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

Abstract

We integrate recent data to shed new light on the thorny controversy of how teeth arose in evolution. Essentially we show (a) how teeth can form equally from any epithelium, be it endoderm, ectoderm or a combination of the two and (b) that the gene expression programs of oral vs. pharyngeal teeth are remarkably similar. Classic theories suggest that (i) skin denticles evolved first and odontode-inductive surface ectoderm merged inside the oral cavity to form teeth (the 'outside-in' hypothesis) or that (ii) patterned odontodes evolved first from endoderm deep inside the pharyngeal cavity (the 'inside-out' hypothesis). We propose a new perspective that views odontodes as structures sharing a deep molecular homology, united by sets of co-expressed genes defining a competent thickened epithelium and a collaborative neural crest derived ectomesenchyme. Simply put, odontodes develop 'inside and out,' wherever and whenever these co-expressed gene sets signal to one another. Our perspective complements the classic theories and highlights an agenda for specific experimental manipulations in model and non-model organisms.

Coevolutionary patterning of teeth and taste buds

“…Interestingly, genetic ablation of Follistatin increases BMP signal in the mouse tongue and gives rise to ectopic posterior papillae that express Sox2 and Foxa2, but which appear to invaginate rather than evaginate like typical taste buds (54). Overall, teeth and taste buds share gene synexpression and a deep molecular homology (12). Our work here implies that the Wnt-BMP-Hh regulatory hierarchy patterning these organs is conserved, despite release from the constraint of spatial colocalization in mammals (and other vertebrates).…”

“…Taste buds often colocalize with teeth at these sites as both organs are regenerated, with pattern fidelity, throughout the lifetime of an individual. Teeth and taste buds may share an evolutionary origin and deep molecular homology (12). There is tremendous variation in tooth and taste bud numbers among vertebrates.…”

Signals and Switches in Mammalian Neural Crest Cell Differentiation

“…2) but, at the same time, is an important antagonist of the chondrogenic pathway (Kolpakova and Olsen 2005;Hartmann 2006). Interestingly, the conditional deletion of Wnt/b-catenin in the dermis gives rise to skeletogenic differentiation in mice (Day et al 2005;Hill et al 2005;Tran et al 2010) and may thus provide some insight into the wide array of dermal armor and skeletal elements found across various extant and fossil vertebrates (Vickaryous and Sire 2009;Fraser et al 2010), which may potentially be of neural crest origin.…”

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

“…regeneration | stem cells | odontogenesis | chondrichthyes | evolutionary novelty T he evolutionary origin of teeth, a key vertebrate innovation, is a long-disputed question in vertebrate biology (1)(2)(3). Anatomical and developmental similarities between teeth and denticles, both consisting of basal bone, dentine, and a hypermineralized enamel-related tissue surrounding a pulp cavity, have long been recognized (4,5).…”

“…Despite these similarities, teeth in extant vertebrates are functionally, topographically, and organizationally distinct from the rest of the exoskeleton and considered a largely independent developmental module (6,7). Current hypotheses posit that oral teeth evolved either from odontodes in the external dermal skeleton (outside-in) or deeper within the pharynx (insideout) before their eventual cooption and elaboration in jaws of early gnathostomes (1,3). However, neither the developmental genetic basis of this cooption event nor the evolutionary mechanisms underlying the elaboration and diversification of this peculiar odontode module are known.…”