Evolution of developmental pattern for vertebrate dentitions: an oro‐pharyngeal specific mechanism

Abstract

Classically the oral dentition with teeth regulated into a successional iterative order was thought to have evolved from the superficial skin denticles migrating into the mouth at the stage when jaws evolved. The canonical view is that the initiation of a pattern order for teeth at the mouth margin required development of a sub-epithelial, permanent dental lamina. This provided regulated tooth production in advance of functional need, as exemplified by the Chondrichthyes. It had been assumed that teeth in the Osteichthyes form in this way as in tetrapods. However, this has been shown not to be true for many osteichthyan fish where a dental lamina of this kind does not form, but teeth are regularly patterned and replaced. We question the evolutionary origin of pattern information for the dentition driven by new morphological data on spatial initiation of skin denticles in the catshark. We review recent gene expression data for spatio-temporal order of tooth initiation for Scyliorhinus canicula, selected teleosts in both oral and pharyngeal dentitions, and Neoceratodus forsteri. Although denticles in the chondrichthyan skin appear not to follow a strict pattern order in space and time, tooth replacement in a functional system occurs with precise timing and spatial order. We suggest that the patterning mechanism observed for the oral and pharyngeal dentition is unique to the vertebrate oro-pharynx and independent of the skin system. Therefore, co-option of a successional iterative pattern occurred in evolution not from the skin but from mechanisms existing in the oro-pharynx of now extinct agnathans.

Cutting blade dentitions in squaliform sharks form by modification of inherited alternate tooth ordering patterns

“…The slight overlap of teeth within the alternate developmental rows is preserved as overlap in teeth within the functional row, ‘locking’ the teeth together. This overlapping pattern has been noted in other squaliforms [18] and termed ‘imbricate overlap’ [19]. …”

“…The dentition of the early ontogenetic stages of Squalus is reminiscent of that seen in the shark Scyliorhinus [18] and batoids [11] but with some very significant differences that cannot be satisfactorily explained by previous tooth addition models. The first developmental tooth row in S. acanthias and S. blainville embryonic specimens comprises only two parasymphyseal teeth, with no mineralized symphyseal tooth being present (i.e.…”

Scales and Tooth Whorls of Ancient Fishes Challenge Distinction between External and Oral ‘Teeth’

“…Such a pattern implies the existence of a highly organized odontogenetic process, involving a persistent strip of odontode-producing tissue along the ventral edge of the scale that is activated in a stereotypic manner at regular time intervals. This type of organized odontogenetic program characterizes the dentition of gnathostome jaws, where the generative tissue would be described as an odontogenetic band or dental lamina [3], [7].…”

“…Because they are readily available for study, sharks have been used extensively to discuss problems related to the origin of the dentition in jawed vertebrates [1]–[6]. Consistent differences between the spatial organization of dermal odontodes and teeth have given rise to the hypothesis that the oro-pharyngeal odontode skeleton has a unique pattern, independent of the dermal odontodes [7]. This oro-pharyngeal pattern, consisting of odontodes arranged into a successional iterative order and induced by the covering dental lamina or odontogenic band, has been considered as a diagnostic character of true teeth [2]–[6], [8]–[11].…”

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

“…General body denticles (Fig. 1f, g) are the most prevalent denticle type, appearing just before hatching at 145–175 dpf (Stage 34) [23], covering the skin in an intricate pattern when space is available and not in discrete rows [25, 26]. Before dorsal and body denticles appear, four rows of caudal denticles emerge at 52–60 dpf (Stage 30) [23]; two rows are present (dorsal and ventral) laterally on either side of the tail fin tip (Fig.…”