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

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.

References

  1. Nielsen, C. Animal Evolution 2nd edn (Oxford Univ. Press, 2001)

    Google Scholar 

  2. Arendt, D. & Nübler-Jung, K. Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech. Dev. 61, 7–21 (1997)

    Article  CAS  PubMed  Google Scholar 

  3. Remane, A. Die Entstehung der Metamerie der Wirbellosen. Zool. Anz. 14, 18–23 (1950)

    Google Scholar 

  4. Sedgwick, W. On the origin of metameric segmentation and some other morphological questions. Q. J. Microsc. Sci. 24, 43–82 (1884)

    Google Scholar 

  5. Baguñá, J. & Riutort, M. The dawn of bilaterian animals: the case of acoelomorph flatworms. Bioessays 26, 1046–1057 (2004)

    Article  PubMed  Google Scholar 

  6. Ruiz-Trillo, I. et al. Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 283, 1919–1923 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Wallberg, A., Curini-Galletti, M., Ahmadzadeh, A. & Jondelius, U. Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades. Zool. Scr. 36, 509–523 (2007)

    Article  Google Scholar 

  8. Arendt, D., Technau, U. & Wittbrodt, J. Evolution of the bilaterian larval foregut. Nature 409, 81–85 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Simeone, A. et al. Orthopedia, a novel homeobox-containing gene expressed in the developing CNS of both mouse and Drosophila . Neuron 13, 83–101 (1994)

    Article  CAS  PubMed  Google Scholar 

  10. Wu, L. H. & Lengyel, J. A. Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125, 2433–2442 (1998)

    CAS  PubMed  Google Scholar 

  11. Grobben, K. Die systematische Einteilung des Tierreichs. Verh. Zool. Bot. Ges. Wien 58, 491–511 (1908)

    Google Scholar 

  12. von Graff, L. Die Organisation der Turbellaria Acoela (von Wilhelm Engelmann, 1891)

    Google Scholar 

  13. Haeckel, E. Die Gastraea-Theorie, die phylogenetische Classification des Thierreiches und die Homologie der Keimblätter. Jena. Z. Naturwiss. 8, 1–55 (1874)

    Google Scholar 

  14. Hyman, L. H. The Invertebrates. Vol II. Platyhelminthes and Rhynchocoela (McGraw-Hill, 1951)

    Google Scholar 

  15. Jägersten, G. On the early phylogeny of the Metazoa: the bilatero-gastraea theory. Zool. Bidr. Uppsala. 30, 321–354 (1955)

    Google Scholar 

  16. Salvini-Plawen, L. On the origin and evolution of the lower Metazoa. Z. Zool. Syst. Evolutionsforsch 16, 40–88 (1978)

    Article  Google Scholar 

  17. Haszprunar, G. Plathelminthes and Plathelminthomorpha—paraphyletic taxa. J. Zool. Syst. Evol. Res. 34, 41–48 (1996)

    Article  Google Scholar 

  18. Marcellini, S. When Brachyury meets Smad1: the evolution of bilateral symmetry during gastrulation. Bioessays 28, 413–420 (2006)

    Article  CAS  PubMed  Google Scholar 

  19. Tagawa, K., Humphreys, T. & Satoh, N. Novel pattern of Brachyury gene expression in hemichordate embryos. Mech. Dev. 75, 139–143 (1998)

    Article  CAS  PubMed  Google Scholar 

  20. Lartillot, N., Lespinet, O., Vervoort, M. & Adoutte, A. Expression pattern of Brachyury in the mollusc Patella vulgata suggests a conserved role in the establishment of the AP axis in Bilateria. Development 129, 1411–1421 (2002)

    CAS  PubMed  Google Scholar 

  21. Neidert, A. H., Panopoulou, G. & Langeland, J. A. Amphioxus goosecoid and the evolution of the head organizer and prechordal plate. Evol. Dev. 2, 303–310 (2000)

    Article  CAS  PubMed  Google Scholar 

  22. Fröbius, A. C. & Seaver, E. C. ParaHox gene expression in the polychaete annelid Capitella sp. I . Dev. Genes Evol. 216, 81–88 (2006)

    Article  PubMed  Google Scholar 

  23. Lowe, C. J. et al. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113, 853–865 (2003)

    Article  CAS  PubMed  Google Scholar 

  24. Christiaen, L. et al. Evolutionary modification of mouth position in deuterostomes. Semin. Cell Dev. Biol. 18, 502–511 (2007)

    Article  PubMed  Google Scholar 

  25. Henry, J. Q., Martindale, M. Q. & Boyer, B. C. The unique developmental program of the acoel flatworm, Neochildia fusca . Dev. Biol. 220, 285–295 (2000)

    Article  CAS  PubMed  Google Scholar 

  26. Denes, A. S. et al. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129, 277–288 (2007)

    Article  CAS  PubMed  Google Scholar 

  27. Lowe, C. J. et al. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 4, e291 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  28. Reisinger, E. Allgemeine Morphologie der Metazoa. Fortschr. Zool. 13, 1–82 (1961)

    Google Scholar 

  29. Dunn, C. W. et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Martindale, M. Q., Pang, K. & Finnerty, J. R. Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131, 2463–2474 (2004)

    Article  CAS  PubMed  Google Scholar 

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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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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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