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Morphology and evolution of the nervous system in Gnathostomulida (Gnathifera, Spiralia)

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Abstract

Within Spiralia, Gnathifera may represent the deepest branching lineage comprising the jaw worms Gnathostomulida and their sister group Micrognathozoa + Syndermata. Yet, very few nervous system studies have been conducted on this lineage of microscopic, jaw-bearing worms, limiting our understanding of the evolution of this organ system in Spiralia. The nervous system of representatives from all major groups of Gnathostomulida was here mapped using confocal laser scanning microscopy and immunohistochemistry. Their intra-epidermal, unsegmented nervous systems comprise an anterior brain and three to five ventral and two to four dorsal longitudinal nerves, connected by few transverse commissures. Neurites of the stomatogastric nervous system were found lining the pharynx and connecting to a prominent buccal ganglion. Supposedly, sensory ciliated cells in the pharynx and the gut were documented for the first time. Based on these morphological results, primary homologies of neural structures in Gnathostomulida and other Gnathifera were hypothesized and thereafter tested using parsimony. This first neurophylogeny of Gnathostomulida resulted in a topology congruent with molecular data, supporting the monophyly of Bursovaginoidea, Conophoralia, and Scleroperalia. From this topology, the evolution of the gnathostomulid nervous system was reconstructed. It suggests a specialization and diversification of cords and serotonin-like immunoreactive cell patterns from a plesiomorphic neuroarchitecture of three unsegmented nerve cords and a compact anterior brain and buccal ganglion. These plesiomorphic states resemble the nervous system of Micrognathozoa, and possibly the ancestral states of Spiralia.

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References

  • Ahlrichs, W. H. (1995). Seison annulatus und Seison nebaliae – Ultrastruktur und Phylogenie. Verhandlungen der Deutschen Zoologischen Gesellschaft, 88, 155.

    Google Scholar 

  • Ax, P. (1956). Die Gnasthostomulida, eine rätselhafte Wurmgruppe aus dem Meeressand. Verlag der Akademie der Wissenschaften und der Literatur Mainz, mathematisch-naturwissenschaftliche Klasse, 8, 1–32.

    Google Scholar 

  • Beckers, P., & van Döhren, J. (2016). Nemertea. In A. Schmidt-Rhaesa, S. Harzsch, & G. Purschke (Eds.), Structure and evolution of invertebrate nervous systems (pp. 148–165). New York: Oxford University Press.

    Google Scholar 

  • Bekkouche, N., & Worsaae, K. (2016). Nervous system and ciliary structures of Micrognathozoa (Gnathifera): evolutionary insight from an early branch in Spiralia. Open Science, 3(10), 160289.

    Google Scholar 

  • Bekkouche, N., Kristensen, R. M., Hejnol, A., Sørensen, M. V., & Worsaae, K. (2014). Detailed reconstruction of the musculature in Limnognathia maerski (Micrognathozoa) and comparison with other Gnathifera. Frontiers in Zoology, 11, 71.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brenzinger, B., Haszprunar, G., & Schrödl, M. (2013). At the limits of a successful body plan—3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod. Frontiers in Zoology, 10, 37.

    Article  PubMed  PubMed Central  Google Scholar 

  • Clement, P., & Wurdak, E. (1991). Rotifera. In F. W. Harris & E. E. Ruppert (Eds.), Microscopic anatomy of invertebrates (Vol. Volume 4, pp. 219–297). New York: Wiley-Liss.

    Google Scholar 

  • De Guerne, J. (1888). Excursions zoologiques dans les Isles de Fayal et de San Miguel (Açores). VII. Note monographique sur les rotiferes de la famille Asplanchnidae. In J. De Guerne (Ed.), Campagnes scientifiques du yacht monégasque l'Hirondelle (pp. 50–65). Paris: Gauthier-Villars et Fils, Imprimeurs-Libraires.

    Google Scholar 

  • Di Domenico, M., Martínez, A., Lana, P., & Worsaae, K. (2014). Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences. Molecular Phylogenetics and Evolution, 75, 202–218.

    Article  CAS  PubMed  Google Scholar 

  • Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., et al. (2008). Broad phylogenomic sampling improves resolution of the animal tree of life. Nature, 452(7188), 745–749.

    Article  CAS  PubMed  Google Scholar 

  • Ehrenberg, C. G. (1834). Organisation in der Richtung des kleinsten Raumes. Physiologische Abhandlungen: Dritter Beitrag.

    Google Scholar 

  • Farris, R. A. (1977). Three new species of Gnathostomulida from the West Atlantic. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 62(6), 765–796.

    Article  Google Scholar 

  • Fontaneto, D., & De Smet, W. (2015). 4. Rotifera. In A. Schmidt-Rhaesa (Ed.), Handbook of zoology, Gastrotricha and Gnathifera (pp. 217–300). Berlin, Munich and Boston: De Gruyter.

    Google Scholar 

  • Golombek, A., Tobergte, S., & Struck, T. H. (2015). Elucidating the phylogenetic position of Gnathostomulida and first mitochondrial genomes of Gnathostomulida, Gastrotricha and Polycladida (Platyhelminthes). Molecular Phylogenetics and Evolution, 86, 49–63.

    Article  PubMed  Google Scholar 

  • Hejnol, A., & Lowe, C. J. (2015). Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution. Philosophical Transactions of the Royal Society B, 370(1684), 20150045.

    Article  Google Scholar 

  • Herlyn, H., & Ehlers, U. (1997). Ultrastructure and function of the pharynx of Gnathostomula paradoxa (Gnathostomulida). Zoomorphology, 117(3), 135–145.

    Article  Google Scholar 

  • Higgins, R. P., & Thiel, H. (1988). Introduction to the study of meiofauna. Smithsonian Institution Press.

  • Hochberg, R. (2006). On the serotonergic nervous system of two planktonic rotifers, Conochilus coenobasis and C. dossuarius (Monogononta, Flosculariacea, Conochilidae). Zoologischer Anzeiger-A Journal of Comparative Zoology, 245(1), 53–62.

    Article  Google Scholar 

  • Hochberg, R. (2007). Topology of the nervous system of Notommata copeus (Rotifera: Monogononta) revealed with anti-FMRFamide, -SCPb, and -serotonin (5-HT) immunohistochemistry. Invertebrate Biology, 126(3), 247–256.

    Article  Google Scholar 

  • Hyman, L. H. (1951). IV. Class Rotifera. In L. H. Hyman (Ed.), The invertebrates: Acanthocephala, Aschelminthes, and Entoprocta. The pseudocoelomate Bilateria (Vol. Volume III, pp. 59–151). New York, Toronto, London: McGraw-Hill Book Company, Inc..

    Google Scholar 

  • Jenner, R. A. (2004). Towards a phylogeny of the Metazoa: evaluating alternative phylogenetic positions of Platyhelminthes, Nemertea, and Gnathostomulida, with a critical reappraisal of cladistic characters. Contributions to Zoology, 73(1/2), 3–163.

    Google Scholar 

  • Kerbl, A., Bekkouche, N., Sterrer, W., & Worsaae, K. (2015). Detailed reconstruction of the nervous and muscular system of Lobatocerebridae with an evaluation of its annelid affinity. BMC Evolutionary Biology, 15, 277.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirsteuer, E. (1969). On some species of Gnathostomulida from Bimini, Bahamas. Museum Novitates, 2356, 1–21.

    Google Scholar 

  • Knauss, E. B. (1979). Indication of an anal pore in Gnathostomulida. Zoologica Scripta, 8(1–4), 181–186.

    Article  Google Scholar 

  • Kocot, K. M., Struck, T. H., Merkel, J., Waits, D. S., Todt, C., Brannock, P. M. et al. (2016). Phylogenomics of Lophotrochozoa with consideration of systematic error. Systematic Biology, syw079.

  • Kotikova, E. A. (1998). Catecholaminergic neurons in the brain of rotifers. In E. Wurdak, R. Wallace, & H. Segers (Eds.), Rotifera VIII: a comparative approach (pp. 135–140) .Springer Netherlands

    Google Scholar 

  • Kotikova, E. A., Raikova, O. I., Reuter, M., & Gustafsson, M. K. (2005). Rotifer nervous system visualized by FMRFamide and 5-HT immunocytochemistry and confocal laser scanning microscopy. In A. Herzig, R. D. Gulati, C. D. Jersabek, & L. May (Eds.), Rotifera X: rotifer research: trends, new tools and recent advances (pp. 239–248). Netherlands: Springer.

    Google Scholar 

  • Kristensen, R. M., & Funch, P. (2000). Micrognathozoa: a new class with complicated jaws like those of Rotifera and Gnathostomulida. Journal of Morphology, 246(1), 1–49.

    Article  CAS  PubMed  Google Scholar 

  • Kristensen, R. M., & Nørrevang, A. (1977). On the fine structure of Rastrognathia macrostoma gen. et sp. n. placed in Rastrognathiidae fam. n. (Gnathostomulida). Zoologica Scripta, 6, 27–41.

    Article  Google Scholar 

  • Lammert, V. (1984). The fine structure of spiral ciliary receptors in Gnathostomulida. Zoomorphology, 104, 360–364.

    Article  Google Scholar 

  • Lammert, V. (1986). Vergleichende Ultrastruktur-Untersuchungen an Gnathostomuliden und die phylogenetische Bewertung ihrer Merkmale. PhD thesis, University of Göttingen.

  • Lammert, V. (1991). Gnathostomulida. In F. W. Harrison & E. E. Ruppert (Eds.), Microscopic anatomy of invertebrates (pp. 19–39). New York: Wiley-Liss.

    Google Scholar 

  • Laumer, C. E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R. C., Sørensen, M. V., et al. (2015). Spiralian phylogeny informs the evolution of microscopic lineages. Current Biology, 25(15), 2000–2006.

    Article  CAS  PubMed  Google Scholar 

  • Leasi, F., Pennati, R., & Ricci, C. (2009). First description of the serotonergic nervous system in a bdelloid rotifer: Macrotrachela quadricornifera Milne 1886 (Philodinidae). Zoologischer Anzeiger-A Journal of Comparative. Zoology, 248(1), 47–55.

    Google Scholar 

  • Leasi, F., Fontaneto, D., & Melone, G. (2010). Phylogenetic constraints in the muscular system of rotifer males: investigation on the musculature of males versus females of Brachionus manjavacas and Epiphanes senta (Rotifera, Monogononta). Journal of Zoology, 282(2), 109–119.

    Google Scholar 

  • Littlewood, D. T. J., Telford, M. J., Clough, K. A., & Rohde, K. (1998). Gnathostomulida—an enigmatic metazoan phylum from both morphological and molecular perspectives. Molecular Phylogenetics and Evolution, 9(1), 72–79.

    Article  CAS  PubMed  Google Scholar 

  • Martínez, A., Di Domenico, M., Rouse, G. W., & Worsaae, K. (2015). Phylogeny and systematics of Protodrilidae (Annelida) inferred with total evidence analyses. Cladistics, 31(3), 250–276.

    Article  Google Scholar 

  • Milne, W. (1886). On the defectiveness of the eye-spot as a means of generic distinction in the Philodinaea, with a description of two other Rotifera. Proceedings of the Philosophical Society of Glasgow.

  • Moraczewski, J., Czubaj, A., & Bąkowska, J. (1977). Organization and ultrastructure of the nervous system in Catenulida (Turbellaria). Zoomorphologie, 87(1), 87–95.

    Article  Google Scholar 

  • Müller, M. C., & Sterrer, W. (2004). Musculature and nervous system of Gnathostomula peregrina (Gnathostomulida) shown by phalloidin labeling, immunohistochemistry, and cLSM, and their phylogenetic significance. Zoomorphology, 123(3), 169–177.

    Article  Google Scholar 

  • Nielsen, C., & Worsaae, K. (2010). Structure and occurrence of cyphonautes larvae (Bryozoa, Ectoprocta). Journal of Morphology, 271(9), 1094–1109.

    Article  PubMed  Google Scholar 

  • Philippe, H., Brinkmann, H., Copley, R. R., Moroz, L. L., Nakano, H., Poustka, A. J., et al. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature, 470(7333), 255–258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pleijel, F. (1995). On character coding for phylogeny reconstruction. Cladistics, 11(3), 309–315.

    Article  Google Scholar 

  • Remane, A. (1927). Neue Gastrotricha Macrodasyidea. Zoologische Jahrbuecher Systematik, 54, 203–242.

    Google Scholar 

  • Reuter, M., Maule, A. G., Halton, D. W., Gustafsson, M. K. S., & Shaw, C. (1995). The organization of the nervous system in Plathelminthes. The neuropeptide Fimmunoreactive pattern in Catenulida, Macrostomida, Proseriata. Zoomorphology, 115, 83–97.

    Article  Google Scholar 

  • Riedl, R. J. (1970). On Labidognathia longicollis, nov. gen., nov. spec., from the West Atlantic Coast (Gnathostomulida). Internationale Revue der gesamten Hydrobiologie und Hydrographie, 55(2), 227–244.

    Article  Google Scholar 

  • Rieger, R. M., & Tyler, S. (1995). Sister-group relationship of Gnathostomulida and Rotifera-Acanthocephala. Invertebrate Biology, 114(2), 186–188.

    Article  Google Scholar 

  • Rieger, V., Perez, Y., Müller, C. H., Lipke, E., Sombke, A., Hansson, B. S., & Harzsch, S. (2010). Immunohistochemical analysis and 3D reconstruction of the cephalic nervous system in Chaetognatha: insights into the evolution of an early bilaterian brain? Invertebrate Biology, 129(1), 77–104.

    Article  Google Scholar 

  • Rothe, B. H., & Schmidt-Rhaesa, A. (2009). Architecture of the nervous system in two Dactylopodola species (Gastrotricha, Macrodasyida). Zoomorphology, 128(3), 227–246.

    Article  Google Scholar 

  • Rothe, B. H., Schmidt-Rhaesa, A., & Kieneke, A. (2011). The nervous system of Neodasys chaetonotoideus (Gastrotricha: Neodasys) revealed by combining confocal laserscanning and transmission electron microscopy: evolutionary comparison of neuroanatomy within the Gastrotricha and basal Protostomia. Zoomorphology, 130(1), 51–84.

    Article  Google Scholar 

  • Schmidt-Rhaesa, A. (2016). Gnathostomulida. In A. Schmidt-Rhaesa, S. Harzsch, & G. Purschke (Eds.), Structure and evolution of invertebrate nervous systems (pp. 118–121). New York: Oxford University Press.

    Google Scholar 

  • Schmidt-Rhaesa, A., & Rothe, B. H. (2016). Gastrotricha. In A. Schmidt-Rhaesa, S. Harzsch, & G. Purschke (Eds.), Structure and evolution of invertebrate nervous systems (pp. 141–147). New York: Oxford University Press.

    Google Scholar 

  • Sørensen, M. V. (2000). An SEM study of the jaws of Haplognathia rosea and Rastrognathia macrostoma (Gnathostomulida), with a preliminary comparison with the rotiferan trophi. Acta Zoologica, 81(1), 9–16.

    Article  Google Scholar 

  • Sørensen, M. V. (2002). Phylogeny and jaw evolution in Gnathostomulida, with a cladistic analysis of the genera. Zoologica Scripta, 31(5), 461–480.

    Article  Google Scholar 

  • Sørensen, M. V., & Giribet, G. (2006). A modern approach to rotiferan phylogeny: combining morphological and molecular data. Molecular Phylogenetics and Evolution, 40(2), 585–608.

    Article  PubMed  Google Scholar 

  • Sørensen, M. V., Tyler, S., Hooge, M. D., & Funch, P. (2003a). Organization of pharyngeal hard parts and musculature in Gnathostomula armata (Gnathostomulida: Gnathostomulidae). Canadian Journal of Zoology, 81(9), 1463–1470.

    Article  Google Scholar 

  • Sørensen, M. V., Funch, P., Hooge, M., & Tyler, S. (2003b). Musculature of Notholca acuminata (Rotifera: Ploima: Brachionidae) revealed by confocal scanning laser microscopy. Invertebrate Biology, 122(3), 223–230.

    Article  Google Scholar 

  • Sørensen, M. V., Sterrer, W., & Giribet, G. (2006). Gnathostomulid phylogeny inferred from a combined approach of four molecular loci and morphology. Cladistics, 22(1), 32–58.

    Article  Google Scholar 

  • Sterrer, W. (1966). Gnathostoula paradoxa und Vertreter von Pterognathia (ein neues Gnathostomuliden-Genus) von der schwedischen Westküste. Arkiv för Zoologi, Serie 2, 18(16), 405–413.

    Google Scholar 

  • Sterrer, W. (1969). Beiträge zur Kenntnis der Gnathostomulida I. Anatomie und Morphologie des Genus Pterognathia Sterrer. Arkiv för Zoologi, Serie 2, 22(1), 1–125.

    Google Scholar 

  • Sterrer, W. (1970). On some species of Austrognatharia, Pterognathia and Haplognathia nov. gen. from the North Carolina coast (Gnathostomulida). Internationale Revue der gesamten Hydrobiologie und Hydrographie, 55(3), 371–385.

    Article  Google Scholar 

  • Sterrer, W. (1972). Systematics and evolution within the Gnathostomulida. Systematic Biology, 21(2), 151–173.

    Article  Google Scholar 

  • Sterrer, W. (1998). Gnathostomulida from the (sub)tropical northwestern Atlantic. Studies on the natural history of the Caribbean region, 74(1), 1–178.

    Google Scholar 

  • Sterrer, W., & Sørensen, M. (2015). 2. Gnathostomulida. In A. Schmidt-Rhaesa (Ed.), Handbook of zoology, Gastrotricha and Gnathifera (pp. 135–196). Berlin, Munich and Boston: De Gruyter.

    Google Scholar 

  • Struck, T. H., Wey-Fabrizius, A. R., Golombek, A., Hering, L., Weigert, A., Bleidorn, C., et al. (2014). Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia. Molecular Biology and Evolution, 31(7), 1833–1849.

    Article  CAS  PubMed  Google Scholar 

  • Tyler, S., & Hooge, M. D. (2001). Musculature of Gnathostomula armata Riedl 1971 and its ecological significance. Marine Ecology, 22(1–2), 71–83.

    Article  Google Scholar 

  • Ware, R. W., & Lopresti, V. (1975). Three-dimensional reconstruction from serial sections. International Review of Cytology, 40, 325–440.

    Article  CAS  PubMed  Google Scholar 

  • Wilts, E. F., Ahlrichs, W. H., & Arbizu, P. M. (2009). The somatic musculature of Bryceella stylata (Milne, 1886)(Rotifera: Proalidae) as revealed by confocal laser scanning microscopy with additional new data on its trophi and overall morphology. Zoologischer Anzeiger-A Journal of Comparative Zoology, 248(3), 161–175.

    Article  Google Scholar 

  • Wilts, E. F., Wulfken, D., Ahlrichs, W. H., & Martínez Arbizu, P. (2012). The musculature of Squatinella rostrum (Milne, 1886) (Rotifera: Lepadellidae) as revealed by confocal laser scanning microscopy with additional new data on its trophi and overall morphology. Acta Zoologica, 93(1), 14–27.

    Article  Google Scholar 

  • Worsaae, K. (2005). Phylogeny of Nerillidae (Polychaeta, Annelida) as inferred from combined 18S rDNA and morphological data. Cladistics, 21(2), 143–162.

    Article  Google Scholar 

  • Worsaae, K., & Kristensen, R. M. (2003). A new species of Paranerilla (Polychaeta: Nerillidae) from northeast Greenland waters, arctic ocean. Cahiers de Biologie Marine, 44(1), 23–39.

    Google Scholar 

  • Worsaae, K., & Kristensen, R. M. (2005). Evolution of interstitial Polychaeta (Annelida). In T. Bartolomaeus & G. Purschke (Eds.), Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa (pp. 319–340). Netherlands: Springer.

    Chapter  Google Scholar 

  • Worsaae, K., & Müller, M. (2004). Nephridial and gonoduct distribution patterns in Nerillidae (Annelida: Polychaeta) examined by tubulin staining and cLSM. Journal of Morphology, 261(3), 259–269.

    Article  PubMed  Google Scholar 

  • Worsaae, K., & Rouse, G. W. (2008). Is Diurodrilus an annelid? Journal of Morphology, 269(12), 1426–1455.

    Article  PubMed  Google Scholar 

  • Worsaae, K., & Rouse, G. W. (2010). The simplicity of males: dwarf males of four species of Osedax (Siboglinidae; Annelida) investigated by confocal laser scanning microscopy. Journal of Morphology, 271(2), 127–142.

    Article  PubMed  Google Scholar 

  • Worsaae, K., Sterrer, W., & Iliffe, T. M. (2004). Longipalpa saltatrix, a new genus and species of the meiofaunal family Nerillidae (Annelida: Polychaeta) from an anchihaline cave in Bermuda. Proceedings of the Biological Society of Washington, 117(3), 346–362.

    Google Scholar 

  • Worsaae, K., Rimskaya-Korsakova, N. N., & Rouse, G. W. (2016). Neural reconstruction of bone-eating Osedax spp.(Annelida) and evolution of the siboglinid nervous system. BMC evolutionary biology, 16, 83.

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Acknowledgements

We are very grateful to Wolfgang Sterrer, who helped with taxonomical identification of examined Gnathostomulida. We are also indebted to M.V. Sørensen, R. M. Kristensen, and A. Schmidt-Rhaesa, who shared information on good sampling sites for Gnathostomulida; R. M. Kristensen additionally aided with helpful comments on sensory structures and discussions of his unpublished material. We wish to thank as well all our colleagues, who helped with sampling and collecting of the material (especially A. Kerbl, B. Gonzalez and A. Martínez). This study was supported by the Villum Foundation (grant no. 102544).

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  1. Marine Biological Section, Department of Biology, University of Copenhagen, Universitetsparken 4, 2100, Copenhagen Ø, Denmark

    Ludwik Gąsiorowski, Nicolas Bekkouche & Katrine Worsaae

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Gąsiorowski, L., Bekkouche, N. & Worsaae, K. Morphology and evolution of the nervous system in Gnathostomulida (Gnathifera, Spiralia). Org Divers Evol 17, 447–475 (2017). https://doi.org/10.1007/s13127-017-0324-8

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