Marrying the Old and the New: Evolutionary Innovation and Conservation in the Embryonic Derivation of the Vertebrate Skull
Evolutionary change in the morphology of the skull underlies every major adaptive transition in vertebrate history. Its developmental basis has been a subject of intense study for more than 150 years, yet many essential features remain unexplored in most taxa. A key unresolved issue, but one central to gaining an understanding of the genetic and developmental mechanisms that underlie cranial form and pattern, concerns the extent to which embryonic derivation of individual bones is evolutionarily conserved or labile. It is generally assumed that the pattern of embryonic origin of skull bones is highly conserved among vertebrates, but data from key groups, such as amphibians, are lacking. We performed long-term fate-mapping using GFP-transgenic Mexican axolotl (Ambystoma mexicanum) and African clawed frog (Xenopus laevis) to document the contribution of individual cranial neural crest streams to the adult osteocranium in these amphibians. We show that the axolotl pattern is strikingly similar to that reported in aminiotes; it likely represents the ancestral condition for tetrapods. Unexpectedly, we also show that the pattern in Xenopus is much different from that observed in all other vertebrates studied to date, including the axolotl. The pattern in Xenopus constitutes a unique, derived condition that evolved after the anuran characteristic of frogs. Embryonic derivation of the bony skull, while highly conserved among many species, exhibits extensive evolutionary innovation in at least one conspicuous vertebrate lineage. Such changes exemplify the phenomenon of "developmental system drift," in which interspecific divergence in developmental processes that underlie homologous characters occurs with little or no concomitant change in the resulting adult phenotype. They also reveal an underappreciated link between developmental mechanisms and life history evolution.