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Enigmatic Gnathostomulida (Gnathifera, Spiralia): about monociliated pharyngeal receptors and the pharyngeal nervous system

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Abstract

It was lately suggested that cilia inside the pharynx of Gnathostomulida are a novel finding and that Herlyn and Ehlers (Zoomorphology 117:135–145, 1997) did not observe anything corresponding to a buccal ganglion in the pharynx of Gnathostomula paradoxa (Gnathostomulida). However, monociliated pharyngeal receptors were repeatedly reported for Gnathostomulida since the 1980th, and every statement of absent ciliation in the cited study referred to the pharyngeal epithelium excluding the imbedded receptors. Moreover, Herlyn and Ehlers stated that they did not regard the questionable nervous differentiation in the hind pharynx of Gnathostomulida as a buccal ganglion due to lacking evidence of an extra basal lamina sheath. The present study shows that it is also uncertain if the structure fulfills another frequently applied criterion of a ganglion, i.e., an arrangement of perikarya and neuropil in such a manner that the first enclose the latter. Notwithstanding the alternative definitions used, the transmission electron micrographs presented herein also confirm previous findings. Thus, the nervous differentiation in the posterior pharynx (buccal ganglion) gives rise to one weaker dorso-median nerve and two stronger lateral nerves which connect with the distal ciliated portions of the pharyngeal receptors. The single cilium of each receptor extends from the bottom of a pit into the pharyngeal cavity, whereby its proximal section is surrounded by eight microvilli. A survey on the considerable discrepancies between the descriptions of buccal/mastax/pharyngeal ganglia in Gnathostomulida, Micrognathozoa, Monogononta, Bdelloidea, Seisonidea, and Acanthocephala (present/absent, inside/outside the pharynx, ventrally/dorsally in the pharynx, ganglion/plexus, etc.) concludes this study.

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Fig. 1
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Fig. 4

All transmission electron micrographs modified after Lammert (1986, his Figs. 22A, 22B, 49D, 54A, 63A, 61A, 48C)

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Notes

  1. To the best of my knowledge, Sterrer et al. (1985) referred to Lammert (1981).

  2. According to the common definition (e.g., Lammert 1986), a myoepitheliocyte contains myofilaments and resides distally of the basal lamina.

  3. A single neurite crossing an agglomeration of perikarya in Fig. 9 of Kristensen and Nørrevang (1977) is not to be concealed; but a neuropil is actually defined as a cluster of neurites (see Richter et al. 2010).

References

  • Ahlrichs WH (1995) Ultrastruktur und Phylogenie von Seison nebaliae (Grube 1859) und Seison annulatus (Claus 1876)—Hypothesen zu phylogenetischen Verwandtschaftsverhältnissen innerhalb der Bilateria. Cuvillier Verlag, Göttingen (Dissertation, University of Göttingen)

  • Ahlrichs WH (1997) Epidermal ultrastructure of Seison nebaliae and Seison annulatus, and a comparison of epidermal structures within the Gnathifera. Zoomorphology 117:41–48

    Article  Google Scholar 

  • Amin OM (2013) Classification of the Acanthocephala. Folia Parasitol 60:273–305

    Article  PubMed  Google Scholar 

  • Ax P (1956) Die Gnasthostomulida, eine rätselhafte Wurmgruppe aus dem Meeressand. Abh math-naturw Kl Akad Wiss Mainz 8:1–32

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Clément P, Wurdak E (1991) Rotifera. In: Harris FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 4. Wiley-Liss, New York, pp 219–297

    Google Scholar 

  • Dunagan TT, Miller DM (1976) Nerves originating from the cerebral ganglion of Moniliformis moniliformis (Acanthocephala). J Parasitol 62:442–450

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Fröbius AC, Funch P (2016) Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans. Nat Commun 8:9

    Article  Google Scholar 

  • Gąsiorowski L, Bekkouche N, Worsaae K (2017) Morphology and evolution of the nervous system in Gnathostomulida (Gnathifera, Spiralia). Org Divers Evol 17:447–475

    Article  Google Scholar 

  • Giribet G (2016) New animal phylogeny: future challenges for animal phylogeny in the age of phylogenomics. Org Divers Evol 16:419–426

    Article  Google Scholar 

  • Herlyn H (1996) Ultrastruktur des Verdauungssystems von Gnathostomula paradoxa (Ax 1956) mit ausführlicher Betrachtung von Kiefer und Basalplatte—Phylogenetische Bewertung der Merkmale. Diploma thesis, University of Göttingen

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

    Article  Google Scholar 

  • Herlyn H, Taraschewski H (2017) Evolutionary anatomy of the muscular apparatus involved in the anchoring of Acanthocephala to the intestinal wall of their vertebrate hosts. Parasitol Res 116:1207–1225

    Article  PubMed  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 (2007) 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 A, Hochberg R (2015) Serotonin immunoreactivity in the nervous system of the free-swimming larvae and sessile adult females of Stephanoceros fimbriatus (Rotifera: Gnesiotrocha). Invertebr Biol 134:261–270

    Article  Google Scholar 

  • Hochberg R, Lilley G (2010) Neuromuscular organization of the freshwater colonial rotifer, Sinantherina socialis, and its implications for understanding the evolution of coloniality in Rotifera. Zoomorphology 129:153–162

    Article  Google Scholar 

  • Horseman ND, Collier RJ (2014) Serotonin: a local regulator in the mammary gland epithelium. Annu Rev Anim Biosci 2:353–374

    Article  CAS  PubMed  Google Scholar 

  • Kotikova EA (1995) Localization and neuroanatomy of catecholaminergic neurons in some rotifer species. Hydrobiologia 313(314):123–127

    Article  Google Scholar 

  • Kotikova EA (1998) Catecholaminergic neurons in the brain of rotifers. Hydrobiologia 387(388):135–140

    Article  Google Scholar 

  • Kotikova EA, Raikova OI, Reuter M, Gustafsson MK (2005) Rotifer nervous system visualized by FMRFamide and 5-HT immunocytochemistry and confocal laser scanning microscopy. Hydrobiologia 546:239–248

    Article  Google Scholar 

  • Kristensen RM, Nørrevang A (1977) On the fine structure of Rastrognathia macrostoma gen. et sp.n. placed in Rastrognathiidae fam.n. (Gnathostomulida). Zool Scr 6:27–41

    Article  Google Scholar 

  • Lammert V (1981) Ultrastruktur des Pharynx von Haplognathia rosea (Sterrer, 1968). Diploma thesis, University of Göttingen

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

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

    Google Scholar 

  • Laumer CE, Bekkouche N, Kerbl A Goetz, Neves RC, Sørensen MV, Kristensen RM, Hejnol A, Dunn CW, Giribet G, Worsaae K (2015) Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol 25:1–7

    Article  Google Scholar 

  • Leasi F, Ricci C (2010) Musculature of two bdelloid rotifers, Adineta ricciae and Macrotrachela quadricornifera: organization in a functional and evolutionary perspective. J Zool Syst Evol Res 48:33–39

    Article  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). Zool Anz 248:47–55

    Article  Google Scholar 

  • Melone G, Ricci C, Segers H, Wallace RL (1998) Phylogenetic relationships of phylum Rotifera with emphasis on the families of Bdelloidea. Hydrobiologia 387(388):101–107

    Article  Google Scholar 

  • Monks S, Richardson DJ (2011) Phylum Acanthocephala. Zootaxa 3148:234–237

    Google Scholar 

  • Müller MC, 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 

  • Ricci C (2017) Bdelloid rotifers: ‘sleeping beauties’ and ‘evolutionary scandals’, but not only. Hydrobiologia 796:277–285

    Article  Google Scholar 

  • Ricci C, Melone C, Sotgia C (1993) Old and new data on Seisonidea (Rotifera). Hydrobiologia 255(256):495–511

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Rieger RM, Tyler S (1995) Sister-group relationship of Gnathostomulida and Rotifera-Acanthocephala. Invertebr Biol 114:186–188

    Article  Google Scholar 

  • Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, Oxford

    Book  Google Scholar 

  • Sielaff M, Schmidt H, Struck TH, Rosenkranz D, Welch M, David B, Hankeln T, Herlyn H (2016) Phylogeny of Syndermata (syn. Rotifera): mitochondrial gene order verifies epizoic Seisonidea as sister to endoparasitic Acanthocephala within monophyletic Hemirotifera. Mol Phylogenet Evol 96:79–92

    Article  CAS  PubMed  Google Scholar 

  • Sterrer W, Mainitz M, Rieger RM (1985) Gnathostomulida: enigmatic as ever. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp 181–199

    Google Scholar 

  • Struck TH, Wey-Fabrizius AR, Golombek A, Hering L, Weigert A, Bleidorn C, Klebow S, Iakovenko N, Hausdorf B, Petersen M, Kück P, Herlyn H, Hankeln T (2014) Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia. Mol Biol Evol 31:1833–1849

    Article  CAS  PubMed  Google Scholar 

  • von Haffner K (1950) Organisation und systematische Stellung der Acanthocephalen. Zool Anz 145:243–274

    Google Scholar 

  • Welch DBM (2000) Evidence from a protein-coding gene that acanthocephalans are rotifers. Invertebr Biol 119:17–26

    Article  Google Scholar 

  • Wey-Fabrizius AR, Herlyn H, Rieger B, Rosenkranz D, Witek A, Welch DBM, Mark EI, Hankeln T (2014) Transcriptome data reveal syndermatan relationships and suggest the evolution of endoparasitism in Acanthocephala via an epizoic stage. PLoS One 9:e88618

    Article  PubMed  PubMed Central  Google Scholar 

  • Witek A, Herlyn H, Ebersberger I, Mark Welch DB, Hankeln T (2009) Support for the monophyletic origin of Gnathifera from phylogenomics. Mol Phylogenet Evol 53:1037–1041

    Article  PubMed  Google Scholar 

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Acknowledgements

The beginning of the title is borrowed from Sterrer et al. (1985), and picks up the title of Ax’ (1956) seminal paper “Die Gnasthostomulida, eine rätselhafte Wurmgruppe aus dem Meeressand.” Lammert could not be asked for permission of using his TEM images in present Fig. 4 as he passed away. I would like to thank Bernd Baumgart, University of Göttingen, Germany, whose archival inclination has proved to be highly advantageous for the present study. My thanks go further to two reviewers, whose comments improved the manuscript.

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Herlyn, H. Enigmatic Gnathostomulida (Gnathifera, Spiralia): about monociliated pharyngeal receptors and the pharyngeal nervous system. Zoomorphology 136, 425–434 (2017). https://doi.org/10.1007/s00435-017-0369-4

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