Tooth development in frogs: Implications for the re-evolution of lost mandibular teeth and the origin of a morphological innovation

Abstract

Teeth have been a prominent feature of most vertebrates for 400 million years, and the core regulatory network underlying embryonic tooth formation is deeply conserved from fishes to amniotes. In frogs, however, odontogenesis is delayed, occurring instead during the postembryonic metamorphosis. Nearly all adult frogs have teeth on the upper jaw and lack lower jaw dentition, but a single species re-evolved mandibular teeth. Developmental-genetic mechanisms that underlie tooth formation in frogs are poorly understood, including whether an ancestral program is partially retained in the lower jaw that could facilitate the evolutionary reappearance of lost mandibular teeth. Using a developmental series of an unconventional model species, we assessed 1) if the gene network underlying odontogenic competence is conserved in the late-forming teeth of frogs; 2) if unique keratinized mouthparts, which function as an alternative feeding tool in anuran larvae, impede tooth induction; and 3) if transient tooth rudiments form in the anuran mandible. The tooth development network is conserved in the frog upper jaw, which displays dental expression patterns comparable to those of other vertebrates. There is, however, no evidence of tooth development in the mandible. Teeth emerge before keratinized mouthparts degenerate, but their location may be spatially constrained by keratin, and gene expression patterns of keratinized mouthparts and teeth overlap. We hypothesize that the novel mouthparts of tadpoles did not arise de novo but instead originated by partially co-opting the developmental program that typically mediates true tooth development.