid- and Late Cretaceous, the 50 Myr that preceded their extinction, and yet this explosion of dinosaur diversity may be explained largely by sampling bias. It has long been debated whether dinosaurs were part of the Cretaceous Terrestrial Revolution (KTR), from 125-80 Myr ago, when flowering plants, herbivorous and social insects, squamates, birds and mammals all underwent a rapid expansion. Although an apparent explosion of dinosaur diversity occurred in the mid-Cretaceous, coinciding with the emergence of new groups (e.g. neoceratopsians, ankylosaurid ankylosaurs, hadrosaurids and pachycephalosaurs), results from the first quantitative study of diversification applied to a new supertree of dinosaurs show that this apparent burst in dinosaurian diversity in the last 18 Myr of the Cretaceous is a sampling artefact. Indeed, major diversification shifts occurred largely in the first one-third of the group's history. Despite the appearance of new clades of medium to large herbivores and carnivores later in dinosaur history, these new originations do not correspond to significant diversification shifts. Instead, the overall geometry of the Cretaceous part of the dinosaur tree does not depart from the null hypothesis of an equal rates model of lineage branching. Furthermore, we conclude that dinosaurs did not experience a progressive decline at the end of the Cretaceous, nor was their evolution driven directly by the KTR.     

Assessing dinosaur growth patterns: a microscopic revolution

Some of the longest standing questions in dinosaur paleontology pertain to their development. Did dinosaurs grow at slow rates similar to extant reptiles or rapidly similar to living birds and mammals? How did some forms attain gigantic proportions? Conversely, how did birds (avian dinosaurs) become miniaturized? New data on dinosaur longevity garnered from bone microstructure (i.e. osteohistology) are making it possible to assess basic life-history parameters of the dinosaurs such as growth rates and timing of developmental events. Analyses of these data in an evolutionary context are enabling the identification of developmental patterns that lead to size changes within the Dinosauria. Furthermore, this rich new database is providing inroads for studying individual and population biology. All in all, paleohistological research is proving to be the most promising avenue towards gaining a comprehensive understanding of dinosaur biology.     

Fungal Ferromanganese Mineralisation in Cretaceous Dinosaur Bones from the Gobi Desert,Mongolia

Well-preserved mycelia of fungal- or saprolegnia-like biota mineralised by ferromanganese oxides were found for the first time in long bones of Late Cretaceous dinosaurs from the Gobi Desert (Nemegt Valley, Mongolia). The mycelia formed a biofilm on the wall of the bone marrow cavity and penetrated the osteon channels of the nearby bone tissue. Optical microscopy, Raman, SEM/EDS, SEM/BSE, electron microprobe and cathodoluminescence analyses revealed that the mineralisation of the mycelia proceeded in two stages. The first stage was early post-mortem mineralisation of the hyphae by Fe/Mn-oxide coatings and microconcretions. Probably this proceeded in a mildly acidic to circumneutral environment, predominantly due to heterotrophic bacteria degrading the mycelial necromass and liberating Fe and Mn sorbed by the mycelia during its lifetime. The second stage of mineralisation, which proceeded much later following the final burial of the bones in an alkaline environment, resulted from the massive precipitation of calcite and occasionally barite on the iron/manganese-oxide-coated mycelia. The mineral phases produced by fungal biofilms colonising the interiors of decaying dinosaur bones not only enhance the preservation (fossilisation) of fungal remains but can also be used as indicators of the geochemistry of the dinosaur burial sites.     

Study on the Fossil Woods Found in Zigong,Sichuan, China

This paper describes three fossil woods, which were firstly found in Zigong city, Sichuan Province, China. The localities of the fossil woods are close to the locality of the famous Dashanpu dinosaur quarry of Zigong. The strata of the fossil woods beating are Xiashaximiao Formation and Xintiangou Formation of the Middle Jurassic, approximately match the strata of the Dashanpu dinosaurs. According to the structures of the secondary xylem, the fossil woods belonged to the primitive conifer genus-Araucarioxylon. Because it was comparatively and obviously different from the other species in this genus, it is assigned as a new species: A. zigongensis. As there was neither fossil leaf nor fossil pollen or spore found in the dinosaur bearing strata before, the discovery of these fossil woods might bear some important significance in the dinosaur research.     

Metabolic pathways of the fossil dinosaur bones Part II. Vascular canal in the communication system

Examination was made on the fossil dinosaur bone 80 million years old. Samples to be examined were prepared by specially elaborated methods. The vascular canal of the dinosaur bone was the object of study. The microscopic and ultrastructural images of the canal revealed three zones therein: proper, perivascular, and vascular. The zone proper was formed by the mineralized wall of the canal, the perivascular zone was a space between the proper and the vascular zone, and the vascular zone was made up of the canal contents identified with blood vessels. The perivascular zone contained collagen fibres; moreover, histochemical examinations revealed in it mucopolysaccharides and lipids. In the wall of the vascular canal (zone proper) the outlets of the bone canaliculi departing from the osteocyte lacunae were detected. The endings of these canaliculi were of two kinds: they were either of the same diameter as the rest of the canaliculus (more numerous) or assumed a widening funnel form as the canaliculi reached the vascular canal (less numerous). By analogy with modern bone appropriate functions may be ascribed to particular zones distinguished in the vascular canal and to the varied endings of the bone canaliculi in the system of conveyance of nutrient and conservative elements as well as metabolites.     

Dinosaur protofeathers: pushing back the origin of feathers into the Middle Triassic?

Reports of primordial feathers (protofeathers) in dinosaurs have received widespread interest. Recently, it was proposed that a novel protofeather in the theropod dinosaur Beipiaosaurus completes the transitional series in the evolution of the feather and provides the first evidence of filamentous feathers as display in nonavian theropods. A more far-reaching evolutionary ramification is the claim that these structures push the origin of monofilamentous integumentary structures into the Middle Triassic or earlier. I discuss problems with the analyses within the broader context of studies concerning the hypothesis of protofeathers, and show that affinity between the integumentary structures in Beipiaosaurus and feathers is improbable. The scientific methodology is questioned by its failure to make phenomena perceivable by objective means, by questionable rationalizations in critical issues, and by lack of consideration of exceptions to the postulated thesis. The notion that primordial feathers occurred in a clade more inclusive than the Coelurosauria and that it is supported by the presence of integumental structures in Psittacosaurus is analyzed and rejected.     

Bone microstructure and developmental plasticity in birds and other dinosaurs

Patterns of bone microstructure have frequently been used to deduce dynamics and processes of growth in extant and fossil tetrapods. Often, the various types of primary bone tissue have been associated with different bone deposition rates and more recently such deductions have extended to patterns observed in dinosaur bone microstructure. These previous studies are challenged by the findings of the current research, which integrates an experimental neontological approach and a paleontological comparison. We use tetracycline labeling and morphometry to study the variability of bone deposition rates in Japanese quail (Coturnix japonica) growing under different experimental conditions. We compare resulting patterns in bone microstructure with those found in fossil birds and other dinosaurs. We found that a single type of primary bone varies significantly in rates of growth in response to environmental conditions. Ranging between 10-50 microm per day, rates of growth overlap with the full range of bone deposition rates that were previously associated with different patterns of bone histology. Bone formation rate was significantly affected by environmental/experimental conditions, skeletal element, and age. In the quail, the experimental conditions did not result in formation of lines of arrested growth (LAGs). Because of the observed variation of bone deposition rates in response to variation in environmental conditions, we conclude that bone deposition rates measured in extant birds cannot simply be extrapolated to their fossil relatives. Additionally, we observe the variable incidence of LAGs and annuli among several dinosaur species, including fossil birds, extant sauropsids, as well as nonmammalian synapsids, and some extant mammals. This suggests that the ancestral condition of the response of bone to environmental conditions was variable. We propose that such developmental plasticity in modern birds may be reduced in association with the shortened developmental time during the later evolution of the ornithurine birds.     

A novel method for biomaterial scaffold internal architecture design to match bone elastic properties with desired porosity

An often-proposed tissue engineering design hypothesis is that the scaffold should provide a biomimetic mechanical environment for initial function and appropriate remodeling of regenerating tissue while concurrently providing sufficient porosity for cell migration and cell/gene delivery. To provide a systematic study of this hypothesis, the ability to precisely design and manufacture biomaterial scaffolds is needed. Traditional methods for scaffold design and fabrication cannot provide the control over scaffold architecture design to achieve specified properties within fixed limits on porosity. The purpose of this paper was to develop a general design optimization scheme for 3D internal scaffold architecture to match desired elastic properties and porosity simultaneously, by introducing the homogenization-based topology optimization algorithm (also known as general layout optimization). With an initial target for bone tissue engineering, we demonstrate that the method can produce highly porous structures that match human trabecular bone anisotropic stiffness using accepted biomaterials. In addition, we show that anisotropic bone stiffness may be matched with scaffolds of widely different porosity. Finally, we also demonstrate that prototypes of the designed structures can be fabricated using solid free-form fabrication (SFF) techniques.     

An analysis of dinosaurian biogeography: evidence for the existence of vicariance and dispersal patterns caused by geological events

As the supercontinent Pangaea fragmented during the Mesozoic era, dinosaur faunas were divided into isolated populations living on separate continents. It has been predicted, therefore, that dinosaur distributions should display a branching ('vicariance') pattern that corresponds with the sequence and timing of continental break-up. Several recent studies, however, minimize the importance of plate tectonics and instead suggest that dispersal and regional extinction were the main controls on dinosaur biogeography. Here, in order to test the vicariance hypothesis, we apply a cladistic biogeographical method to a large dataset on dinosaur relationships and distributions. We also introduce a methodological refinement termed 'time-slicing', which is shown to be a key step in the detection of ancient biogeographical patterns. These analyses reveal biogeographical patterns that closely correlate with palaeogeography. The results provide the first statistically robust evidence that, from Middle Jurassic to mid-Cretaceous times, tectonic events had a major role in determining where and when particular dinosaur groups flourished. The fact that evolutionary trees for extinct organisms preserve such distribution patterns opens up a new and fruitful direction for palaeobiogeographical research.     

The first 50Myr of dinosaur evolution: macroevolutionary pattern and morphological disparity

The evolutionary radiation of dinosaurs in the Late Triassic and Early Jurassic was a pivotal event in the Earth's history but is poorly understood, as previous studies have focused on vague driving mechanisms and have not untangled different macroevolutionary components (origination, diversity, abundance and disparity). We calculate the morphological disparity (morphospace occupation) of dinosaurs throughout the Late Triassic and Early Jurassic and present new measures of taxonomic diversity. Crurotarsan archosaurs, the primary dinosaur 'competitors', were significantly more disparate than dinosaurs throughout the Triassic, but underwent a devastating extinction at the Triassic-Jurassic boundary. However, dinosaur disparity showed only a slight non-significant increase after this event, arguing against the hypothesis of ecological release-driven morphospace expansion in the Early Jurassic. Instead, the main jump in dinosaur disparity occurred between the Carnian and Norian stages of the Triassic. Conversely, dinosaur diversity shows a steady increase over this time, and measures of diversification and faunal abundance indicate that the Early Jurassic was a key episode in dinosaur evolution. Thus, different aspects of the dinosaur radiation (diversity, disparity and abundance) were decoupled, and the overall macroevolutionary pattern of the first 50Myr of dinosaur evolution is more complex than often considered.