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The evolutionary origin of chordate segmentation: revisiting the enterocoel theory

Abstract

One of the definitive characteristics of chordates (cephalochordates, vertebrates) is the somites, which are a series of paraxial mesodermal blocks exhibiting segmentation. The presence of somites in the basal chordate amphioxus and in vertebrates, but not in tunicates (the sister group of vertebrates), suggests that the tunicates lost the somites secondarily. Somites are patterned from anterior to posterior during embryogenesis. How such a segmental pattern evolved from deuterostome ancestors is mysterious. The classic enterocoel theory claims that chordate mesoderm evolved from the ancestral deuterostome mesoderm that organizes the trimeric body parts seen in extant hemichordates. Recent progress in molecular embryology has been tremendous, which has enabled us to test this classic theory. In this review, the history of the study on the evolution of the chordate mesoderm is summarized. This is followed by a review of the current understanding of genetic mapping on anterior/posterior (A/P) mesodermal patterning between chordates (cephalochordates, vertebrates) and a direct developing hemichordate (Saccoglossus kowalevskii). Finally, a possible scenario about the evolution of the chordate mesoderm from deuterostome ancestors is discussed.

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Acknowledgements

The author thanks Dr. Y. Henmi, H. Shimasaki, A. Maenaka and K. Shimohira of Kumamoto University for the collection of adult amphioxus in Amakusa, Kumamoto, Japan, and Dr. M. Okauchi of National Research Institute of Aquaculture for the algal culture. The author also thanks Dr. N. D. Holland, Dr. L. Z. Holland of UCSD and Dr. S. Green of Caltech for critically reading of the manuscript and for providing many suggestions for improvement, and Dr. S. Kuratani, Dr. Y. Oisi of RIKEN, Dr. C. J. Lowe of Stanford University, Dr. R. Cherny of Charles University and Dr. G. P. Wagner of Yale University for discussion. The author also thanks the reviewer for constructive comments on the manuscript. This research was supported by University of Fukui, Life Science Innovation Center.

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TO wrote the paper and performed all the experiments.

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Correspondence to Takayuki Onai.

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I declare I have no conflict of interests.

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Onai, T. The evolutionary origin of chordate segmentation: revisiting the enterocoel theory. Theory Biosci. 137, 1–16 (2018). https://doi.org/10.1007/s12064-018-0260-y

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  • DOI: https://doi.org/10.1007/s12064-018-0260-y

Keywords

  • Metamerism
  • Chordates
  • Deuterostomes
  • Somites
  • Mesoderm