Dermal Bones Research Articles

The salamandrid Chelotriton paradoxus from Enspel and Randeck Maars (Oligocene–Miocene, Germany)

The late Paleogene to early Neogene salamander Chelotriton paradoxus is redescribed on the basis of new and excellent material from two deposits, the late Oligocene Enspel locality and the Miocene Randeck Maar. C. paradoxus is characterised by the following features: (1) skull outline broad and parabolic, (2) snout abbreviated, with nasal only half the length of the frontal, (3) quadratojugal with a series of 3–5 spikes on the lateral margin, and (4) osteoderms larger than in other genera. Like extant Echinotriton, its trunk ribs bear extensive spikes (epipleural processes), with an elongated one on the 3rd rib. The Enspel sample of C. paradoxus shows greater variation in the size and number of quadratojugal spikes, whereas the best-preserved Randeck specimen bears exceptionally tall tubercles on all dermal bones and osteoderms and has a larger quadratojugal. Based on preliminary taphonomical data, we suggest that C. paradoxus probably led a predominantly aquatic life.

Emerging from the rib: resolving the turtle controversies.

Two of the major controversies in the present study of turtle shell development involve the mechanism by which the carapacial ridge initiates shell formation and the mechanism by which each rib forms the costal bones adjacent to it. This paper claims that both sides of each debate might be correct-but within the species examined. Mechanism is more properly "mechanisms," and there is more than one single way to initiate carapace formation and to form the costal bones. In the initiation of the shell, the rib precursors may be kept dorsal by either "axial displacement" (in the hard-shell turtles) or "axial arrest" (in the soft-shell turtle Pelodiscus), or by a combination of these. The former process would deflect the rib into the dorsal dermis and allow it to continue its growth there, while the latter process would truncate rib growth. In both instances, though, the result is to keep the ribs from extending into the ventral body wall. Our recent work has shown that the properties of the carapacial ridge, a key evolutionary innovation of turtles, differ greatly between these two groups. Similarly, the mechanism of costal bone formation may differ between soft-shell and hard-shell turtles, in that the hard-shell species may have both periosteal flattening as well as dermal bone induction, while the soft-shelled turtles may have only the first of these processes.

A taxonomic reassessment of Ophiopsis (Halecomorphi, Ionoscopiformes), with a revision of Upper Jurassic species from the Solnhofen Archipelago, and a new genus of Ophiopsidae

ABSTRACTAlthough the type species of Ophiopsis was long considered O. procera, the genus originally included the single species Ophiopsis muensteri, which subsequent authors moved to Furo. Following the International Commission on Zoological Nomenclature code, Furo muensteri is here recognized as the type species of Ophiopsis by monotypy (Article 68.3). Ophiopsiella, gen. nov., is erected to include all remaining previously described ‘Ophiopsis’ species. Exceptionally well preserved new Ophiopsiella attenuata from the Upper Jurassic plattenkalk of Ettling (Bavaria, Germany) represents the first record of this species from Ettling, allowing for a partial revision of it and Ophiopsiella procera. New evidence allows for an emended diagnosis of Ophiopsiella attenuata, which differs from all other Ophiopsidae in the following combination of features: 27–28 dorsal fin rays, 42 vertical scale rows, and a long, low, posteroventrally inclined dorsal fin lacking elongate anterior fin rays or a strongly concave posterior border. A neotype for O. attenuata is designated, as the type is lost. ‘Ophiopsis’ attenuata actually contains two anatomically different morphotypes corresponding to distinct species, one of which is indistinguishable from ‘Ophiopsis’ procera. Exceptional preservation of the new material provides new morphological information, particularly regarding the dermal cranial bones. This revision changes the known distribution of ophiopsids in the Upper Jurassic of southern Germany and France, with possible broader paleobiogeographic and paleoecological implications for this region during the Late Jurassic. Ophiopsids remain poorly known compared with other halecomorphs (e.g., Amiidae), and closer investigation of their morphology and taxonomic relationships is therefore important to understanding broader patterns of halecomorph evolution.http://zoobank.org/urn:lsid:zoobank.org:pub:6B250A32-9FAA-4EF6-9D91-6D1C5E91E547

On the development of surface ornamentation of skull bones in the ontogeny of Early Triassic benthosuchids (Amphibia, Temnospondyli)

The rate of developmental changes in ornamentation of the dermal skull observed at the submature stages of the trematosauroid Benthosuchus (Amphibia, Temnospondyli) shows a wide range of individual variation divided into two dominant modes. The analysis of this variation based on comparisons within samples of two dermal bones (supratemporal and squamosal) displays that such a bimodality is distinctly expressed at the earliest known growth stage and tends to disappear with age.

Amphibian skull evolution: The developmental and functional context of simplification, bone loss and heterotopy

Despite their divergent morphology, extant and extinct amphibians share numerous features in the timing and spatial patterning of dermal skull elements. Here, I show how the study of these features leads to a deeper understanding of morphological evolution. Batrachians (salamanders and frogs) have simplified skulls, with dermal bones appearing rudimentary compared with fossil tetrapods, and open cheeks resulting from the absence of other bones. The batrachian skull bones may be derived from those of temnospondyls by truncation of the developmental trajectory. The squamosal, quadratojugal, parietal, prefrontal, parasphenoid, palatine, and pterygoid form rudimentary versions of their homologs in temnospondyls. In addition, failure to ossify and early fusion of bone primordia both result in the absence of further bones that were consistently present in Paleozoic tetrapods. Here, I propose a new hypothesis explaining the observed patterns of bone loss and emargination in a functional context. The starting observation is that jaw-closing muscles are arranged in a different way than in ancestors from the earliest ontogenetic stage onwards, with muscles attaching to the dorsal side of the frontal, parietal, and squamosal. The postparietal and supratemporal start to ossify in a similar way as in branchiosaurids, but are fused to neighboring elements to form continuous attachment areas for the internal adductor. The postfrontal, postorbital, and jugal fail to ossify, as their position is inconsistent with the novel arrangement of adductor muscles. Thus, rearrangement of adductors forms the common theme behind cranial simplification, driven by an evolutionary flattening of the skull in the batrachian stem.

Amphibian skull evolution: The developmental and functional context of simplification, bone loss and heterotopy.

Despite their divergent morphology, extant and extinct amphibians share numerous features in the timing and spatial patterning of dermal skull elements. Here, I show how the study of these features leads to a deeper understanding of morphological evolution. Batrachians (salamanders and frogs) have simplified skulls, with dermal bones appearing rudimentary compared with fossil tetrapods, and open cheeks resulting from the absence of other bones. The batrachian skull bones may be derived from those of temnospondyls by truncation of the developmental trajectory. The squamosal, quadratojugal, parietal, prefrontal, parasphenoid, palatine, and pterygoid form rudimentary versions of their homologs in temnospondyls. In addition, failure to ossify and early fusion of bone primordia both result in the absence of further bones that were consistently present in Paleozoic tetrapods. Here, I propose a new hypothesis explaining the observed patterns of bone loss and emargination in a functional context. The starting observation is that jaw-closing muscles are arranged in a different way than in ancestors from the earliest ontogenetic stage onwards, with muscles attaching to the dorsal side of the frontal, parietal, and squamosal. The postparietal and supratemporal start to ossify in a similar way as in branchiosaurids, but are fused to neighboring elements to form continuous attachment areas for the internal adductor. The postfrontal, postorbital, and jugal fail to ossify, as their position is inconsistent with the novel arrangement of adductor muscles. Thus, rearrangement of adductors forms the common theme behind cranial simplification, driven by an evolutionary flattening of the skull in the batrachian stem. J. Exp. Zool. (Mol. Dev. Evol.) 9999B: XX-XX, 2014. © 2014 Wiley Periodicals, Inc.

Embryonic development of fin spines in Callorhinchus milii (Holocephali); implications for chondrichthyan fin spine evolution.

Fin spines are commonly known from fossil gnathostomes (jawed vertebrates) and are usually associated with paired and unpaired fins. They are less common among extant gnathostomes, being restricted to the median fins of certain chondrichthyans (cartilaginous fish), including chimaerids (elephant sharks) and neoselachians (sharks, skates, and rays). Fin spine growth is of great interest and relevance but few studies have considered their evolution and development. We investigated the development of the fin spine of the chimaerid Callorhinchus milii using stained histological sections from a series of larval, hatchling, and adult individuals. The lamellar trunk dentine of the Callorhinchus spine first condenses within the mesenchyme, rather than at the contact surface between mesenchyme and epithelium, in a manner more comparable to dermal bone formation than to normal odontode development. Trabecular dentine forms a small component of the spine under the keel; it is covered externally with a thin layer of lamellar trunk dentine, which is difficult to distinguish in sectioned adult spines. We suggest that the distinctive characteristics of the trunk dentine may reflect an origin through co-option of developmental processes involved in dermal bone formation. Comparison with extant Squalus and a range of fossil chondrichthyans shows that Callorhinchus is more representative than Squalus of generalized chondrichthyan fin-spine architecture, highlighting its value as a developmental model organism.

A new haplolepid fauna (Osteichthyes: Actinopterygii) from the Lower Coal Measures of Scotland: Westphalian A; Langsettian,Carbonicola communischronozone (Bashkirian)

ABSTRACTSeven new species and one new genus of the family Haplolepidae (Actinopterygii: Palaeonisciformes) are described from new material obtained from the Drumgray coal shales, North Lanarkshire: Westphalian A (Bashkirian):Protohaplolepis isabellae; Protohaplolepis limnades;Protohaplolepis traquairi; Parahaplolepis alexandrae; Parahaplolepis elenae; Pyritocephalus youngiiandMillerolepis eleionomae. The discovery of these new taxa increases the number of haplolepid species found in Europe to 16, thus producing a faunal count more than comparable to that of North America. This high concentration of haplolepid remains in limnic deposits is also a strong indication that these fish were not only adapted to a coastal paralic basin, but also well-adapted to a freshwater brackish environment. A comprehensive description of the skull roof morphology, including a short description of some of the larger dermal bones, is given of seven new haplolepid species obtained from the coal shale tips at Wester Bracco and Shotts in North Lanarkshire. In consequence, a revised table of the stratigraphical distribution of the Haplolepidae in Europe is provided. Furthermore, the new genusMillerolepisis assigned to the subfamily Parahaplolepinae and the generic position of the problematicHaplolepis attheyifrom Newsham, Northumberland is discussed, with the taxonomic position ofProtohaplolepisproposed.

Carboniferous (Tournaisian) fish assemblages from the Isle of Bute, Scotland: systematics and palaeoecology

We describe fish assemblages from the Carboniferous (mid- to late Tournaisian) Ballagan Formation at two localities, Hawk's Nib and Mill Hole, on the Isle of Bute, Scotland. Fossil material occurs in thin, locally reworked dolomitic limestone beds, interpreted as the deposits of very shallow lakes or lagoons, developed on, or adjacent to, a seasonally dry coastal plain. The mostly disarticulated fossils comprise isolated teeth, mandibles, scales, tesserae, dermal bones, lepidotrichia and vertebrae. The fauna includes rhizodonts (cf. Archichthys portlocki, cf. Strepsodus sauroides), lungfish (Sagenodus sp.), other sarcopterygians (Megalichthys sp.), one shark (Ageleodus pectinatus), climatiiform acanthodians and indeterminate actinopterygians. The Mill Hole assemblage is especially noteworthy because it includes some putative juvenile forms (Archichthys and Sagenodus). A critical review of the habitat preferences of the documented taxa suggests that most were either euryhaline or, in the case of Archichthys, probably endemic to brackish or freshwater settings. The Bute fish beds fall within a crucial evolutionary period during which many fish and other animal groups were infiltrating nonmarine environments, either passively or actively. It may be that lakes and lagoons may have functioned as protected nurseries for juveniles during this wave of colonization.

Mamulichthys ignotus gen. et sp. nov., a new actinopterygian from the Middle Permian of the southeastern East Europe Platform

A new actinopterygian genus and species of the family Discordichthyidae, Mamulichthys ignotus gen. et sp. nov., from the upper part of the Urzhumian Stage of the Middle Permian of the southeastern East Europe Platform is described. The fish has a large rounded operculum and dorsal and pectoral fin spines. The side scales are high. The abdomen has longitudinal rows of large, massive, strongly overlapping falciform scales. All dermal bones are ornamented with many hollow tubercles varying in shape and size. At present, representatives of Discordichthyidae are only known from Eastern Europe.

Coelacanths

Coelacanths

Parallel developmental genetic features underlie stickleback gill raker evolution

BackgroundConvergent evolution, the repeated evolution of similar phenotypes in independent lineages, provides natural replicates to study mechanisms of evolution. Cases of convergent evolution might have the same underlying developmental and genetic bases, implying that some evolutionary trajectories might be predictable. In a classic example of convergent evolution, most freshwater populations of threespine stickleback fish have independently evolved a reduction of gill raker number to adapt to novel diets. Gill rakers are a segmentally reiterated set of dermal bones important for fish feeding. A previous large quantitative trait locus (QTL) mapping study using a marine × freshwater F2 cross identified QTL on chromosomes 4 and 20 with large effects on evolved gill raker reduction.ResultsBy examining skeletal morphology in adult and developing sticklebacks, we find heritable marine/freshwater differences in gill raker number and spacing that are specified early in development. Using the expression of the Ectodysplasin receptor (Edar) gene as a marker of raker primordia, we find that the differences are present before the budding of gill rakers occurs, suggesting an early change to a lateral inhibition process controlling raker primordia spacing. Through linkage mapping in F2 fish from crosses with three independently derived freshwater populations, we find in all three crosses QTL overlapping both previously identified QTL on chromosomes 4 and 20 that control raker number. These two QTL affect the early spacing of gill raker buds.ConclusionsCollectively, these data demonstrate that parallel developmental genetic features underlie the convergent evolution of gill raker reduction in freshwater sticklebacks, suggesting that even highly polygenic adaptive traits can have a predictable developmental genetic basis.

The Zebrafish Infraorbital Bones: A Descriptive Study

The infraorbital (IO) bone series, a component of the circumorbital series, makes up five of the eight dermal bones found in the orbital region of the zebrafish skull. Ossifying in a set sequence, the IOs are closely associated with the cranial lateral line system as they house neuromast sensory receptors in bony canals. We conducted a detailed analysis of the condensation to mineralization phases of development of these bones. Our analyses involved both bone and osteoblast staining of zebrafish at 20 different time points. IO bone condensations are shaped as templates for the final bone shape, and they mineralize at one or more centers of ossification. Initially, mineralization is closely associated with the lateral line canals and/or foramen, and the onset of mineralization is temporally variable. Canal wall mineralization is a process that continues into adulthood and completely mineralized canal roofs were not found. Our comprehensive growth series detailing the ossification of each IO bone provides important insight into the growth and development of this series of neural crest-derived flat bones in the zebrafish craniofacial skeleton.

Origins of bone repair in the armour of fossil fish: response to a deep wound by cells depositing dentine instead of dermal bone

The outer armour of fossil jawless fishes (Heterostraci) is, predominantly, a bone with a superficial ornament of dentine tubercles surrounded by pores leading to flask-shaped crypts (ampullae). However, despite the extensive bone present in these early dermal skeletons, damage was repaired almost exclusively with dentine. Consolidation of bone, by dentine invading and filling the vascular spaces, was previously recognized in Psammolepis and other heterostracans but was associated with ageing and dermal shield wear (reparative). Here, we describe wound repair by deposition of dentine directly onto a bony scaffold of fragmented bone. An extensive wound response occurred from massive deposition of dentine (reactionary), traced from tubercle pulp cavities and surrounding ampullae. These structures may provide the cells to make reparative and reactionary dentine, as in mammalian teeth today in response to stimuli (functional wear or damage). We suggest in Psammolepis, repair involved mobilization of these cells in response to a local stimulatory mechanism, for example, predator damage. By comparison, almost no new bone is detected in repair of the Psammolepis shield. Dentine infilling bone vascular tissue spaces of both abraded dentine and wounded bone suggests that recruitment of this process has been evolutionarily conserved over 380 Myr and precedes osteogenic skeletal repair.

A Silurian placoderm with osteichthyan-like marginal jaw bones

The gnathostome (jawed vertebrate) crown group comprises two extant clades with contrasting character complements. Notably, Chondrichthyes (cartilaginous fish) lack the large dermal bones that characterize Osteichthyes (bony fish and tetrapods). The polarities of these differences, and the morphology of the last common ancestor of crown gnathostomes, are the subject of continuing debate. Here we describe a three-dimensionally preserved 419-million-year-old placoderm fish from the Silurian of China that represents the first stem gnathostome with dermal marginal jaw bones (premaxilla, maxilla and dentary), features previously restricted to Osteichthyes. A phylogenetic analysis places the new form near the top of the gnathostome stem group but does not fully resolve its relationships to other placoderms. The analysis also assigns all acanthodians to the chondrichthyan stem group. These results suggest that the last common ancestor of Chondrichthyes and Osteichthyes had a macromeric dermal skeleton, and provide a new framework for studying crown gnathostome divergence.

Late‐emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron

The turtle plastron is composed of a keratinized epidermis overlying nine dermal bones. Its developmental origin has been controversial; recent evidence suggests that the plastral bones derive from trunk neural crest cells (NCCs). This study extends the observations that there is a turtle-specific, second wave of trunk NCC delamination and migration, after the original NCCs have reached their destination and differentiated. This second wave was confirmed by immunohistochemistry in whole-mounts and serial sections, by injecting DiI (1,1', di-octadecyl-3,3,3',3',-tetramethylindo-carbocyanine perchlorate) into the lumen of the neural tube and tracing labeled cells into the plastron, and by isolating neural tubes from older turtle embryos and observing delaminating NCCs. This later migration gives rise to a plastral ectomesenchyme that expresses NCC markers and can be induced to initiate bone formation. The NCCs of this second migration have properties similar to those of the earlier NCCs, but also express markers characteristic of cranial NCCs. The majority of the cells of the plastron mesenchyme express neural crest markers, and have osteogenic differentiation capabilities that are similar or identical to craniofacial ectomesenchyme. Our evidence supports the contention that turtle plastron bones are derived from a late emigrating population of cells derived from the trunk neural crest.

A titanosaur (Dinosauria: Sauropoda) osteoderm from the Alcântara Formation (Cenomanian), São Luís Basin, Northeastern Brazil

Among titanosaurs, osteoderms are morphologically diverse and have been reported from deposits in South America, Africa, Madagascar, Eurasia and Oceania. In Brazil, titanosaur osteoderms are rare and have only been recorded from Bauru Basin sedimentary rocks. Here, we describe a keeled titanosaur osteoderm, which is the first occurrence of an osteoderm specimen in the São Luís Basin, Northeastern Brazil. This osteoderm is characterized by an external bulb, an internal root, and a very rugose cingulum limiting the external and internal surfaces. These characteristics are typical of Titanosauria dermal bones, and this specimen strengthens the idea that the armored sauropods were present during the early Late Cretaceous of Northeastern Brazil, extending their distribution in the northernmost portion of South America.

Scales and Tooth Whorls of Ancient Fishes Challenge Distinction between External and Oral ‘Teeth’

The debate about the origin of the vertebrate dentition has been given fresh fuel by new fossil discoveries and developmental studies of extant animals. Odontodes (teeth or tooth-like structures) can be found in two distinct regions, the ‘internal’ oropharyngeal cavity and the ‘external’ skin. A recent hypothesis argues that regularly patterned odontodes is a specific oropharyngeal feature, whereas odontodes in the external skeleton lack this organization. However, this argument relies on the skeletal system of modern chondrichthyans (sharks and their relatives), which differ from other gnathostome (jawed vertebrate) groups in not having dermal bones associated with the odontodes. Their external skeleton is also composed of monoodontode 'placoid scales', whereas the scales of most early fossil gnathostomes are polyodontode, i.e. constructed from several odontodes on a shared bony base. Propagation phase contrast X-ray Synchrotron microtomography (PPC-SRµCT) is used to study the polyodontode scales of the early bony fish Andreolepis hedei. The odontodes constructing a single scale are reconstructed in 3D, and a linear and regular growth mechanism similar to that in a gnathostome dentition is confirmed, together with a second, gap-filling growth mechanism. Acanthodian tooth whorls are described, which show that ossification of the whorl base preceded and probably patterned the development of the dental lamina, in contrast to the condition in sharks where the dental lamina develops early and patterns the dentition.The new findings reveal, for the first time, how polyodontode scales grow in 3D in an extinct bony fish. They show that dentition-like odontode patterning occurs on scales and that the primary patterning unit of a tooth whorl may be the bony base rather than the odontodes it carries. These results contradict the hypothesis that oropharyngeal and external odontode skeletons are fundamentally separate and suggest that the importance of dermal bone interactions to odontode patterning has been underestimated.

Prednisolone induces osteoporosis-like phenotype in regenerating zebrafish scales

We demonstrate that glucocorticoids induce an osteoporotic phenotype in regenerating scales of zebrafish. Exposure to prednisolone results in altered mineral content, enhanced matrix breakdown, and an osteoporotic gene-expression profile in osteoblasts and osteoclasts. This highlights that the zebrafish scale provides a powerful tool for preclinical osteoporosis research. This study aims to evaluate whether glucocorticoid (prednisolone) treatment of zebrafish induces an osteoporotic phenotype in regenerating scales. Scales, a readily accessible dermal bone tissue, may provide a tool to study direct osteogenesis and its disturbance by glucocorticoids. In adult zebrafish, treated with 25 μM prednisolone phosphate via the water, scales were removed and allowed to regenerate. During regeneration scale morphology and the molar calcium/phosphorus ratio in scales were assessed and osteoblast and osteoclast activities were monitored by time profiling of cell-specific genes; mineralization was visualized by Von Kossa staining, osteoclast activity by tartrate-resistant acid phosphatase histochemistry. Prednisolone (compared to controls) enhances osteoclast activity and matrix resorption and slows down the build up of the calcium/phosphorus molar ratio indicative of altered crystal maturation. Prednisolone treatment further impedes regeneration through a shift in the time profiles of osteoblast and osteoclast genes that commensurates with an osteoporosis-like imbalance in bone formation. A glucocorticoid-induced osteoporosis phenotype as seen in mammals was induced in regenerating scalar bone of zebrafish treated with prednisolone. An unsurpassed convenience and low cost then make the zebrafish scale a superior model for preclinical studies in osteoporosis research.

Styracopterid (Actinopterygii) ontogeny and the multiple origins of post-Hangenberg deep-bodied fishes

The Carboniferous fish family Styracopteridae (Actinopterygii) originated as part of the initial radiation of ray-finned fishes following the end-Devonian Hangenberg extinction. Specimens of Styracopterus fulcratus (Traquair, 1890) have been collected from post-extinction Tournaisian and Visean Scottish sediments for over 100 years, including sites containing some of the earliest ‘Romer's Gap’ tetrapods. Re-examination of this supposedly long-lived, static species has revealed two genera, Styracopterus and Fouldenia White, 1927, divergent from each other and previous descriptions. Here, we show that styracopterids are among the earliest actinopterygians with durophagous dentition and toothplates, the latter likely to have derived from the ectopterygoids and coronoids. On the basis of this and other traits, such as the presence of an enameloid ‘beak’, the fusiform styracopterids are linked to some, but not all, the deep-bodied actinopterygians previously placed in the suborder Platysomoidei. A new plesion, Eurynotiformes, is erected to contain the styracopterids, the deeply fusiform Eurynotus and the widespread Amphicentrum, among other laterally compressed fishes. This implies that platysomoids are polyphyletic: deep-bodied and/or durophagous fishes evolved multiple times following the Hangenberg event. Reconstructed styracopterid growth series show that trunk depth increased during maturation, mirroring the shape variation observed among the Eurynotiformes. Other ontogenetic changes involve fin-ray differentiation, jaw form, dermal bone ornamentation, and scale morphology; all of these are widely used as actinopterygian diagnostic characters. Further investigation of Eurynotiformes should reveal the extent of evolutionary and ontogenetic change within the earliest actinopterygian radiation, and are likely to rewrite their phylogeny. © 2013 The Linnean Society of London