Evolution of ectomesenchymal potential of the cranial neural crest
Updated: Jun 19, 2021
How did the cranial neural crest gain its ability to form bone and cartilage?
The neural crest is a vertebrate-specific embryonic stem cell population that was long thought to have played a critical role in vertebrate evolution by giving rise to the bone and cartilage of the jaw, thereby facilitating active predatory behavior. The subpopulation of the neural crest that contributes to the jaw is designated as cranial neural crest, which is genetically unique from the subpopulation originating in the lower parts of the embryo, known as trunk neural crest. Contribution of the neural crest towards the craniofacial architecture of vertebrates led to the genesis of the “new head hypothesis,” according to which the possession of distinct craniofacial derivatives enabled diversification of the brain and acquisition of predatory behavior in vertebrates, as compared to filter feeding chordates.
To address the question of how evolution of the neural crest impacted the vertebrate body plan, I collaborated with Dr. Megan Martik, now Assistant professor at University of California, Berkeley (Martik Lab). We examined the molecular circuits that control neural crest development along the anteroposterior axis of a jawless vertebrate, the sea lamprey (Martik et al., Nature, 2019).
Gene expression analyses showed that the lamprey cranial neural crest lacks most components of an amniote cranial-specific transcriptional circuit that confers the ability to form craniofacial cartilage onto other neural crest populations. Consistent with this, hierarchical clustering revealed that the transcriptional profile of the lamprey cranial crest is more similar to the amniote trunk crest. Analysis of the cranial neural crest in little skate and zebrafish embryos demonstrated that the cranial-specific transcriptional circuit emerged via a gradual addition of network components to the neural crest of gnathostomes, which subsequently became restricted to the cranial region. Our results indicate that the ancestral neural crest at the base of vertebrates possessed a trunk-like identity, and we propose that the emergence of the cranial neural crest, by progressive assembly of a novel axial-level-specific regulatory circuit, allowed for the elaboration of the New Head during vertebrate evolution.