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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

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Abstract

We present a reconstruction of the nervous system of Neodasys chaetonotoideus Remane, 1927 (Gastrotricha, Chaetonotida) based on different microscopical methods: (1) immunohistochemistry (anti-acetylated α- and β-tubulin-, anti-5-HT- and anti-FMRFamide labelling) and (2) histochemistry (labelling of musculature and nuclei) by the means of confocal laser scanning microscopy (cLSM) and (iii) ultrastructure by means of transmission electron microscopy (TEM). All parts of the nervous system contain structures with an immunoreaction against the used immunohistochemical markers and labelling of histochemical markers. Results of both techniques (cLSM, TEM) reveal that the nervous system of N. chaetonotoideus is composed of a “dumb-bell-shaped” brain and one pair of posterior longitudinal neurite bundles. The brain is made up of a pair of laterally located clusters of neuronal somata, a large dorsal interconnecting dorsal commissure and two tiny ventral commissures in the region of the lateral clusters. From this, it follows that the brain is circumpharyngeal in position. The innervation of the head region is conducted by three pairs of anterior-directed neurite bundles. We describe here the gross anatomy of the nervous system and give additional details of the ultrastructure and the 5-HT and RFamide-like IR components of the nervous system. We compare our newly obtained data with already published data on the nervous system of gastrotrichs to reconstruct the hypothetical ground pattern of the nervous system in Gastrotricha, respectively, in Macrodasyida.

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References

  • Abbot NJ (1995) Morphology of nonmamalian glia cells: functional implications. In: Kettenmann H, Ransom BR (eds) Neuroglia. Oxford University Press Inc, New York, pp 97–119

    Google Scholar 

  • Ahlrichs W (1995) Ultrastruktur und Phylogenie von Seison nebaliae (Grube 1859) und Seison annulatus (Claus 1876). Hypothesen zu phylogenetischen Verwandtschafts-verhältnissen innerhalb der Bilateria. Cuvillier Verlag, Göttingen

    Google Scholar 

  • Ax P (2001) Multicellular animals III. Order in nature—system made by Man. Springer, Berlin

    Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and Function in the nervous system of invertebrates, vol 2. Freeman, San Francisco

    Google Scholar 

  • Chase DL, Koelle MR (2007). Biogenic amine neurotransmitters in C. elegans. In WormBook, pp 1–15

  • Colacino JM, Kraus DW (1984) Hemoglobine-containing cells of Neodasys (Gastrotricha, Chaetonotida)—II. Respiratory significance. Camp Biochem Physiol 79A(3):363–369

    CAS  Google Scholar 

  • Crittenden SL, Kimble J (1999) Confocal methods for Caenorhabditis elegans. In: Paddock SW (ed) Confocal microscopy methods and protocols. Humana Press, Totowa, New Jersey, pp 141–153

    Google Scholar 

  • Czeczuga B (1961) Haemoglobin in the Chironomus (Tendipes) annularius Meig. larvae from various growth classes. Naturwissenschaften 48:651–652

    Article  Google Scholar 

  • Duham-Scheel M, Patel NH (1999) Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126:2327–2334

    Google Scholar 

  • Ehlers U, Ahlrichs W, Lemburg C, Schmidt-Rhaesa A (1996) Phylogenetic systematization of the nemathelminthes (Aschelminthes). Verh Dtsch Zool Ges 89(1):8

    Google Scholar 

  • Gaerber CW, Salvenmoser W, Rieger RM, Gschwentner R (2007) The nervous system of Convolutriloba (Acoela) and its patterning during regeneration after asexual reproduction. Zoomorphology 126:73–87

    Article  Google Scholar 

  • Giribet G, Distel DLD, Polz M, Sterrer W, Wheeler WC (2000) Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Syst Biol 49:539–562

    Article  PubMed  CAS  Google Scholar 

  • Hirsch RE, Vidugiris GJ, Friedman JM, Harrington JP (1994) Alteration of tryptophan fluorescence properties upon dissociation of Lumbricus terrestris hemoglobin. Biochem Biophys Acta 1205(2):248–251

    Article  PubMed  CAS  Google Scholar 

  • Hirth F, Reichert H (2007) Basic nervous system types: one or many? In: Bullock TH, Krubitzer LA, Preuss TM, Rubenstein JLR, Strausfeld NJ, Striedter GF (eds) Evolution of nervous systems, vol I. Elsevier, London, San Diego, pp 57–69

    Google Scholar 

  • Hochberg R (2005) Musculature of the primitive gastrotrich Neodasys (Chaetonotida): functional adaptations to the interstitial environment and phylogenetic significance. Mar Biol 146:315–323

    Article  Google Scholar 

  • Hochberg R (2006) On the serotonergic nervous system of two planktonic rotifers, Conochilus coenobasis and C. dossuarius (Monogononta, Flosculariacea, Conochilidae). Zool Anz 245:53–62

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hochberg R (2007b) Comparative immunohistochemistry of the cerebral ganglion in Gastrotricha: an analysis of FMRFamidelike immunoreactivity in Neodasys cirritus (Chaetonotida), Xenodasys riedli and Turbanella cf. hyalina (Macrodasyida). Zoomophology 126:245–264

    Article  Google Scholar 

  • Hochberg R, Litvaitis MK (2000) Phylogeny of gastrotricha: a morphology-based framework of gastrotrich relationships. Biol Bull 198:299–305

    Article  PubMed  CAS  Google Scholar 

  • Hochberg R, Litvaitis MK (2001) The muscular system of Dactylopodola baltica and other macrodasyidan gastrotrichs in a functional and phylogenetic perspective. Zoologica Scripta 30:325–336

    Article  Google Scholar 

  • Hochberg R, Livaitis MK (2003) Ultrastructural and immunocytochemical observations of the nervous systems of three macrodasyidan gastrotrichs. Acta Zool 84:171–178

    Article  Google Scholar 

  • Joffe BI, Wikgren M (1995) Immunocytochemical distribution of 5-Ht (serotonin) in the nervous system of the gastrotrich Turbanella cornuta. Acta Zool 76:7–9

    Article  Google Scholar 

  • Kieneke A, Martínez Arbizu P, Ahlrichs WH (2007) Ultrastructure of the Protonephridial system of Neodasys chaetonotoideus (Gastrotricha: Chaetonotida) and in the ground pattern of Gastrotricha. J Morphol 268:602–613

    Article  PubMed  Google Scholar 

  • Kieneke A, Riemann O, Ahlrichs WH (2008) Novel implications for the basal internal relationships of Gastrotricha revealed by an analysis of morphological characters. Zool Scripta 37:429–460

    Article  Google Scholar 

  • Kieneke A, Ahlrichs WH, Martínez Arbizu P (2009) Morphology and function of reproductive organs in Neodasys chaetonotoideus (Gastrotricha: Neodasys) with a phylogenetic assessment of the reproductive system in Gastrotricha. Zool Scripta 38:289–311

    Article  Google Scholar 

  • Kraus DW, Travis PB, Colacino JM, Ruppert EE (1981) Occurrence of hemoglobin in Gastrotricha. Am Zool 21:950

    Google Scholar 

  • Ladurner P, Mair GR, Reiter D, Salvenmoser W, Rieger RM (1997) Serotonergic nervous system of two macrostomid species: recent or ancient divergence? Invertebr Biol 116(3):178–191

    Article  Google Scholar 

  • Lammert V (1986) Vergleichende ultrastruktur-untersuchungen an gnathostomuliden und die phylogenetische bewertung ihrer merkmale. PhD-Thesis. Universität Göttingen

  • Lammert V (1991) Gnathostomulida. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates 4: Aschelminthes. Wiley-Liss, New York, pp 19–39

    Google Scholar 

  • Loer-Lab homepage: http://home.sandiego.edu/~cloer/loerlab/5htcells.html

  • Luft JH (1964) Electron microscopy of cell extraneous coats as revealed by ruthenium red staining. J Cell Biol 23:54A–55A

    Google Scholar 

  • Luft JH (1971a) Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec 171:347–368

    Article  PubMed  CAS  Google Scholar 

  • Luft JH (1971b) Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat Rec 171:369–416

    Article  PubMed  CAS  Google Scholar 

  • Maddison WP, Maddison DR (1989) Interactive analysis of phylogeny and character evolution using the computer program MACCLADE. Folia Primatol 53:190–202

    Article  PubMed  CAS  Google Scholar 

  • Maddison DR, Maddison WP (2000) MACCLADE—analysis of phylogeny and character evolution, version 4.0. [computer software and manual]. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Maddison DR, Swofford DL, Maddison WP (1997) NEXUS: an extendible file format for systematic information. Syst Biol 46:590–621

    Article  PubMed  CAS  Google Scholar 

  • Maule AG, Geary TG, Marks NJ, Bowman JW, Friedman AR, Thompson DP (1999) Nematode FMRFamide peptide (FaRP)-systems: occurrence, distribution and physiology. Int J Parasitol 26(8/9):927–936

    Google Scholar 

  • Morris J, Cardona A, Del Mar De Miguel Bonet M, Hartenstein V (2007) Neurobiology of the basal platyhelminth Macrostomum lignano: map and digital 3D model of the juvenile brain neuropile. Dev Genes Evol 217:569–584

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nielsen C (2001) Animal evolution. Interrelationships of the living phyla, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Page RDM (2001). NDE—nexus data editor version 0.5.0. [computer software and manual]. Available via http://taxonomy.zoology.gla.ac.uk/rod/rod.html

  • Plesnila N, Putz C, Rinecker M, Wiezorrek J, Schleinkofer L, Goetz AE, Kuebler WM (2002) Measurement of absolute values of hemoglobin oxygenation in the brain of small rodents by near infrared reflection spectrophotometry. J Neurosci Methods 114:107–117

    Article  PubMed  CAS  Google Scholar 

  • Price DA, Greenberg MJ (1989) The hunting of the FaRPs: the distribution of FMRFamide-related peptides. Biol Bull 177:198–205

    Article  CAS  Google Scholar 

  • Remane A (1926) Morphologie und Verwandtschaftsbeziehungen der aberranten Gastrotrichen I. Z Morph Ökol Tiere 5:625–754

    Article  Google Scholar 

  • Remane A (1927) Neue Gastrotricha Macrodasyidea. Zool Jahrb Syst 54:203–242

    Google Scholar 

  • Remane A (1936) Gastrotricha und Kinorhyncha. In: Bronns HG (ed) Kl Ordn Tierreichs, vol 4, pp 1–385

  • Richter S, Loesel R, Purschke P, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Döring C, Faller S, Fritsch M, Grobe P, Hausen H, Heuer CM, Kaul S, Møller OS, Müller CHG, Rieger V, Rothe BH, Stegner MEJ, Harzsch S (2010) Invertebrate neurophylogeny—suggestions of terms and definitions for a neuroanatomical glossary. Front Zool 7(1):29

    Article  PubMed  Google Scholar 

  • Rieger RM, Ruppert EE (1978) Resin embedments of quantitative meiofauna samples for ecological and structural studies—description and application. Mar Biol 46:223–235

    Article  Google Scholar 

  • Romer AS, Parson TS (1991) Vergleichende Anatomie der Wirbeltiere, 5th edn. Verlag Paul Parey, Hamburg, Berlin

    Google Scholar 

  • Rothe BH, Schmidt-Rhaesa A (2008) Variation in the nervous system in three species of the genus Turbanella (Gastrotricha, Macrodasyida). Meiofauna Mar 16:175–184

    Google Scholar 

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

    Article  Google Scholar 

  • Rothe BH, Schmidt-Rhaesa A (2010a) Oregodasys cirratus, a new species of Gastrotricha (Macrodasyida) from Tenerife (Canary Islands), with a description of the muscular and nervous system. Meiofauna Mar 18:49–66

    Google Scholar 

  • Rothe BH, Schmidt-Rhaesa A (2010b) The structure of the nervous system in Tubiluchus troglodytes (Priapulida). Invertebr Biol 129(1):39–58

    Article  Google Scholar 

  • Ruppert EE (1982) Comparative ultrastructure of the gastrotrich pharynx and the evolution of myoepithelial foreguts in Aschelminthes. Zoomorphology 99:181–220

    Article  Google Scholar 

  • Ruppert EE (1991) Gastrotricha. In: Harrison F, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 4, Aschelminthes. Wiley, Washington, pp 41–109

    Google Scholar 

  • Ruppert EE, Travis PB (1983) Hemoglobin containing cells of Neodasys (Gastrotricha, Chaetonotida). I. Morphology and ultrastructure. J Morphol 175:57–64

    Article  Google Scholar 

  • Schinkmann K, Li C (1992) Localization of FMRFamide-like peptides in Caenorhabditis elegans. J Comp Neurol 316:251–260

    Article  PubMed  CAS  Google Scholar 

  • Teuchert G (1977) The ultrastructure of the marine gastrotrich Turbanella cornuta Remane (Macrodasyoidea) and its functional and phylogenetic importance. Zoomorphologie 88:189–246

    Article  Google Scholar 

  • Todaro MA, Hummon WD (2008) An overview and a dichotomous key to genera of the phylum Gastrotricha. Meiofauna Mar 16:3–20

    Google Scholar 

  • Todaro MA, Littlewood DTJ, Balsamo M, Herniou EA, Cassanelli S, Manicardi G, Wirz A, Tongiorgi P (2003) The interrelationships of the Gastrotricha using nuclear small rRNA subunit sequence data, with an interpretation based on morphology. Zool Anz 242:145–156

    Article  Google Scholar 

  • Todaro AM, Telford MJ, Lockyer AE, Littlewood DTJ (2006) Interrelationships of the Gastrotricha and their place among the Metazoa inferred from 18S rRNA genes. Zool Scripta 35(3):251–259

    Article  Google Scholar 

  • Travis PB (1983) Ultrastructural study of body wall organization and Y-cell composition in the Gastrotricha. Z Zool Syst Evol 21:52–68

    Article  Google Scholar 

  • Uhlig G (1964) Eine einfache Methode zur Extraction der vagilen, mesopsammalen Mikrofauna. Helgoländer Wiss Meeresunt 11:151–157

    Google Scholar 

  • Van der Ploet M, van Dujin P (1979) Reflection versus fluorescence—a note on the physical backgrounds of two types of light microscopy. Histochem 62:227–232

    Article  Google Scholar 

  • Wallberg A, Curini-Galletti M, Ahmadzadeh A, Jondelius U (2007) Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades. Zool Scripta 36:509–523

    Article  Google Scholar 

  • Wanninger A (2007) The application of confocal microscopy and 3D imaging software in functional, evolutionary, and developmental zoology: reconstructing myo- and neurogenesis in space and time. In: Mendez-Vilas A, Dias J (eds) Modern research and educational topics in microscopy. Formatex, Badajoz, Spain, pp 353–361

    Google Scholar 

  • Wiedermann A (1995) Zur ultrastruktur des nervensystems bei Cephalodasys maximus (Macrodasyida, Gastrotricha). Microfauna Mar 10:173–233

    Google Scholar 

  • Zeis B, Becher B, Goldmann T, Clark R, Vollmer E, Bölke B, Bredebusch I, Lamkemeyer T, Pinkhaus O, Pirow R, Paul RJ (2003) Differential haemoglobin gene expression in the crustacean Daphnia magna exposed to different oxygen partial pressures. Biol Chem 384:1133–1145

    Article  PubMed  CAS  Google Scholar 

  • Zelinka C (1889) Die gastrotrichen. Eine monographische darstellung ihrer anatomie, biologie und systematik. Zeitschr f Wissensch Zoologie 49:209–384

    Google Scholar 

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Acknowledgments

Many thanks to the people at the Wadden Sea Station (AWI) in List/Sylt, especially to Werner Armonies. BHR and ASR were supported by a grant of the Deutsche Forschungsgemeinschaft (DFG) (SCHM 1278/8-2) within the frame of the focal program Deep Metazoan phylogeny (SPP 1174). Two anonymous referees are also acknowledged for offering suggestions that greatly improved the manuscript.

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  1. Biozentrum Grindel und Zoologisches Museum, Universität Hamburg, Niedere Tiere I. Martin-Luther-King Platz 3, 20146, Hamburg, Germany

    Birgen H. Rothe & Andreas Schmidt-Rhaesa

  2. Forschungsinstitut und Naturmuseum Senckenberg, Deutsches Zentrum für Marine Biodiversitätsforschung, Südstrand 44, 26382, Wilhelmshaven, Germany

    Alexander Kieneke

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  1. Birgen H. Rothe
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Correspondence to Birgen H. Rothe.

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Communicated by T. Bartolomaeus.

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Rothe, B.H., Schmidt-Rhaesa, A. & Kieneke, A. 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, 51–84 (2011). https://doi.org/10.1007/s00435-011-0123-2

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