Retention of fish-like odontode overgrowth in Permian tetrapod dentition supports outside-in theory of tooth origins

Abstract

Teeth are often thought of as structures that line the margins of the mouth; however, tooth-like structures called odontodes are commonly found on the dermal bones of many Palaeozoic vertebrates including early jawless fishes. 'Odontode' is a generalized term for all tooth-like dentine structures that have homologous tissues and development. This definition includes true teeth and the odontodes of early 'fishes', which have been recently examined to gain new insights into the still unresolved origin of teeth. Two leading hypotheses are frequently referenced in this debate: the 'outside-in' hypothesis, which posits that dermal odontodes evolutionarily migrate into the oral cavity, and the 'inside-out' hypothesis, which posits that teeth originated in the oropharyngeal cavity and then moved outwards into the oral cavity. Here, we show that, unlike the well-known one-to-one replacement patterns of marginal dentition, the palatal dentition of the early Permian tetrapods, including the dissorophoid amphibian Cacops and the early reptile Captorhinus, is overgrown by a new layer of bone to which the newest teeth are then attached. This same overgrowth pattern has been well documented in dermal and oral odontodes (i.e. teeth) of early fishes. We propose that this pattern represents the primitive condition for vertebrates and may even predate the origin of jaws. Therefore, this pattern crosses the fish-tetrapod transition, and the retention of this ancestral pattern in the palatal dentition of early terrestrial tetrapods provides strong support for the 'outside-in' hypothesis of tooth origins.

Keywords: dental evolution; dentition; odontode; overgrowth; tooth origins.

Figure 1.

Histological thin sections showing odontode overgrowth. (a) Representative heterostracan Drepanaspis showing region sampled. (b) Sampled heterostracan Psammolepis sp. dermal armour fragment section. (c) Magnified inset showing multiple odontodes overgrown with acellular bone. (d–f) Glyptolepis sp., skull roof fragment. (f) Magnified inset of (e), multiple odontodes stacked on one another overlain by bone tissue; dentine tubules indicate location of dentine. (g–i) Laccognathus sp., skull roof fragment. (i) Magnified inset of (h), two odontodes overlaying one another with bone tissue in between. (j–l) cf. Cacops, palatine. (k) Oblique section through the palatine shows a fragment of a tooth at the oral surface and at least two generations embedded within lamellar bone. (l) Magnified inset of (k), a palatal tooth fully embedded in lamellar bone showing enamel, dentine, pulp cavity. (m–s) Captorhinus sp., pterygoid. (n–p) Organized lamellar bone overlaying and embedding teeth along the antero-medial edge of the bone; pulp cavity still visible in partially embedded teeth. (q–s) Transverse flange of the pterygoid embedding multiple generations of teeth. The arrows (a–i) point dorsally and (j–s) point orally. Labels are as follows: de, dentine; en, enamel; lb, lamellar bone; pc, pulp cavity; wb, woven bone. Broken line arrows = the direction of the dorsal surface. Solid line arrows = oral surface. Scale bars = 500 µm. Line drawings redrawn from the following sources: psammosteid heterostracan Drepanaspis gemuendenensis [13]; Glyptolepis [14]; Laccognathus [15]; Cacops [16]; Captorhinus [D. Scott].

Figure 2.

Step-wise schematic of the outside-in hypothesis of tooth origins and phylogenetic distribution of odontode overgrowth. (a,b) Sequential movement of odontodes into the oral cavity. (c) Depiction of hypothetical variable selection pressures on different odontode regions, with the black oval showing hypothetical selection on the odontodes leading to marginal dentition, the teal oval showing hypothetical selection on the odontodes leading to coronoid or other non-marginal dentition on the mandible and the orange oval showing hypothetical selection on the odontodes leading to palatal dentition and preservation of odontode overgrowth in palatal dentition. (d) Differentiation of odontodes into regional dentitions. (e) Distribution of odontode overgrowth across vertebrates. Symbols indicate the location of the overgrowth pattern. Labels are as follows: cd, coronoid dentition; do, dermal odontode; md, marginal dentition; oro, oral odontode; pd, palatal dentition.