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Evolution of the bilaterian larval foregut

Abstract

Bilateria are subdivided into Protostomia and Deuterostomia1,2. Indirect development through primary, ciliary larvae occurs in both of these branches; however, the closing blastopore develops into mouth and anus in Protostomia and into anus only in Deuterostomia. Because of this important difference in larval gut ontogeny, the tube-shaped guts in protostome and deuterostome primary larvae are thought to have evolved independently2,3. To test this hypothesis, we have analysed the expression of brachyury, otx and goosecoid homologues in the polychaete Platynereis dumerilii4, which develops by means of a trochophora larva—the primary, ciliary larva prototypic for Protostomia2. Here we show that brachyury expression in the ventral portion of the developing foregut in Platynereis and also otx expression along ciliated bands in the mouth region of the trochophora larva parallels expression in primary larvae in Deuterostomia5,6,7,8,9. In addition, goosecoid expression in the foregut of Platynereis mirrors the function in higher Deuterostomia10. We present molecular evidence for the evolutionary conservation of larval foreguts and mouth regions of Protostomia and Deuterostomia. Our data indicate that Urbilateria, the common bilaterian ancestors, developed through a primary, ciliary larva that already possessed a tripartite tube-shaped gut.

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Figure 1: Different ontogeny but similar body plans of Protostomia and Deuterostomia primary larvae as shown by similar expression of brachyury in the ventral developing foregut and otx in ciliary bands bordering the mouth region.
Figure 2: Expression of Pd-bra.
Figure 3: Expression of Pd-otx.
Figure 4: Expression of Pd-gsc.

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Acknowledgements

We thank A. A. W. Dorresteijn, F. Loosli and R. Rieger for discussions; S. Cohen, B. Hobmayer, T. Holstein, T.-E. Rusten and L. Teixeira for comments on the manuscript; and members of the Wittbrodt laboratory for support. cDNA libraries were provided by C. Heimann, University of Mainz. This work was supported by a fellowship from the European Molecular Biology Organisation (EMBO) (D.A.), and by grants from the Deutsche Forschungsgemeinschaft (DFG) Schwerpunkt “Evolution entwicklungsbiologischer Prozesse” (U.T. and J.W.).

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Correspondence to Joachim Wittbrodt.

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Arendt, D., Technau, U. & Wittbrodt, J. Evolution of the bilaterian larval foregut. Nature 409, 81–85 (2001). https://doi.org/10.1038/35051075

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