Abstract: This study considers stem cells for odontogenic capability in biological tooth renewal in the broad context of gnathostome dentitions and the derivation of them from oral epithelium. The location of the developmental site and cell dynamics of the dental lamina are parameters of a possible source for odontogenic epithelial stem cells, but the phylogenetic history is not known. Understanding the phylogenetic basis for stem cell origins throughout continuous tooth renewal in basal jawed vertebrates is the ultimate objective of this study. The key to understanding the origin and location of stem cells in the development of the dentition is sequestration of stem cells locally for programmed tooth renewal. We suggest not only the initial pattern differences in each dentate field but local control subsequently for tooth renewal within each family. The role of the specialized odontogenic epithelium (odontogenic band) is considered as that in which the stem cells reside and become partitioned. These regulate time, position and shape in sequential tooth production. New histological data for chondrichthyan fish show first a thickening of the oral epithelium (odontogenic band). After this, all primary and successive teeth are only generated deep to the oral epithelium from a dental lamina. In contrast, in osteichthyan fish the first teeth develop directly within the odontogenic band. In addition, successors are initiated at each tooth site in the predecessor tooth germ (without a dental lamina). We suggest that stem cells specified for each tooth family are set up and located in intermediate cells between the outer and inner dental epithelia.
Abstract: We report a temporal order of tooth addition in the Australian lungfish where timing of tooth induction is sequential in the same pattern as osteichthyans along the lower jaw. The order of tooth initiation in Neoceratodus starts from the midline tooth, together with left and right ones at jaw position 2, followed by 3 and then 1. This is the pattern order for dentary teeth of several teleosts and what we propose represents a stereotypic initiation pattern shared with all osteichthyans, including the living sister group to all tetrapods, the Australian lungfish. This is contrary to previous opinions that the lungfish dentition is otherwise derived and uniquely different. Sonic hedgehog (shh) expression is intensely focused on tooth positions at different times corresponding with their initiation order. This deployment of shh is required for lungfish tooth induction, as cyclopamine treatment results in complete loss of these teeth when applied before they develop. The temporal sequence of tooth initiation is possibly regulated by shh and is know to be required for dentition pattern in other osteichthyans, including cichlid fish and snakes. This reflects a shared developmental process with jawed vertebrates at the level of the tooth module but differs with the lack of replacement teeth.
Abstract: For a dentition representing the most basal extant gnathostomes, that of the shark can provide us with key insights into the evolution of vertebrate dentitions. To detail the pattern of odontogenesis, we have profiled the expression of sonic hedgehog, a key regulator of tooth induction. We find in the catshark (Scyliorhinus canicula) that intense shh expression first occurs in a bilaterally symmetrical pattern restricted to broad regions in each half of the dentition in the embryo jaw. As in the mouse, there follows a changing temporal pattern of shh spatial restriction corresponding to epithelial bands of left and right dental fields, but also a subfield for symphyseal teeth. Then, intense shh expression is restricted to loci coincident with a temporal series of teeth in iterative jaw positions. The developmental expression of shh reveals previously undetected timing within epithelial stages of tooth formation. Each locus at alternate, even then odd, jaw positions establishes precise sequential timing for successive replacement within each tooth family. Shh appears first in the central cusp, iteratively along the jaw, then reiteratively within each tooth for secondary cusps. This progressive, sequential restriction of shh is shared by toothed gnathostomes and conserved through 500 million years of evolution.
Abstract: Placoderms are extinct jawed fishes of the class Placodermi and are basal among jawed vertebrates. It is generally thought that teeth are absent in placoderms and that the phylogenetic origin of teeth occurred after the evolution of jaws. However, we now report the presence of tooth rows in more derived placoderms, the arthrodires. New teeth are composed of gnathostome-type dentine and develop at specific locations. Hence, it appears that these placoderm teeth develop and are regulated as in other jawed vertebrates. Because tooth development occurs only in derived forms of placoderms, we suggest that teeth evolved at least twice, through a mechanism of convergent evolution.
Abstract: New evidence shows that teeth evolved with a greater degree of independence from jaws than previously considered. Pharyngeal denticles occur in jawless fish and also in early gnathostomes and precede jaw teeth in phylogeny. Many of these denticles form joined polarized sets on each branchial arch; these resemble whorl-shaped tooth sets on the jaws of stem and crown gnathostomes and are proposed as homologous units. Therefore, the source of patterning of these pharyngeal denticle and tooth sets is conserved from jawless conditions. It is proposed that developmental regulatory systems, responsible for all such tooth patterns on the jaws, are co-opted from the pharyngeal region and not from the skin as classically understood. This strongly implicates embryonic endoderm as opposed to ectoderm in the genetic control of dentition patterning. New interpretations of ontogenetic data on patterning dentitions of extant sharks are proposed, together with those of osteichthyan fish. Two entirely fossil groups, placoderms and acanthodians, at the base of gnathostome phylogeny are reassessed on the basis of a new model. It is concluded that within stem group and crown group gnathostomes several different strategies, unique to each taxon, were adopted to produce different developmental models of dentition patterning from pharyngeal denticles. One shared developmental pattern is that of initiation from primordial tooth sites, independently in each dentate zone of the jaws. The new model is proposed as a framework for data on evolutionary developmental genetics.
Abstract: The lungfish dentition is different from other osteichthyan fish because it has a characteristic and unique pattern of teeth arranged as toothplates. Growth, addition of teeth, and retention as part of a statodont dentition are determined by the initiation pattern. In adult lungfish new teeth are only added laterally to each radial row in the dentition. This is in marked contrast to marginal rows of teeth with regular, alternating replacement in most osteichthyans. We analyze development from fossil hatchling forms of the Late Devonian dipnoan Andreyevichthys and compare with those of Neoceratodus, the Australian lungfish. The specific pattern of development, unique within lungfish, is also present in the transitory, marginal, anterior dentition in both, reflecting a strongly conserved developmental pattern. These marginal teeth form but are then lost in both, so that also this program of development is conserved within lungfish for 360 million years, from the earliest known form.
Abstract: Although the 3 genera of living lungfish have different-shaped adult tooth plates, their larval stages have similar patterns of development. The sequence in the pattern of initiation of teeth and their modification through ontogeny in Neoceratodus hatchlings provides a developmental model for fossil hatchling tooth plates (smallest 1-2 mm) recovered as 3-dimensional dentitions from Andreyevichthys. This Late Devonian lungfish demonstrates that these also have a similar dentition pattern and suggests strongly conserved developmental processes. We postulate that a specific pattern of development, derived within lungfish, has been conserved in extant forms through evolution from the earliest known lungfish. The most basal early dipnoan, Diabolepis speratus, is also known from juveniles with tooth plates formed in this pattern. The lungfish pattern is in marked contrast to the typical linear rows of teeth with lingual replacement for each tooth position, characteristic of most osteichthyan and chondrichthyan dentitions. Uniquely for lungfish, teeth are only added to the lateral ends of the radial rows in the palatal and lingual dentition and are consolidated into dental plates without loss through shedding. It is proposed that this tooth pattern is set up from primordial teeth at the patterning stage of the dentition, one in each dentate region of the larval jaws. Although in post-Devonian lungfish marginal dentate bones are absent in the adult, in both the fossil and extant hatchling, teeth are present and function on some of the marginal bones. This pattern of development and loss is described and we conclude that in both forms it is also based on a radial pattern of successive tooth initiation. We propose that this ontogenetic pattern constrained the phylogenetic pattern of adult form, through evolution of dipnoan dentitions from 360 MYBP until the present. The universality amongst dipnoans and the implications for such a conserved constraint in the developmental module for the dentition is discussed.
