The mosasaur tooth attachment apparatus as paradigm for the evolution of the gnathostome periodontium

SUMMARY Vertebrate teeth are attached to jaws by a variety of mechanisms, including acrodont, pleurodont, and thecodont modes of attachment. Recent studies have suggested that various modes of attachment exist within each subcategory. Especially squamates feature a broad diversity of modes of attachment. Here we have investigated tooth attachment tissues in the late cretaceous mosasaur Clidastes and compared mosasaur tooth attachment with modes of attachment found in other extant reptiles. Using histologic analysis of ultrathin ground sections, four distinct mineralized tissues that anchor mosasaur teeth to the jaw were identified: (i) an acellular cementum layer at the interface between root and cellular cementum, (ii) a massive cone consisting of trabecular cellular cementum, (iii) the mineralized periodontal ligament containing mineralized Sharpey's fibers, and (iv) the interdental ridges connecting adjacent teeth. The complex, multilayered attachment apparatus in mosasaurs was compared with attachment tissues in extant reptiles, including Iguana and Caiman . Based on our comparative analysis we postulate the presence of a quadruple-layer tissue architecture underlying reptilian tooth attachment, comprised of acellular cementum, cellular cementum, mineralized periodontal ligament, and interdental ridge (alveolar bone). We propose that the mineralization status of the periodontal ligament is a dynamic feature in vertebrate evolution subject to functional adaptation.     

Dental histology of Coelophysis bauri and the evolution of tooth attachment tissues in early dinosaurs

Studies of dinosaur teeth have focused primarily on external crown morphology and thus, use shed or in situ tooth crowns, and are limited to the enamel and dentine dental tissues. As a result, the full suites of periodontal tissues that attach teeth to the jaws remain poorly documented, particularly in early dinosaurs. These tissues are an integral part of the tooth and thus essential to a more complete understanding of dental anatomy, development, and evolution in dinosaurs. To identify the tooth attachment tissues in early dinosaurs, histological thin sections were prepared from the maxilla and dentary of a partial skull of the early theropod Coelophysis bauri from the Upper Triassic (Rhaetian‐ 209–201 Ma) Whitaker Quarry, New Mexico, USA. As one of the phylogenetically and geologically oldest dinosaurs, it is an ideal candidate for examining dental tissues near the base of the dinosaurian clade. The teeth of C. bauri exhibited a fibrous tooth attachment in which the teeth possessed five tissues: enamel, dentine, cementum, periodontal ligament (PDL), and alveolar bone. Our findings, coupled with those of more recent studies of ornithischian teeth, indicate that a tripartite periodontium, similar to that of crocodilians and mammals, is the plesiomorphic condition for dinosaurs. The occurrence of a tripartite periodontium in dinosaurs adds to the growing consensus that the presence of these tissues is the plesiomorphic condition for the major amniote clades. Furthermore, this study establishes the relative timing of tissue development and growth directions of periodontal tissues and provides the first comparative framework for future studies of dinosaur periodontal development, tooth replacement, and histology. J. Morphol. 277:916–924, 2016. © 2016 Wiley Periodicals, Inc.     

Histology of tooth attachment tissues and plicidentine in Varanus (Reptilia: Squamata), and a discussion of the evolution of amniote tooth attachment

Few recent studies have examined the histological basis for tooth attachment in squamates. In the past few years, a surge of interest in this topic has led to the intriguing suggestion that the major tissues derived from the tooth germ (enamel, dentine, cementum and alveolar bone), are conservative and are present in all amniotes. In this study, we describe the histology and development of the tooth attachment complex in Varanus rudicollis, the rough‐neck monitor. We provide the first published evidence for the role of cementum and alveolar bone in tooth attachment in varanoid lizards. In Varanus, cementum is deposited on the external surface of the tooth root as well as at the base of the tooth, where it plays a role in the attachment of the tooth to the jawbone. Alveolar bone is also involved in tooth ankylosis. Our results support the hypothesis that the major tooth germ tissues are found in all amniotes. We provide insights into the structure and development of plicidentine, defined as infolding of the dentine around the tooth base. This feature is unique to varanoids among extant tetrapods and is the third tissue implicated in tooth attachment in Varanus. Plicidentine develops asymmetrically along the labial‐lingual axis of a tooth. Varanus is characterized by the presence of both primary and higher‐order lamellae, which anastomose to form a honeycomb‐like surface that then interacts with the more basal attachment tissues. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Morphology of the tooth of the American alligator (Alligator mississippiensis): The fine structure and elemental analysis of the cementum

The fine structure and the concentration of trace elements in the cementum layer in functional teeth of subadult alligators (ca. 120 cm to 160 cm total length) was studied by using scanning electron microscopy (SEM), microradiography, and electron microprobe analysis (EMPA). The cementum layer was hypertrophic and consisted of two layers: the fibrous layer and the calcified layer. The two layers undergo developmental changes as a result of resorption and replacement. During the tooth replacement in the American alligator, trace elements decreased at the base of the dentine layer; the resorption of the alveolar bone occurred simultaneously at the tooth socket. We concluded that the resorption of the cementum in the alligator provided a useful indication of the mechanism of tooth replacement in crocodilian.     

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.     

The cytology of the dental follicle and adjacent alveolar bone during tooth eruption in the dog

Previous studies from our laboratories have shown that premolar eruption in dogs depends upon the presence of the dental follicle and is independent of root or crown growth or attachment to the oral epithelium. The present study is an analysis of the cellular composition of the dental follicle and the cellular investment of the adjacent walls of the bony crypt before and during eruption of the third and fourth mandibular permanent premolars in young beagle dogs. Four premolar follicles and their adjacent bony crypts were examined at 2-week intervals over 12 weeks before and during eruption of these teeth. Tissues were removed, fixed, processed, and oriented so that each follicle and the adjacent crypt wall could be reproducibly examined in vertical and horizontal planes. Mononuclear cells with abundant cytoplasm, euchromatic nuclei, and prominent nucleoli were present in juxtavascular location in the coronal part of the dental follicle; and these cells increased in number immediately preceding and during tooth eruption in parallel with an increase in osteoclasts on the adjacent crypt wall. These data are interpreted to mean that the coronal part of the dental follicle may coordinate the alveolar bone resorption required for tooth eruption by attracting and directing to the crypt wall a population of mononuclear cells, which either become osteoclasts and/or direct osteoclastic activity during tooth eruption.     

Enlarged occlusal surfaces on first molars due to severe attrition and hypercementosis: examples from prehistoric coastal populations of Texas

During an examination of prehistoric samples from the Texas coast, individuals consistently exhibited a suite of traits on the first molars that included severe wear, hypercementosis, and resorption of the buccal margin of the alveolus. The occlusal surface of the tooth was worn below the cervical margin, with the subsequent incorporation of the buccal surface of the buccal roots into the occlusal plane. This expanded occlusal surface, which extends the buccal surface beyond the normal edge of the tooth, is composed of a combination of original enamel, secondary dentin, and cementum. There is a marked rounding of the buccal aspect of the occlusal surface. These conditions were noted in both maxillary and mandibular first molars. The resorption of alveolar bone surrounding the buccal roots resembles resorption associated with periodontal infection and is thought to be the result of severe levels of stress being applied to this portion of the dentition.     

Ultrastructure of alveolar bone during tooth eruption in the dog

Previous work from our laboratories has established that eruption of the permanent mandibular premolars in dogs is dependent upon the presence of the dental follicle and that it involves resorption of alveolar bone and the roots of the deciduous predecessor above and formation of alveolar bone below the developing crown. This study illustrates the topography of the bone surfaces of the crypt by scanning electron microscopy and the ultrastructure of the cells on alveolar bone surfaces during tooth eruption. Above the developing crown where the eruption pathway forms, the bone surface is a pitted sheet, the characteristic topographic feature of bone resorption; between the crown and the mandibular canal, the bone surface has numerous interconnecting trabeculae. Transmission electron microscopy of bone cells lining the eruption pathway area of the crypt showed numerous osteoclasts with adjacent mononuclear cells. Both cell types contained specific, membrane-bound cytoplasmic vesicles shown by the work of others to be characteristic features of osteoclasts and their precursors. Basal trabeculated bone in the crypt was covered by plump osteoblasts. These data show that the metabolic events in alveolar bone associated with tooth eruption have the appropriate cellular and bony surface correlates and that the suspected control of alveolar bone resorption by the dental follicle may be mediated by its recruiting and directing to adjacent bone surfaces the mononuclear precursors of osteoclasts.     

The cytology of submandibular glands of the opossum

Tooth attachment in the majority of the bony fish is by ankylosis or fibrous membrane. However, in one group of the osteichthys, the trigger-fish or balistids, tooth attachment is by means of a periodontium composed of a shallow alveolar socket, a periodontal ligament and acellular cementum. Histologically, the balistid periodontal ligament is composed of a dense fibro-cellular connective tissue possessing an abundance of typical fibrocytes, collagen fiber bundles, and oxytalan fibers. The collagen fiber bundles which resemble the principal fiber bundles of the mammalian periodontal ligament are inserted into the bone of the shallow alveolar sockets and are anchored to the teeth by means of a layer of amorphous acellular cementum that covers the radicular dentin. No cementoblasts were found in functional teeth, and epithelial rests are lacking. The mid-central zone of the balistid periodontal ligament is occupied by small blood vessels.     

The tooth of perfection: functional and spatial constraints on mammalian tooth shape

This paper addresses the question of how close mammalian teeth are to ideal functional forms. An 'ideal' form is a morphology predicted to be the best functional shape according to information of the relationships between shape and function. Deviations from an ideal form are likely to indicate the presence of developmental or genetic constraints on form. Model tools were constructed to conform to functional principles from engineering and dental studies. The final model shapes are very similar to several mammalian tooth forms (carnassial teeth and tribosphenic-like cusps), suggesting that these tooth forms very closely approach ideal functional forms. Further evidence that these tooth forms are close to ideal comes from the conservation over 140 million years, the independent derivation and/or the occurrence over a size range of several orders of magnitude of these basic tooth forms. One of the main functional shapes derived here is the 'protoconoid', a fundamental design for double-bladed tools that fits a large number of functional parameters. This shape occurs in tooth forms such as tribosphenic, dilambdodont and zalambdodont. This study extends our understanding of constraints on tooth shape in terms of geometry (how space influences tooth shape) and function (how teeth divide food).  © 2003 The Linnean Society of London . Biological Journal of the Linnean Society , 2003, 78 , 173–191.     

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.     

Sexual dimorphism in modern human permanent teeth

On average, males possess larger tooth crowns than females in contemporary human populations, although the degree of dimorphism varies within different populations. In previous studies, different amounts of either enamel or dentine were implicated as the cause of this dimorphism. In this study, we attempt to determine the nature of sexual dimorphism in the crowns of permanent modern human teeth and to determine if two contrasting tooth types (permanent third molars and canines) show identical patterns of dimorphism in enamel and dentine distribution. We estimated the relative contributions of both enamel and dentine to total crown size, from buccolingual sections of teeth. Our sample consisted of a total of 144 mandibular permanent third molars and 25 permanent mandibular canines of known sex. We show that sexual dimorphism is likely due, in part, to the presence of relatively more dentine in the crowns of male teeth. However, whatever the underlying cause, dimorphism in both tooth root and tooth crown size should produce measurable dimorphism in tooth weight, though this has not been previously explored. Therefore, we provide some preliminary data that indicate the usefulness of wet tooth weight as a measure of sexual dimorphism. Both male permanent third molars and canines are significantly heavier than those of females. The weight dimorphism reported here for both classes of teeth may prove a useful finding for future forensic studies. In particular, weights of canines may be more useful as a means of sexing modern human skeletal material than linear or area measurements of teeth.     

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.     

Interdental distraction osteogenesis and rapid orthodontic tooth movement: a novel approach to approximate a wide alveolar cleft or bony defect

The closure of a wide alveolar cleft and fistula in cleft patients and the reconstruction of a maxillary dentoalveolar defect in traumatic patients are challenging for both orthodontists and surgeons. This is due to the difficulty in achieving complete closure by using local attached gingiva and the great volume of bone required for the graft. In this article, the authors propose using interdental distraction osteogenesis to create a segment of new alveolar bone and attached gingiva for the complete approximation of a wide alveolar cleft/fistula and the reconstruction of a maxillary dentoalveolar defect. They performed this procedure on one patient with a traumatic maxillary dentoalveolar defect and 10 patients with unilateral or bilateral cleft lips and palates who had varied dentoalveolar clefts/fistulas. Interdental and maxillary osteotomies were performed on one side of the dental arch by the cleft or defect. After a latency period of 3 days, the osteotomized distal segment of the dental arch was then distracted and transported toward the cleft or defect by using a toothborne intraoral distraction device. The alveoli and gingivae on both ends of the cleft or defect were approximated after distraction osteogenesis. The need for extensive alveolar bone grafting was eliminated. A segment of new edentulous alveolus and attached gingiva was created interdentally at a site distant to the cleft or defect. In the cleft patients, teeth were moved orthodontically into the regenerate (newly formed alveolar bone) dental crowding 1 week after distraction. The orthodontic tooth movement was rapidly completed in 3 months, and the edentulous space was eliminated. Interdental distraction osteogenesis minimizes an alveolar cleft/fistula and helps reconstruct a maxillary dentoalveolar defect by approximating the native alveoli and gingivae; it also creates new alveolar bone and gingiva for rapid orthodontic tooth movement.     

Ontogeny of postcanine tooth form in the ferret,Mustela putorius (Carnivora: Mammalia), and the evolution of dental diversity within the mustelidae

This study describes dental development within the ferret, Mustela putorius, through study of the form of the carnassial teeth and the upper first molar at progressive growth stages. Primordial teeth were serially sectioned in sagittal and transverse planes and three-dimensional reconstructions of tooth primordia were generated using MacReco software. Regional growth of the crown and asynchronous maturation of the dental tissues were observed in each tooth. The upper carnassial blade develops early and the tooth increases in length rapidly. Lingual growth of the upper carnassial is less pronounced and the protocone and its surrounding region mature late. The lower carnassial blade develops early and the talonid is late to mature. Development of the upper first molar differs from carnassial development in the early emphasis upon transverse growth and reduced lengthwise expansion. The early development of the carnassial blades in the ferret is shared with other carnivores, and may reflect the functional significance of this feature. Later stages of tooth ontogeny differ among carnivoran taxa and the specialized morphology of ferret teeth results from an apparently truncated period of late tooth ontogeny. This suggests that carnivoran species may share a common path of early development that specifies the ontogeny of homologous tooth features and that in later stages developmental differences result in species-specific tooth forms. J. Morphol. 237:69–90, 1998. © 1998 Wiley-Liss, Inc.     

Attachment tissues of the teeth in Caiman sclerops (Crocodilia)

As the Crocodilia are the only non-mammalian vertebrates with tooth sockets, the attachment tissues of the teeth were studied in Caiman sclerops mainly at the ultrastructural level and were compared with those of mammals. All three attachment tissues (alveolar bone, cementum and periodontal ligament) in the Caiman showed both similarities and differences with their mammalian counterparts. Highly organized, lamellated structures, probably representing specialized sensory nerve endings were observed within the Caiman ligament. No such structure has ever been described in the mammalian ligament.     

Morphology and development of teeth and epidermal brushes in loricariid catfishes

Loricariidae or suckermouth armored catfishes are one of several aquatic taxa feeding on epilithic and epiphytic algae. Their upper and lower jaws bear exquisitely curved teeth, which usually are asymmetrically bicuspid. The enlarged lower lip carries papillae with keratinous unicellular epidermal brushes or unculi. Teeth, and probably unculi too, assist in scraping food off substrates. Their morphology, growth, and replacement is examined and compared among several loricariid species, using cleared and stained specimens, serial sections, and SEM. Apart from the general tooth form and crown shape, the anterior layer of soft tissue on the lower shaft region, present in several species, appears to be a specialization for enhancing the mobility of individual teeth when scraping on uneven surfaces. During early ontogeny, a transition from simple conical to mature tooth occurs. The first unculi appear together with the first teeth carrying a bicuspid crown, 2 days after the first exogenous feeding, but synchronous with the complete resorption of the yolk sac.     

Do all geckos hatch in the same way? Histological and 3D studies of egg tooth morphogenesis in the geckos Eublepharis macularius Blyth 1854 and Lepidodactylus lugubris Duméril & Bibron 1836

The egg tooth of squamates evolved to facilitate hatching from mineralized eggshells. Squamate reptiles can assist their hatching with a single unpaired egg tooth (unidentates) or double egg teeth (geckos and dibamids). Egg tooth ontogeny in two gekkotan species, the leopard gecko Eublepharis macularius and the mourning gecko Lepidodactylus lugubris, was compared using microtomography, scanning electron microscopy, and light microscopy. Investigated species are characterized by different hardnesses of their eggshells. Leopard geckos eggs have a relatively soft and flexible parchment (leathery) shell, while eggshells of mourning geckos are hard and rigid. Embryos of both species, like other Gekkota, have double egg teeth, but the morphology of these structures differs between the investigated species. These differences in shape, localization, and spatial orientation were present from the earliest stages of embryonic development. In mourning gecko, anlagen of differentiating egg teeth change their position on the palate during embryonic development. Initially they are separated by condensed mesenchyme, but later in development, their enamel organs are connected. In leopard geckos, the localization of egg tooth germs does not change, but their spatial orientation does. Egg teeth of this species shift from inward to outward orientation. This is likely related to differences in structure and mechanical properties of eggshells in the studied species. In investigated species, two hatching mechanisms are possible during emergence of young individuals. We speculate that mourning geckos break the eggshell through puncturing action with egg teeth, similar to the pipping phase of chick and turtles embryos. Egg teeth of leopard geckos cut egg membranes similarly to most squamates. Our results also revealed differences in egg tooth implantation between Gekkota and Unidentata: gekkotan egg teeth are subthecodont (in shallow sockets), while those in unidentates are acrodont (attached to the top of the alveolar ridge). © 2020 Wiley Periodicals LLC     

Tooth morphology in function of selfprotective mechanism

The degree of curvature of vestibular and oral tooth surfaces is determined by the shape sequence from the tooth crown to the epithelial attachment and the alveolar bone, and directly influences the health of gingiva and the entire tooth support system. The goal of this research was to determine vestibulo-oral planes of upper and lower permanent premolars and molars and the thickness of the associated alveolar osseous wall, and 2,727 measurings were processed using pertinent statistical procedures. The results have shown the degree of curvature of vestibular and oral tooth surfaces to be higher in upper teeth than in lower ones (p > 0.05); vestibular convexities higher than oral ones and especially noticeable at the junction from the meandle to the lower third of the crown. Higher vestibular curvature also entailed thicker osseous wall. All results were higher than the ones found in literature. We consider our results to be relevant for our population. The research on the relationship of teeth and the alveolar bone should be continued by using even more test points and more sophisticated research procedures.     

AGING LIVE ANTARCTIC FUR SEALS AND SOUTHERN ELEPHANT SEALS

This study describes a method for extracting post-canine or incisor teeth from live antarctic fur seals ( Arctocephalus gazella ) and southern elephant seals ( Mirounga leonina ) respectively and their use to determine age in a field situation. Dental elevators were used to loosen the teeth from the alveolus and periodental ligament. Most teeth were removed within l-2 min and a total of 214 and 81 teeth were collected by this method from antarctic fur seals and southern elephant seals respectively. No seal recaptured at intervals up to a year after a tooth was extracted showed signs of infection or distress related to removal of the tooth. Teeth were thin-sectioned for the purpose of aging. In both species cementum growth layer groups were a more satisfactory indicator of age than dentinal growth layer groups. Estimates of age from cementum growth layers were confirmed for Antarctic fur seals using seals which had been tagged as pups up to 16 yr before sampling.