Letter

Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest

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Accepted:
Published online:

Abstract

The enteric nervous system of jawed vertebrates arises primarily from vagal neural crest cells that migrate to the foregut and subsequently colonize and innervate the entire gastrointestinal tract. Here we examine development of the enteric nervous system in the basal jawless vertebrate the sea lamprey (Petromyzon marinus) to gain insight into its evolutionary origin. Surprisingly, we find no evidence for the existence of a vagally derived enteric neural crest population in the lamprey. Rather, labelling with the lipophilic dye DiI shows that late-migrating cells, originating from the trunk neural tube and associated with nerve fibres, differentiate into neurons within the gut wall and typhlosole. We propose that these trunk-derived neural crest cells may be homologous to Schwann cell precursors, recently shown in mammalian embryos to populate post-embryonic parasympathetic ganglia1,2, including enteric ganglia3. Our results suggest that neural-crest-derived Schwann cell precursors made an important contribution to the ancient enteric nervous system of early jawless vertebrates, a role that was largely subsumed by vagal neural crest cells in early gnathostomes.

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Acknowledgements

We thank C. Baker, M. Piacentino, and L. Kerosuo for discussion, and M. Martik, M. Simoes-Costa, and R. Uribe for their comments on this manuscript.

Author information

Author notes

    • Stephen A. Green
    •  & Benjamin R. Uy

    These authors contributed equally to this work.

Affiliations

  1. Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, USA

    • Stephen A. Green
    • , Benjamin R. Uy
    •  & Marianne E. Bronner

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Contributions

The project was conceived by M.E.B., and analyses were designed by S.A.G. and M.E.B. Descriptive analyses of enteric neurons were performed by S.A.G. Cranial DiI labelling was performed by B.R.U., M.E.B., and S.A.G. Trunk DiI labelling was performed by B.R.U., S.A.G. and M.E.B. Surgeries were performed, imaged and analysed by S.A.G. and B.R.U. Schematics were drawn by S.A.G. The manuscript was written by M.E.B., S.A.G. and B.R.U.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Marianne E. Bronner.

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