Comparison of teeth and dermal denticles (odontodes) in the teleost Denticeps clupeoides (Clupeomorpha)

The present work is a contribution to an extensive comparative structural and developmental study we have undertaken to understand the evolution of the dermal skeleton in osteichthyans. We have investigated the structure of developing and functional tooth-like dermal denticles located on the head of Denticeps clupeoides, a clupeomorph, and compared their features to those of oral teeth. Morphological (scanning electron microscopy) and structural (light microscopy and transmission electron microscopy) observations clearly demonstrate that these small, sharp, conical and slightly backward-oriented denticles are true odontodes, i.e., homologous to oral teeth. They are composed of a dentine cone surrounding a pulp cavity, the top being covered by a hypermineralized cap. These odontodes are attached to a circular pedicel of attachment bone by a ligament that mineralizes, and the attachment bone matrix merges with that of the bony support. The pedicel of attachment bone surrounds a vascular cavity that is connected to the pulp cavity which is devoid of blood vessels and of nerve endings. Once the odontode is functional, the deposition of collagen matrix (called circumpulpar dentine) continues against the dentine, ligament, and attachment bone surfaces, thereby provoking a narrowing of the pulp cavity. Odontodes are shed by resorption occurring at the base, but their pedicels of attachment bone persist at the bone surface and become embedded in the bone matrix, within which they are clearly visible. The oral teeth are similar in shape, size, and structure to the odontodes, and they show only small differences probably related to the different function of these elements: They are more firmly anchored to the attachment bone, and the amount of dentine is relatively smaller than in odontodes. Despite their different functions, this close structural agreement between teeth and odontodes in Denticeps suggests that 1) competent cells from the same (ecto)mesenchymal population might be involved and 2) the genetic control of the developmental processes could be identical. It is suggested that the odontode expression in extra-oral positions is a relatively late novelty in this lineage. J. Morphol. 237:237–255, 1998. © 1998 Wiley-Liss, Inc.     

Teeth outside the mouth in teleost fishes: how to benefit from a developmental accident

SUMMARY Evolution proceeds by the selection of characters that enhance survival rates so that the long-term outcome for a species is better adaptation to its environment. These new characters are "accidentally" acquired, mostly through mutations leading to modifications of developmental events. However, changes that lead to the ectopic expression of an organ are rare and, whereas their subsequent selection for a new role is even more rare, such a scenario has apparently occurred for denticles in some teleost fish. Small, conical denticles are present, mainly on the dermal bones of the head, in a few, unrelated lineages of living teleosts. Here, I show that the morphology and structure of the denticles in Atherion elymus , an atheriniform, is similar to those of teeth inside the oral cavity. These denticles are not derived evolutionarily from odontodes of early vertebrates, nor do they represent a re-expression as such (i.e., a long-lasting ability to make odontodes outside the oral cavity). Teeth and odontodes are homologous organs but the origin of the denticles is to be found in teeth, not in odontodes. The denticles are simply teeth that form outside the mouth, probably derived from a sub-population of odontogenically pre-specified neural crest cells. These "accidental" extra-oral teeth have arisen independently in these lineages and were selectively advantageous in a hydrodynamic context.     

Origin and evolution of gnathostome dentitions: a question of teeth and pharyngeal denticles in placoderms

The fossil group Placodermi is the most phylogenetically basal of the clade of jawed vertebrates but lacks a marginal dentition comparable to that of the dentate Chondrichthyes, Acanthodii and Osteichthyes (crown-group Gnathostomata). The teeth of crown-group gnathostomes are part of an ordered dentition replaced from, and patterned by, a dental lamina, exemplified by the elasmobranch model. A dentition recognised by these criteria has been previously judged absent in placoderms, based on structural evidence such as absence of tooth whorls and typical vertebrate dentine. However, evidence for regulated tooth addition in a precise spatiotemporal order can be observed in placoderms, but significantly, only within the group Arthrodira. In these fossils, as in other jawed vertebrates with statodont, non-replacing dentitions, new teeth are added at the ends of rows below the bite, but in line with biting edges of the dentition. The pattern is different on each gnathal bone and probably arises from single odontogenic primordia on each, but tooth rows are arranged in a distinctive placoderm pattern. New teeth are made of regular dentine comparable to that of crown-gnathostomes, formed from a pulp cavity. This differs from semidentine previously described for placoderm gnathalia, a type present in the external dermal tubercles. The Arthrodira is a derived taxon within the Placodermi, hence origin of teeth in placoderms occurs late in the phylogeny and teeth are convergently derived, relative to those of other jawed vertebrates. More basal placoderm taxa adopted other strategies for providing biting surfaces and these vary substantially, but include addition of denticles to the growing gnathal plates, at the margins of pre-existing denticle patches. These alternative strategies and apparent absence of regular dentine have led to previous interpretations that teeth were entirely absent from the placoderm dentition. A consensus view emerged that a dentition, as developed within a dental lamina, is a synapomorphy characterising the clade of crown-group gnathostomes. Recent comparisons between sets of denticle whorls in the pharyngeal region of the jawless fish Loganellia scotica (Thelodonti) and those in sharks suggest homology of these denticle sets on gill arches. Although the placoderm pharyngeal region appears to lack denticles (placoderm gill arches are poorly known), the posterior wall of the pharyngeal cavity, formed by a bony flange termed the postbranchial lamina, is covered in rows of patterned denticle arrays. These arrays differ significantly, both in morphology and arrangement, from those of the denticles located externally on the head and trunkshield plates. Denticles in these arrays are homologous to denticles associated with the gill arches in other crown-gnathostomes, with pattern similarities for order and position of pharyngeal denticles. From their location in the pharynx these are inferred to be under the influence of a cell lineage from endoderm, rather than ectoderm. Tooth sets and tooth whorls in crown-group gnathostomes are suggested to derive from the pharyngeal denticle whorls, at least in sharks, with the patterning mechanisms co-opted to the oral cavity. A comparable co-option is suggested for the Placodermi.     

The structure and stratigraphy of<Emphasis Type="Italic">Speonesydrion</Emphasis> from New South Wales,Australia, and the dentition of primitive dipnoans

New material ofSpeonesydrion iani, an Early Devonian dipnoan from New South Wales, has provided additional Information on the dentition and jaws. Two new partial palates have been found, and X-rays of the parasphenoid shows that the structure is well preserved. The palatal teeth are well worn even in partly grown material, and they do not originate at a growth point, but at a thickening of the palate. More mandibles have been collected, and thin sections have been prepared to allow a discussion of their histology. On the mandible the teeth are clear, and they are much more defined than they are on the palate. The dental heel is variably developed, and grows in phases by thickening of the dentine at the contact with the bone. Dentine forms on the bone at the base of the heel, partly by Solution of the bone and the addition of dentine from the pulp canals, but also by direct growth from the pulp canals dorsal to the bone. In the latter case the dentine and bone are in contact, and the two tissues intermingle. The teeth are also formed on a thickened bone and consist of dentine capped with enamel making a crest. Dentine and bone are related as in the heel. We conclude that the teeth inSpeonesydrion are not homologous with the teeth in other dipnoans, and are formed by a different process involving the aggregation of denticles.     

Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach

Osteichthyan and chondrichthyan fish present an astonishing diversity of skeletal and dental tissues that are often difficult to classify into the standard textbook categories of bone, cartilage, dentine and enamel. To address the question of how the tissues of the dermal skeleton evolved from the ancestral situation and gave rise to the diversity actually encountered, we review previous data on the development of a number of dermal skeletal elements (odontodes, teeth and dermal denticles, cranial dermal bones, postcranial dermal plates and scutes, elasmoid and ganoid scales, and fin rays). A comparison of developmental stages at the tissue level usually allows us to identify skeletogenic cell populations as either odontogenic or osteogenic on the basis of the place of formation of their dermal papillae and of the way of deposition of their tissues. Our studies support the evolutionary affinities (1) between odontodes, teeth and denticles, (2) between the ganoid scales of polypterids and the elasmoid scales of teleosts, and (3) to a lesser degree between the different bony elements. There is now ample evidence to ascertain that the tissues of the elasmoid scale are derived from dental and not from bony tissues. This review demonstrates the advantage that can be taken from developmental studies, at the tissue level, to infer evolutionary relationships within the dermal skeleton in chondrichthyans and osteichthyans.     

Odontode morphology and skin surface features of Andean astroblepid catfishes (Siluriformes,Astroblepidae)

Two types of odontodes, or dermal teeth, occur in the neotropical Andean astroblepid catfishes. Both odontode types conform in structure to dermal teeth of gnathostomes in having dentine surrounding a central pulp cavity covered by a superficial layer of enameloid, but differ from one another in terms of attachment and association with other epidermis features. Type I odontodes in astroblepids, also found in all representatives of the superfamily Loricarioidea, are larger (40-50 microm base diameter), generally conical and sharply pointed, occur on the fin rays, and are associated with dermal bone. Type I odontodes attach to an elevated pediment of dermal bone of the fin lepidotrich, and to dermal bone generally in loricarioids, via a ring of connective tissue. Type II odontodes of astroblepids are smaller (15-20 microm base diameter) and blunt, occur in the skin of the head, maxillary barbels, nasal flap, and lip margins, and are not associated with dermal bone. Observations based on histology and scanning electron microscopy indicate that Type II odontodes are associated with other epithelial structures to form a putative mechanosensory organ. The odontode base lies deep in the dermis. The shaft is surrounded by a dense patch of microvillous epithelium and projects from within a pit formed by an elevated ring of laminar epithelial cells bearing several columnar, knob-like putative mechanosensory structures. Type II odontode organs have thus far been observed in only three astroblepid species, Astroblepus longifilis, A. chotae, A. rosei, where they occur in especially dense arrays on the maxillary barbels, surrounded by discrete patches of microvilli and separate mechanoreceptors. Type II odontode organs are less dense elsewhere on the body, but also occur in the skin of the snout, head, and lips. Typical taste buds are absent from the barbels of these species, but present in other astroblepids. The presence of Type II odontodes and their association with specialized epithelial pit organs are unique to astroblepids among siluriforms and may be potentially important adaptations to life in torrential mountain streams.     

Structure and Development of the Odontodes in an Armoured Catfish,Corydoras aeneus (Siluriformes,Callichthyidae)

Abstract In some living osteichthyans (e.g. the armoured catfishes) the postcranial dermal skeleton exhibits tooth-like structures (odontodes) similar to those present in the dermal skeleton of the ancient craniates. We have undertaken this work to compare odontode with tooth development, structure, attachment to a bony support and replacement. We studied the odontodes fixed on the scutes (i.e. postcranial dermal plates) in a growth series of Corydoras aeneus using light, scanning and transmission electron microscopy. Odontodes are constituted of a pulp cavity surrounded by a cone of dentine itself capped with hypermineralized substance. The pulp cavity is devoid of nerves and blood vessels and there are no odontoblastic processes in the dentine. The dentine cone is firmly attached to a circular bony protuberance of the scute surface, the pedicel or attachment bone, by means of a ligament. An odontode anlage develops as a small invagination of a dermal papilla projecting into the epidermis, the basal cell layer of which constitutes a dental epithelium. First, dentine is deposited, next the hypermineralized substance, then the ligament and attachment bone. Odontodes develop in two positions with regard to the scute surface: a primary position when new odontodes form at the posterior border of the enlarging scute; a secondary position when new odontodes replace old odontodes that have been shed during thickening of the scute. In this case, the ligament and part of the base of the dentine cone are resorbed but not the pedicel of attachment bone, which is covered by deposition of scute matrix after the odontode has been shed. Within the scute matrix, the embedded pedicels of successive generations of odontodes are preserved, forming piles in the scutes of adult specimens.     

Teeth outside the mouth: The evolution and development of shark denticles

Vertebrate skin appendages are incredibly diverse. This diversity, which includes structures such as scales, feathers, and hair, likely evolved from a shared anatomical placode, suggesting broad conservation of the early development of these organs. Some of the earliest known skin appendages are dentine and enamel-rich tooth-like structures, collectively known as odontodes. These appendages evolved over 450 million years ago. Elasmobranchs (sharks, skates, and rays) have retained these ancient skin appendages in the form of both dermal denticles (scales) and oral teeth. Despite our knowledge of denticle function in adult sharks, our understanding of their development and morphogenesis is less advanced. Even though denticles in sharks appear structurally similar to oral teeth, there has been limited data directly comparing the molecular development of these distinct elements. Here, we chart the development of denticles in the embryonic small-spotted catshark (Scyliorhinus canicula) and characterize the expression of conserved genes known to mediate dental development. We find that shark denticle development shares a vast gene expression signature with developing teeth. However, denticles have restricted regenerative potential, as they lack a sox2+ stem cell niche associated with the maintenance of a dental lamina, an essential requirement for continuous tooth replacement. We compare developing denticles to other skin appendages, including both sensory skin appendages and avian feathers. This reveals that denticles are not only tooth-like in structure, but that they also share an ancient developmental gene set that is likely common to all epidermal appendages.     

Placoderm fishes,pharyngeal denticles,and the vertebrate dentition

The correlation of the origin of teeth with jaws in vertebrate history has recently been challenged with an alternative to the canonical view of teeth deriving from separate skin denticles. This alternative proposes that organized denticle whorls on the pharyngeal (gill) arches in the fossil jawless fish Loganellia are precursors to tooth families developing from a dental lamina along the jaw, such as those occurring in sharks, acanthodians, and bony fishes. This not only indicates that homologs of tooth families were present, but also illustrates that they possessed the relevant developmental controls, prior to the evolution of jaws. However, in the Placodermi, a phylogenetically basal group of jawed fishes, the state of pharyngeal denticles is poorly known, tooth whorls are absent, and the presence of teeth homologous to those in extant jawed fishes (Chondrichthyes + Osteichthyes) is controversial. Thus, placoderms would seem to provide little evidence for the early evolution of dentitions, or of denticle whorls, or tooth families, at the base of the clade of jawed fishes. However, organized denticles do occur at the rear of the placoderm gill chamber, but are associated with the postbranchial lamina of the anterior trunkshield, assumed to be part of the dermal cover. Significantly, these denticles have a different organization and morphology relative to the external dermal trunkshield tubercles. We propose that they represent a denticulate part of the visceral skeleton, under the influence of pharyngeal patterning controls comparable to those for pharyngeal denticles in other jawed vertebrates and Loganellia.     

Occipital spine of Orthacanthus (Xenacanthidae,Elasmobranchii): Structure and growth

The morphology of 16 occipital spines of the xenacanthid Orthacanthus from Upper Carboniferous deposits of Robinson (Kansas, USA), Nýřan (Czech Republic) and Puertollano (Spain) is described. The nonreplaced spines reveal the growth pattern of the shark. Moreover, the relationship between growth and paleoenvironmental conditions can be used to determine paleoecological conditions. Both external and internal morphology indicate that the spine was superficially inserted in the skin. During growth, the spine moved from a deep position in the dermis, in which trabecular dentine is formed, to a more superficial location in which centrifugally growing lamellar dentine was formed. Centripetally growing lamellar dentine was deposited more slowly than the centrifugally growing dentine; it obliterated the pulp cavity. The denticles are independent dermal elements formed by a dermal papilla and secondarily attached by dentine to the spine proper. The number of denticles per annual cycle and the density of denticulation vary with the growth rate. Moreover, the ratio of length of denticulated region to total length of the spine changes throughout ontogeny. In consequence, those features cannot be used for systematic purposes without a careful analysis of the variability. Centrifugally growing lamellar dentine in spines from Robinson shows a regular alternation of layers, suggesting tidal conditions in the environment in which the sharks lived. Monthly and seasonal cycles also occur. Tidal (lunar) cyclicity is also observed in the denticles: size and distance between denticles increase and decrease gradually, forming waves that are considered seasonal and yearly cycles. The observed regularity could be related to the variation in calcium phosphate deposition following the cyclical changes in water temperature produced in the tidal zone. Monthly and seasonal cycles are the result of the interaction of the solar and tidal (lunar) cycles. The cyclical pattern of growth is used to determine the age and growth rates. Orthacanthus was a fast‐growing shark like the Recent sharks Isurus, Mustelus, and Negaprion. J. Morphol. 242:1–45, 1999. © 1999 Wiley‐Liss, Inc.     

Convergent dental adaptations in the serrations of hypercarnivorous synapsids and dinosaurs

Theropod dinosaurs are well known for having a ziphodont dentition: serrated, blade-shaped teeth that they used for cutting through prey. Serrations along the carinae of theropod teeth are composed of true denticles, a complex arrangement of dentine, enamel, and interdental folds. This structure would have supported individual denticles and dissipated the stresses associated with feeding. These particular serrations were previously thought to be unique to theropod dinosaurs and some other archosaurs. Here, we identify the same denticles and interdental folds forming the cutting edges in the teeth of a Permian gorgonopsian synapsid, extending the temporal and phylogenetic distribution of this dental morphology. This remarkable instance of convergence not only represents the earliest record of this adaptation to hypercarnivory but also demonstrates that the first iteration of this feature appeared in non-mammalian synapsids. Comparisons of tooth serrations in gorgonopsians with those of earlier synapsids and hypercarnivorous mammals reveal some gorgonopsians acquired a complex tissue arrangement that differed from other synapsids.     

A revised hypothesis on the evolutionary origin of the vertebrate dentition

Despite claims to the contrary, the evolutionary origin of teeth has not been definitely established. The classical ‘outside in’ theory stating that teeth derive from odontodes that invaded the oral cavity in conjunction with the origin of jaws has been challenged by an alternative, ‘inside out’, hypothesis suggesting that teeth evolved from pharyngeal denticles, as endodermal derivatives, prior to the origin of jaws. We propose a third scenario, a revised ‘outside in’ hypothesis ( Huysseune et al., 2009 ). Our hypothesis is consistent with the current data and avoids speculations about convergent tooth evolution. We suggest that teeth may indeed have arisen before the origin of jaws, a pillar of the ‘inside out’ hypothesis, but not from the endodermally lined posterior pharynx. Rather, teeth would have been the result of competent, odontode‐forming ectoderm invading the oropharyngeal cavity through the mouth as well as through the gill slits, interacting with neural‐crest derived mesenchyme. Arguments in support of this hypothesis are: (i) the observation that pharyngeal teeth are present only in species known to possess gill slits, and disappear from the pharyngeal region in early tetrapods concomitant with the closure of gill slits; (ii) the assumption that endoderm alone, together with neural crest, cannot form teeth; (iii) observations on pharyngeal tooth and gill slit formation in extant species; (iv) the observation that the dental lamina (sensu Reif, 1982 ) is not a prerequisite for tooth formation; (v) evidence that patterning does not distinguish pharyngeal from skin denticles, and (vi) the observation on zebrafish mutants affected in the dermal skeleton. This ‘modified outside in’ hypothesis can be tested both on paleontological data (it predicts a correlation of the presence of pharyngeal teeth and of gill slits), and on developmental data in extant species (it predicts the necessity of an ectodermal signal to make [pharyngeal] teeth).     

Structure and formation of ankylosis in Xenopus laevis

The structure of ankylotic teeth in Xenopus laevis was studied by light, transmission, and scanning electron microscopy as well as by microradiography in decalcified and undecalcified specimens. The mature teeth of Xenopus laevis are calcified from the crown to the base, fused to the jaw bone, and have no uncalcified area, such as a fibrous ring separating the tooth into the crown and pedicle. Microradiography shows that the mature tooth and jaw bone appear as an X-ray opaque area, except for the basal region of the dentine. This region is composed of an X-ray translucent area and an X-ray opaque thin layer on the lingual side of the translucent area. The mature tooth is composed of two differently calcified areas: (1) a highly calcified area, which makes up almost all of the tooth and contains a thin layer of the basal dentine on the lingual side, and (2) a lowly calcified basal dentine, which is fused to the jaw bone. Therefore, the lowly calcified area does not completely separate the dentine and jaw bone. Repeating banding patterns among the collagen fibrils differ among the dentine-forming area and the matrices of dentine and jaw bone. During the formation of ankylosis of the tooth germ, collagen bundles in the dentine-forming area accumulate directly on the surface of the jaw bone. Consequently, the mature teeth of Xenopus laevis fuse to the jaw bone directly without the mediation of the other structures.     

Structure and topographic distribution of oral denticles in elasmobranch fishes

The placoid scales, or denticles, of the external epidermis of elasmobranchs are well known as a hard protective coat over the skin to reduce abrasion or as elements to reduce hydrodynamic drag. However, the structure and function of denticles within the oral cavity is uncertain. Using stereological and scanning electron microscopy, this study examines the structure and distribution of oral denticles in a range of elasmobranchs. Of the batoids analyzed, only members of the Rhinobatidae possessed oral denticles, with no denticles found in the members sampled in the Gymnuridae or Dasyatidae. In contrast, oral denticles were located in all the selachians examined, except for members of the Orectolobidae. Within the selachians, the denticles of the Carcharhinidae have a grooved surface and a central spine, which is angled toward the posterior of the mouth. These denticular adaptations are beneficial to reduce hydrodynamic drag, an advantage for these free-swimming species with ram ventilation. Alternatively, members of the Hemiscyllidae have broad bulbous denticles that often overlap, providing a hard surface to protect the epithelium from abrasion during the consumption of hard-bodied prey. The distribution and high number of oral denticles appears to spatially compromise the capacity for oral (taste) papillae to populate the oropharyngeal cavity but provides increased friction and grip on prey items as they are manipulated within the mouth.     

Trigonognathus kabeyai,a new genus and species of the squalid sharks from Japan

Two specimens of the peculiar squalid shark,Trigonognathus kabeyai gen. et sp. nov., were collected from the coastal waters of Wakayama and Tokushima, Japan, by bottom trawl at depths of 330 and 360 meters. Shape of teeth similar in both jaws; slender, unicuspid, canine-like, without any cusplets or serrations, with weak thin fold on both lingual and labial sides in anterior teeth on both jaws; tooth at symphysis of each jaw longest. Interspace between teeth very wide. Both jaws triangular in shape. Most of dermal denticles on body and head roughly rhombic, swollen very much near central part, with about 10–40 facets on the dorsal surface of its crown. Preoral snout length very short. Many small organs considered to be photophores present mainly on ventral surfaces of head and body.     

Unique features of pedicellate attachment of the upper jaw teeth in the adult gobiid fish Sicyopterus japonicus (Teleostei,Gobiidiae): Morphological and structural characteristics and development

Sicyopterus japonicus (Teleostei, Gobiidae), a hill‐stream herbivorous gobiid fish, possesses an unusual oral dentition among teleost fishes on account of its feeding habitat. By using scanning electron microscopy, light microscopy, and transmission electron microscopy, including vital staining with tetracycline, we examined the development of the attachment tissues of the upper jaw teeth in this fish. The functional teeth of S. japonicus had an asymmetrical dentine shaft. The dentine shaft attached to the underlying uniquely shaped pedicel by means of two different attachment mechanisms. At the lingual base, collagen fiber bundles connected the dentine shaft with the pedicel (hinged attachment), whereas the labial base articulated with an oval‐shaped projection of the pedicel (articulate attachment). The pedicel bases were firmly ankylosed to the crest of the thin flange of porous spongy bone on the premaxillary bone, which afforded a flange‐groove system on the labial surface of the premaxillary bone. Developmentally, the pedicel and thin flange of spongy bone were completely different mineralized attachment tissues. The pedicel had a dual origin, i.e., the dental papilla cells, which differentiated into odontoblasts that constructed the internal surface of the pedicel, and the mesenchymal cells, which differentiated into osteoblasts that formed the outer face of the pedicel. A thin flange of spongy bone was deposited on the superficial resorbed labial side of the premaxillary bone proper, and later rapid bone remodeling proceeded toward the pedicel base. These unique features of pedicellate tooth attachment for the upper jaw teeth in the adult S. japonicus are highly modified teeth for enhancing the ability of individual functional teeth to move closely over irregularities in the rock surfaces during the scraping of algae. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Teeth of extant Polypteridae and Amiidae have plicidentine organization

The study of teeth of the lower jaws of Amia calva and Polypterus senegalus, with non -destructive X-ray tomography, has revealed that there are dentine folds in the tooth pulp cavity in both species. These folds are simple and present only in the base of the pulp cavity where they strengthen the fixation of teeth on the jaw. So the teeth of these two basal actinopterygian taxa have a simplexodont type of plicidentine like the extinct †Cheirolepis and various extant teleostean predators, whereas the extant Lepisosteids, the sister group of Amiidae, have polyplocodont plicidentine. The phylogenetic/adaptive significance of this simplexodont plicidentine is discussed.     

DEVELOPMENT AND EVOLUTIONARY ORIGINS OF VERTEBRATE SKELETOGENIC AND ODONTOGENIC TISSUES

This review deals with the following seven aspects of vertebrate skeletogenic and odontogenic tissues.

• 1 The evolutionary sequence in which the tissues appeared amongst the lower craniate taxa.
• 2 The topographic association between skeletal (cartilage, bone) and dental (dentine, cement, enamel) tissues in the oldest vertebrates of each major taxon.
• 3 The separate developmental origin of the exo- and endoskeletons.
• 4 The neural-crest origin of cranial skeletogenic and odontogenic tissues in extant vertebrates.
• 5 The neural-crest origin of trunk dermal skeletogenic and odontogenic tissues in extant vertebrates.
• 6 The developmental processes that control differentiation of skeletogenic and odontogenic tissues in extant vertebrates.
• 7 Maintenance of developmental interactions regulating skeletogenic/odontogenic differentiation across vertebrate taxa. We derive twelve postulates, eight relating to the earliest vertebrate skeletogenic and odontogenic tissues and four relating to the development of these tissues in extant vertebrates and extrapolate the developmental data back to the evolutionary origin of vertebrate skeletogenic and odontogenic tissues. The conclusions that we draw from this analysis are as follows.
• 8 The dermal exoskeleton of thelodonts, heterostracans and osteostracans consisted of dentine, attachment tissue (cement or bone), and bone.
• 9 Cartilage (unmineralized) can be inferred to have been present in heterostracans and osteostracans, and globular mineralized cartilage was present in Eriptychius, an early Middle Ordovician vertebrate unassigned to any established group, but assumed to be a stem agnathan.
• 10 Enamel and possibly also enameloid was present in some early agnathans of uncertain affinities. The majority of dentine tubercles were bare.
• 11 The contemporaneous appearance of cellular and acellular bone in heterostracans and osteostracans during the Ordovician provides no clue as to whether one is more primitive than the other.
• 12 We interpret aspidin as being developmentally related to the odontogenic attachment tissues, either closer to dentine or a form of cement, rather than as derived from bone.
• 13 Dentine is present in the stratigraphically oldest (Cambrian) assumed vertebrate fossils, at present some only included as Problematica, and is cladistically primitive, relative to bone.
• 14 The first vertebrate exoskeletal skeletogenic ability was expressed as denticles of dentine.
• 15 Dentine, the bone of attachment associated with dentine, the basal bone to which dermal denticles are fused and cartilage of the Ordovician agnathan dermal exoskeleton were all derived from the neural crest and not from mesoderm. Therefore the earliest vertebrate skeletogenic/odontogenic tissues were of neural-crest origin.
• 16 Given the separate developmental and evolutionary origin of the cranial exo- and endoskeletons (both derivatives of the cranial neural crest) we conclude that bone (of attachment) was the primary skeletogenic tissue in the exoskeleton (cartilage being secondary), but that uncalcified cartilage was the primary skeletogenic tissue in the endoskeleton (bone – perichondral – being secondary).
• 17 Using evidence from developmental biology we conclude that the trunk neural crest of Ordovician agnathans was odontogenic, forming both dentine and bone of attachment of the trunk dermal exoskeleton.
• 18 Initiation of differentiation of skeletogenic and odontogenic tissues is controlled epigenetically by one or more epithelial-mesenchymal interactions in epigenetic cascades.
• 19 Changes in timing of steps in these epigenetic cascades provides an evolutionary mechanism for altering the types of skeletogenic/odontogenic tissues and/or structures formed.
• 20 The appearance of epithelial-mesenchymal interactions and the origin of the skeletogenic/odontogenic neural crest at the outset of vertebrate evolution provided the developmental basis for the evolutionary origin of vertebrate skeletogenic and odontogenic tissues and for the appearance and evolution of the vertebrate 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.     

New data on the systematics and interrelationships of sawfishes (Elasmobranchii, Batoidea, Pristiformes)

New characters based on the arrangement and morphology of dermal denticles show that sawfishes can be divided into two distinctive groups. The first group, comprising the knifetooth sawfish Anoxypristis cuspidata , is characterized by tricuspid denticles variably located on both dorsal and ventral parts of the body. The second group is represented by species of the genus Pristis , showing an uniform and homogenous dermal covering of monocuspidate denticles on both dorsal and ventral sides of the body and within the buccopharyngeal cavity. Pristis is further divided into two subgroups: the first comprises species with denticles lacking any keels and furrows (the smalltooth sawfish Pristis pectinata , the green sawfish Pristis zijsron and the dwarf sawfish Pristis clavata ); the second comprises species with denticles presenting keels and furrows well differentiated on their anterior part (the common sawfish Pristis pristis , the largetooth sawfish Pristis perotteti and the greattooth sawfish Pristis microdon ). This investigation of the dermal covering provides results which agree with studies that separate the same two species groups of Pristis on the basis of other morphological data.