Tooth and consequences: Heterodonty and dental replacement in piranhas and pacus (Serrasalmidae)

Tooth replacement in piranhas is unusual: all teeth on one side of the head are lost as a unit, then replaced simultaneously. We used histology and microCT to examine tooth‐replacement modes across carnivorous piranhas and their herbivorous pacu cousins (Serrasalmidae) and then mapped replacement patterns onto a molecular phylogeny. Pacu teeth develop and are replaced in a manner like piranhas. For serrasalmids, unilateral tooth replacement is not an “all or nothing” phenomenon; we demonstrate that both sides of the jaws have developing tooth rows within them, albeit with one side more mineralized than the other. All serrasalmids (except one) share unilateral tooth replacement, so this is not an adaptation for carnivory. All serrasalmids have interlocking teeth; piranhas interdigitate lateral tooth cusps with adjacent teeth, forming a singular saw‐like blade, whereas lateral cusps in pacus clasp together. For serrasalmids to have an interlocking dentition, their teeth need to develop and erupt at the same time. We propose that interlocking mechanisms prevent tooth loss and ensure continued functionality of the feeding apparatus. Serrasalmid dentitions are ubiquitously heterodont, having incisiform and molariform dentitions reminiscent of mammals. Finally, we propose that simultaneous tooth replacement be considered as a synapomorphy for the family.     

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.     

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.     

Developmental mechanisms underlying tooth patterning in continuously replacing osteichthyan dentitions

The dentition of osteichthyans presents an astonishing diversity with regard to the distribution of teeth in the oral cavity, tooth numbers, arrangements, shapes, and sizes. Taking examples from three unrelated teleosts--the most speciose group of osteichthyans--and from the literature, this study explores how the initial tooth pattern is set up, and how this relates to the establishment and maintenance (or modification) of the tooth replacement pattern. In teleosts, first-generation teeth (the very first teeth in ontogeny to develop at a particular locus) are commonly initiated in adjacent or in alternate (odd and even) positions. The mechanisms responsible for these divergent developmental patterns remain to be elucidated, in particular, whether they reflect a field or local type of control. However, patterns of adjacent or alternate tooth initiation, set up by the first-generation teeth, can easily turn into replacement patterns where new teeth are initiated simultaneously every second, or even every third position, by synchronizing the formation of new first-generation teeth to the formation of replacement teeth at older loci. Our observations suggest that, once established, the replacement pattern appears to be maintained, as a kind of "default" state. Variations and modifications in this pattern are nevertheless common and suggest that tooth replacement is under local control, exerted at the level of the initiation of replacement teeth. Further studies are needed to test the hypothesis that regular replacement patterns are more frequent in association with the plesiomorphic condition of extramedullary replacement (replacement on the surface of the dentigerous bone) and more rare in the derived condition of intramedullary replacement (replacement within the medullary cavity of the dentigerous bone).     

The appearance pattern of tooth germs in the round crucian carp,Carassius auratus grandoculis

Cyprinid fishes generally replace their teeth alternately and cephalad. The larvae ofCarassius auratus grandoculis also replace their teeth alternately and cephalad, in a pattern of 4-2-3-1-. However, adults ofCarassius species replace their teeth from anterior to posterior, in a pattern of 1-2-3-4-1-. So I analyzed the appearance pattern of tooth germs in larvae and juveniles inCarassius auratus grandoculis. At stage 5 of the post-larval period, developmental difference is made between both sides. In the pharyngeal dentition on one side developing poorly, the anterior tooth on the fifth replacement wave, tooth₄[An2] appeared later than the central teeth on following replacement wave, tooth₅[Pol]. Moreover, the anterior tooth on the seventh replacement wave, tooth₆[An2], appeared later than the central teeth on the following replacement wave, tooth₇[Pol], on both sides. The reverse of tooth germ appearance between anterior teeth and central teeth makes a change of replacement pattern from 4-2-3-1-4- to 1-2-3-4-1-. The change of replacement pattern is caused by the confusion of tooth germs of anterior teeth on both sides.Mylopharyngodon piceus andCyprinus carpio make a change of replacement patterns in the early juvenile period, too. This change of replacement pattern may be a specialized character among the subfamily Cyprininae.     

扁圆吻鲴下咽齿的个体发生及替换规律

扁圆吻鲴下咽齿的个体发生可分为三个阶段：初齿期、过渡齿期和成齿期。初步期符合鲤科鱼类的一般规律;过渡齿期相当延长,产生全部齿位,６或７枚齿,齿的发生存在两种类型;成齿与幼齿的替换规律完全不同,发育进入成齿阶段后,主行齿由奇数齿位与偶数齿位交错替换转变为相二枚齿进行替换,替换公式为１－４,２－５,３－６或１－４－７,２－５,３－６（主行齿６枚或７枚）,全部替换一次分三列替换波完成,可将扁圆吻鲴下咽齿的发育模式视为新的类型,副行齿在过渡齿期出现,与主行齿的发展模式不同,替换形式始终为相令齿位交错进行,本文还探讨了咽骨的发育及其对下咽发生的影响。     

Molecular genetics of supernumerary tooth formation

Despite advances in the knowledge of tooth morphogenesis and differentiation, relatively little is known about the aetiology and molecular mechanisms underlying supernumerary tooth formation. A small number of supernumerary teeth may be a common developmental dental anomaly, while multiple supernumerary teeth usually have a genetic component and they are sometimes thought to represent a partial third dentition in humans. Mice, which are commonly used for studying tooth development, only exhibit one dentition, with very few mouse models exhibiting supernumerary teeth similar to those in humans. Inactivation of Apc or forced activation of Wnt/β(catenin signalling results in multiple supernumerary tooth formation in both humans and in mice, but the key genes in these pathways are not very clear. Analysis of other model systems with continuous tooth replacement or secondary tooth formation, such as fish, snake, lizard, and ferret, is providing insights into the molecular and cellular mechanisms underlying succesional tooth development, and will assist in the studies on supernumerary tooth formation in humans. This information, together with the advances in stem cell biology and tissue engineering, will pave ways for the tooth regeneration and tooth bioengineering.     

Tooth replacement pattern of Coloborhynchus robustus (Pterosauria) from the Lower Cretaceous of Brazil

The well preserved anterior upper and lower jaw fragment of an adult specimen of Coloborhynchus robustus (Pterosauria: Ornithocheiridae), SMNK 2302 PAL, allowed investigations of the replacement pattern of the dentition macroscopically and by using CT scans. The quantification of the dentition by Zahnreihen, Z-Spacing, and replacement waves indicates a complex pattern of different replacement stages in which large gaps within the dentition were avoided. The specialized prey-catching apparatus of Coloborhynchus thus could retain its function even following tooth replacement. The replacement process in the specimen took about 2/3 of the total life-time of a tooth, and damaged teeth in the anterior jaw region may have been replaced more rapidly than posterior teeth. The distolingual replacement of the functional teeth delayed the time of their shedding in comparison with the circular resorption present in crocodiles. In contrast to these, the distolingual position of the replacement tooth did not decrease the biomechanical stability of the functional tooth, which can also be observed as a convergence in other thecodont dentitions, e.g., recent carnivore mammals. Teeth were shed when their replacement had reached about 60% of the full-grown height. A comparison of the observed pattern is constricted by the preservation and preparation of other specimens. Unfortunately, no known specimen in public collections reaches the quality of Coloborhynchus robustus, SMNK 2302 PAL, so that comparable patterns in other specimens are not likely to be detected.     

Observations on the dental anatomy of piranhas (Characidae) with special reference to tooth structure

A study of the tissues of the teeth and jaws in piranhas, using the scanning electron microscope and various techniques of light microscopy, revealed many dental adaptations related to the specialized feeding habits of these carnivorous fishes. The dentition is primarily sectorial, although some anterior teeth may be used in grasping. The scissor-like rows of teeth are maintained by the specialized pattern of tooth replacement. The bones of the jaws and the tooth attachment support the teeth very firmly. In its structural organization, the enameloid covering the teeth closely resembles that on the sectorial teeth of sharks and is adapted to the probable stress patterns set up in biting.     

Dentition and tooth replacement pattern in Chalcides (Squamata; Scincidae)

This study was undertaken as a prerequisite to investigations on tooth differentiation in a squamate, the Canarian scincid Chalcides. Our main goal was to determine whether the pattern of tooth replacement, known to be regular in lizards, could be helpful to predict accurately any stage of tooth development. A growth series of 20 laboratory-reared specimens, aged from 0.5 month after birth to about 6 years, was used. The dentition (functional and replacement teeth) was studied from radiographs of jaw quadrants. The number of tooth positions, the tooth number in relation to age and to seasons, and the size of the replacement teeth were recorded. In Chalcides, a single row of pleurodont functional teeth lies at the labial margin of the dentary, premaxillary, and maxillary. Whatever the age of the specimens, 16 tooth positions were recorded, on average, in each quadrant, suggesting that positions are maintained throughout life. Replacement teeth were numerous whatever the age and season, while the number of functional teeth was subject to variation. Symmetry of tooth development was evaluated by comparing teeth two by two from the opposite side in the four jaw quadrants of several specimens. Although the relative size of some replacement teeth fitted perfectly, the symmetry criterion was not reliable to predict the developmental stage of the opposite tooth, whether the pair of teeth compared was left-right or upper-lower. The best fit was found when comparing the size of successive replacement teeth from the front to the back of the jaw. Every replacement tooth that is 40-80% of its definitive size is followed, in the next position on the arcade, by a tooth that is, on average, 20% less developed. Considering teeth in alternate positions (even and odd series), each replacement tooth was a little more developed than the previous, more anterior, one (0.5-20% when the teeth are from 10-40% of their final size). The latter pattern showed that tooth replacement occurred in alternate positions from back to front, forming more or less regular rows (i.e., "Zahnreihen"). In Chalcides, the developmental stage of a replacement tooth in a position p can be accurately predicted provided the developmental stage of the replacement tooth in position p-1 or, to a lesser degree, in position p-2 is known. This finding will be particularly helpful when starting our structural and ultrastructural studies of tooth differentiation in this lizard.     

Tooth function and replacement in early Mesozoic ornithischian dinosaurs: implications for aestivation

Thulborn (1978, Leihaia II ) suggests that ornithischian dinosaurs of the upper Stormberg Series (Late Triassic-Early Jurassic) of southern Africa underwent aestivation during an annual dry season. His argument, based on an interpretation of tooth function and replacement in heterodontosaurids, is: (1) unequivocal evidence of tooth replacement is not seen, and (2) piecemeal replacement of the dentition would be incompatible with maintenance of a fore-aft grinding function of the teeth; therefore, the entire dentition must have been rapidly replaced as a unit during periods of non-feeding, i.e. during aestivation. However, study of tooth wear patterns in Lanasaurus, Lycorhinus , and Heterodontosaurus show that jaw movements during mastication were orthal (open-and-close) and lateral to medial, not forwards and backwards. Differences in degree of tooth wear would not interfere with masticatory movements. Patterns of differential wear indicate that tooth replacement was not periodic but continuous, as in other reptiles. Zahnreihen , with a Z-spacing of about 3.0, are recognizable. Replacement ceased in mature individuals. The dentition shows adaptations for prolonging its effective life despite heavy wear. Differential tooth wear is incompatible with the idea of replacement of the entire dentition as a unit during an hypothesized period of aestivation. Thulborn's suggestion of aestivation in fabrosaurid ornithischians is also shown to be unlikely.     

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 (Olfers, 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.     

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.     

Expression pattern of E‐cadherin during development of the first tooth in zebrafish (Danio rerio)

Although the importance of cell adhesion in morphogenesis is already known for quite some time, there are remarkably few studies on the distribution and function of adhesion molecules in tooth development. We have chosen the zebrafish to study the role of specific cell adhesion molecules in the development and renewal of teeth. Zebrafish lack an oral dentition but have pharyngeal teeth which are renewed throughout life. Here we focus on the expression of E (epithelial)‐cadherin during the development of the first tooth to develop in the dentition, ‘initiator tooth’ 4V¹. E‐cadherin is expressed exclusively in the pharyngeal epithelium and in the enamel organ throughout all stages of development of this first‐generation tooth. Further studies are needed to compare this expression pattern with protein distribution, both in this and other first‐generation teeth as well as in replacement teeth.     

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.     

The relationships of Uronemus: a carboniferous dipnoan with highly modified tooth plates

Previous accounts of the dentition of the Carboniferous dipnoan Uronemus have stressed the significance of the scattered small denticles. These, together with the marginal teeth and ridges, have been interpreted as primitive characters of the dipnoan dentition shared with three other genera: the Devonian Uranlophus and Griphognathus and the Carboniferous to Permian Conchopoma. Genera with tooth plates have been considered to be a monophyletic group in which tooth plates are a derived character; Uronemus has been excluded from this group in all previous investigations dealing with the significance of the dentition for determining relationships among dipnoans. The macromorphology of the dentition of Uronemus has been re-examined and correlated with the histology of all the dental tissues. Optical study of thin sections and scanning electron microscope study of the adjacent cut surfaces has shown that the hard, wear-resistant dentine of the teeth and ridges is petrodentine. The arrangement, growth, wear and histology of the dental tissues have been compared with those of denticulated and tooth-plated genera. The arrangement of new teeth relative to the tooth ridge, the pattern of wear along the ridge, and the type of dentine and its growth indicate that the dentition of Uronemus is best interpreted as a tooth plate with one long lingual tooth ridge and reduced lateral tooth rows. Therefore the marginal tooth ridges are not considered to be homologous with those of denticulate dipnoans such as Uranolophus. The presence of petrodentine, a tissue type only found in forms with tooth plates, is consistent with the view that the dentition is derived by modification of a radiate tooth plate. The denticles covering restricted regions of the palate and lower jaw are considered to have been a secondary acquisition. The suggestion that Conchopoma is a close relative of Uronemus is not accepted, and possible new relationships have been proposed. New data on Scaumenacia and Phaneropleuron, two other genera previously compared with Uronemus, are presented. Rhinodipterus, a form with elongate lingual ridges, is also discussed. Phaneropleuron is shown to have radiate tooth plates and not a marginal row of conical teeth as previously described. It is proposed that the tooth plate of Uronemus is derived from a dipterid type of plate. A discussion of some of the other factors involved in determining the relationships of the genus is given.(ABSTRACT TRUNCATED AT 400 WORDS)     

A morphometric study of bone and tooth volumes in the pipid frog Xenopus laevis (Daudin), with comments on the importance of tooth resorption during normal tooth replacement

Volumetric estimations of teeth and bone on serial sections using a semiautomatic image analyzer indicate that, in the polyphyodont dentition of the pipid anuran Xenopus laevis (Daudin), the mean volume of the dentine composing the teeth is about 23.5% of the volume of the supporting maxillae and premaxillae. During tooth replacement, osteoclasts resorb up to 98% of the dentine. Teeth may be resorbed rather than shed in order to conserve tooth constituents because, if shedding of complete teeth did occur, a quantity of calcified tissue equal to perhaps 45 times the volume of the bone of the upper jaw might be lost over an animal's projected life span of about 13-15 years.     

On the control of tooth replacement in reptiles and its relationship to growth

The teeth of nearly all non-mammalian vertebrates are replaced in waves which sweep through alternate tooth positions. It is argued that tooth replacement in these animals represents growth of the dentition. It is shown that the pattern of tooth replacement could be described by the exponential equation t_(n)r, = k e^ar+bn when t(n)r is the time at which the rth replacement erupts in the nth position and k, a and b are constants. The length of a replacement wave (w) which is visible in the mouth, can be calculated from the equation w = 2(a?b)/a?2b for forward travelling waves. The effect of different ratios, $\text{a}\text{b}$, on wavelength is described. The model can be interpreted as describing the effect of a zone of inhibition which (it is argued) temporarily surrounds any newly initiated tooth. The increasing time required to dissipate the inhibition around successive replacement teeth is related to the age of the animal. This increasing time permits successive teeth to grow for longer periods than their predecessors and can account for a gradual increase in the size of successive teeth. A similar mechanism could account for the phasic nature of bone growth. It is indicated that the model could be difficult to test.     

Formation of a successional dental lamina in the zebrafish (Danio rerio): support for a local control of replacement tooth initiation

In order to test whether the formation of a replacement tooth bud in a continuously replacing dentition is linked to the functional state of the tooth predecessor, I examined the timing of development of replacement teeth with respect to their functional predecessors in the pharyngeal dentition of the zebrafish. Observations based on serial semithin sections of ten specimens, ranging in age from four week old juveniles to adults, indicate that (i) a replacement tooth germ develops at the distal end of an epithelial structure, called the successional dental lamina, budding off from the crypt epithelium surrounding the erupted part of a functional tooth; (ii) there appears to be a developmental link between the eruption of a tooth and the formation of a successional dental lamina and (iii) there can be a time difference between successional lamina formation and initiation of the new tooth germ, i.e., the successional dental lamina can remain quiescent for some time. The data suggest that the formation of a successional lamina and the differentiation of a replacement tooth germ from this lamina, are two distinct phases of a process and possibly under a different control. The strong spatio-temporal coincidence of eruption of a tooth and development of a successional dental lamina is seen as evidence for a local control over tooth replacement.