Tooth Ontogeny Research Articles

Plicidentine and the repeated origins of snake venom fangs.

Snake fangs are an iconic exemplar of a complex adaptation, but despite striking developmental and morphological similarities, they probably evolved independently in several lineages of venomous snakes. How snakes could, uniquely among vertebrates, repeatedly evolve their complex venom delivery apparatus is an intriguing question. Here we shed light on the repeated evolution of snake venom fangs using histology, high-resolution computed tomography (microCT) and biomechanical modelling. Our examination of venomous and non-venomous species reveals that most snakes have dentine infoldings at the bases of their teeth, known as plicidentine, and that in venomous species, one of these infoldings was repurposed to form a longitudinal groove for venom delivery. Like plicidentine, venom grooves originate from infoldings of the developing dental epithelium prior to the formation of the tooth hard tissues. Derivation of the venom groove from a large plicidentine fold that develops early in tooth ontogeny reveals how snake venom fangs could originate repeatedly through the co-option of a pre-existing dental feature even without close association to a venom duct. We also show that, contrary to previous assumptions, dentine infoldings do not improve compression or bending resistance of snake teeth during biting; plicidentine may instead have a role in tooth attachment.

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.

Description of Tooth Ontogeny and Replacement Patterns in a Juvenile Tarbosaurus bataar (Dinosauria: Theropoda) Using CT-Scan Data.

Teeth are continually replaced in most of non-mammalian gnathostomes to maintain their functional dentitions. To clarify the tooth replacement patterns in tyrannosaurid theropod dinosaurs, we examined well-preserved dentitions (both premaxillae, left maxilla, partial right maxilla, and both dentaries) of a juvenile Tarbosaurus bataar (MPC-D 107/7) using X-ray computed tomographic (CT) imaging. Three-dimensional (3D) rendering of the dentitions and staging of replacement teeth allowed quantitative analyses of the tooth ontogeny and replacement patterns in this specimen. These strategies were validated by comparing the results between MPC-D 107/7 and extant crocodilians, which are taxa that have previously been studied using non-CT methods. 3D-rendered dentitions of MPC-D 107/7 showed alternate replacement patterns between odd- and even-numbered alveoli. Such patterns were discontinuous at the premaxilla-maxilla junctions, suggesting the division of replacement patterns between the two dentitions possessing morpho-functionally different features. The replacement process in the odd-numbered alveoli of the left maxilla sequentially proceeded from distal alveoli. Meanwhile, in the both dentaries, there were simple alternate patterns in which functional teeth would be simultaneously shed out in every second alveoli. Such a simple alternation had never been reported in the adult tyrannosaurid dentaries. Under this pattern, the half of functional teeth in a single dentition would be shed at the same time, which may hamper foraging functions. We conclude that the simple alternate patterns found in the dentary dentitions of MPC-D 107/7 represent transient condition in juvenile tyrannosaurids, suggesting ontogenetic changes in tooth replacement patterns in the tyrannosaurid dentary. Anat Rec, 302:1210-1225, 2019. © 2018 Wiley Periodicals, Inc.

Ontogeny reveals function and evolution of the hadrosaurid dinosaur dental battery.

BackgroundHadrosaurid dinosaurs, dominant Late Cretaceous herbivores, possessed complex dental batteries with up to 300 teeth in each jaw ramus. Despite extensive interest in the adaptive significance of the dental battery, surprisingly little is known about how the battery evolved from the ancestral dinosaurian dentition, or how it functioned in the living organism. We undertook the first comprehensive, tissue-level study of dental ontogeny in hadrosaurids using several intact maxillary and dentary batteries and compared them to sections of other archosaurs and mammals. We used these comparisons to pinpoint shifts in the ancestral reptilian pattern of tooth ontogeny that allowed hadrosaurids to form complex dental batteries.ResultsComparisons of hadrosaurid dental ontogeny with that of other amniotes reveals that the ability to halt normal tooth replacement and functionalize the tooth root into the occlusal surface was key to the evolution of dental batteries. The retention of older generations of teeth was driven by acceleration in the timing and rate of dental tissue formation. The hadrosaurid dental battery is a highly modified form of the typical dinosaurian gomphosis with a unique tooth-to-tooth attachment that permitted constant and perfectly timed tooth eruption along the whole battery.ConclusionsWe demonstrate that each battery was a highly dynamic, integrated matrix of living replacement and, remarkably, dead grinding teeth connected by a network of ligaments that permitted fine scale flexibility within the battery. The hadrosaurid dental battery, the most complex in vertebrate evolution, conforms to a surprisingly simple evolutionary model in which ancestral reptilian tissue types were redeployed in a unique manner. The hadrosaurid dental battery thus allows us to follow in great detail the development and extended life history of a particularly complex food processing system, providing novel insights into how tooth development can be altered to produce complex dentitions, the likes of which do not exist in any living vertebrate.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0721-1) contains supplementary material, which is available to authorized users.

Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis

The dental anatomy of elasmobranch fishes (sharks, rays and relatives) creates a functional system that is more dynamic than that of mammalian dentition. Continuous dental replacement (where new teeth are moved rostrally to replace older ones) and indirect fibrous attachment of the dentition to the jaw allow teeth to reorient relative to the jaw over both long- and short-term scales, respectively. In this study, we examine the processing behavior and dental anatomy of the lesser electric ray Narcine brasiliensis (Ölfers, 1831) to illustrate that the freedom of movement of elasmobranch dentition allows a functional flexibility that can be important for complex prey processing behaviors. From static manipulations of dissected jaws and observations of feeding events in live animals, we show that the teeth rotate during jaw protrusion, resulting in a secondary grasping mechanism that likely serves to hold prey while the buccal cavity is flushed free of sediment. The function of teeth is not always readily apparent from morphology; in addition to short-term reorientation, the long-term dental reorientation during replacement allows a given tooth to serve multiple functions during tooth ontogeny. Unlike teeth inside the mouth, the cusps of external teeth (on the portion of the tooth pad that extends past the occlusal plane) lay flat, such that the labial faces act as a functional battering surface, protecting the jaws during prey excavation.

Spatial and temporal variations in the isotopic composition of bison tooth enamel from the Early Holocene Hudson–Meng Bone Bed, Nebraska

The Hudson–Meng bone bed in northwestern Nebraska is an early Holocene deposit of hundreds of bison of differing ages that were killed in a catastrophic event of unknown origin. The M 1, M 2, and M 3 molars of individuals, ranging from ca. 1 to 7 years of age at the time of their death, were examined to determine inter- and intra-tooth isotopic variability, and to link this variability to time in order to better understand the environments that existed prior to the mass death event. The δ 13C value of molar structural carbonate increases by 2–3‰ from the M 1 to M 3 molars, reflecting increasing direct forage signals, and decreasing maternal influences. The δ 18O value of molar structural carbonate in a given individual shows no consistent trend with time from birth, indicating a fairly direct linkage to ‘dietary water’ regardless of tooth ontogeny. Detailed ‘down-tooth’ isotopic measurements indicate a small seasonal signal in the δ 13C value of forage/maternal milk, which appeared to have been largely dominated by C 4 flora. In contrast, there was almost a 10‰ range in the isotopic composition of dietary water, a range that is within present-day summer versus winter precipitation in the region. The δ 18O value of bulk tooth enamel, arranged by approximate time prior to the death event, indicate a consistent increase in the δ 18O value of body water (2–3‰), suggesting a long-term decrease in winter/spring precipitation and/or drought. The δ 18O trend with time, coupled with the high C 4 grass abundance, suggest environmental stresses on the herd preceding the catastrophic death event.

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.

Changes in the distribution of tenascin during tooth development

Tenascin is an extracellular matrix molecule that was earlier shown to be enriched in embryonic mesenchyme surrounding the budding epithelium in various organs including the tooth. In the present study tenascin was localized by immunohistology throughout the course of tooth development in the mouse and rat using polyclonal antibodies against chick tenascin. The results indicate that tenascin is expressed by the lineage of dental mesenchymal cells throughout tooth ontogeny. The intensity of staining with tenascin antibodies in the dental papilla mesenchyme was temporarily reduced at cap stage when the tooth grows rapidly and undergoes extensive morphogenetic changes. During the bell stage of morphogenesis, the staining intensity increased and tenascin was accumulated in the dental pulp even after completion of crown development and eruption. Tenascin was present in the dental basement membrane at the time of odontoblast differentiation. The dental papilla cells ceased to express tenascin upon differentiation into odontoblasts and tenascin was completely absent from dentin. It can be speculated that the remarkable expression of tenascin in the dental mesenchymal cells as compared to other connective tissues is associated with their capacity to differentiate into hard-tissue-forming cells.

Biochemical study of changes in non-specific alkaline phosphomonoesterase activity during mouse tooth ontogeny

The reaction velocity of an alkaline phosphatase substrate (paranitrophenylphosphate) was measured during tooth ontogeny to help clarify the biological function of alkaline phosphatase (APase, EC 1.3.1.3). Mouse molars from the early bell stage to adult mature stages were used. Epithelial and mesenchymal components of tooth germs were analyzed separately, and crowns only from fully developed teeth. After homogenizing in Triton X-100 detergent, the rate of hydrolysis of paranitrophenylphosphate was then determined. Low enzyme activities and statistically non-significant differences were seen in the epithelial and mesenchymal parts of tooth germs. One day after birth, a significant increase was seen in both parts, but activity was 4 times higher in the mesenchymal part, continuing up to the 7th day. At day 11, a decrease occurred in both parts. Adult levels were reached by day 18. The protein content of the epithelial part began to rise before the increase in APase activity occurred. It is probable that the reactions catalyzed by APase are activated in the germs between the 18th prenatal and first postnatal days. The onset of the rise in enzyme activity in the 2 components corresponds with the onset of the secretory phases.

Tooth onoteny in Didelphis virginiana (Marsupialia : Didelphidae)

The ontogenetic development of the teeth was studied in a series of seven specimens of Didelphis virginiana whose crown-rump length varied from 11 to 49 mm. Though all developing teeth showed undifferentiated lingual downgrowths of dental lamina, there was no evidence of any non-functional teeth. No more than five upper incisors were present at any one time. The metacone was the first cusp to calcify in the upper deciduous and fist permanent molar teeth. The protoconid was the first cusp to calcify in the lower molar teeth. The results were compared with findings from a recent study of tooth ontogeny in Antechinus flavipes.

A histochemical study of various dehydrogenases in human tooth ontogeny

Summary Lactate dehydrogenase (LDH), succinate dehydrogenase (SDH), glutamate dehydrogenase (GDH) and NADH 2 dehydrogenase were studied using histochemical staining methods in human tooth and supporting tissue ontogeny as representative of the different energy source pathways in these developing and differentiating structures. Except for enamel and dentine, all structures of the tooth germ revealed LDH, SDH, GDH and NADH 2 dehydrogenase activities in different patterns. LDH and GDH activities decreased during the development in the epithelium of the oral cavity and in the subjacent mesoderm up to the stage of apposition. At the stage of apposition, ameloblasts and odontoblasts revealed intense LDH, as well as NADH 2 diaphorase activity and weak SDH activity. At this stage only the outer and inner enamel epithelium revealed weak GDH activity. The results are thought to indicate that, though the anaerobic glycolysis as an energy source seems to dominate the mineralizing cells, when the actual formation of enamel and dentine starts, the energy of the citric acid cycle is also needed for the highly active metabolism.

A histochemical study of hydrolytic enzymes in human tooth ontogeny.

Arylaminopeptidase and glycosidase activities were studied by histochemical staining methods in human tooth and supporting tissue ontogeny in order to demonstrate the possible metabolic differences in the differentiated and undifferentiated cells of the formation, modelling and re‐modelling metabolism of the tissue involved. The enzyme activities were studied using various N‐L‐ aminoacyl‐2‐naphthylamines and 1‐ and 2‐naphthol glycosides and ‐esters as substrates. The arylaminopeptidase activity (EC 3.4.11) was observed (1) in the basal cell layer of oral epithelium in the stomodeum, (2) in the subjacent mesoderm, (3) in the outer and (4) inner enamel epithelium, (5) in the dental papilla, (6) in the dental lamina, and (7) in the primordium of permanent tooth. No arylaminopeptidase activity could be observed in ameloblasts. odontoblasts. enamel, dentin, stellate reticulum and pulp, and the inner enamel epithelium also lost its activity during the stage of apposition. The following glycosidases were observed in the same structures as the arylaminopeptidases: β‐N‐acetylglucosaminidase (EC 3.2.1.30), β‐glucosidase (EC 3.2.1.21), β‐galactosidase (EC3.2.1.23). β‐glucuronidase (EC 3.2.1.31), as well as arylsulphatase (EC 3.1.6.1) The whole thickness of oral epithelium revealed β‐galactosidase and arylsulphatase activity, not only the basal cell layer. These observations were‐ thought to give support to the suggestions that differeniation is a stage of highly active metabolism and thus at the stage of apposition the cells of the outer enamel epithelium are actively differentiating.

Processes of mammalian tooth development as illustrated by dental ontogeny in the mole Scapanus latimanus (Talpidae: Insectivora)

Tooth ontogeny in the dentally primitive placental Scapanus latimanus was investigated by means of serial sections and wax-plate reconstructions. The anterior two milk incisors, the posterior milk premolar, and first molar generally remain the most advanced teeth throughout ontogeny. At any stage, there is a developmental decline from either end of the milk—and often the adult—tooth row towards the middle of the series, centred on the first premolar site. The unreplaced first premolar and molars fit more smoothly into the developmental gradient curves of the milk, rather than the adult, antemolars and thus appear serially homologous with the milk dentition. Although a functionless residual dental lamina forms briefly at each adult tooth primordium, no other structures that could be interpreted as either “post-permanent” or “pre-lacteal” dentitions are evident. Certain milk primordia may extend their development antero-laterally from the dental lamina into the oral epithelium, subsequently becoming suspended by means of a “lateral string”. The antero-lateral growth area is fully functional only in the incisor region, where it alleviates crowding between both adjacent milk primordia and corresponding milk and adult primordia. The developmental gradients along the embryonic tooth row suggest that in most dentally unspecialized mammals, at least, evolutionary tooth loss occurs posteroanteriorly for incisors and antero-posteriorly for premolars. Posterior molars may easily be evolutionarily added or subtracted, as selective pressures dictate, by variations in length of the embryonic tooth-forming period.

Tissue interactions in embryonic mouse tooth germs: I. Reorganization of the dental epithelium during tooth-germ reconstruction

ABSTRACT The ability of fragments of incisor enamel organ and lip-furrow epithelium from 15-and 16-day old embryonic mice to regulate into harmonious tooth constructions is described. The cervical loop and upper half portions of the incisor enamel organ were confronted with incisor or molar dental papillae. Similar combinations were made from lip-furrow epithelium and incisor or molar papillae. The cultures were grown in the anterior chambers of homologous host eyes. The epithelial fragments from the incisor enamel organ when associated with the dental papillae reconstruct teeth typical in all respects; enamel and dentin matrices are deposited. Lip-furrow epithelium arises from the oral epithelium and is temporally and spatially related to the incisor dental epithelium proper. This ectopic epithelium was confronted by incisor and molar papillae. Harmonious teeth developed in these explants. It is concluded that the ability of the dental papillae to elicit new cytodifferentiative and biochemical syntheses from the lip-furrow epithelium indicates that the dental papillae act inductively during tooth ontogeny. The shape of the teeth reconstructed from enamel organ fragments and lip-furrow epithelium were incisiform or molariform in response to the incisor or molar dental papillae. These data confirm the conclusion that the structural specificity for tooth shape resides in the dental papilla.

A histochemical demonstration of ATPase activity during tooth ontogeny in the mouse

By the reversible inhibition test of Padykula and Herman at pH 9.4, using p-chloro-mercuri-benzoic acid (PCMB) and 2 ·. 3-dimercapto-1-propanol (BAL) as an -SH inhibitor and an -SH activator respectively, it was possible to study the correlation between the onset of matrix formation in dentine and enamel and the appearance of ATPase activity (EC 3.6. 1.3) in the tooth germs of the lower first molar in the mouse. The findings were consistent throughout the study in specimens derived from foetuses at insemination day 19 and newborn animals at insemination day 21. The enzymic origin of the stained precipitate was shown by the lack of staining of control sections incubated without substrate. The importance of the enzyme function as energy and/or phosphate contributor to the mineralizing tissues was discussed.

Some stages in the early development of the post‐incisor dentition of Trichosurus vulpecula (Phalangeroidea: Marsupialia)

The present paper reports observations from serial sections of five pouch‐young specimens on the early stages of tooth ontogeny in the post‐incisor dentition of Trichosurus vulpecula. The order of cusp development and calcification for the molariform teeth is recorded and closely resembles that of placentals. Some features concerning the development of the replacing premolar are noted and compared with the conditions observed in Setonix brachyurus, another marsupial. A number of non‐functional cheek teeth are reported.

An account of the enamel cord in setonix brachyurus (marsupialia) and on the presence of an enamel knot in trichosurus vulpecula

The disposition of the enamel cord was studied in a dated series of pouchyoung of Setonix sectioned transversely and stained with Masson's trichrome. In the upper jaw the enamel cord was associated with the incisal edges of the three functional incisors, the crest of the ridge of the first functional premolar and the paracone of the deciduous premolar. In the lower jaw the enamel cord was associated with the crest of the ridge of the first functional premolar, the protoconid of the deciduous premolar, the protoconid, metaconid and crest of the protolophid of the first molar as the cord passed transversely across the surface of the crown, and the metaconid of the second molar. Two exceptions to the normal disposition of the enamel cord, which generally runs antero-posteriorly in relation to the primary ridge, were observed in the lower jaw. In the first molar the enamel cord passed transversely across the crown in relation to the protolophid, and in the second molar the cord was associated with the anterolingual metaconid. The antero-posterior dimension of the enamel cord in certain enamel organs, especially the upper second incisor, was such that the structure should more correctly be called an enamel septum. It would seem that the enamel septum has been derived from the enamel cord. The alternative explanation is that the enamel cord and the enamel septum are entirely different structures. In the upper second incisor an enamel septum was present 22 days after the appearance of the enamel cord. The significance of the enamel cord is discussed. An enamel cord was not encountered in every tooth germ in Setonix and indicates either that the cord is sometimes so transitory as to pass unobserved or that the cord is not essential during tooth ontogeny. An enamel knot was observed in the upper second molar of Trichosurus.