Development of dentition and dermal skeleton in embryonic Scyliorhinus canicula
01 Dec 1980-Journal of Morphology (Wiley Subscription Services, Inc., A Wiley Company)-Vol. 166, Iss: 3, pp 275-288
TL;DR: Serial sections ranging from very young embryos to hatched juveniles and whole embryos of Scyliorhinus show that dentition and dermal skeleton belong to two independent secondary developmental fields that differ both developmentally and structurally.
Abstract: Serial sections ranging from very young embryos to hatched juveniles and whole embryos of Scyliorhinus show that dentition and dermal skeleton belong to two independent secondary developmental fields that differ both developmentally and structurally. The development of the dentition starts very early, with a thickening of the ectoderm in the region of the mouth (stage 04), the invagination of the dental lamina (stage 18), and the formation of the germs of the first generation (stage 20). Tooth replacement movements start only near the end of embryogenesis (stage 35). Scale germs, on the other hand, first begin to form at stage 24. Scales erupt shortly before the animal hatches (stage 43). Only one scale generation is formed during embryogenesis. The forces which erupt the scales may come from fluid pressures in vacuoles of the fibrous layer of the dermis. Those which erupt the teeth probably also result from similar fluid pressures. The crown and upper part of the base of scales and teeth are formed by cells of the inner dental epithelium which are differentiated from the ectoderm. They are also formed by odontoblasts which are derived from the vascular layer of the dermis. However, the basal plates of scales and teeth containing the anchoring fibers are formed by osteoblasts, which are derived from the fibrous layer of the dermis.
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01 Jan 1982
TL;DR: The starting point of comparative evolutionary studies of the dermal skeleton of vertebrates is Hertwig’s series of papers (1874, 1876/1879/1882), which directly stimulated many dozens of papers, most of them in German and some of them long forgotten.
Abstract: The starting point of comparative evolutionary studies of the dermal skeleton of vertebrates is Hertwig’s series of papers (1874, 1876/1879/1882), which directly stimulated many dozens of papers, most of them in German and some of them long forgotten. The literature on comparative histology and histogenesis of the dermal skeleton and on regulatory and morphogenetic processes of the vertebrate integument is so voluminous that it can hardly be summarized. Ever since Hertwig, attempts have been made not only to contribute descriptive and experimental data, but also to arrive at a synthesis. Most of the synthetic papers, however, address only a small section of the theoretical problems, and it seems that some important questions have never been asked.
260 citations
TL;DR: The formation of the squamation pattern suggests a pre-patterning of the skin before scale initiation, and the potential that scale development offers as a model to study organogenesis mediated by epithelial-mesenchymal interactions is illustrated.
Abstract: In the first part of this paper we review current knowledge regarding fish scales, focusing on elasmoid scales, the only type found in two model species, the zebrafish and the medaka. After reviewing the structure of scales and their evolutionary origin, we describe the formation of the squamation pattern. The regularity of this process suggests a pre-patterning of the skin before scale initiation. We then summarise the dynamics of scale development on the basis of morphological observations. In the absence of molecular data, these observations support the existence of genetic cascades involved in the control of scale development. In the second part of this paper, we illustrate the potential that scale development offers as a model to study organogenesis mediated by epithelial-mesenchymal interactions. Using the zebrafish (Danio rerio), we have combined alizarin red staining, light and transmission electron microscopy and in situ hybridisation using an anti-sense RNA probe for the sonic hedgehog (shh) gene. Scales develop late in ontogeny (30 days post-fertilisation) and close to the epidermal cover. Only cells of the basal epidermal layer express shh. Transcripts are first detected after the scale papillae have formed. Thus, shh is not involved in the mechanisms controlling squamation patterning and scale initiation. As the scales enlarge, shh expression is progressively restricted to a subset of basal epidermal cells located in the region that overlies their posterior field. This pattern of expression suggests that shh may be involved in the control of scale morphogenesis and differentiation in relationship with the formation of the epidermal fold in the posterior region.
234 citations
TL;DR: 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.
Abstract: 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.
199 citations
Cites background from "Development of dentition and dermal..."
...This view is based largely on the developmental resemblance of shark odontodes (placoid scales ) to teeth, despite the fact that they do not grade into each other (Reif, 1980)....
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TL;DR: The organization of the vertebrate dentition as a system of repeated parts provides an opportunity to study the extent to which phenotypic modules, identified by their evolutionary independence from other such units, are related to modularity in the genetic control of development.
Abstract: The construction of organisms from units that develop under semi-autonomous genetic control (modules) has been proposed to be an important component of their ability to undergo adaptive phenotypic evolution. The organization of the vertebrate dentition as a system of repeated parts provides an opportunity to study the extent to which phenotypic modules, identified by their evolutionary independence from other such units, are related to modularity in the genetic control of development. The evolutionary history of vertebrates provides numerous examples of both correlated and independent evolution of groups of teeth. The dentition itself appears to be a module of the dermal exoskeleton, from which it has long been under independent genetic control. Region-specific tooth loss has been a common trend in vertebrate evolution. Novel deployment of teeth and reacquisition of lost teeth have also occurred, although less frequently. Tooth shape differences within the dentition may be discontinuous (referred to as heterodonty) or graded. The occurrence of homeotic changes in tooth shape provides evidence for the decoupling of tooth shape and location in the course of evolution. Potential mechanisms for region-specific evolutionary tooth loss are suggested by a number of mouse gene knockouts and human genetic dental anomalies, as well as a comparison between fully-developed and rudimentary teeth in the dentition of rodents. These mechanisms include loss of a tooth-type-specific initiation signal, alterations of the relative strength of inductive and inhibitory signals acting at the time of tooth initiation and the overall reduction in levels of proteins required for the development of all teeth. Ectopic expression of tooth initiation signals provides a potential mechanism for the novel deployment or reacquisition of teeth; a single instance is known of a gene whose ectopic expression in transgenic mice can lead to ectopic teeth. Differences in shape between incisor and molar teeth in the mouse have been proposed to be controlled by the region-specific expression of signalling molecules in the oral epithelium. These molecules induce the expression of transcription factors in the underlying jaw mesenchyme that may act as selectors of tooth type. It is speculated that shifts in the expression domains of the epithelial signalling molecules might be responsible for homeotic changes in tooth shape. The observation that these molecules are regionally restricted in the chicken, whose ancestors were not heterodont, suggests that mammalian heterodonty may have evolved through the use of patterning mechanisms already acting on skeletal elements of the jaws. In general, genetic and morphological approaches identify similar types of modules in the dentition, but the data are not yet sufficient to identify exact correspondences. It is speculated that modularity may be achieved by gene expression differences between teeth or by differences in the time of their development, causing mutations to have cumulative effects on later-developing teeth. The mammalian dentition, for which virtually all of the available developmental genetic data have been collected, represents a small subset of the dental diversity present in vertebrates as a whole. In particular, teleost fishes may have a much more extensive dentition. Extension of research on the genetic control of tooth development to this and other vertebrate groups has great potential to further the understanding of modularity in the dentition.
116 citations
TL;DR: Current research and recent progress in this field during the last decade that have promoted the understanding of tooth diversity in an evolutionary developmental context are reviewed, and how tooth replacement and dental regeneration have impacted the evolution of the tooth-jaw module in vertebrates are shown.
100 citations
References
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TL;DR: The model is described, which can explain regulative behavior in cockroach legs, the imaginal disks of Drosophila, and regenerating and developing amphibian limbs, and suggests that it may have general applicability to epimorphic fields.
Abstract: We have described a formal model for pattern regulation in epimorphic fields in which positional information is specified in terms of polar coordinates in two dimensions. We propose that cells within epimorphic fields behave according to two simple rules, the shortest intercalation rule and the complete circle rule, for both of which there is direct experimental evidence. It is possible to understand a large number of different behaviors of epimorphic fields as a straight-forward consequence of these two rules, and the model therefore provides a context in which to view many of the results of experimental embryology. Although we have confined our discussion to cockroach legs, the imaginal disks of Drosophila, and regenerating and developing amphibian limbs, the fact that the model can explain regulative behavior in such evolutionarily diverse animals suggests that it may have general applicability to epimorphic fields. The predictions which the model makes should make it possible to assess its applicability to other developing systems, and to investigate the cellular mechanisms involved.
844 citations
TL;DR: The tissue of origin and molecular nature of basal laminar glycosaminoglycan are described and speculations are made regarding its possible mode of action in the context of a model for branching morphogenesis.
Abstract: The concept that extracellular matrix materials are involved in the morphogeuetic process is supported by substantial indirect evidence. Essential morphogenetically active materials are obscure with regard to their nature, their mode of action, and whether they are causally involved in tissue interactions.
Studies are presented indicating that glycosaminoglycans are components of embryonic epithelial basal laminae, and that materials within the basal lamina which are, at least in part, glycosaminoglycan are required for establishing and maintaining braching epithelial morphogenesis. The tissue of origin and molecular nature of basal laminar glycosaminoglycan are described and speculations are made regarding its possible mode of action in the context of a model for branching morphogenesis.
130 citations