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Evolution of the bilaterian mouth and anus

Abstract

It is widely held that the bilaterian tubular gut with mouth and anus evolved from a simple gut with one major gastric opening. However, there is no consensus on how this happened. Did the single gastric opening evolve into a mouth, with the anus forming elsewhere in the body (protostomy), or did it evolve into an anus, with the mouth forming elsewhere (deuterostomy), or did it evolve into both mouth and anus (amphistomy)? These questions are addressed by the comparison of developmental fates of the blastopore, the opening of the embryonic gut, in diverse animals that live today. Here we review comparative data on the identity and fate of blastoporal tissue, investigate how the formation of the through-gut relates to the major body axes, and discuss to what extent evolutionary scenarios are consistent with these data. Available evidence indicates that stem bilaterians had a slit-like gastric opening that was partially closed in subsequent evolution, leaving open the anus and most likely also the mouth, which would favour amphistomy. We discuss remaining difficulties, and outline directions for future research.

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Fig. 1: Theories for the evolutionary origin of mouth and anus in the bilaterians.
Fig. 2: Two conflicting possibilities of how the body axes in cnidarians and bilaterians are related, based on different interpretations of axial Hox, canonical Wnt and Bmp activity.
Fig. 3: Fates of the blastoporal opening and of the periblastoporal tissue.
Fig. 4: Ancestral state reconstruction of the fate of blastoporal tissue.
Fig. 5: Gene expression in the circumblastoporal tissue.
Fig. 6: Morphology of the central nervous system in bilaterians and the evolution of a bilaterian ancestor from the trochaea.

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Acknowledgements

We thank R. Schnabel (TU Braunschweig, Germany) for new information about Caenorhabditis embryology.

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C.N. conceived the paper and wrote the sections on morphology and embryology in the Supplementary Information. T.B. wrote the sections gene expression and performed ancestral state reconstructions. D.A. elaborated and illustrated options for mouth and anus evolution. All three authors wrote the main paper and discussed the whole manuscript.

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Correspondence to Claus Nielsen, Thibaut Brunet or Detlev Arendt.

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Nielsen, C., Brunet, T. & Arendt, D. Evolution of the bilaterian mouth and anus. Nat Ecol Evol 2, 1358–1376 (2018). https://doi.org/10.1038/s41559-018-0641-0

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