The Origin of Tooth Replacement: Three-dimensional Synchrotron Histology Visualizes the Dental Development of Silurian Stem Osteichthyans

Mechanisms of tooth replacement distribute incongruently among extant gnathostomes (jawed vertebrates): a permanent tooth-generating dental lamina exists in chondrichthyans (cartilaginous fish) and tetrapods but not teleosts, whereas tooth shedding by basal hard tissue resorption occurs in tetrapods and teleosts but not chondrichthyans. Theories about the evolution of tooth development have been biased towards the chondrichthyan conveyor-belt replacement, since there has been no fossil evidence for the origin of osteichthyan (bony fish and tetrapods) tooth replacement until now. 3D virtual dissections with submicron-scale resolution, based on propagation phase contrast synchrotron microtomography (PPC-SRµCT), reveal the growth history of the dentitions of Andreolepis and Lophosteus, 423-Myr-old Silurian stem osteichthyans close to the common ancestor of tetrapods and teleosts. Their marginal jawbones and “tooth cushions” (possible homologues of coronoids) shed teeth by in situ cyclic basal resorption, the earliest examples of osteichthyan-style tooth replacement. The replacement cycles were site-autonomic, and occurred in broad irregular multi-row tooth fields, including at sites separated from the margin of the bone by intervening teeth, showing that the production of replacement teeth did not occur in a single deep dental lamina, but in pockets associated with each tooth, as in many teleosts. It suggests that the functionally and anatomically similar laminae of chondrichthyans and tetrapods are convergent. The marginal jaw bones of both genera carry an initial non-shedding dentition arranged in alternate transverse files, labial to the shedding tooth field, overgrown by later dermal ornament and probably not belonging to the oral domain, but bearing in vivo biting damage showing that they functioned as teeth. The most lingual of these odontodes have been resorbed apically and are overlain by shedding teeth. The firstgeneration teeth on the tooth cushions display basal resorption in Andreolepis, but semi-basal resorption in Lophosteus. The latter leaves a basal dentine ring from each tooth, implying only odontoclasts are involved in the semi-basal resorption, which is probably the first step towards evolving a site-specific resorption. The polarized displacement of each generation of resorption surfaces reflects the fact that the cyclic replacement, as well as the sequential addition of tooth sites, is closely related to bone growth. Resorption surfaces and growth arrest surfaces also record the life history and the replacement rate. These data provide unique insights into the origin of osteichthyan tooth replacement.