Evolutionary and developmental origins of the vertebrate dentition

Abstract

According to the classical theory, teeth derive from odontodes that invaded the oral cavity in conjunction with the origin of jaws (the 'outside in' theory). A recent alternative hypothesis suggests that teeth evolved prior to the origin of jaws as endodermal derivatives (the 'inside out' hypothesis). We compare the two theories in the light of current data and propose a third scenario, a revised 'outside in' hypothesis. We suggest that teeth may have arisen before the origin of jaws, as a result of competent, odontode-forming ectoderm invading the oropharyngeal cavity through the mouth as well as through the gill slits, interacting with neural crest-derived mesenchyme. This hypothesis revives the homology between skin denticles (odontodes) and teeth. Our hypothesis is based on (1) the assumption that endoderm alone, together with neural crest, cannot form teeth; (2) the observation that pharyngeal teeth are present only in species known to possess gill slits, and disappear from the pharyngeal region in early tetrapods concomitant with the closure of gill slits, and (3) the observation that the dental lamina (sensu Reif, 1982) is not a prerequisite for teeth to form. We next discuss the progress that has been made to understand the spatially restricted loss of teeth from certain arches, and the many questions that remain regarding the ontogenetic loss of teeth in specific taxa. The recent advances that have been made in our knowledge on the molecular control of tooth formation in non-mammalians (mostly in some teleost model species) will undoubtedly contribute to answering these questions in the coming years.

Fig. 1

Comparison of the arrangement of the gill slits, the position of the branchial arches and of the gills in agnathans (A) and gnathostomes (B,C). Odontodes and dermal bones are indicated in red. (A,B) Extent of ectoderm (blue) and endoderm (yellow) as usually assumed. In (C) we postulate (contra B) that the ectoderm penetrates further inwards (arrowheads), and possibly covers the endoderm, as observed by Edwards (1929) (cf. Fig. 3) (modified after Jollie, 1968).

Fig. 3

Three stages in the development of the gill slits and pharynx of the carp (Cyprinus carpio). (A–C) respectively 36, 56 and 78 h post-fertilization. An ectodermal plug (blue) invaginates the endodermal pharyngeal folds (yellow) (A) and forms a layer of flattened (ectoderm-derived) cells (blue) on top of the columnar (endoderm-derived) epithelial cells (yellow) (B,C). The latter produce the enamel organs of the teeth. 4v, fourth ventricle; Br, brain; Ep, proliferating ectodermal plug; Es, epidermal stratum; Ga, gill arch; Gs, gill slit; Ha, hyoid arch; Nl, inner layer of ectoderm; No, notochord; Ov, otic vesicle; Pf, pharyngeal fold (modified after Edwards, 1929).

Fig. 2

Semithin sections of forming pharyngeal pouches in zebrafish (Danio rerio) at 56 h (A) and 72 h (B) post-fertilization. (A) An epithelial connection (black arrowheads) is seen between the epidermis (white asterisks) and the foregut (black asterisk). (B) The first tooth germs (white arrowhead) are forming whilst the gill slits are still closed (black arrowheads), and the pharyngeal lumen opens (black asterisk). Scale bars = 40 µm.

Fig. 4

Different types of dental lamina (black arrowheads) during tooth replacement. Replacement tooth formation without the presence of a dental lamina (A, Atlantic salmon, Salmo salar); with a transient, successional dental lamina (B, zebrafish, Danio rerio, and C, jewel cichlid, Hemichromis bimaculatus), or with a permanent dental lamina (D, Pleurodeles waltl, a urodele amphibian; E, Chalcides sexlineatus, a scincid lizard; F, human first lower deciduous molar). boa, bone of attachment; db, dentigerous bone; dp, dental papilla; eo, enamel organ; oe, oral epithelium; pe, pharyngeal epithelium; t, tooth. Scale bars (A–E) = 50 µm, (F) = 500 µm. (F), courtesy of Ralf J. Radlanski.

Fig. 5

Branchial denticulated plates (branchial ossicles) in the pre-metamorphosis stage of Onchiodon labyrinthicus, a temnospondyl amphibian from the lower Permian (reproduced from Schoch, 2001, Fig. 3, with permission from the author).