This review deals with the following seven aspects of vertebrate skeletogenic and odontogenic tissues. 1. The evolutionary sequence in which the tissues appeared amongst the lower craniate taxa. 2. The topographic association between skeletal (cartilage, bone) and dental (dentine, cement, enamel) tissues in the oldest vertebrates of each major taxon. 3. The separate developmental origin of the exo- and endoskeletons. 4. The neural-crest origin of cranial skeletogenic and odontogenic tissues in extant vertebrates. 5. The neural-crest origin of trunk dermal skeletogenic and odontogenic tissues in extant vertebrates. 6. The developmental processes that control differentiation of skeletogenic and odontogenic tissues in extant vertebrates. 7. Maintenance of developmental interactions regulating skeletogenic/odontogenic differentiation across vertebrate taxa. We derive twelve postulates, eight relating to the earliest vertebrate skeletogenic and odontogenic tissues and four relating to the development of these tissues in extant vertebrates and extrapolate the developmental data back to the evolutionary origin of vertebrate skeletogenic and odontogenic tissues. The conclusions that we draw from this analysis are as follows. 8. The dermal exoskeleton of thelodonts, heterostracans and osteostracans consisted of dentine, attachment tissue (cement or bone), and bone. 9. Cartilage (unmineralized) can be inferred to have been present in heterostracans and osteostracans, and globular mineralized cartilage was present in Eriptychius, an early Middle Ordovician vertebrate unassigned to any established group, but assumed to be a stem agnathan. 10. Enamel and possibly also enameloid was present in some early agnathans of uncertain affinities. The majority of dentine tubercles were bare. 11. The contemporaneous appearance of cellular and acellular bone in heterostracans and osteostracans during the Ordovician provides no clue as to whether one is more primitive than the other. 12. We interpret aspidin as being developmentally related to the odontogenic attachment tissues, either closer to dentine or a form of cement, rather than as derived from bone. 13. Dentine is present in the stratigraphically oldest (Cambrian) assumed vertebrate fossils, at present some only included as Problematica, and is cladistically primitive, relative to bone. 14. The first vertebrate exoskeletal skeletogenic ability was expressed as denticles of dentine. 15. Dentine, the bone of attachment associated with dentine, the basal bone to which dermal denticles are fused and cartilage of the Ordovician agnathan dermal exoskeleton were all derived from the neural crest and not from mesoderm. Therefore the earliest vertebrate skeletogenic/odontogenic tissues were of neural-crest origin.(ABSTRACT TRUNCATED AT 400 WORDS)
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.
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.
The theory that teeth evolved from dermal denticles linked with the origin of jaws no longer accounts for the diversity of new data emerging from the fossil record. We have reviewed oropharyngeal dental patterns in all fossil groups of early vertebrates to establish the primitive condition, in order to understand the polarity of change. The evolutionary precedence of dermal denticles before teeth now seems less likely; both may be alternative manifestations of a common morphogenetic system. This developmental system involves regulatory changes affecting the odontode, a fundamental exoskelctal unit, and can explain skeletal diversity. However, tooth and denticle differences may have diverged at loci deep within vertebrate phylogeny, as real differences exist between them. Teeth were conceived as evolving from non‐growing odontodes with regulation of precise increase in size, position, sequence of time of development, and polarity of shape. A characteristic feature of teeth is the ability to replace from a developing sequence, programmed with these parameters, prior to demand. Tooth whorls, a feature of denticles in the oropharyngeal region, may be regarded as a preadaptation of this tooth replacement mechanism. The new fossil evidence suggests that teeth may have evolved from these more specialised oropharyngeal denticles in agnathan vertebrates.
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