Phenogenetic drift in evolution: the changing genetic basis of vertebrate teeth

Vertebrate mineralized tissues are vital to the adaptive evolution of various traits. Among these traits is the tooth, which consists of two characteristic mineralized tissues, a highly mineralized surface layer (enamel in tetrapods and enameloid in fish) and a softer body (dentin), both supported by basal bone. However, enamel and enameloid are significantly different in development, and dentin shows many histological variations; hence their evolution has been intensively studied. Nevertheless, their genetic basis has been revealed only in tetrapods. We previously reported that many genes involved in tetrapod tissue mineralization arose from a common ancestor and constitute the secretory calcium-binding phosphoprotein (SCPP) gene family. Now we show that teleost fish also use many SCPPs for enameloid and dentin mineralization, but none of these directly corresponds to tetrapod SCPPs. This finding suggests that teleost and tetrapod SCPP genes have experienced independent parallel duplication histories. Thus, through phenogenetic drift, the tooth has remained a stable trait in jawed vertebrates, while evolving distinct genetic bases in teleosts and tetrapods. The characteristics of teleost SCPP genes and their expression domains in tooth development suggest the possibility that enameloid arose from dentin and enamel from enameloid more than once in vertebrate evolution. In fugu (puffer fish), expression of SCPP genes is also detected in an unusual beak-like structure that shelters numerous teeth. Their expression pattern suggests that the jaw consists of the dentin beak and supportive bone. These findings illustrate the complexity of the homology concept in understanding evolution, particularly the evolution of mineralized tissues.