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Ultrastructure of mesoderm formation and development in Membranipora membranacea (Bryozoa: Gymnolaemata)

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Abstract

Mesoderm origin in Bryozoa is largely unknown. In this study, embryonic and early larval stages of Membranipora membranacea, a bryozoan exhibiting a planktotrophic cyphonautes larva, are investigated using mainly ultrastructural techniques. Shortly after the onset of gastrulation, an ectodermal cell, which is situated centrally at the prospective anterior pole of the larva, can be recognized by its constricted apical surface and enlarged basal part. It is also distinct from other ectodermal cells by the composition of its cytoplasm. In later stages, it has left the epidermis, lost its epithelial character, and is situated subepithelially, between the basal sides of the ectodermal and endodermal sheets. A blastocoelic cavity is not present at this stage. This cell divides and gives rise to a group of cells forming a muscular and neuronal strand at the anterior side of the larva. The majority of the larval musculature originates from this ingression. Despite this evidence for an ectodermal origin, additional sources of mesoderm can so far not be excluded. The literature on mesoderm origin in Bryozoa is reviewed and the results are compared to known data from other metazoan taxa.

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References

  • Ackermann C, Dorresteijn A, Fischer A (2005) Clonal domains in postlarval Platynereis dumerilii (Annelida : Polychaeta). J Morphol 266:258–280

    Article  PubMed  Google Scholar 

  • Barrois J (1880) Mémoire sur la metamorphose des Bryozoaires. Ann Sci Nat Zool Ser 13(9):1–67 + 4pls

    Google Scholar 

  • Bartolomaeus T (2001) Ultrastructure and formation of the body cavity lining in Phoronis muelleri (Phoronida, Lophophorata). Zoomorphology 120:135–148

    Article  Google Scholar 

  • Borg F (1927) Studies on recent cyclostomatous Bryozoa. Zool Bidr Uppsala 10:181–507

    Google Scholar 

  • Boyer BC, Henry JQ (1998) Evolutionary modifications of the spiralian developmental program. Amer Zool 38:621–633

    Google Scholar 

  • Boyer BC, Henry JJ, Martindale MQ (1996) Dual origins of mesoderm in a basal spiralian: cell lineage analyses in the polyclad turbellarian Hoploplana inquilina. Dev Biol 197:329–338

    Article  Google Scholar 

  • Boyer BC, Henry JJ, Martindale MQ (1998) The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev Biol 204:111–123

    Article  PubMed  CAS  Google Scholar 

  • Braem F (1890) Untersuchungen über die Bryozoen des süssen Wassers. Zoologica 2:1–134, pls. 1–15

    Google Scholar 

  • Braem F (1897) Die geschlechtliche Entwicklung von Plumatella fungosa. Zoologica 10:1–96

    Google Scholar 

  • Braem F (1908) Die geschlechtliche Entwicklung von Fredericella sultana. Zoologica 52:1–37

    Google Scholar 

  • Brien P (1953) Études sur les Phylactolémates Evolution de la zoecie—Bourgeonnement d’accroissement Bourgeonnement statoblastique—Embryogenese—L’Ontogenese multiple. Ann Soc R Zool Belg 84:301–444

    Google Scholar 

  • Burton PM (2008) Insights from diploblasts: the evolution of mesoderm and muscle. J Exp Zool 310B:5–14

    Article  Google Scholar 

  • Calvet L (1900) Contribution à l’histoire naturelle des bryozoaires ectoproctes marins. Trav Inst Zool Univ Montpellier 8:1–488

    Google Scholar 

  • Cook PL (1962) The early larval development of Membranipora seurati (Canu) and Electra crustulenta (Pallas), Polyzoa. Cah Biol Mar 3:57–60

    Google Scholar 

  • Corrêa DD (1948) A embryologia de Bugula flabellata (J. V. Thompson) (Bryozoa Ectoprocta). Zoologia, Sao Paulo 13:7–71

    Google Scholar 

  • d’Hondt JL (1983) Sur l’évolution des quatre macroméres du pôle végétatif chez les embryons de Bryozoaires Eurystomes. Cah Biol Mar 24:177–185

    Google Scholar 

  • d’Hondt JL (2005) État des connaissances sur le développement embryonaire des Bryozoaires Phylactolaemates. Denisia 16:59–68

    Google Scholar 

  • Davenport CB (1891) Observations on budding in Paludicella and some other Bryozoa. Bull Mus Comp Zool 22:1–114

    Google Scholar 

  • Davidson EH, Cameron RA, Ransick A (1998) Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125:3269–3290

    PubMed  CAS  Google Scholar 

  • de Selys-Longchamps M (1907) Phoronis. Fauna Flora Golf Neapel 30:1–280

    Google Scholar 

  • Dilly PN (1973) The larva of Rhabdopleura compacta (Hemichordata). Mar Biol 18:69–86

    Article  Google Scholar 

  • Dudley JE (1973) Observations on the reproduction, early larval development, and colony astogeny of Conopeum tenuissimum (Canu). Chesap Sci 14:270–278

    Article  Google Scholar 

  • Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Article  PubMed  CAS  Google Scholar 

  • Freeman G (1993) Regional specification during embryogenesis in the articulate brachiopod Terebratalia. Dev Biol 160:196–218

    Article  PubMed  CAS  Google Scholar 

  • Freeman G (1995) Regional specification during embryogenesis in the inarticulate brachiopod Glottidia. Dev Biol 172:15–36

    Article  PubMed  CAS  Google Scholar 

  • Freeman G (1999) Regional specification during embryogenesis in the inarticulate brachiopod Discinisca. Dev Biol 209:321–339

    Article  PubMed  CAS  Google Scholar 

  • Freeman G (2000) Regional specification during embryogenesis in the inarticulate brachiopod Crania anomala. Dev Biol 227:219–238

    Article  PubMed  CAS  Google Scholar 

  • Freeman G (2003) Regional specification during embryogenesis in rhynchonelliform brachiopods. Dev Biol 261:268–287

    Article  PubMed  CAS  Google Scholar 

  • Freeman G, Martindale MQ (2002) The origin of mesoderm in phoronids. Dev Biol 252:301–311

    Article  PubMed  CAS  Google Scholar 

  • Fuchs J, Obst M, Sundberg P (2009) The first comprehensive molecular phylogeny of Bryozoa (Ectoprocta) based on combined analyses of nuclear and mitochondrial genes. Mol Phylogenet Evol 52:225–233

    Article  PubMed  CAS  Google Scholar 

  • Grobe P (2008) Larval development, the origin of the coelom and the phylogenetic relationships of the Phoronida. Dissertation, Freie Universität Berlin, Germany

  • Gruhl A (2008) Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata). Zoomorphology 127:143–159

    Article  Google Scholar 

  • Halanych KM (2004) The new view of animal phylogeny. Ann Rev Ecol Syst 35:229–256

    Article  Google Scholar 

  • Harmer SF (1893) On the occurrence of embryonic fission in cyclostomatous Polyzoa. Q J Microsc Sci N S 34:199–241

    Google Scholar 

  • Harmer SF (1898) On the development of Tubulipora, and some British and northern species of this genus. Q J Microsc Sci N S 41:73–157

    Google Scholar 

  • Hejnol A, Martindale MQ, Henry JQ (2007) High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. Dev Biol 305:63–76

    Article  PubMed  CAS  Google Scholar 

  • Helmkampf M, Bruchhaus I, Hausdorf B (2008) Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Mol Phylogenet Evol 46:206–214

    Article  PubMed  CAS  Google Scholar 

  • Henry JJ, Martindale MQ (1998) Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus. Dev Biol 201:253–269

    Article  PubMed  CAS  Google Scholar 

  • Henry JJ, Martindale MQ (1999) Conservation and innovation in spiralian development. Hydrobiologia 402:255–265

    Article  Google Scholar 

  • Henry JQ, Tagawa K, Martindale MQ (2001) Deuterostome evolution: early development in the enteropneust hemichordate, Ptychodera flava. Evol Dev 3:375–390

    Article  PubMed  CAS  Google Scholar 

  • Herrmann K (1980) Die archimere Gliederung bei Phoronis muelleri (Tentaculata). Zool Jb Anat Ontog Tiere 103:234–249

    Google Scholar 

  • Herrmann K (1986) Die Ontogenese von Phoronis mülleri (Tentaculata) unter besonderer Berücksichtigung der Mesodermdifferenzierung und Phylogenese des Coeloms. Zool Jb Anat Ontog Tiere 114:441–463

    Google Scholar 

  • Jang K, Hwang U (2009) Complete mitochondrial genome of Bugula neritina (Bryozoa, Gymnolaemata, Cheilostomata): phylogenetic position of Bryozoa and phylogeny of lophophorates within the Lophotrochozoa. BMC Genomics 10:167

    Article  PubMed  CAS  Google Scholar 

  • Kraepelin K (1892) Die Deutschen Süsswasser-Bryozoen. Eine Monographie. II. Entwickelungsgeschichtlicher Teil. Abh Naturwiss Verein Hamburg 12:1–67, pls. 1–5

  • Lambert JD (2008) Mesoderm in spiralians: the organizer and the 4d cell. J Exp Zoolog B Mol Dev Evol 310:15–23

    Article  Google Scholar 

  • Long JA, Stricker SA (1991) Brachiopoda. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates VI. Echinoderms and lophophorates. Boxwood Press, Pacific Groove, pp 47–84

    Google Scholar 

  • Lüter C (2000) The origin of the coelom in Brachiopoda and its phylogenetic significance. Zoomorphology 120:15–28

    Article  Google Scholar 

  • Marcus E (1926) Beobachtungen und Versuche an lebenden Meeresbryozoen. Zool Jb 52:1–102

    Google Scholar 

  • Marcus E (1934) Über Lophopus cristallinus (Pall.). Zool Jb Anat Ontog Tiere 58:501–606

    Google Scholar 

  • Mawatari S, Mawatari SF (1975) Development and metamorphosis of the cyphonautes of Membranipora serrilamella Osburn. In: Pouyet S (ed) Bryozoa 1974. Université Claude Bernard, Lyon, pp 13–18, 2pl

  • Morgan TH (1891) The growth and metamorphosis of tornaria. J Morphol 5:407–458

    Article  Google Scholar 

  • Nielsen C (1970) On metamorphosis and ancestrula formation in cylostomatous bryzoans. Ophelia 7:217–256

    Google Scholar 

  • Nielsen C (1971) Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9:209–341

    Google Scholar 

  • Nielsen C (1990) Bryozoa Ectoprocta. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates vol IV, Part B, Fertilization, development and parental care. Wiley, London, pp 185–200

    Google Scholar 

  • Nielsen C (1991) The development of the brachiopod Crania (Neocrania) anomala. Acta Zool 27:7–28

    Article  Google Scholar 

  • Nielsen C (2001) Animal evolution. Interrelationships of the living phyla. Oxford University Press, Oxford

    Google Scholar 

  • Nielsen C (2004) Trochophora larvae: Cell-lineages, ciliary bands, and body regions. 1. Annelida and Mollusca. J Exp Zool B 302:35–68

    Google Scholar 

  • Nielsen C (2005) Trochophora larvae: Cell-lineages, ciliary bands, and body regions. 2. Other groups and general discussion. J Exp Zool B 304:401–447

    Article  Google Scholar 

  • Ostrovsky AN (2008a) External versus internal and self- versus cross-fertilization in Bryozoa: transformation of the view and evolutionary considerations. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of bryozoology 2. International Bryozoology Association/Trinity College, Dublin, pp 103–115

    Google Scholar 

  • Ostrovsky AN (2008b) The parental care in cheilostome bryozoans: a historical review. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of bryozoology 2. International Bryozoology Association/Trinity College, Dublin, pp 211–245

    Google Scholar 

  • Ostrovsky AN, Vavra N, Porter JS (2008) Sexual reproduction in gymnolaemate Bryozoans: history and perspectives of the research. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of bryozoology 2. International Bryozoology Association/Trinity College, Dublin, pp 117–210

    Google Scholar 

  • Pace RM (1906) On the early stages in the development of Flustrella hispida (Fabricius), and on the existence of a “yolk nucleus” in the egg of this form. Q J Microsc Sci 50:435–478 + 4 pls

    Google Scholar 

  • Passamaneck YJ, Halanych KM (2004) Evidence from Hox genes that bryozoans are lophotrochozoans. Evol Dev 6:275–281

    Article  PubMed  CAS  Google Scholar 

  • Passamaneck YJ, Halanych KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phylogenet Evol 40:20–28

    Article  PubMed  CAS  Google Scholar 

  • Prouho H (1892) Contribution a l’histoire des bryozoaires. Arch Zool Exp Gén 10(2.Ser.):557–656

    Google Scholar 

  • Reed CG (1987) Phylum Bryozoa. In: Strathmann MF (ed) Reproduction and development of marine invertebrates of the Northern Pacific coast. University of Washington Press, Seattle, pp 494–511

    Google Scholar 

  • Reed CG (1991) Bryozoa. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates VI. Echinoderms and lophophorates. Boxwood Press, Pacific Groove, pp 85–245

    Google Scholar 

  • Reed CG, Cloney RA (1982) The larval morphology of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesicularioidea). Zoomorphology 100:23–54

    Article  Google Scholar 

  • Reed CG, Woollacott RM (1982) Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (Cheilostomata, Cellularioidea) I. Attachment to the substratum. J Morphol 172:335–348

    Article  Google Scholar 

  • Rieger MR, Ladurner P (2003) The significance of muscle cells for the origin of mesoderm in Bilateria. Integ Comp Biol 43:47–54

    Article  Google Scholar 

  • Robertson A (1903) Embryology and embryonic fission in the genus Crisia. Univ Calif Publ Zool 1:115–156

    Google Scholar 

  • Ruppert EE, Balser EJ (1986) Nephridia in the larvae of hemichordates and echinoderms. Biol Bull 171:188–196

    Article  Google Scholar 

  • Santagata S (2004) Larval development of Phoronis pallida (Phoronida): implications for morphological convergence and divergence among larval body plans. J Morphol 259:347–358

    Article  PubMed  Google Scholar 

  • Shook D, Keller R (2003) Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech Dev 120:1351–1383

    Article  PubMed  CAS  Google Scholar 

  • Silén L (1966) On the fertilization problem in the gymnolaematous Bryozoa. Ophelia 3:113–140

    Google Scholar 

  • Stricker SA, Reed CG, Zimmer RL (1988) The cyphonautes larva of the marine bryozoan Membranipora membranacea. I. General morphology, body wall, and gut. Can J Zool 66:368–383

    Article  Google Scholar 

  • Ström R (1969) Sexual reproduction in a stoloniferous bryozoan, Triticella koreni (G.O. Sars). Zool Bidr Uppsala 38:113–127

    Google Scholar 

  • Ström R (1977) Brooding patterns of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 23–55

    Google Scholar 

  • Sun M, Wu Z, Shen X, Ren J, Liu X, Liu H, Liu B (2009) The complete mitochondrial genome of Watersipora subtorquata (Bryozoa, Gymnolaemata, Ctenostomata) with phylogenetic consideration of Bryozoa. Gene 439:17–24

    Article  PubMed  CAS  Google Scholar 

  • Tagawa K, Nishino A, Humphreys T, Satoh N (1998) The spawning and early development of the hawaiian acorn worm (hemichordate), Ptychodera flava. Zool Sci 15:85–91

    Article  PubMed  CAS  Google Scholar 

  • Technau U, Scholz CB (2003) Origin and evolution of endoderm and mesoderm. Int J Dev Biol 47:531–539

    PubMed  Google Scholar 

  • Temkin MH (1996) Comparative fertilization biology of gymnolaemate bryozoans. Mar Biol 127:329–339

    Article  Google Scholar 

  • Vigelius WJ (1886) Zur Ontogenie der marinen Bryozoen. Mitt Zool Stn Neapel 6:499–541

    Google Scholar 

  • Waeschenbach A, Telford MJ, Porter JS, Littlewood DTJ (2006) The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa. Mol Phylogenet Evol 40:195–207

    Article  PubMed  CAS  Google Scholar 

  • Wood TS (2008) Development and metamorphosis of cyphonautes larvae in the freshwater ctenostome bryozoan, Hislopia malayensis Annandale, 1916. In: Hageman GS, Key MM Jr, Winston JE (eds) Bryozoan studies 2007. Virginia Museum of Natural History, Martinsville

    Google Scholar 

  • Woollacott RM, Zimmer RL (1971) Attachment and metamorphosis of the cheilo-ctenostome bryozoan Bugula neritina (Linné). J Morphol 134:351–382

    Article  Google Scholar 

  • Wray GA (1997) Echinoderms. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer Associates, Sunderland, pp 309–329

    Google Scholar 

  • Zimmer RL (1980) Mesoderm proliferation and formation of the protocoel and metacoel in early embryos of Phoronis vancouverensis. Zool Jb Anat Ontog Tiere 103:219–233

    Google Scholar 

  • Zimmer RL (1997) Phoronids, brachiopods, and bryozoans, the lophophorates. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer Associates, Sunderland, pp 279–305

    Google Scholar 

  • Zimmer RL, Woollacott RM (1977) Structure and classification of gymnolaemate larvae. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 57–89

    Google Scholar 

  • Zimmer RL, Woollacott RM (1989) Larval morphology of the bryozoan Watersipora arcuata (Cheilostomata: Ascophora). J Morphol 199:125–150

    Article  Google Scholar 

  • Zimmer RL, Woollacott RM (1993) Anatomy of the larva of Amathia vidovici (Bryozoa: Ctenostomata) and phylogenetic significance of vesiculariform larva. J Morphol 215:1–29

    Article  Google Scholar 

  • Zimmer RL (1964) Reproductive biology and development of Phoronida. Dissertation, University of Washington

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Acknowledgments

I thank Thomas Bartolomaeus (Bonn) for helpful comments and discussions on the manuscript. Many thanks go to Dennis Willows for providing facilities at Friday Harbour Laboratories (Washington, USA) and especially to Richard Strathmann for advice on rearing of Membranipora embryos. I also thank three anonymous reviewers for their valuable remarks.

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  1. Alexander Gruhl

    Present address: Department of Zoology, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

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  1. Systematik und Evolution der Tiere, Institut für Biologie, Freie Universität Berlin, Königin-Luise-Str. 1-3, 14195, Berlin, Germany

    Alexander Gruhl

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Gruhl, A. Ultrastructure of mesoderm formation and development in Membranipora membranacea (Bryozoa: Gymnolaemata). Zoomorphology 129, 45–60 (2010). https://doi.org/10.1007/s00435-009-0099-3

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