Evolution of the new head by gradual acquisition of neural crest regulatory circuits

Research output: Contribution to journalArticle

Authors

  • Megan L. Martik
  • Shashank Gandhi
  • Benjamin R. Uy
  • J. Andrew Gillis
  • Stephen A. Green
  • Marcos Simoes-Costa
  • Marianne E. Bronner

External Institution(s)

  • California Institute of Technology
  • University of Cambridge
  • The University of Chicago
  • Cornell University

Details

Original languageEnglish (US)
Pages (from-to)675-678
Number of pages4
JournalNature
Volume574
Issue number7780
StatusPublished - Oct 31 2019
Peer-reviewedYes

Abstract

The neural crest, an embryonic stem-cell population, is a vertebrate innovation that has been proposed to be a key component of the ‘new head’, which imbued vertebrates with predatory behaviour1,2. Here, to investigate how the evolution of neural crest cells affected the vertebrate body plan, we examined the molecular circuits that control neural crest development along the anteroposterior axis of a jawless vertebrate, the sea lamprey. Gene expression analysis showed that the cranial subpopulation of the neural crest of the lamprey lacks most components of a transcriptional circuit that is specific to the cranial neural crest in amniotes and confers the ability to form craniofacial cartilage onto non-cranial neural crest subpopulations3. Consistent with this, hierarchical clustering analysis revealed that the transcriptional profile of the lamprey cranial neural crest is more similar to the trunk neural crest of amniotes. Notably, analysis of the cranial neural crest in little skate and zebrafish embryos demonstrated that the transcriptional circuit that is specific to the cranial neural crest emerged via the gradual addition of network components to the neural crest of gnathostomes, which subsequently became restricted to the cephalic region. Our results indicate that the ancestral neural crest at the base of the vertebrate lineage possessed a trunk-like identity. We propose that the emergence of the cranial neural crest, by progressive assembly of an axial-specific regulatory circuit, allowed the elaboration of the new head during vertebrate evolution.

Citation formats

APA

Martik, M. L., Gandhi, S., Uy, B. R., Gillis, J. A., Green, S. A., Simoes-Costa, M., & Bronner, M. E. (2019). Evolution of the new head by gradual acquisition of neural crest regulatory circuits. Nature, 574(7780), 675-678. https://doi.org/10.1038/s41586-019-1691-4

Harvard

Martik, ML, Gandhi, S, Uy, BR, Gillis, JA, Green, SA, Simoes-Costa, M & Bronner, ME 2019, 'Evolution of the new head by gradual acquisition of neural crest regulatory circuits', Nature, vol. 574, no. 7780, pp. 675-678. https://doi.org/10.1038/s41586-019-1691-4