Microstructure and Growth of the Dermal Skeleton in Fossil Actinopterygian Fishes: Boreosomus, Plegmolepis and Gyrolepis

The odontodes of some of the palatal dermal bones in Boreosomus piveteaui Nielsen tend to form odontocomplexes, e.g. symmetrical areal ones where some degree of superimposition may occur between ganoin layers belonging to the component odontodes, and asymmetrical areal ones where this is quite insignificant. In the areal odontocomplexes of the dermal bones in Plegmolepis sp., the degree of overlap between the corresponding layers is somewhat more pronounced. Finally, in the areal odontocomplexes of the dermal bones in Gyrolepis cf. albertii Agassiz, we have a more advanced stage of phyletic specialization where each of the ganoin layers of the component odontodes lies directly superimposed on the preceding one throughout the extent of the latter. At the same time, the effect of phyletic dentine reduction is clearly noticeable here by the development of "extra" ganoin layers no more retaining their original connections with that hard tissue (also developed in the scales of Plegmolepis sp.). Remarks are i.a. given on the characters by which Acropholis and Plegmolepis are said to be distinguishable from each other.     

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.     

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.     

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.     

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.     

Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica

Traditional hypotheses posit that teeth evolved from dermal scales, through the expansion of odontogenetically competent ectoderm into the mouth of jawless vertebrates. The discovery of tooth‐like scales inside thelodonts, an extinct group of jawless vertebrates, led to the alternative hypothesis that teeth evolved from endodermal derivatives and that there exists a fundamental developmental and phylogenetic distinction between oral/pharyngeal and external odontodes. We set out a test of this latter hypothesis, examining the development of scales of the thelodont Loganellia scotica using synchrotron radiation X‐ray tomographic microscopy (SRXTM). We reveal that the internal scales are organized into fused patches and rows, a key distinction from the discrete dermal scales. The pattern of growth of oral scale patches is polarized, but not along a particular vector, whereas pharyngeal scale rows grew along a vector. Our test of the phylogenetic distribution of oral and pharyngeal scales and teeth in vertebrates indicates that odontodes are first expressed in an external position. Internal scales, where present, are always located near to external orifices; the sequential development of pharyngeal scales in Loganellia is peculiar among thelodonts and other stem gnathostomes. It represents a convergence on, rather than the establishment of, the developmental pattern underpinning tooth replacement in jawed vertebrates. The available evidence suggests that internal odontodes evolved through the expansion of odontogenic competence from external to internal epithelia.     

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.     

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.     

Scales and Dermal Skeletal Histology of an Early Bony Fish Psarolepis romeri and Their Bearing on the Evolution of Rhombic Scales and Hard Tissues

Recent discoveries of early bony fishes from the Silurian and earliest Devonian of South China (e.g. Psarolepis, Achoania, Meemannia, Styloichthys and Guiyu) have been crucial in understanding the origin and early diversification of the osteichthyans (bony fishes and tetrapods). All these early fishes, except Guiyu, have their dermal skeletal surface punctured by relatively large pore openings. However, among these early fishes little is known about scale morphology and dermal skeletal histology. Here we report new data about the scales and dermal skeletal histology of Psarolepis romeri, a taxon with important implications for studying the phylogeny of early gnathostomes and early osteichthyans. Seven subtypes of rhombic scales with similar histological composition and surface sculpture are referred to Psarolepis romeri. They are generally thick and show a faint antero-dorsal process and a broad peg-and-socket structure. In contrast to previously reported rhombic scales of osteichthyans, these scales bear a neck between crown and base as in acanthodian scales. Histologically, the crown is composed of several generations of odontodes and an irregular canal system connecting cylindrical pore cavities. Younger odontodes are deposited on older ones both superpositionally and areally. The bony tissues forming the keel of the scale are shown to be lamellar bone with plywood-like structure, whereas the other parts of the base are composed of pseudo-lamellar bone with parallel collagen fibers. The unique tissue combination in the keel (i.e., extrinsic Sharpey''s fibers orthogonal to the intrinsic orthogonal sets of collagen fibers) has rarely been reported in the keel of other rhombic scales. The new data provide insights into the early evolution of rhombic (ganoid and cosmoid) scales in osteichthyans, and add to our knowledge of hard tissues of early vertebrates.     

Sclerotic plates or circumorbital bones in early jawed fishes?

Abstract: Circumorbital dermal bones are found in most groups of early vertebrates that have dermal bony plates on the head. Taxonomic distribution of dermal sclerotic plates on the eye itself is less clear, partly because the eyeball is rarely preserved and sometimes because sclerotic bones have been misinterpreted as circumorbital bones. Based on the examination of climatiid Climatius plus mesacanthid, cheiracanthid and acanthodid acanthodiform acanthodians, we conclude that most, if not all, acanthodiforms and climatiids had sclerotic rings. Presence and number of these elements should be included as a character in phylogenetic analyses of early jawed vertebrates.     

Osteocranial development in the viviparous surfperch Amphistichus argenteus (pisces: Embiotocidae)

The development of the cranial and branchial skeleton of the surfperch Amphistichus argenteus, a member of the family Embiotocidae, is described, and phylogenetic and functional aspects of the skull development of this species are discussed. The earliest bones to appear are those dermal elements of the branchial skeleton involved with feeding, and the bones, both dermal and endochondral, located in the basicranial region of the neurocranium. These are followed by dermal bones associated with the lateral line system and finally by the remainder of the bones of the branchial skeleton and the cartilaginous bones of the otic capsules. The last bone to develop is the ethmoid.     

Development of the head skeleton and pectoral girdle in Esox.

A consideration of head development in two species of Esox, lucius and americanus (ssp. vermiculatus) representing the two subgenera Esox and Kenozoa respectively, focused on the significance of the variations of the latero-sensory canal system, its associated bones, and other skeletal elements. In living forms only aspects of "regression" or specialization can be studied. Canals tend to be reduced to pit lines first at their termini but can be broken in their course. Pit lines range from nearly canals to surface structures, or even fail to develop. The number of neuromasts varies. Canal bones develop from two centers: neuromast related and deeper membranous centers which may have no relationship to neuromasts. Tooth-bearing and non-canal-related dermal bones have only membranous (original) centers. The number of neuromasts associated with a bone usually does not affect its development or form. In the case of the circumorbital bones, the extrascapulars, and the nasal, a one to one relationship has developed by regression--towards the development of the latero-sensory component only. The idea that reductions in bone number are commonly traceable to fusion is rejected although examples of fusion are know. Most bones that disappear are simply lost (no blastema or other evidence of their presence seen in development). The relationship between dermal bone and chondral bone is examined and there is evidence of the former giving rise to the latter. The ontogenic order of appearances shows a feeding (functional) correlation.     

Structure and Development of Teeth in Three Armoured Catfish, Corydoras aeneus, C. arcuatus and Hoplosternum littorale (Siluriformes, Callichthyidae)

We have studied the premaxillary teeth in three armoured catfish, Corydoras aeneus, C. arcuatus and Hoplosternum littorale , by means of light and electron microscopy, in order to compare their development, fine structure and mode of attachment with that of odontodes and other teleost teeth. A premaxillary dentition consisting of small (50–100 μm long) slender pointed teeth showing no true replacement is only present in larval and juvenile stages and is subsequently lost, possibly in relation to a change in feeding mode from predatory to bottom feeder. Like odontodes, teeth are composed of dentine surrounding a pulp cavity and are covered by a hypermineralized cap. Particular features, also found in odontodes, are the absence of dentinal tubules and of nerves and capillaries in the pulp cavity, both possibly related to the small size of the teeth. The irregular pattern of implantation and the variability in attachment mode (primary and/or secondary attachment bone, fusion, mere apposition or ligamentous connection) distinguish the teeth from most other teleost teeth and from odontodes and are interpreted as reflecting considerable differences in dynamics of remodeling of the supporting element (premaxillary bone vs scute). This comparison of teeth and odontodes strongly supports current views according to which teeth and odontodes are two very closely related phenotypic expressions of a single, modifiable, morphogenetic system probably rooted in the earliest stages of vertebrate evolution.     

Primitive bony fishes, with especial reference to Cheirolepis and palaeonisciform actinopterygians

The relationships of the Devonian palaeonisciform fish Cheirolepis are examined and the early evolutionary trends within the Actinopterygii and the Osteichthyes are considered.
Cheirolepis is the most primitive known actinopterygian. The contemporary stegotrachelid palaeonisciforms are more advanced in their cranial and locomotor anatomy. The general directions of these advances are similar to those subsequently displayed by later palaeonisciforms over the stegotrachelids themselves. Cheirolepis , furthermore, possesses many characters which can be logically interpreted as primitive for the Osteichthyes by extrapolation of trends in actinopterygian and sarcopterygian lineages. 11 is the most primitive known osteichthyan.
The Osteichthyes are considered to have arisen from a micromerically-scaled acanthodian or acanthodian-like ancestor at the end of the Silurian period.     

Early development of the cephalic skeleton of Barbus barbus (Teleostei, Cyprinidae)

The inception, and development of the cephalic skeleton of Barbus barbus from hatching to 24 days passes through periods of fast and slow growth; these rates are not the same in different parts of the skull. Trabeculae, parachordal plates, Meckelian cartilages and hyposymplectics are present at hatching. Then the cartilaginous floor of the neurocranium develops, the pars quadrata, the hyoid bars and branchial arches elements appear shortly before the first movable dermal bones, the dentaries, maxillae and opercles. The first bone of the braincase to appear is the parasphenoid; other bones develop subsequently and at the same time: the angular, quadrate, interopercle and fifth ceratobranchial. Later the splanchnocranium continues to develop at a relatively fast rate while the neurocranium shows little growth. The braincase does not begin to close before the 24th day, nor do the first bones of the skull roof appear, while the bucco-pharyngeal apparatus is complete, having the adult shape. The early constitution of the latter structures seems to be linked with the mechanical demands of biological functions such as breathing and feeding.     

The identification of the dermal bones of the head

The discovery of the ichthyostegid Amphibia in Upper Devonian rocks by Säve-Söderbergh (1932) introduced further difficulties into the already complex problems of the dermal bones of the skull roof. For some years previously ideas about the origin of the tetrapods had been dominated by Watson's (1926) Croonian Lecture in which he had demonstrated beyond reasonable doubt that the crossopterygian fishes and not the Dipnoi were their ancestors, and had attempted to show that many of the features of the Carboniferous labyrinthodonts were a direct inheritance from these fishes. It was to be expected, therefore, that any Amphibia from the Upper Devonian would be intermediate in their structures between the Middle Devonian osteolepids and the Carboniferous labyrinthodonts, but when discovered the ichthyostegids did not conform at all well to this expectation. While their skulls showed some very primitive features which might have been expected, the pattern of the dermal bones did not conform to plan, for these new animals had lost, it seemed, the intertemporals, bones found in both the osteolepids and nearly all early labyrinthodonts, and had a single postparietal bone in place of the paired bones of all other early Amphibia. The osteolepid skull had many more bones than these earliest Amphibia.     

Inter‐ and intraspecific variation in the surface pattern of the dermal bones of two sturgeon species

Archaeological bone remains of sturgeon (Acipenser sturio/Acipenser oxyrinchus) from northwestern Europe are often identified to species on the basis of their surface morphology and then used to reconstruct the spatial distribution of the two species through time. The dermal bones of A. sturio are said to have an exterior surface pattern consisting of tubercles, while those of A. oxyrinchus are said to display alveoli. In the present paper, the validity of the surface pattern as a species‐specific characteristic is critically assessed. To this purpose, dermal plates from modern, genetically identified museum specimens were studied and the surface morphology observed in a series of archaeological remains was compared with the genetic identifications obtained on these same remains. The analyses show that the surface pattern of dermal bones is related to the size of the individual, with the pattern of small A. oxyrinchus being similar to that of A. sturio. In addition, variations in the surface pattern among the bones of a single individual and within the same bone have been observed. These findings explain previous conflicting results between morphological and genetic identifications and allow the formulation of some recommendations for more accurate morphological identification of isolated archaeological sturgeon dermal bones.     

Cosmine resorption structures on three osteolepid jaws and their biological significance

Cosmine resorption structures on three osteolepid jaws provide evidence for two different types of resorption process, one superficial and one initially internal. The superficial process starts in the pore canal openings. and the internal probably in the dentine pulp cavities or other cavities within the cosminc. Different stages of the superficial process that have previously not been recorded can he seen. Their positions show that superficial resorption may start in a few centers, from which it may spread in all directions but at different rates in different directions. There is no observable correspondence between the occurrence of resorption and the growth of the dermal bones along their sutures. Thus, the primary reason for resorption is not to allow marginal growth of the dermal bones. □ Cosmine resorption, osteolepids, Middle Devonian.     

Dermal morphogenesis controls lateral line patterning during postembryonic development of teleost fish

The lateral line system displays highly divergent patterns in adult teleost fish. The mechanisms underlying this variability are poorly understood. Here, we demonstrate that the lateral line mechanoreceptor, the neuromast, gives rise to a series of accessory neuromasts by a serial budding process during postembryonic development in zebrafish. We also show that accessory neuromast formation is highly correlated to the development of underlying dermal structures such as bones and scales. Abnormalities in opercular bone morphogenesis, in endothelin 1-knockdown embryos, are accompanied by stereotypic errors in neuromast budding and positioning, further demonstrating the tight correlation between the patterning of neuromasts and of the underlying dermal bones. In medaka, where scales form between peridermis and opercular bones, the lateral line displays a scale-specific pattern which is never observed in zebrafish. These results strongly suggest a control of postembryonic neuromast patterns by underlying dermal structures. This dermal control may explain some aspects of the evolution of lateral line patterns.