Gastrulation in Calcareous Sponges: In Search of Haeckel's Gastraea
Abstract
Haeckel's studies of development in calcareous sponges (1872) led him to develop the "Gastraea Theory," which proposes that the ancestral mode of germ layer formation, or gastrulation, was by invagination to produce a functional gut. His observations that gastrulation in the Calcarea occurs by invagination of a ciliated larva upon settlement and metamorphosis were supported by remarkable photomicrographs of the stage by Hammer in 1908. Although no later work found the same stage, these concepts are repeated in texts today. We have re-examined embryogenesis and metamorphosis in Sycon sp. cf. S. raphanus in order to understand when gastrulation occurs. Almost all larvae settle on their ciliated anterior pole and metamorphose into a bilayered juvenile whose interior cells rapidly differentiate into choanocytes and other cells of the young sponge. After a four-year search we have found the transitory stage shown by Hammer in which the anterior cells invaginate into the posterior half of the larva. The hole closes and it is not until some days later that the sponge forms an osculum at its apical pole. To understand whether invagination comprises gastrulation and if the hole can be considered to be a blastopore we have carried out a review of the literature dealing with this brief moment in calcaronean sponge development. Despite the intrigue of this type of metamorphosis, we conclude that gastrulation occurs earlier, during formation of the two cellular regions of the larva, and that metamorphosis involves the reorganization of these already differentiated regions. Considering the pivotal position occupied by the Calcarea as the possible sister-group to all other Metazoa, these results call for a reassessment of germ layer formation and of the relationships of the primary germ layers among basal metazoan phyla.
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Some sponge larvae settle with the blastopore facing downwards.
“In line with this, some sponge larvae settle with the blastopore facing downwards [41].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [41]
Cites
Systema Porifera. A Guide to the Classification of Sponges
Hooper, J. N. A., & van Soest, R. W. M. (2002) · Springer eBooks · doi:10.1007/978-1-4615-0747-5_1 · Cited by 1,191 · see citing works
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041 · see citing works
Settlement and metamorphosis of marine invertebrate larvae
Chia, F., & Rice, M. E. (1978) · Cited by 636 · see citing works
Embryology: constructing the organism
(1998) · Choice Reviews Online · doi:10.5860/choice.35-3280 · Cited by 423 · see citing works
Gastrulation: from cells to embryo
(2005) · Choice Reviews Online · doi:10.5860/choice.42-4013 · Cited by 414 · see citing works
Medina, M., Collins, A. G., Silberman, J. D., & Sogin, M. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171316998 · Cited by 395 · see citing works
Sponge paraphyly and the origin of Metazoa
Borchiellini, C., Manuel, M., Alivon, E., Boury-Esnault, N., Vacelet, J., & Le Parco, Y. (2001) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2001.00244.x · Cited by 275 · see citing works
Heterochrony and the Phylotypic Period
Richardson, M. K. (1995) · Developmental Biology · doi:10.1006/dbio.1995.8041 · Cited by 190 · see citing works
Manuel, M., Borchiellini, C., Alivon, E., Parco, Y. L., Vacelet, J., & Boury‐Esnault, N. (2003) · Systematic Biology · doi:10.1080/10635150309322 · Cited by 158 · see citing works
Leys, S. P., & Degnan, B. M. (2002) · Invertebrate Biology · doi:10.1111/j.1744-7410.2002.tb00058.x · Cited by 138 · see citing works
Self-citationKruse, M., Leys, S. P., Müller, I. M., & Müller, W. E. G. (1998) · Journal of Molecular Evolution · doi:10.1007/pl00006353 · Cited by 119 · see citing works
Self-citationLankester, E. R. (1877) · Journal of Cell Science · doi:10.1242/jcs.s2-17.68.399 · Cited by 106 · see citing works
Boury‐Esnault, N., Efremova, S. M., Bézac, C., & Vacelet, J. (1999) · Invertebrate Reproduction & Development · doi:10.1080/07924259.1999.9652385 · Cited by 90 · see citing works
Barnes, R. D., & Dougherty, E. C. (1964) · The American Midland Naturalist · doi:10.2307/2423524 · Cited by 70 · see citing works
Gastrulation and the evolution of development
Wolpert, L. (1992) · Development · doi:10.1242/dev.116.supplement.7 · Cited by 63 · see citing works
Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea)
Franzen, W. (1988) · Zoomorphology · doi:10.1007/bf00312218 · Cited by 62 · see citing works
Adell, T., Grebenjuk, V. A., Wiens, M., & M�ller, W. E. G. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0345-5 · Cited by 61 · see citing works
Phylogeny and evolution of calcareous sponges
Manuel, M. (2006) · Canadian Journal of Zoology · doi:10.1139/z06-005 · Cited by 53 · see citing works
The Germ-Cells, Fertilization. and Early Development of Grantia (Sycon) compressa*
Gatenby, J. B., & Goodrich, E. S. (1920) · Zoological Journal of the Linnean Society · doi:10.1111/j.1096-3642.1920.tb01790.x · Cited by 52 · see citing works
Amano, S., & Hori, I. (2001) · Biological Bulletin · doi:10.2307/1543082 · Cited by 50 · see citing works
Üntersuchungen über den Bau und die Entwicklung der Spongien
Schulze, F. E. (1877) · Medical Entomology and Zoology · Cited by 48 · see citing works
Amano, S., & Hori, I. (1996) · Biological Bulletin · doi:10.2307/1542536 · Cited by 44 · see citing works
L'Ovogénèse, la fécondation et les premiers stades du développement des éponges calcaires
Duboscq, O., & Tuzet, O. (1937) · Medical Entomology and Zoology · Cited by 42 · see citing works
Metamorphosis of calcareous sponges I. Ultrastructure of free-swimming larvae
Amano, S., & Hori, I. (1992) · Invertebrate Reproduction & Development · doi:10.1080/07924259.1992.9672223 · Cited by 42 · see citing works
Class Calcarea Bowerbank, 1864
Manuel, M., Borojević, R., Boury‐Esnault, N., & Vacelet, J. (2002) · Springer eBooks · doi:10.1007/978-1-4615-0747-5_115 · Cited by 41 · see citing works
Metamorphosis of calcareous sponges II. Cell rearrangement and differentiation in metamorphosis
Amano, S., & Hori, I. (1993) · Invertebrate Reproduction & Development · doi:10.1080/07924259.1993.9672327 · Cited by 37 · see citing works
Schmidt, O. (1864) · Cited by 31 · see citing works
Manuel, M., Parco, Y. L., & Borchiellini, C. (2004) · Gene · doi:10.1016/j.gene.2004.07.021 · Cited by 27 · see citing works
SPONGE LARVAL PHOTOTAXIS: A COMPARATIVE STUDY
Elliott, G. R., & Leys, S. P. (2004) · Cited by 26 · see citing works
Self-citationMinchin, E. A. (1897) · Proceedings of the Royal Society of London · doi:10.1098/rspl.1896.0013 · Cited by 23 · see citing works
Characteristics Of Metazoan Development
Brusca, G. J., Brusca, R. C., & Gilbert, S. F. (1997) · Works - Scholarship, Research, & Creative Expression (Swarthmore College) · Cited by 19 · see citing works
Invertebrate Zoology: A Laboratory Manual
WALLACE, R. L., & Taylor, W. K. (1996) · Cited by 8 · see citing works
Johnson, M. F. (1979) · Occidental College Scholar (Occidental College) · Cited by 6 · see citing works
Gastrulation inHalocordyle disticha(Hydrozoa, Athecata)
Thomas, M. B., Edwards, N. C., & Norris, T. A. (1987) · International Journal of Invertebrate Reproduction and Development · doi:10.1080/01688170.1987.10510305 · Cited by 3 · see citing works
Denis, H. (1997) · médecine/sciences · doi:10.4267/10608/591 · Cited by 2 · see citing works
Flagged first, then by citations
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Domazet‐Lošo, T., & Tautz, D. (2010) · Nature · doi:10.1038/nature09632 · Cited by 445 · see citing works
Domazet‐Lošo, T., Brajković, J., & Tautz, D. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.08.014 · Cited by 409 · see citing works
Six major steps in animal evolution: Are we derived sponge larvae?
Nielsen, C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00231.x · Cited by 343 · see citing works
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Maldonado, M. (2006) · Canadian Journal of Zoology · doi:10.1139/z05-177 · Cited by 282 · see citing works
From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system
Arendt, D., Tosches, M. A., & Marlow, H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.15 · Cited by 279 · see citing works
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
Deep Phylogeny and Evolution of Sponges (Phylum Porifera)
Wörheide, G., Dohrmann, M., Erpenbeck, D., Larroux, C., Maldonado, M., Voigt, O., Borchiellini, C., & Lavrov, D. V. (2012) · Advances in Marine Biology · doi:10.1016/b978-0-12-387787-1.00007-6 · Cited by 166 · see citing works
The origin of Metazoa: a transition from temporal to spatial cell differentiation
Mikhailov, K. V., Константинова, А. В., Nikitin, M. A., Troshin, P. V., Rusin, L. Y., Lyubetsky, V., Panchin, Y. V., Mylnikov, A. P., Moroz, L. L., Kumar, S., et al. (2009) · BioEssays · doi:10.1002/bies.200800214 · Cited by 151 · see citing works
Cavalier‐Smith, T. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0476 · Cited by 142 · see citing works
Leininger, S., Adamski, M., Bergum, B., Guder, C., Liu, J., Laplante, M., Bråte, J., Hoffmann, F., Fortunato, S., Jordal, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4905 · Cited by 136 · see citing works
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · see citing works
Evolutionary origin of gastrulation: insights from sponge development
Nakanishi, N., Sogabe, S., & Degnan, B. M. (2014) · BMC Biology · doi:10.1186/1741-7007-12-26 · Cited by 106 · see citing works
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Leys, S. P., & Ereskovsky, A. V. (2006) · Canadian Journal of Zoology · doi:10.1139/z05-170 · Cited by 100 · see citing works
Self-citationEreskovsky, A. V., Borchiellini, C., Gazave, E., Ivanišević, J., Lapébie, P., Pérez, T., Renard, E., & Vacelet, J. (2009) · BioEssays · doi:10.1002/bies.080058 · Cited by 93 · see citing works
Fortunato, S., Adamski, M., Bergum, B., Guder, C., Jordal, S., Leininger, S., Zwafink, C., Rapp, H. T., & Adamska, M. (2012) · EvoDevo · doi:10.1186/2041-9139-3-14 · Cited by 75 · see citing works
Wanninger, A. (2015) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2015.00054 · Cited by 71 · see citing works
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What sponges can tell us about the evolution of developmental processes
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The problem of germ layers in sponges (Porifera) and some issues concerning early metazoan evolution
Ereskovsky, A. V., & Dondua, A. K. (2006) · Zoologischer Anzeiger · doi:10.1016/j.jcz.2006.04.002 · Cited by 63 · see citing works
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Sheng, G., Arias, A. M., & Sutherland, A. E. (2021) · Science · doi:10.1126/science.abg1727 · Cited by 62 · see citing works
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Yamamoto, M. P. (2004) · Springer eBooks · doi:10.1007/978-3-662-10360-9_19 · Cited by 41 · see citing works
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Lanna, E., & Klautau., M. R. L. (2025) · Molecular Reproduction and Development · doi:10.1002/mrd.70060 · Cited by 2 · see citing works
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El-Bawab, F. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814114-4.00004-7 · Cited by 1 · see citing works
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Opisthokonta Cavalier-Smith 1987, emend. Adl et al., 2005
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- Authors
- Leys, S. P.
- Affiliations
- University of Alberta (CA)
- Corresponding author
- Leys, S. P.
- ORCID
- Leys, S. P.
- Venue
- Integrative and Comparative Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-04-01
- Volume
- 45
- Issue
- 2
- Pages
- 342-351
- ISSN
- 1540-7063 (ISSN-L)
- 1557-7023
- OpenAlex
- W2104914324
- Cited by
- 57
- References
- 36
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2022: 2 · 2021: 1 · 2020: 2 · 2019: 5 · 2018: 1 · 2017: 1 · 2016: 3 · 2015: 8 · 2014: 3 · 2013: 2 · 2012: 5
- FWCI
- 2.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Integrative and Comparative Biology (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
- Keywords
- gastrulation, calcareous sponges, germ layer formation, metamorphosis, blastopore, osculum, choanocytes, embryonic development, metazoan origin
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