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.

The odontode explosion: The origin of tooth‐like structures in vertebrates

“…In concordance with the classic ‘outside-in’ theory, evolutionary precursors of teeth are believed to be epidermal (ectodermal) denticles, where teeth evolved only after an odontogenic competent ectodermal tissue had mixed inside via the mouth and each of the gill slits [38]. In contrast to the original ‘outside-in’ scenario where teeth develop solely from ectoderm [1], this ‘modified’ hypothesis allows that the initial odontogenic potential of the ectoderm may have been subsequently transferred to endoderm upon contact and cell mixing.…”

“…Recently, a ‘modified outside-in hypothesis’ has been suggested [38]. In concordance with the classic ‘outside-in’ theory, evolutionary precursors of teeth are believed to be epidermal (ectodermal) denticles, where teeth evolved only after an odontogenic competent ectodermal tissue had mixed inside via the mouth and each of the gill slits [38].…”

“…The arguments for this are as follows: 1) experimental and in vitro studies indicate that both ectoderm and endoderm cells are needed for teeth to develop; however, until now these studies were undertaken mostly on salamanders [39–41]; 2) classical observations on the ecto-endoderm boundaries within the pharyngeal cavity of cypriniform fishes revealed complex epithelial morphodynamics with pharyngeal teeth developing from the endoderm epithelia, with the ectoderm lining in close proximity [42, 43] (see Figure 1: A2). Further support for this ‘modified’ hypothesis is offered by the fact that pharyngeal teeth are only found in species with gill slits and that, accordingly, pharyngeal teeth are absent in tetrapods, coincident with the retained closure of the pharyngeal cavity [38]. However, in some tetrapods like salamanders or frog tadpoles, gill slits remain open, but no pharyngeal teeth develop [44, 45].…”

“…As in the case of oral development, perforation of the branchial membranes probably causes a loss of definitive ectoderm-endoderm boundaries. Subsequent cell rearrangements potentially occur to produce a cryptic distribution of these epithelia [38, 43],.…”

Ectoderm, endoderm, and the evolution of heterodont dentitions

“…In mammals, the oral epithelium from which tooth buds originate has traditionally been believed to be of ectodermal origin. However, in teleost fish such as zebrafish (Danio rerio) mineralized tooth-like structures exist in the endodermal pharynx, although it is not definitively proven that zebrafish teeth are endodermally derived (Huysseune et al, 2009). In addition, the pharyngeal endoderm is reported to be capable of forming teeth in amphibians (Barlow and Northcutt, 1995;Cassin and Capuron, 1979;Graveson et al, 1997).…”