Developmental and evolutionary origins of the vertebrate dentition: molecular controls for spatio-temporal organisation of tooth sites in osteichthyans

Abstract

The rainbow trout (Oncorhynchus mykiss) as a developmental model surpasses both zebrafish and mouse for a more widespread distribution of teeth in the oro-pharynx as the basis for general vertebrate odontogenesis, one in which replacement is an essential requirement. Studies on the rainbow trout have led to the identification of the initial sequential appearance of teeth, through differential gene expression as a changing spatio-temporal pattern, to set in place the primary teeth of the first generation, and also to regulate the continuous production of replacement tooth families. Here we reveal gene expression data that address both the field and clone theories for patterning a polyphyodont osteichthyan dentition. These data inform how the initial pattern may be established through up-regulation at tooth loci from a broad odontogenic band. It appears that control and regulation of replacement pattern resides in the already primed dental epithelium at the sides of the predecessor tooth. A case is presented for the developmental changes that might have occurred during vertebrate evolution, for the origin of a separate successional dental lamina, by comparison with an osteichthyan tetrapod dentition (Ambystoma mexicanum). The evolutionary origins of such a permanent dental lamina are proposed to have occurred from the transient one demonstrated here in the trout. This has implications for phylogenies based on the homology of teeth as only those developed from a dental lamina. Utilising the data generated from the rainbow trout model, we propose this as a standard for comparative development and evolutionary theories of the vertebrate dentition.