The odontode explosion: the origin of tooth-like structures in vertebrates

Abstract

Essentially we show 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 versus 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.

Figure 1. Theories of odontode evolution

Schematic diagrams represent a generalised (hypothetical) early vertebrate/fish in lateral/sagittal view: A1: Outside-in theory; ectodermal tissue is hypothesized to have integrated (green arrow) into the oro-pharyngeal cavity (opc), leading to the evolution of oral odontodes and subsequently oral and pharyngeal teeth. A2: Modified outside-in theory; ectodermal tissue integrated (green arrow) into the endodermal oral cavity via the mouth opening (the anterior boundary of the endoderm and ectoderm) and the gill slits (gs) in early vertebrates to initiate/transfer dental competence (arrow) to the endoderm of the oro-pharyngeal cavity. The point is made that ectoderm must be in regional contact with endoderm for teeth to form. B: Inside-out theory; skin denticles and teeth are structures forming independently from ectoderm and endoderm, respectively. This theory states that teeth originated in the posterior pharyngeal endoderm of jawless vertebrates; a dental competence that was co-opted anteriorly (red arrow) in concert with the evolution of oral jaws. This theory states that skin denticles did not grade into teeth. e, eye; n, nasal placode; opc, oro-pharyngeal cavity.

Figure 2. The inside and out gene regulatory hypothesis for odontode evolution

A. Schematic diagram represents a generalised early vertebrate/fish in lateral/sagittal view: We propose that regardless of tissue origin (endoderm or ectoderm), the ingredients for odontode evolution, instigated by the appearence of the putative odontode gene regulatory network (oGRN), involved the collaboration of two pre-existing gene co-expression groups: (i) the neural crest-derived ectomesenchymal co-expression group (mesCEG) and (ii) the epithelial co-expression group (epCEG), which operates within both the endoderm and ectoderm (B). C: The evolution of both skin denticles and teeth were separate operations of the combination of epCEG and mesCEG in alternative locations, the epidermis and the oro-pharngeal cavity (opc). Within the opc, co-option of the oGRN potential was transfered to the oral jaws during the transition from jawless (agnathans) to jawed vertebrates (gnathostomes).

Figure 3. Epithelial transitions and innovative network consolidation

A. a generalised epithelia from which a thickened epithelial placode initiates, B: The genes expressed within this thickening can be described as the epithelial co-expression group (epCEG). From this thickened epithelial placode the epithelium can transition into a number of structures: C: a taste bud, a similar sensory unit, is a superficial epithelial element possing a unique epithelial gene expression signature (tbCEG); D: a denticle and E: a tooth recruit the underlying mesenchyme that contains the neural crest-derived cell population and the set of genes associated with the neural crest-derived ectomesenchyme (mesCEG). Note that this collection of genes is related to and influenced by the ncGRN. For a more complete list of genes that interact in the ncGRN, embryo-wide, see [69, 70]. We propose the mesCEG collaborated with the epCEG to provide the ingredients for the oGRN (see also Figure 2). Skin denticles and teeth are born from the odontode GRN as they are both odontodes by definition. The tooth itself houses a unique subset of genes (collectively the dental GRN). This coordinated gene network contains genes that are not shared with scales and thus we assume dermal denticles, highlighting their evolutionary and developmental separation. The divergence between members of the oGRN and dGRN reflects those genes only expressed in the dentition versus those expressed across odontodes determined from expression during teleost scale development; it remains to be tested whether these expression trends hold for denticles of extant sharks and rays.