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Acoel development indicates the independent evolution of the bilaterian mouth and anus

Nature volume 456, pages 382–386 (2008)Cite this article

Abstract

Most bilaterian animals possess a through gut with a separate mouth and anus1. It is commonly believed that during the transition from radial to bilateral symmetry, both openings evolved simultaneously by the lateral closure of a slit-like blastopore1,2,3,4. Molecular phylogenies however, place the acoel flatworms, which have only one opening to their digestive system, as the sister group to all remaining Bilateria5,6,7. To address how this single body opening is related to the mouth and anus of the protostomes and deuterostomes, we studied the expression of genes involved in bilaterian foregut and hindgut patterning during the development of the acoel Convolutriloba longifissura. Here we show that the genes brachyury and goosecoid are expressed in association with the acoel mouth, suggesting that this single opening is homologous to the mouth of other bilaterians8. In addition, we find that the genes caudal, orthopedia and brachyury—which are expressed in various bilaterian hindguts8,9,10—are expressed in a small region at the posterior end of the animal, separated from the anterior oral brachyury-expressing region by a dorsal domain of ectodermal bmp2/4 expression. These results contradict the hypothesis that the bilaterian mouth and anus evolved simultaneously from a common blastoporal opening, and suggest that a through gut might have evolved independently in different animal lineages.

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Figure 1: Competing hypotheses for the evolution of the through gut and the position of acoel flatworms.
Figure 2: Gene expression during development of the acoel C. longifissura.
Figure 3: Position of the Metazoan mouth and anus relative to the expression of bra, gsc, cdx and otp.

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Acknowledgements

This work is supported by the National Science Foundation under the AToL program (EF05-31558) and NASA to M.Q.M. A.H. received further support from the Deutsche Forschungsgemeinschaft (HE5183/2-1). We thank K. Pang for improving the manuscript and A. Okuso for the drawings of the cnidarian and annelid.

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Authors and Affiliations

  1. Kewalo Marine Laboratory, PBRC, University of Hawaii, 41 Ahui Street, Honolulu, Hawaii 96813, USA ,

    Andreas Hejnol & Mark Q. Martindale

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  1. Andreas Hejnol
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  2. Mark Q. Martindale
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Correspondence to Andreas Hejnol.

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Hejnol, A., Martindale, M. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456, 382–386 (2008). https://doi.org/10.1038/nature07309

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