Abstract
The process of inversion observed during the development of Calcaronea (Calcarea, Porifera) species is a unique and remarkable event in the Metazoa. However, few studies have focused on the embryogenesis of Calcaronea species or on the ultrastructure of their larva and its accessory epithelium, the so-called placental membrane. Herein, using light and electron microscopy, we describe the embryogenesis and ultrastructure of the amphiblastula of Paraleucilla magna (Porifera, Calcarea, Calcaronea). It was observed that the cleavage in this species is of the table-like palyntomy type, typical of calcaroneans. Cleavage leads to the formation of a stomoblastula, which becomes inverted in the mesohyl. At the same time, the accessory epithelium (here called epilarval trophocyte epithelium) rises, isolating and nursing the early larva. The amphiblastula is formed by an epithelium composed of ciliated cells, granular cells, and cross-cells, this latter persisting even after larval release. Some degenerating amoeboid cells and bacteria were found in the larval cavity, possibly helping with larval nutrition. The possibility of cross-cells being precursors of the germ cell lineage and the vertical transmission of bacteria found in the larva are discussed.
Similar content being viewed by others
References
Adams EDM, Goss GG, Leys SP (2010) Freshwater sponges have functional, sealing epithelia with high transepithelial resistance and negative transepithelial potential. PLoS ONE 5:e15040. doi:10.1371/journal.pone.0015040
Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12:494–518. doi:10.1111/j.1525-142X.2010.00435.x
Adamska M, Degnan BM, Green K, Zwafink C (2011) What sponges can tell us about the evolution of developmental processes. Zoology 114(1):1–10. doi:10.1016/j.zool.2010.10.003
Amano S, Hori I (1992) Metamorphosis of calcareous sponges 1. Ultrastructure of free-swimming larvae. Invertebr Reprod Dev 21:81–90
Anakina RP (1997) The cleavage specificity in embryos of the Barents Sea sponge Leucosolenia complicata Montagu (Calcispongiae, Calcaronea). In: Ereskovsky AV, Keupp H, Kohring R (eds) Modern problems of poriferan biology. Berliner Geowissenschaftliche Abhandlung, Berlin, pp 45–53
Bancroft JD, Stevens A (1996) Theory and practice of histological techniques. Churchill Livingstone, New York
Boury-Esnault N, Ereskovsky A, Bézac C, Tokina D (2003) Larval development in the Homoscleromorpha (Porifera, Demospongiae). Invertebr Biol 122(3):187–202. doi:10.1111/j.1744-7410.2003.tb00084.x
Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer Ass, Inc, Sunderland
Dendy A (1891) Studies on the comparative anatomy of sponges: III.—On the anatomy of Grantia labyrinthica, Carter, and the so-called family Teichonida. Quart J Micr Sci 32:1–39
Duboscq O, Tuzet O (1933) Quelques structures des amphiblastules d’Éponges calcaires. C R Acad Sci 197:561
Duboscq O, Tuzet O (1937) L’ovogenèse, la fécondation et les premiers stades du développement des éponges calcaires. Arch Zool Exp Gén 79:157–316
Duboscq O, Tuzet O (1941) Sur les cellules en croix des Sycon (Sycon ciliatum Fabr., Sycon coronatum Ellis et Sol., Sycon elegans Bower.) et leur signification. Arch Zool Exp Gén 81:151–163
Duboscq O, Tuzet O (1942) Recherches complémentaires sur l′ovogenèse la fecondation et les premiers stades du développement des éponges calcaires. Arch Zool Exp Gén 81:395–466
Duboscq O, Tuzet O (1944) L′ovogenèse, la fécondation et les premiers stades du développement du Sycon elegans Bower. Arch Zool Exp Gén 83:445–459
Eckelbarger KJ, Larson R (1992) Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa. Mar Biol 114:633–643. doi:10.1007/BF00357260
Eerkes-Medrano DI, Leys SP (2006) Ultrastructure and embryonic development of a syconoid calcareous sponge. Invertebr Biol 125:177–194. doi:10.1111/j.1744-7410.2006.00051.x
Ereskovsky AV (2010) The comparative embryology of sponges. Springer, Dordrecht. doi:10.1007/978-90-481-8575-7
Ereskovsky AV, Willenz P (2008) Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127:175–187. doi:10.1007/s00435-008-0061-9
Ereskovsky AV, Gonobobleva E, Vishnyakov A (2005) Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar Biol 146:869–875. doi:10.1007/s00227-004-1489-1
Franzen W (1988) Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea). Zoomorphology 107:349–357. doi:10.1007/BF00312218
Gallissian M-F (1983) Étude ultrastructurale du developpement embryonnaire chez Grantia compressa F. (Porifera, Calcarea). Arch Anat Micr 72:59–75
Gallissian M-F, Vacelet J (1992) Ultrastructure of the oocyte and embryo of the calcified sponge, Petrobiona massiliana (Porifera, Calcarea). Zoomorphology 112:133–141. doi:10.1007/BF01633104
Gatenby JB (1920) The germ-cells, fertilization, and early development of Grantia (Sycon) compressa. Linn J Zool 36:261–297
Gazave E, Lapébie P, Ereskovsky A, Vacelet J, Renard E, Cárdenas P, Borchiellini C (2012) No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia 687:1–3. doi:10.1007/s10750-011-0842-x
Gilbert SF (2010) Developmental biology. Sinauer Associates, Sunderland
Gilbert S, Raunio AM (1997) Embryology: constructing the organism. Sinauer Associates, Sunderland
Gilis M, Gosselin P, Dubois P, Willenz P (2011) Seasonal modifications and morphogenesis of the hypercalcified sponge Petrobiona massiliana (Calcarea, Calcaronea). Invertebr Biol 130:193–210. doi:10.1111/j.1744-7410.2011.00239.x
Haeckel E (1874) The Gastraea-Theory, the phylogenetic classification of the animal kingdom and the homology of the germ-lamellae. Quart J Micr Sci 14:142–247
Holstien K, Rivera A, Windsor P, Ding SY, Leys SP, Hill M, Hill A (2010) Expansion, diversification, and expression of T-box family genes in Porifera. Dev Gen Evol 220:251–262. doi:10.1007/s00427-010-0344-2
Ivanova-Kazas OM (1995) Evolutionary embryology of animals. Nauka Press, St. Petersburg
Lanna E, Klautau M (2010) Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea). Zoomorphology 129:249–261. doi:10.1007/s00435-010-0117-5
Lanna E, Monteiro LC, Klautau M (2007) Life cycle of Paraleucilla magna Klautau, Monteiro and Borojevic, 2004 (Porifera, Calcarea). In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G (eds) Porifera research—biodiversity, innovation and sustainability. Museu Nacional—Série Livros, Rio de Janeiro, pp 413–418
Leys SP (2004) Gastrulation in sponges. In: Stern C (ed) Gastrulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 23–31
Leys SP, Eerkes-Medrano D (2005) Gastrulation in calcareous sponges: in search of Haeckel’s Gastraea. Integr Comp Biol 45:342–351. doi:10.1093/icb/45.2.342
Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Can J Zool 84:262–287. doi:10.1139/Z05-170
Leys SP, Riesgo A (2011) Epithelia, an evolutionary novelty of metazoans. J Exp Zool B: Mol Dev Evol 314B. doi:10.1002/jez.b.21442
Lufty RG (1957a) On the origin of the so-called mesoblast cells in the amphiblastula larva of calcareous sponges. Cellule 58:231–237
Lufty RG (1957b) On the placental membrane of calcareous sponges. Cellule 58:239–247
Maldonado M (2007) Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically-compartmented bacterial types. J Mar Biol Assoc UK 87(6):1701–1713. doi:10.1017/S0025315407058080
Maldonado M, Riesgo A (2008) Reproduction in Porifera: a synoptic overview. Treb Soc Cat Biol 59:29–49. doi:10.2436/20.1501.02.56
Metschnikoff E (1874) Zur Entwickelungsgeschichte der Kalkschwämme. Zeitschr Wiss Zool 24:1–14
Nickel M, Scheer C, Hammel JU, Herzen J, Beckmann F (2011) The contractile sponge epithelium sensu lato—body contraction of the demosponge Tethya wilhelma is mediated by the pinacoderm. J Exp Biol 214(10):1692–1698. doi:10.1242/jeb.049148
Philippe H, Derelle R, Lopez P et al (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712. doi:10.1016/j.cub.2009.02.052
Reunov A (2004) Is there a germ plasm in mouse oocytes? Zygote 12(4):329–332. doi:10.1017/S0967199404002916
Schulze FE (1875) Ueber den Bau und die Entwicklung von Sycandra raphanus Haeckel. Zeitschr Wiss Zool 25:247–280
Simpson TL (1984) The cell biology of sponges. Springer, New York
Srivastava M, Simakov O, Chapman J et al (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726. doi:10.1038/nature09201
Turque AS, Batista D, Silveira CB et al (2010) Environmental shaping of sponge associated archaeal communities. PLoS ONE 5(12):e15774. doi:10.1371/journal.pone.0015774
Usher KM, Kuo J, Fromont J, Sutton DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461:15–23. doi:10.1023/A:1012792426770
Vacelet J (1964) Étude monographique de l’éponge calcaire pharétronide de Méditerranée, Petrobiona massiliana Vacelet et Lévi. Les pharétronides actuelles et fossiles. Recl Trav Stn Mar Endoume 34(50):1–125
Windsor PJ, Leys SP (2010) Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer. Evol Dev 12:484–493. doi:10.1111/j.1525-142X.2010.00434.x
Woollacott RM, Pinto RL (1995) Flagellar basal apparatus and its utility in phylogenetic analyses of the Porifera. J Morphol 226(3):247–265. doi:10.1002/jmor.1052260302
Acknowledgments
We are grateful to the staff of the Laboratório de Biologia de Porifera (IB/UFRJ) for helping with the field work. We also thank the staff of the Laboratório de Ultraestrutura Celular Hertha Meyer (IBCCF) (especially Noêmia Rodrigues) and the staff of the Serviço de Microscopia Eletrônica-CPqGM-FIOCRUZ (especially M. Lucia Moreno) for their help with the preparation of the specimens and the use of the electron microscopes. We also thank Bernardo Pascarelli for his help with confocal microscopy at the Plataforma de Microscopia Confocal, FIOCRUZ-RJ. We are in debt to Inácio DS Neto for allowing us to borrow some fixatives and to Michael Nickel and to an anonymous reviewer for their fruitful comments that improved the original manuscript. Grants and fellowships were provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação Carlos Chagas de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (E-26/111.541/2008), and the Brazilian National Counsel of Technological and Scientific Development (CNPq) (480368/2008 2). This work was part of the Master Thesis of E. Lanna, presented to the Post-Graduation Program in Zoology of the Museu Nacional do Rio de Janeiro/UFRJ.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Schmidt-Rhaesa.
Rights and permissions
About this article
Cite this article
Lanna, E., Klautau, M. Embryogenesis and larval ultrastructure in Paraleucilla magna (Calcarea, Calcaronea), with remarks on the epilarval trophocyte epithelium (“placental membrane”). Zoomorphology 131, 277–292 (2012). https://doi.org/10.1007/s00435-012-0160-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-012-0160-5