Dental homologies in lamniform sharks (Chondrichthyes: Elasmobranchii).

The dentitions of lamniform sharks are said to exhibit a unique heterodonty called the "lamnoid tooth pattern." The presence of an inflated hollow "dental bulla" on each jaw cartilage allows the recognition of homologous teeth across most modern macrophagous lamniforms based on topographic correspondence through the "similarity test." In most macrophagous lamniforms, three tooth rows are supported by the upper dental bulla: two rows of large anterior teeth followed by a row of small intermediate teeth. The lower tooth row occluding between the two rows of upper anterior teeth is the first lower anterior tooth row. Like the first and second lower anterior tooth rows, the third lower tooth row is supported by the dental bulla and may be called the first lower intermediate tooth row. The lower intermediate tooth row occludes between the first and second upper lateral tooth rows situated distal to the upper dental bulla, and the rest of the upper and lower tooth rows, all called lateral tooth rows, occlude alternately. Tooth symmetry cannot be used to identify their dental homology. The presence of dental bullae can be regarded as a synapomorphy of Lamniformes and this character is more definable than the "lamnoid tooth pattern." The formation of the tooth pattern appears to be related to the evolution of dental bullae. This study constitutes the first demonstration of supraspecific tooth-to-tooth dental homologies in nonmammalian vertebrates.     

Homologies of the anterior teeth in Indriidae and a functional basis for dental reduction in primates

In a recent paper Schwartz ('74) proposes revised homologies of the deciduous and permanent teeth in living lemuriform primates of the family Indriidae. However, new evidence provided by the deciduous dentition ofAvahi suggests that the traditional interpretations are correct, specifically: (1) the lateral teeth in the dental scraper of Indriidae are homologous with the incisors of Lemuridae and Lorisidae, not the canines; (2) the dental formula for the lower deciduous teeth of indriids is 2.1.3; (3) the dental formula for the lower permanent teeth of indriids is 2.0.2.3; and (4) decrease in number of incisors during primate evolution was usually in the sequence I3, then I2, then I1. It appears that dental reduction during primate evolution occurred at the ends of integrated incisor and cheek tooth units to minimize disruption of their functional integrity.     

Supernumerary molars in anthropoidea,adapidae, and Archaeolemur: Implications for primate dental homologies

The model of primate dental homologies and development recently proposed by Schwartz ('75, '78) is re-evaluated in view of documented exceptions to his account of postcanine supernumerary teeth in both anthropoids and prosimians. Schwartz concluded that catarrhines and living indriids retain only two true molars in each dental quadrant. As many as six molars on one side of the jaw can develop in rare instances in catarrhines, and supernumerary molars are also known for a wide range of other primates, including Cebidae, Adapidae, and subfossil Indriidae. Polydontia cannot be explained exclusively by atavistic development. More convincing explanations regard supernumerary teeth as the result of excessive growth of the dental lamina or localized twinning of tooth buds during early development. Conventional dental formulae of catarrhines and indriids including three permanent molars remain the most plausible.     

Sizes of deciduous teeth in 47,XYY males.

Deciduous teeth of six 47,XYY males have been examined, and the tooth sizes were found to be larger than those of controls. We concluded that a factor or factors which influence excess dental growth in 47,XYY males are probably in effect before the age of a few months. The time needed for the achievement of final tooth growth excess seems to be limited to a 9--18 month period. It also became evident that excess dental growth of 47,XYY individuals is a developmentally stable process, and the Y chromosome apparently regulates quantitative variation of the teeth in normal males [2]. These observations on tooth sizes in 47,XYY males suggest a chromosomal influence on dental determination.     

Developmental origins and homologies of the hyracoid dentition

Understanding the origins of morphological specializations in mammals is a key goal in evolutionary biology. It can be accomplished by studying dental homology, which is at the core of most evolutionary and developmental studies. Here, we focused on the evolution and development of the specialized dentition of hyraxes for which dental homologies have long been debated, and could have implications on early placental evolution. Specifically, we analysed dental mineralization sequences of the three living genera of hyraxes and 17 fossil species using X‐ray computed microtomography. Our results point out the labile position of vestigial upper teeth on jaw bones in extant species, associated with the frequently unusual premolar shape of deciduous canines over 50 Ma of hyracoid evolution. We proposed two evolutionary and developmental hypotheses to explain these original hyracoid dental characteristics. (a) The presence of a vestigial teeth on the maxilla in front of a complex deciduous canine could be interpreted as extra‐teeth reminiscent of early placental evolution or sirenians, an order phylogenetically close to hyracoids and showing five premolars. (b) These vestigial teeth could also correspond to third incisors with a position unusually shifted on the maxilla, which could be explained by the dual developmental origin of these most posterior incisors and their degenerated condition. This integrative study allows discussion on the current evolutionary and developmental paradigms associated with the mammalian dentition. It also highlights the importance of nonmodel species to understand dental homologies.     

Studies on dentin. 2. Vestigial lacteal incisor teeth of the rat.

The presence of a vestigial, lacteal incisor tooth is described in the laboratory rat. This tooth is felt to belong to the same dental generation as the other functional teeth. Accordingly, the rat is described as having a monophyodont, first dentition containing two incisor teeth in each quadrant. These vestigial teeth are then compared with other similar mammalian teeth and are defined as transient, partially formed and non-functional. As such, they are differentiated from other transient teeth. The examination of the fossil record suggests that tooth loss is a general phenomenon in rodents, but that this vestigial tooth probably represents a condition present in forms antecedent to rodents. A critical literature review strongly suggests that the teeth of the recent rat are members of the first dental generation. The presence of such a vestigial tooth and of the postincisive diastema in the rat is felt to be an example of phylogenetic reduction and progressive retardation in the sense of de Beer's concepts. These same two phenomena were analyzed with respect to the field theory of Butler and of the Zahnreihen theory of Edmund. Placed within the context of recent data on epithelioectomesenchymal interactions, both theories were supported, and both the vestigial teeth and anodontic diastema were shown to be explicable within these conceptual frameworks.     

Patterns of size variation and correlation in the dentition of the red colobus monkey (Colobus badius)

There have been numerous studies on variability and correlation in dental crown size, but the significance of the resulting patterns remains unclear. Regions of low variation and high correlation have been hypothesized to represent the poles of Butler's morphological fields, to be related to absolute tooth size, or to be related to morphological complexity of the teeth and functional efficiency. Variation and correlation of tooth lengths and breadths were investigated in 138 red colobus monkeys to further assess the relations among size associations, crown morphology, and absolute tooth size. In the maxilla and mandible, the postcanine teeth are the most highly correlated and least variable, followed by the incisors, then the canines. There are also lower correlations between premolars and molars than within either group. While there appears to be a relation between degree of morphological differentiation and levels of correlation and variation, there are no notable differences in the correlation of opponents along the dental arcade, which is the most important functional consideration. This suggests that different levels of correlation and variation within upper or lower teeth are “artifacts” of tooth dimensions that contribute to different geometric designs in different tooth groups as the germs develop. This morphological effect is coupled with the influence of integration fields, indicated by higher variability and lower correlations of the third molar, the largest or most molarized tooth. It is concluded that there are wide functional tolerances in occlusion with respect to the gross dimensions of dental crowns and their interrelationships.     

Gene deployment for tooth replacement in the rainbow trout (Oncorhynchus mykiss): a developmental model for evolution of the osteichthyan dentition

Repeated tooth initiation occurs often in nonmammalian vertebrates (polyphyodontism), recurrently linked with tooth shedding and in a definite order of succession. Regulation of this process has not been genetically defined and it is unclear if the mechanisms for constant generation of replacement teeth (secondary dentition) are similar to those used to generate the primary dentition. We have therefore examined the expression pattern of a sub-set of genes, implicated in tooth initiation in mouse, in relation to replacement tooth production in an osteichthyan fish (Oncorhynchus mykiss). Two epithelial genes pitx2, shh and one mesenchymal bmp4 were analyzed at selected stages of development for O. mykiss. pitx2 expression is upregulated in the basal outer dental epithelium (ODE) of the predecessor tooth and before cell enlargement, on the postero-lingual side only. This coincides with the site for replacement tooth production identifying a region responsible for further tooth generation. This corresponds with the expression of pitx2 at focal spots in the basal oral epithelium during initial (first generation) tooth formation but is now sub-epithelial in position and associated with the dental epithelium of each predecessor tooth. Co-incidental expression of bmp4 and aggregation of the mesenchymal cells identifies the epithelial-mesenchymal interactions and marks initiation of the dental papilla. These together suggest a role in tooth site regulation by pitx2 together with bmp4. Conversely, the expression of shh is confined to the inner dental epithelium during the initiation of the first teeth and is lacking from the ODE in the predecessor teeth, at sites identified as those for replacement tooth initiation. Importantly, these genes expressed during replacement tooth initiation can be used as markers for the sites of "set-aside cells," the committed odontogenic cells both epithelial and mesenchymal, which together can give rise to further generations of teeth. This information may show how initial pattern formation is translated into secondary tooth replacement patterns, as a general mechanism for patterning the vertebrate dentition. Replacement of the marginal sets of teeth serves as a basis for discussion of the evolutionary significance, as these dentate bones (dentary, premaxilla, maxilla) form the restricted arcades of oral teeth in many crown-group gnathostomes, including members of the tetrapod stem group.     

Tooth development in a scincid lizard, Chalcides viridanus (Squamata), with particular attention to enamel formation

Comparative analysis of tooth development in the main vertebrate lineages is needed to determine the various evolutionary routes leading to current dentition in living vertebrates. We have used light, scanning and transmission electron microscopy to study tooth morphology and the main stages of tooth development in the scincid lizard, Chalcides viridanus, viz., from late embryos to 6-year-old specimens of a laboratory-bred colony, and from early initiation stages to complete differentiation and attachment, including resorption and enamel formation. In C. viridanus, all teeth of a jaw have a similar morphology but tooth shape, size and orientation change during ontogeny, with a constant number of tooth positions. Tooth morphology changes from a simple smooth cone in the late embryo to the typical adult aspect of two cusps and several ridges via successive tooth replacement at every position. First-generation teeth are initiated by interaction between the oral epithelium and subjacent mesenchyme. The dental lamina of these teeth directly branches from the basal layer of the oral epithelium. On replacement-tooth initiation, the dental lamina spreads from the enamel organ of the previous tooth. The epithelial cell population, at the dental lamina extremity and near the bone support surface, proliferates and differentiates into the enamel organ, the inner (IDE) and outer dental epithelium being separated by stellate reticulum. IDE differentiates into ameloblasts, which produce enamel matrix components. In the region facing differentiating IDE, mesenchymal cells differentiate into dental papilla and give rise to odontoblasts, which first deposit a layer of predentin matrix. The first elements of the enamel matrix are then synthesised by ameloblasts. Matrix mineralisation starts in the upper region of the tooth (dentin then enamel). Enamel maturation begins once the enamel matrix layer is complete. Concomitantly, dental matrices are deposited towards the base of the dentin cone. Maturation of the enamel matrix progresses from top to base; dentin mineralisation proceeds centripetally from the dentin–enamel junction towards the pulp cavity. Tooth attachment is pleurodont and tooth replacement occurs from the lingual side from which the dentin cone of the functional teeth is resorbed. Resorption starts from a deeper region in adults than in juveniles. Our results lead us to conclude that tooth morphogenesis and differentiation in this lizard are similar to those described for mammalian teeth. However, Tomes processes and enamel prisms are absent.     

Plate-like permanent dental laminae of upper jaw dentition in adult gobiid fish, Sicyopterus japonicus

Sicyopterus japonicus (Teleostei, Gobiidae) possesses a unique upper jaw dentition different from that known for any other teleosts. In the adults, many (up to 30) replacement teeth, from initiation to attachment, are arranged orderly in a semicircular-like strand within a capsule of connective tissue on the labial side of each premaxillary bone. We have applied histological, ultrastructural, and three-dimensional imaging from serial sections to obtain insights into the distribution and morphological features of the dental lamina in the upper jaw dentition of adult S. japonicus. The adult fish has numerous permanent dental laminae, each of which is an infolding of the oral epithelium at the labial side of the functional tooth and forms a thin plate-like structure with a wavy contour. All replacement teeth of a semicircular-like strand are connected to the plate-like dental lamina by the outer dental epithelium and form a tooth family; neighboring tooth families are completely separated from each other. The new tooth germ directly buds off from the ventro-labial margin of the dental lamina, whereas no distinct free end of the dental lamina is present, even adjacent to this region. Cell proliferation concentrated at the ventro-labial margin of the dental lamina suggests that this region is the site for repeated tooth initiation. During tooth development, the replacement tooth migrates along a semicircular-like strand and eventually erupts through the dental lamina into the oral epithelium at the labial side of the functional tooth. This unique thin plate-like permanent dental lamina and the semicircular-like strand of replacement teeth in the upper jaw dentition of adult S. japonicus probably evolved as a dental adaptation related to the rapid replacement of teeth dictated by the specialized feeding habit of this algae-scraping fish.     

An evolutionary view on tooth development and replacement in wild Atlantic salmon (Salmo salar L.)

SUMMARY To gain an insight into the evolution of tooth replacement mechanisms, we studied the development of first-generation and replacement teeth on the dentary of wild Atlantic salmon ( Salmo salar L.), a protacanthopterygian teleost, using serially sectioned heads of early posthatching stages as well as adults. First-generation teeth develop within the oral epithelium. The anlage of the replacement tooth is first seen as a placode-like thickening of the outer dental epithelium of the predecessor, at its lingual and caudal side. Ongoing development of the replacement tooth germ is characterized by the elaboration of a population of epithelial cells, termed here the middle dental epithelium, apposed to the inner dental epithelium on the lingual side of the tooth germ. Before the formation of the new successor, a single-layered outer dental epithelium segregates from the middle dental epithelium. The dental organs of the predecessor and the successor remain broadly interconnected. The absence of a discrete successional dental lamina in salmon stands in sharp contrast to what is observed in other teleosts, even those that share with salmon the extraosseous formation of replacement teeth. The mode of tooth replacement in Atlantic salmon displays several characters similar to those observed in the shark Squalus acanthias . To interpret similarities in tooth replacement between Atlantic salmon and chondrichthyans as a case of convergence, or to see them as a result of a heterochronic shift, requires knowledge on the replacement process in more basal actinopterygian lineages. The possibility that the middle dental epithelium functionally substitutes for a successional lamina, and could be a source of stem cells, whose descendants subsequently contribute to the placode of the new replacement tooth, needs to be explored.     

Developmental and evolutionary origins of the vertebrate dentition: molecular controls for spatio-temporal organisation of tooth sites in osteichthyans

The rainbow trout (Oncorhynchus mykiss) as a developmental model surpasses both zebrafish and mouse for a more widespread distribution of teeth in the oro-pharynx as the basis for general vertebrate odontogenesis, one in which replacement is an essential requirement. Studies on the rainbow trout have led to the identification of the initial sequential appearance of teeth, through differential gene expression as a changing spatio-temporal pattern, to set in place the primary teeth of the first generation, and also to regulate the continuous production of replacement tooth families. Here we reveal gene expression data that address both the field and clone theories for patterning a polyphyodont osteichthyan dentition. These data inform how the initial pattern may be established through up-regulation at tooth loci from a broad odontogenic band. It appears that control and regulation of replacement pattern resides in the already primed dental epithelium at the sides of the predecessor tooth. A case is presented for the developmental changes that might have occurred during vertebrate evolution, for the origin of a separate successional dental lamina, by comparison with an osteichthyan tetrapod dentition (Ambystoma mexicanum). The evolutionary origins of such a permanent dental lamina are proposed to have occurred from the transient one demonstrated here in the trout. This has implications for phylogenies based on the homology of teeth as only those developed from a dental lamina. Utilising the data generated from the rainbow trout model, we propose this as a standard for comparative development and evolutionary theories of the vertebrate dentition.     

Tooth regeneration from newly established cell lines from a molar tooth germ epithelium

In order to investigate tooth development, several cell lines of the dental epithelium and ectomesenchyme have been established. However, no attempt has been reported to regenerate teeth with cell lines. Here, we have established several clonal cell lines of the dental epithelium from a p53-deficient fetal mouse. They expressed specific markers of the dental epithelium such as ameloblastin and amelogenin. A new method has been developed to bioengineer tooth germs with dental epithelial and mesenchymal cells. Reconstructed tooth germs with cell lines and fetal mesenchymal cells were implanted under kidney capsule. The germs regenerated teeth with well-calcified structures as seen in natural tooth. Germs without the cell lines developed bone. This is the first success to regenerate teeth with dental epithelial cell lines. They are useful models in vitro for investigation of mechanisms in morphogenesis and of cell lineage in differentiation, and for clinical application for tooth regeneration.     

Reptilian tooth development

Dental patterns in vertebrates range from absence of teeth to multiple sets of teeth that are replaced throughout life. Despite this great variation, most of our understanding of tooth development is derived from studies on just a few model organisms. Here we introduce the reptile as an excellent model in which to study the molecular basis for early dental specification and, most importantly, for tooth replacement. We review recent snake studies that highlight the conserved role of Shh in marking the position of the odontogenic band. The distinctive molecular patterning of the dental lamina in the labial-lingual and oral-aboral axes is reviewed. We explain how these early signals help to specify the tooth-forming and non-tooth forming sides of the dental lamina as well as the presumptive successional lamina. Next, the simple architecture of the reptilian enamel organ is contrasted with the more complex, mammalian tooth bud and we discuss whether or not there is an enamel knot in reptilian teeth. The role of the successional lamina during tooth replacement in squamate reptiles is reviewed and we speculate on the possible formation of a vestigial, post-permanent dentition in mammals. In support of these ideas, we present data on agamid teeth in which development of a third generation is arrested. We suggest that in diphyodont mammals, similar mechanisms may be involved in reducing tooth replacement capacity. Finally, we review the location of label-retaining cells and suggest ways in which these putative dental epithelial stem cells contribute to continuous tooth replacement.     

What is dental ecology?

Teeth have long been used as indicators of primate ecology. Early work focused on the links between dental morphology, diet, and behavior, with more recent years emphasizing dental wear, microstructure, development, and biogeochemistry, to understand primate ecology. Our study of Lemur catta at the Beza Mahafaly Special Reserve, Madagascar, has revealed an unusual pattern of severe tooth wear and frequent tooth loss, primarily the result of consuming a fallback food for which these primates are not dentally adapted. Interpreting these data was only possible by combining our areas of expertise (dental anatomy [FC] and primate ecology [MS]). By integrating theoretical, methodological, and applied aspects of both areas of research, we adopted the term "dental ecology"-defined as the broad study of how teeth respond to the environment. Specifically, we view dental ecology as an interpretive framework using teeth as a vehicle for understanding an organism's ecology, which builds upon earlier work, but creates a new synthesis of anatomy and ecology that is only possible with detailed knowledge of living primates. This framework includes (1) identifying patterns of dental pathology and tooth use-wear, within the context of feeding ecology, behavior, habitat variation, and anthropogenic change, (2) assessing ways in which dental development and biogeochemical signals can reflect habitat, environmental change and/or stress, and (3) how dental microstructure and macro-morphology are adapted to, and reflect feeding ecology. Here we define dental ecology, provide a short summary of the development of this perspective, and place our new work into this context.     

Extreme dentition does not prevent diet and tooth diversification within combtooth blennies (Ovalentaria: Blenniidae)

The dentition of fishes can be quite striking and is often correlated with a specific diet. Combtooth blennies have long incisiform oral teeth, unlike most actinopterygians. It has been suggested that the long tooth morphology is an adaptation for detritivory, but given the diversity of diets (detritus, coral polyps, polychaetes, and pieces of other fishes), are blenny teeth indeed monomorphic? Or does tooth variation associated with diet still exist at this extreme? To explore tooth and diet diversification, we used a new phylogenetic hypothesis of Blenniidae, measured tooth shape, number, and mode of attachment, and quantified blenniid diet. The ancestral diet of blennies contained detritus and diversified into many different diets, including almost exclusively detritivory. Our results reveal a dental cline that may be constrained by tooth shape, but has not prevented diet diversification. Ancestral state reconstruction of tooth morphologies suggests that the ancestor of blennies had many unattached teeth and featured transitions to fewer attached teeth, with several transitions back to attached or unattached teeth. The dentition of blenniids is not monotypic; rather it is diverse and small changes in tooth shape are accompanied by changes in size, number, attachment, and often diet.     

Patterning the size and number of tooth and its cusps

Mice and rats, two species of rodents, show some dental similarities such as tooth number and cusp number, and differences such as tooth size and cusp size. In this study, the tooth size, tooth number, cusp size and cusp number, which are four major factors of the tooth patterning, were investigated by the heterospecific recombinations of tissues from the molar tooth germs of mice and rats. Our results suggest that the dental epithelium and mesenchyme determine the cusp size and tooth size respectively and the cusp number is co-regulated by the tooth size and cusp size. It is also suggested that the mesenchymal cell number regulates not the tooth size but the tooth number. The relationships among these factors in tooth patterning including micropatterning (cusp size and cusp number) and macropatterning (tooth size and tooth number) were analyzed in a reaction diffusion mechanism. Key molecules determining the patterning of teeth remains to be elucidated for controlling the tooth size and cusp size of bioengineered tooth.     

Homologies of the toothcomb.

A recently described juvenile specimen of Avahi was supposed to show that indriines have an unreplaced deciduous canine and that the indriine toothcomb was composed only of incisors. To the contrary, this specimen demonstrates quite dramatically a growth phenomenon earlier discussed: in indriines, the anteriormost of the four deciduous lower teeth posterior to the toothcomb migrates mesially toward the toothcomb (Schwartz, '74). In this particular Avahi, this tooth has even become associated with the toothcomb. The alignment of this tooth with the toothcomb is a strictly impermanent situation and cannot be taken into consideration when determining homologies of the teeth of the toothcomb. Morphologically and developmentally the lateral teeth of both indriine and lemur and loris toothcombs are similar to each other and distinct from the central set of teeth. Thus, if the lateral teeth of the lemur/loris toothcomb are canines, then the lateral teeth of the indriine toothcomb are canines as well.