Skip to main content
SpringerLink
Log in

Concerning one obsolete tradition: Does gastrulation in sponges exist?

  • Ontogenesis and Evolution
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The analysis of comparative-embryological and molecular-biological data leads to the conclusion that universal basic mechanisms of morphogenesis occurred first in the evolution of animals in the ancestors of modern sponges and eumetazoans, which served as a basis of different evolution of individual development in Parazoa and Eumetazoa lines. In the former, morphogenesis in early embryogenesis led to formation of the water-current system as a means for capturing and delivery of food particles to different parts of the animal. In the latter, morphogenetic movements manifested themselves as gastrulation, during which the germ layers and the digestive system formed. The morphogenetic movements of cells in Metazoa emerged independently of cell specification. They are primary relative to cell differentiation. The unity of all Metazoa is based on the similarity of mechanisms of morphogenesis rather than on the presence of germ layers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adamska, M., Degnan, S.M., Green, K.M., Adamski, M., Larroux, C., and Degnan, B.M., Wnt and TGF-β expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning, PLoS One, 2007, vol. 2, no. 10, p. e1031. doi: 10.1371/journal. pone.0001031

    Article  PubMed  Google Scholar 

  • Adamska, M., Larroux, C., Adamski, M., Green, K., Lovas, E., Koop, D., Richards, G.S., Zwafink, C., and Degnan, B.M., Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica, Evol. Devel., 2010, vol. 12, no. 5, pp. 494–518.

    Article  CAS  Google Scholar 

  • Adamska, M., Degnan, B.M., Green, K., and Zwafink, C., What sponges can tell us about the evolution of developmental processes, Zoology, 2011, vol. 114, pp. 1–10.

    Article  PubMed  Google Scholar 

  • Adell, T. and Müller, W.E., Isolation and characterization of five Fox (Forkhead) genes from the sponge Suberites domuncula, Gene, 2004, vol. 334, pp. 35–46.

    Article  PubMed  CAS  Google Scholar 

  • Allman, G., On the anatomy and physiology of Cordylophora, a contribution to our knowledge of the tubularian zoophytes, Phil. Transact. Roy. Soc., 1853, vol. 143, pp. 367–384.

    Article  Google Scholar 

  • Beklemishev, V.N., Osnovy sravnitel’noi anatomii bespozvonochnykh (Fundamentals of Comparative Anatomy of Invertebrates), 1964.

    Google Scholar 

  • Delage, Y., Sur la place des Spongiaires dans la classification, C. R. Acad. Paris, 1898, vol. 126, pp. 545–548.

    Google Scholar 

  • Ereskovskii, A.V., Sravnitel’naya embriologiya gubok (Porifera) (Comparative Embryology of Sponges (Porifera)), St. Petersburg: Izd. St.-Peterb. Gos Univ., 2005.

    Google Scholar 

  • Ereskovsky, A.V. and Dondua, A.K., The problem of germ layers in sponges (Porifera) and some issues concerning early metazoan evolution, Zool. Anz., 2006, vol. 245, pp. 65–76.

    Article  Google Scholar 

  • Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., and Chera, S., Origins of neurogenesis, a cnidarian view, Dev. Biol., 2009, vol. 332, pp. 2–24.

    Article  PubMed  CAS  Google Scholar 

  • Gazave, E., Lapebie, P., Renard, E., Bezac, C., Boury-Esnault, N., Vacelet, J., Perez, T., Manuel, M., and Borchiellini, C., NK homeobox genes with choanocytespecific expression in homoscleromorph sponges, Dev. Genes Evol., 2008, vol. 218, pp. 479–489.

    Article  PubMed  CAS  Google Scholar 

  • Guder, C., Philipp, I., Lengfeld, T., Watanabe, H., Hobmayer, B., and Holstein, T.W., The Wnt code: cnidarians signal the way, Oncogene, 2006, vol. 25, pp. 7450–7460.

    Article  PubMed  CAS  Google Scholar 

  • Harcet, M., Roller, M., Cetkovic, H., Perina, D., Wiens, M., Müller, W.E., and Vlahovicek, K., Demosponge EST sequencing reveals a complex genetic toolkit of the simplest metazoans, Mol. Biol. Evol., 2010, vol. 27, pp. 2747–2756.

    Article  PubMed  CAS  Google Scholar 

  • Henkart, P., Humphreys, S., and Humphreys, T., Characterization of sponge aggregation factor. a unique proteoglycan complex, Biochemistry, 1973, vol. 12, pp. 3045–3050.

    Article  PubMed  CAS  Google Scholar 

  • Ivanov, P.P., Obshchaya i sravnitel’naya embriologiya (General and Comparative Embryology), Moscow, 1937.

    Google Scholar 

  • Ivanova-Kazas, O.M., Sravnitel’naya embriologiya bespozvonochnykh zhivotnykh (Comparative Embryology of Invertebrates), Novosibirsk: Nauka, 1975.

    Google Scholar 

  • Kumburegama, S., Wijesena, N., Xu, R., and Wikramanayake, A.H., Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/β-catenin-dependent endoderm cell fate specification in Nematostella vectensis (Anthozoa, Cnidaria): implications for the evolution of gastrulation, Evodevo, 2011, vol. 21, p. 2.

    Article  Google Scholar 

  • Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., et al., Unexpected complexity of the Wnt gene family in a sea anemone, Nature, 2005, vol. 433, pp. 156–160.

    Article  PubMed  CAS  Google Scholar 

  • Lapébie, P., Gazave, E., Ereskovsky, A., Derelle, R., Bézac, C., et al., WNT/β-Catenin signalling and epithelial patterning in the homoscleromorph sponge Oscarella, PLoS One, 2009, vol. 4, no. 6, p. e5823. doi: 10.1371

    Article  PubMed  Google Scholar 

  • Larroux, C., Fahey, B., Degnan, S.M., Adamski, M., Rokhsar, D.S., and Degnan, B.M., The NK homeobox gene cluster predates the origin of Hox genes, Curr. Biol., 2007, vol. 17, pp. 706–710.

    Article  PubMed  CAS  Google Scholar 

  • Larroux, C., Luke, G.N., Koopman, P., Rokhsar, D.S., Shimeld, S.M., and Degnan, B.M., Genesis and expansion of metazoan transcription factor gene classes, Mol. Biol. Evol., 2008, vol. 25, pp. 980–996.

    Article  PubMed  CAS  Google Scholar 

  • Manuel, M., Le Parco, Y., and Borchiellini, C., Comparative analysis of brachyury T-domains, with the characterization of two new sponge sequences, from a hexactinellid and a calcisponge, Gene, 2004, vol. 340, pp. 291–301.

    Article  PubMed  CAS  Google Scholar 

  • Mazza, M.E., Pang, K., Martindale, M.Q., and Finnerty, J.R., Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis, J. Exp. Zool. (Mol. Dev. Evol.), 2007, vol. 308B, pp. 494–506.

    Article  CAS  Google Scholar 

  • Müller, W.E.G., Cell membranes in sponges, Int. Rev. Cytol., 1982, vol. 77, pp. 129–181.

    Article  Google Scholar 

  • Müller, W.E.G. and Müller, I.M., Porifera: an enigmatic taxon disclosed by molecular biology/cell biology, in Porifera Research: Biodiversity, Innovation and Sustainability, Custodio, M.R., et al., Eds., 2007, pp. 89–106.

    Google Scholar 

  • Müller, W.E.G. and Zahn, R.K., Purification and characterization of a species-specific aggregation factor in sponges, Exp. Cell Res., 1973, vol. 80, pp. 95–104.

    Article  PubMed  Google Scholar 

  • Müller, W.E.G., Blumbach, B., Wagner-Hülsmann, C., and Lessel, U., Galectins in the phylogenetically oldest Metazoa, the Sponges (Porifera), Trends Glycosci. Glycotechnol., 1997, vol. 9, pp. 123–130.

    Article  Google Scholar 

  • Nichols, S.A., Dirks, W., Pearse, J.S., and King, N., Early evolution of animal cell signaling and adhesion genes, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 12451–12456.

    Article  PubMed  CAS  Google Scholar 

  • Oliveri, P., Walton, K.D., Davidson, E.H., and McClay, D.R., Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo, Development, 2006, vol. 133, pp. 4173–4181.

    Article  PubMed  CAS  Google Scholar 

  • Pancer, Z., Kruse, M., Müller, I., and Müller, W.E.G., On the origin of adhesion receptors of Metazoa: cloning of the integrin α subunit cDNA from the sponge Geodia cydonium, Mol. Biol. Evol., 1997, vol. 14, pp. 391–398.

    Article  PubMed  CAS  Google Scholar 

  • Pfeifer, K., Haasemann, M., Gamulin, V., Bretting, H., Fahrenholz, F., and Müller, W.E.G., S-Type lectins occur also in invertebrates: high conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge Geodia cydonium, Glycobiology, 1993, vol. 3, pp. 179–184.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, J.F. and Baxevanis, A.D., Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla, Biol. Direct., 2007, vol. 2, p. 37.

    Article  PubMed  Google Scholar 

  • Seravin, L.N. and Gudkov, A.V., Trichoplax adhaerens (tip Placozoa) odno iz samykh primitivnykh mnogokletochnykh zhivotnykh (Trichoplax adhaerens (Type Placozoa) Is One of the Most Primitive Multicellular Animals), St. Petersburg, 2005.

    Google Scholar 

  • Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M.E.A., et al., The Amphimedon queenslandica genome and the evolution of animal complexity, Nature, 2010, vol. 466, pp. 720–727.

    Article  PubMed  CAS  Google Scholar 

  • Svetlov, P.G., On the significance of the theory of germ layers in modern science, Arkh. Anat. Gist. Embr., 1963, vol. 44, no. 4, pp. 7–25.

    CAS  Google Scholar 

  • Vacelet, J. and Duport, E., Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae), Zoomorphology, 2004, vol. 123, pp. 179–190.

    Article  Google Scholar 

  • Vogt, C., Embryologie des salmons, in Histoire naturelle des poissons d’eau douce de l’Europe centrale par L. Agassiz, 2° Livraison, 1842.

    Google Scholar 

  • Wimmer, W., Blumbach, B., Diehl-Seifert, B., Koziol, C., Batel, R., Steffen, R., Müller, I.M., and Müller, W.G., Increased expression of integrin and receptor tyrosine kinase genes during autograft fusion in the sponge Geodia cydonium, Cell Adhes. Commun., 1999, vol. 7, pp. 111–124.

    Article  PubMed  CAS  Google Scholar 

  • Windsor, P.J. and Leys, S.P., Wnt signaling and induction in the sponge Aquiferous system: evidence for an ancient origin of the organizer, Evol. Dev., 2010, vol. 12, pp. 481–590.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. St. Petersburg State University, Universitetskaya nab. 7/9, St. Petersburg, 199034, Russia

    A. K. Dondua & R. P. Kostyuchenko

Authors
  1. A. K. Dondua
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. P. Kostyuchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. K. Dondua.

Additional information

Original Russian Text © A.K. Dondua, R.P. Kostyuchenko, 2013, published in Ontogenez, 2013, Vol. 44, No. 5, pp. 357–363.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dondua, A.K., Kostyuchenko, R.P. Concerning one obsolete tradition: Does gastrulation in sponges exist?. Russ J Dev Biol 44, 267–272 (2013). https://doi.org/10.1134/S1062360413050020

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360413050020

Keywords

Search

Navigation