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An evolutionarily conserved odontode gene regulatory network underlies head armor formation in suckermouth armored catfish

Odontodes, i.e., teeth and tooth-like structures, consist of a pulp cavity and dentine covered by a mineralized cap. These structures first appeared on the outer surface of vertebrate ancestors and were repeatedly lost and gained across vertebrate clades; yet, the underlying genetic mechanisms and trajectories of this recurrent evolution remain long-standing mysteries. Here, we established suckermouth armored catfish (Ancistrus sp.; Loricariidae), which have uniquely evolved dermal odontodes (dermal denticles) all over most of their body surface, as an experimental model animal amenable to genetic manipulation for studying odontode development. Our histological analysis showed that suckermouth armored catfish develop dermal denticles through the previously defined odontode developmental stages. De novo transcriptomic profiling identified the conserved odontode genetic regulatory network (oGRN) as well as unique expression of paired like homeodomain 2 (pitx2), previously characterized as an early regulator of oGRN in teeth, in developing dermal denticles. Knockdown of pitx2 perturbed formation of the epithelial placode of dermal denticles and altered expression oGRN genes. By comprehensively identifying the genetic program for dermal odontode development in suckermouth armored catfish, this work illuminates how dermal odontodes independently evolved and diverged in distinct teleost lineages. Summary statement Cranial dermal denticles in suckermouth armored catfish develop via an evolutionarily conserved and unique odontode genetic regulatory network.