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Organisms Diversity & Evolution

, Volume 16, Issue 1, pp 85–104 | Cite as

The plastic nervous system of Nemertodermatida

  • Olga I. Raikova
  • Inga Meyer-Wachsmuth
  • Ulf Jondelius
Original Article

Abstract

Nemertodermatida are microscopic marine worms likely to be the sister group to acoels, forming with them the earliest extant branch of bilaterian animals, although their phylogenetic position is debated. The nervous system of Flagellophora cf. apelti, Sterreria spp. and Nemertoderma cf. westbladi has been investigated by immunohistochemistry and confocal microscopy using anti-tubulin, anti-5-HT and anti-FMRFamide antibodies. The nervous system of F. cf. apelti is composed of a large neuropile and a loose brain at the level of the statocysts with several nerve fibres surrounding them and innervating the broom organ. Sterreria spp. shows a commissural-like brain and several neurite bundles going frontad and caudad from this. At the level of the statocysts there is also a thicker aggregation of immunoreactive fibres. The nervous system of N. cf. westbladi consists of a nerve ring lying outside the body wall musculature at the level of the statocyst and a pair of ventro-lateral neurite bundles, from which extend thinner fibres innervating the ventral side of the animal. Numerous bottle-shaped glands were observed, innervated by fibres starting both from the brain and the neurite bundles. The nervous system of the nemertodermatids studied to date displays no common pattern; instead, there is considerable plasticity in the general morphology of the nervous system. In addition, the musculature of Sterreria spp. has been studied by phalloidin staining. It shows diagonal muscles in the anterior quarter of the body and a simple orthogonal grid in the posterior three quarters, being simpler than that of the other nemertodermatids. High-resolution differential interference contrast microscopy permitted to better visualize some morphological characters of the species studied, such as statocysts, sperm and glands and, in combination with anti-tubulin staining, describe in detail the broom organ in F. cf. apelti. Finally, we note an apparent absence of innervation of the gut in Nemertodermatida similar to the condition in Xenoturbella.

Keywords

Flagellophora Sterreria Nemertoderma Nemertodermatida Nervous system Immunohistochemistry Musculature Statocyst  Broom organ Glands Sperm 

Notes

Acknowledgments

Thanks are extended to the staff of Sven Lovén Centre for Marine Sciences (Sweden), the CCMAR in Faro (Portugal) and the Biologische Anstalt Helgoland (Germany) for their help with collecting the material. We are deeply grateful to Professor Marco Curini-Galletti, to Professor Mark Martindale and to Professor Philippe Bouchet for organizing sampling in Italy, at Hawai’i and in Papua New Guinea, respectively. Collections in Papua New Guinea took place during the Our Planet Reviewed Papua Niugini Expedition in November–December 2012, organized by the Muséum National d’Histoire Naturelle (MNHN), Pro Natura International, the Institut de Recherche pour le Développement (IRD) and the University of Papua New Guinea. The principal investigators of this expedition were Philippe Bouchet, Sarah Samadi (MNHN) and Claude Payri (IRD), and funding was provided by the Total Foundation, Prince Albert II of Monaco Foundation, Fondation EDF, Stavros Niarchos Foundation and Entrepose Contracting, with support from the Divine Word University and operated under a permit delivered by the Papua New Guinea Department of Environment and Conservation. The confocal microscopic observations were carried out at the newly equipped Research Resource Centre “Molecular and Cellular Technologies” at St.-Petersburg State University (Russia). We wish to express our gratitude to the most helpful staff of the Centre, in particular to Nikolai A. Kostin, specialist in confocal microscopy. Financial support was received from the Zoological Institute RAS project 0120135194 and the Russian Basic Research Foundation grant 13-04-02002 to Olga Raikova, the Swedish Research Council through a grant to Ulf Jondelius (grant numbers 2009-5147 and 2012-3913), the Föreningen Riksmusei Vänner (stipend 2011), Stiftelsen Lars Hiertas Minne grant FO2011-0248 and the Royal Swedish Academy of Sciences grant FOA11H-352 to Inga Meyer-Wachsmuth, and from the European Community through an ASSEMBLE grant (agreement no 227799).

References

  1. Achatz, J. G., & Martinez, P. (2012). The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications. Frontiers in Zoology, 9, 27–48.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ax, P. (1963). Relationships and phylogeny of the Turbellaria. In E. C. Dougherty (Ed.), The Lower Metazoa (pp. 191–224). Berkeley, California: University California Press.Google Scholar
  3. Børve, A., & Hejnol, A. (2014). Development and juvenile anatomy of the nemertodermatid Meara stichopi (Bock) Westblad 1949 (Acoelomorpha). Frontiers in Zoology, 11, 50–64.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Coons, A. H., Leduc, E. H., & Conolly, J. M. (1955). Studies on antibody production I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. Journal of Experimental Medicine, 102, 49–60.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Crezée, M. (1975). Monograph of the Solenofilomorphidae (Turbellaria: Acoela). Internationale Revue der gesamten Hydrobiologie und Hydrographie, 60, 769–845.CrossRefGoogle Scholar
  6. Crezée, M. (1978). Paratomella rubra Rieger and Ott, an amphiatlantic acoel turbellarian. Cahiers de Biologie Marine, 19, 1–9.Google Scholar
  7. Dickinson, A. J. G., Nason, J., & Croll, R. P. (1999). Histochemical localization of FMRFamide, serotonin and catecholamines in embryonic Crepidula fornicata (Gastropoda, Prosobranchia). Zoomorphology, 119, 49–62.CrossRefGoogle Scholar
  8. Ehlers, U. (1985). Das Phylogenetische System der Plathelminthes. Stuttgart: G. Fischer.Google Scholar
  9. Ehlers, U. (1992). Frontal glandular and sensory structures in Nemertoderma (Nemertodermatida) and Paratomella (Acoela): ultrastructure and phylogenetic implications for the monophyly of the Euplathelminthes (Plathelminthes). Zoomorphology, 112, 227–236.CrossRefGoogle Scholar
  10. Faubel, A. (1976). Interstitielle Acoela (Turbellaria) aus dem Litoral der nordfriesischen Inseln Sylt und Amrum (Nordsee). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 73, 17–56.Google Scholar
  11. Faubel, A., & Dörjes, J. (1978). Flagellophora apelti gen. n. sp. n.: a remarkable representative of the order Nemertodermatida (Turbellaria: Archoophora). Senckenbergiana maritima, 10, 1–13.Google Scholar
  12. Grimmelikhuijzen, C. J. P. (1983a). Coexistence of neuropeptides in Hydra. Neuroscience, 9(4), 837–845Google Scholar
  13. Grimmelikhuijzen, C. J. P. (1983b). FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry, 78(3), 361–81.Google Scholar
  14. Gröger, H., & Schmid, V. (2001). Larval development in Cnidaria: a connection to bilateria? Genesis, 29, 110–114.CrossRefPubMedGoogle Scholar
  15. Harzsch, S. (2002). Neurobiologie und Evolutionsforschung: “Neurophylogenie” und die stammesgeschichte der Euarthropoda. Neuroforum, 4(2), 267–273.Google Scholar
  16. Hay-Schmidt, A. (1995). The larval nervous system of Polygordius lacteus Scheinder 1868 (Polygordiidae, Polychaeta): immunocytochemical data. Acta Zoologica, 76, 121–140.CrossRefGoogle Scholar
  17. Hejnol, A., Obst, M., Stamatakis, A., et al. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society B, 276, 4261–4270.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hessling, R. (2002). Metameric organization of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology, 121, 221–234.CrossRefGoogle Scholar
  19. Hooge, M. D. (2001). Evolution of the body wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). Journal of Morphology, 249, 171–194.CrossRefPubMedGoogle Scholar
  20. Jondelius, U., Ruiz-Trillo, I., Baguñà, J., & Ruitort, M. (2002). The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zoologica Scripta, 31, 201–215.CrossRefGoogle Scholar
  21. Jondelius, U., Wallberg, A., Hooge, M., & Raikova, O. I. (2011). How the worm got its pharynx: phylogeny, classification and Bayesian assessment of character evolution in Acoela. Systematic Biology, 60, 845–871.CrossRefPubMedGoogle Scholar
  22. Karling, T. G. (1940). Zur Morphologie und Systematik der Alloeocoela Cumulata and Rhabditophora Lecithophora (Turbellaria). Acta Zoologica Fennica, 26, 1–160.Google Scholar
  23. Kotikova, E. A., Raikova, O. I., Reuter, M., & Gustafsson, M. K. S. (2002). The nervous and muscular systems in the free-living flatworm Castrella truncata (Rhabdocoela): an immunocytochemical and phalloidin fluorescence study. Tissue and Cell, 34, 365–374.CrossRefPubMedGoogle Scholar
  24. Leiper, R. T. (1902). On an acoelous turbellarian inhabiting the common heart urchin. Nature, 66, 641.Google Scholar
  25. Loesel, R. (2011). Chapter 11: Neurophylogeny: retracing early metazoan brain evolution. In P. Pontarotti (Ed.), Evolutionary biology—concepts, biodiversity, macroevolution and genome evolution (pp. 169–191). Berlin Heidelberg: Springer.CrossRefGoogle Scholar
  26. Lundin, K. (1998). Symbiotic bacteria on the epidermis of species of the Nemertodermatida (Platyhelminthes, Acoelomorpha). Acta Zoologica, 79, 187–191.CrossRefGoogle Scholar
  27. Lundin, K. (2000). Phylogeny of the Nemertodermatida (Acoelomorpha, Platyhelminthes). A cladistic analysis. Zoologica Scripta, 29, 65–74.CrossRefGoogle Scholar
  28. Lundin, K., & Hendelberg, J. (1995). Ultrastructure of the epidermis of Meara stichopi (Platyhelminthes, Nemertodermatida) and associated extra-epidermal bacteria. Hydrobiologia, 305, 161–165.CrossRefGoogle Scholar
  29. Meyer-Wachsmuth, I., Raikova, O. I., & Jondelius, U. (2013). The muscular system of Nemertoderma westbladi and Meara stichopi (Nemertodermatida, Acoelomorpha). Zoomorphology, 132, 239–252.CrossRefGoogle Scholar
  30. Meyer-Wachsmuth, I., Curini Galletti, M., & Jondelius, U. (2014). Hyper-cryptic marine meiofauna: species complexes in Nemertodermatida. PLOS One, 9(9), 1–25.CrossRefGoogle Scholar
  31. Meyer-Wachsmuth, I., Jondelius, U. (2015). Interrelationships of Nemertodermatida. Organisms Diversity and Evolution, this issue.Google Scholar
  32. Müller, M. C. M., & Sterrer, W. (2004). Musculature and nervous system of Gnathostomula peregrina (Gnathostomulida) shown by phalloidin labelling, immunohistochemistry, and cLSM, and their phylogenetic significance. Zoomorphology, 123, 169–177.Google Scholar
  33. Müller, M. C. M., & Westheide, W. (2000). Structure of the nervous system of Myzostoma cirriferum (Annelida) as revealed by immunohistochemistry and cLSM analyses. Journal of Morphology, 245, 87–98.CrossRefPubMedGoogle Scholar
  34. Müller, M. C. M., & Westheide, W. (2002). Comparative analysis of the nervous systems in presumptive progenetic dinophilid and dorvilleid polychaetes (Annelida) by immunohistochemistry and cLSM. Acta Zoologica, 83, 33–48.CrossRefGoogle Scholar
  35. Nezlin, L. P., & Yushin, V. V. (2004). Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphology, 123, 1–13.CrossRefGoogle Scholar
  36. Paps, J., Baguña, J., & Riutort, M. (2009). Bilaterian phylogeny: a broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal Acoelomorpha. Molecular Biology and Evolution, 26(10), 2397–2406.CrossRefPubMedGoogle Scholar
  37. Perea-Atienza, E., GavilaÏn, B., Chiodin, M., Abril, J. F., Hoff, K. J., Poustk, A. J., & Martinez, P. (2015). The nervous system of Xenacoelomorpha: a genomic perspective. Journal of Experimental Biology, 218, 618–628.CrossRefPubMedGoogle Scholar
  38. Philippe, H., Brinkmann, H., Copley, R. R., et al. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature, 470, 255–258.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Raikova, O. I., Reuter, M., Kotikova, E. A., & Gustafsson, M. K. S. (1998). A commissural brain! The pattern of 5-HT immunoreactivity in Acoela (Plathelminthes). Zoomorphology, 118, 69–77.CrossRefGoogle Scholar
  40. Raikova, O. I., Reuter, M., Jondelius, U., Gustafsson, M. K. S. (2000a). The brain of Nemertodermatida as revealed by anti-5-HT and anti-FMRFamide immunostainings. Tissue and Cell, 32, 358–365.Google Scholar
  41. Raikova, O.I., Reuter, M., Jondelius, U., Gustafsson, M. K. S. (2000b). An immunocytochemical and ultrastructural study of the nervous and muscular systems of Xenoturbella westbladi (Bilateria inc. sed). Zoomorphology, 120, 107–118.Google Scholar
  42. Raikova, O. I., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Halton, D. W., Jondelius, U. (2004a). Basiepidermal nervous system in Nemertoderma westbladi (Nemertodermatida): GYIRFamide immunoreactivity. Zoology, 107, 75–86.Google Scholar
  43. Raikova, O. I., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Halton, D. W. (2004b). Evolution of the nervous system in Paraphanostoma (Acoela). Zoologica Scripta, 33, 71–88.Google Scholar
  44. Raikova, O. I. (2004c). Neuroanatomy of basal bilaterians (Xenoturbellida, Nemertodermatida, Acoela) and its phylogenetic implications (PhD thesis). Åbo, Finland: Åbo Akademi University.Google Scholar
  45. Reisinger, E. (1925). Untersuchungen am Nervensystem der Bothrioplana semperi Braun. (Zugleich ein Beitrag zur Technik der vitalen Nervenfaerbung und zur vergleichenden Anatomie des Plathelminthennervensystems.). Zeitschrift für Morphologie und Ökologie der Tiere, 5, 119–149.Google Scholar
  46. Richter, S., Loesel, R., Purschke, G., Schmidt-Rhaesa, A., et al. (2010). Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Frontiers in Zoology, 7, 29.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Reuter, M., & Halton, D. W. (2001). Comparative neurobiology of Platyhelminthes. In D. T. J. Littlewood & R. A. Bray (Eds.), Interrelationships of the Platyhelminthes (pp. 239–249). London: Taylor & Francis.Google Scholar
  48. Reuter, M., Raikova, O. I., Gustafsson, M. K. S. (2001a). Patterns in the nervous and muscle systems in lower flatworms. Belgian Journal of Zoology, 31, 47–53.Google Scholar
  49. Reuter, M., Raikova O. I., Jondelius, U., Gustafsson, M. K. S., Maule A. G., Halton, D. W. (2001b). Organisation of the nervous system in the Acoela: an immunocytochemical study. Tissue and Cell, 33(2), 119–128.Google Scholar
  50. Riser, N. W. (1987). Nemertinoides elongatus gen. n., sp. n. (Turbellaria: Nemertodermatida) from coarse sand beaches of the western north Atlantic. Proceedings of the Helminthological Society of Washington, 54, 60–67.Google Scholar
  51. Ruppert, E. E. (1978). A review of metamorphosis of turbellarian larvae. In F.-S. Chia & M. E. Rice (Eds.), Settlement and metamorphosis of marine invertebrate larvae (pp. 65–81). New York: Elsevier.Google Scholar
  52. Schmidt-Rhaesa, A. (2007). The evolution of organ systems. Oxford, New York: Oxford University Press.CrossRefGoogle Scholar
  53. Smith, J. P. S., & Tyler, S. (1985). The acoel turbellarians: kingpins of metazoan evolution or a specialized offshoot? In C. Conway-Morris, J. D. George, R. Gibson, & H. M. Platt (Eds.), The origins and relationships of lower invertebrates (pp. 123–142). Oxford University Press: Oxford.Google Scholar
  54. Srivastava, M., Mazza-Curll, K. L., van Wolfswinkel, J. C., & Reddien, P. W. (2014). Whole-body acoel regeneration is controlled by Wnt and Bmp-Admp signaling. Current Biology, 24, 1107–1113.CrossRefPubMedGoogle Scholar
  55. Steinböck, O. (1930). Ergebnisse einer von E. Reisinger & O. Steinböck mit Hilfe des Rask-Ørsted Fonds durchgeführten Reise in Grönland 1926. 2. Nemertoderma bathycola nov. gen. nov. spec. Videnskabelige Meddelelser Dansk Naturhistorisk Forening, 90, 47–84.Google Scholar
  56. Steinböck, O. (1932). Die Turbellarian des arktischen Gebietes. In F. Römer & F. Schaudinn (Eds.), Fauna Arctica (Band 6 (pp. 297–342). Jena: Gustav Fischer.Google Scholar
  57. Steinböck, O. (1938). Über die Stellung der Gattung Nemertoderma Steinböck im System der Turbellarien. Acta Societatis pro Fauna et Flora Fennica, 62, 1–28.Google Scholar
  58. Steinböck, O. (1966). Die Hofsteniiden (Turbellaria acoela): Grundsättzliches zur Evolution der Turbellarien. Zeitschrift für zoologische Systematik und Evolutionsforschung, 4, 58–195.CrossRefGoogle Scholar
  59. Stefanini, M., De Martino, C., & Zamboni, L. (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature, 216, 172–174.CrossRefGoogle Scholar
  60. Sterrer, W. (1970). In R. Riedl (Ed.), Fauna und Flora der Adria. Ein systematischer Meeresführer für Biologen und Naturfreunde. Hamburg, Berlin: Verlag Paul Parey.Google Scholar
  61. Sterrer, W. (1998). New and known Nemertodermatida (Platyhelminthes-Acoelomorpha)—a revision. Belgian Journal of Zoology, 128, 55–92.Google Scholar
  62. Todt, C. (2009). Structure and evolution of the pharynx simplex in acoel flatworms (Acoela). Journal of Morphology, 270, 271–290.CrossRefPubMedGoogle Scholar
  63. Tyler, S. (1986). Ultrastructure of a remarkable food-gathering organ in Flagellophora sp. (Turbellaria, Nemertodermatida). Transactions of the American Microscopical Society, 105, 90A.Google Scholar
  64. Tyler, S., & Hooge, M. (2004). Comparative morphology of the body wall in flatworms (Platyhelminthes). Canadian Journal of Zoology, 82, 194–210.CrossRefGoogle Scholar
  65. Voronezhskaya, E. E., Tyurin, S. A., & Nezlin, L. P. (2002). Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). Journal of Comparative Neurolology, 444, 25–38.CrossRefGoogle Scholar
  66. Voronezhskaya, E. E., Tsitrin, E. B., & Nezlin, L. P. (2003). Neuronal development in the larval polychaete Phyllodoce maculata (Phyllodocidae). Journal of Comparative Neurolology, 455, 299–309.CrossRefGoogle Scholar
  67. Wallberg, A., Curini-Galetti, M., Ahmadzadeh, A., & Jondelius, U. (2007). Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades. Zoologica Scripta, 36, 509–523.CrossRefGoogle Scholar
  68. Wanninger, A., & Haszprunar, G. (2003). The development of the serotonergic and FMRF-amidergic nervous system in Antalis entalis (Mollusca, Scaphopoda). Zoomorphology, 122, 77–85.Google Scholar
  69. Westblad, E. (1937). Die Turbellarien-Gattung Nemertoderma Steinböck. Acta Societatis pro Fauna et Flora Fennica, 60, 45–89.Google Scholar
  70. Westblad, E. (1940). Studien über skandinavische Turbellaria Acoela I. Arkiv för Zoologi, 32A(20), 1–82.Google Scholar
  71. Westblad, E. (1945). Studien über skandinavische Turbellaria Acoela III. Arkiv för Zoologi, 36A(5), 1–56.Google Scholar
  72. Westblad, E. (1946). Studien über skandinavische Turbellaria Acoela IV. Arkiv för Zoologi, 38A(1), 1–56.Google Scholar
  73. Westblad, E. (1948). Studien über skandinavische Turbellaria Acoela V. Arkiv för Zoologi, 41(7), 1–83.Google Scholar
  74. Westblad, E. (1949a). Xenoturbella bocki n.g., n.sp., a peculiar, primitive turbellarian type. Arkiv för Zoologi, 1, 3–29.Google Scholar
  75. Westblad, E. (1949b). On Meara stichopi (Bock) Westblad, a new representative of Turbellaria Archoophora. Arkiv för Zoologi, 1(5), 43–57.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2015

Authors and Affiliations

  • Olga I. Raikova
    • 1
    • 2
  • Inga Meyer-Wachsmuth
    • 3
    • 4
    • 5
  • Ulf Jondelius
    • 3
    • 4
  1. 1.Zoological Institute of the Russian Academy of SciencesSt.-PetersburgRussia
  2. 2.Saint-Petersburg State University, Faculty of Biology, Chair of Invertebrate ZoologySt.-PetersburgRussia
  3. 3.Department of ZoologySwedish Museum of Natural HistoryStockholmSweden
  4. 4.Department of ZoologyStockholm UniversityStockholmSweden
  5. 5.Institute of Parasitology, Biology Centre of the Czech Academy of SciencesČeské BudĕjoviceCzech Republic

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