Moya Meredith Smith

Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues.

This review deals with the following seven aspects of vertebrate skeletogenic and odontogenic tissues.

Vertebrate dentitions at the origin of jaws: when and how pattern evolved

Summary 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.

Conserved deployment of genes during odontogenesis across osteichthyans

Odontogenesis has only been closely scrutinized at the molecular level in the mouse, an animal with an extremely restricted dentition of only two types and one set. However, within osteichthyans many species display complex and extensive dentitions, which questions the extent to which information from the mouse is applicable to all osteichthyans. We present novel comparative molecular and morphological data in the rainbow trout (Oncorhynchus mykiss) that show that three genes, essential for murine odontogenesis, follow identical spatial-temporal expression. Thus, at all tooth bud sites, epithelial genes Pitx–2 and Shh initiate the odontogenic cascade, resulting in dental mesenchymal Bmp–4 expression, importantly, including the previously unknown formation of replacement teeth. Significantly, this spatial–temporal sequence is the same for marginal and lingual dentitions, but we find notable differences regarding the deployment of Pitx–2 in the developing pharyngeal dentition. This difference may be highly significant in relation to the theory that dentitions may have evolved from pharyngeal tooth sets in jawless fishes. We have provided the first data on operational genes in tooth development to show that the same signalling genes choreograph this evolutionary stable event in fishes since the osteichthyan divergence 420 Myr ago, with the identical spatial–temporal expression as in mammals.

A Developmental Model for Evolution of the Vertebrate Exoskeleton and Teeth

An exoskeleton is extensive in the head, trunk, and tail of agnathan and gnathostome fishes, where it forms a thick, rigid armor in most fossil fishes, although many only have a covering of separate denticles. This armor consists of three basic layers of mineralized tissue surrounding soft tissue components. There is a superficial odontode layer (see pp. 391 and 393 for discussion of odontodes) with enamel, dentine, attachment bone, and pulp chambers; a middle layer with trabeculae of cellular or acellular bone surrounding soft tissue vascular spaces; and a basal laminated layer of compact cellular or acellular bone, with zones of attachment fibers. Among extant osteichthyan fishes are those that retain some of these odontode components in their dermal scales as a mineralized exoskeleton. These are the so-called living fossils, the Polypteridae and the extant coelacanth, as well as catfishes. Odontode components are retained as placoid scales in all chondrichthyans (see Figs. 1 and 2).

The ultrastructure of odontogenesis in larval and adult urodeles; differentiation of the dental epithelial cells

SummarySections of undemineralized tooth germs ofAmbystoma andTriturus were examined. The ultrastructure of early germs, both larval and adult, and of dentinogenesis, resembled that of mammals. In adult bicuspid teeth, once the dentine of the cusps was mineralized, mineral crystals of a similar size to early mammalian enamel crystals, appeared between the dentine and the inner dental epithelium (i.d.e). Concomitantly, the i.d.e showed features of mammalian secreting ameloblasts. This new layer, regarded as true enamel, lacked collagen, possessed an ordered arrangement of crystals and reached a maximum thickness of 6 μm.In larval monocuspid teeth, once dentine mineralization had reached the plasma membranes of the i.d.e at the tip of the cusp, the i.d.e developed a ruffled border. At this stage the dentine of the tip, regarded as enameloid, was very hard and difficult to section. The ruffled border, characteristic of other cells which transport materials, was regarded as indicating that the i.d.e was removing organic matter from the enameloid. The differences in development between larval and adult teeth support the concept that there is a change in cellular activity of the i.d.e which occurs during metamorphosis from the larval to the adult urodele.

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

SUMMARY 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.

Dental lamina as source of odontogenic stem cells: evolutionary origins and developmental control of tooth generation in gnathostomes.

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.

Origin and evolution of gnathostome dentitions: a question of teeth and pharyngeal denticles in placoderms

The fossil group Placodermi is the most phylogenetically basal of the clade of jawed vertebrates but lacks a marginal dentition comparable to that of the dentate Chondrichthyes, Acanthodii and Osteichthyes (crown‐group Gnathostomata). The teeth of crown‐group gnathostomes are part of an ordered dentition replaced from, and patterned by, a dental lamina, exemplified by the elasmobranch model. A dentition recognised by these criteria has been previously judged absent in placoderms, based on structural evidence such as absence of tooth whorls and typical vertebrate dentine.

Developmental plasticity and disparity in early dipnoan (lungfish) dentitions.

SUMMARY Although the lungfish (Dipnoi) belong within the Osteichthyes, their dentitions are radically different from other osteichthyans. Lungfish dentitions also show a uniquely high structural disparity during the early evolution of the group, partly owing to the independent variation of odontogenic and odontoclastic processes that are tightly and stereotypically coordinated in other osteichthyans. We present a phylogenetic analysis of early lungfishes incorporating a novel approach to coding these process characters in preference to the resultant adult dental morphology. The results only partially resolve the interrelationships of Devonian dipnoans, but show that the widely discussed hypothesis of separate tooth‐plated, dentine‐plated, and denticulated lineages is unlikely to be true. The dipnoan status of Diabolepis is corroborated. Lungfish dentitions seem to have undergone extensive and nonparsimonious evolution during the early history of the group, but much of the resulting disparity can be explained by a modest number of evolutionary steps in the underlying developmental processes, those for dental formation (odontogenic) and those for the remodeling of dentine tissue (odontoclastic). Later in lungfish evolution, this disparity was lost as the group settled to a pattern of dental development that is just as stereotypic as, but completely different from, that of other osteichthyans.

Reiterative pattern of sonic hedgehog expression in the catshark dentition reveals a phylogenetic template for jawed vertebrates

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.