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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Notes
According to the common definition (e.g., Lammert 1986), a myoepitheliocyte contains myofilaments and resides distally of the basal lamina.
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
Amin OM (2013) Classification of the Acanthocephala. Folia Parasitol 60:273–305
Ax P (1956) Die Gnasthostomulida, eine rätselhafte Wurmgruppe aus dem Meeressand. Abh math-naturw Kl Akad Wiss Mainz 8:1–32
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
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
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
Dunagan TT, Miller DM (1976) Nerves originating from the cerebral ganglion of Moniliformis moniliformis (Acanthocephala). J Parasitol 62:442–450
Fontaneto D, de Smet W (2015) Rotifera. In: Schmidt-Rhaesa A (ed) Handbook of zoology, Gastrotricha and Gnathifera. De Gruyter, Berlin, pp 217–300
Fröbius AC, Funch P (2016) Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans. Nat Commun 8:9
Gąsiorowski L, Bekkouche N, Worsaae K (2017) Morphology and evolution of the nervous system in Gnathostomulida (Gnathifera, Spiralia). Org Divers Evol 17:447–475
Giribet G (2016) New animal phylogeny: future challenges for animal phylogeny in the age of phylogenomics. Org Divers Evol 16:419–426
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
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
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
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
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
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
Horseman ND, Collier RJ (2014) Serotonin: a local regulator in the mammary gland epithelium. Annu Rev Anim Biosci 2:353–374
Kotikova EA (1995) Localization and neuroanatomy of catecholaminergic neurons in some rotifer species. Hydrobiologia 313(314):123–127
Kotikova EA (1998) Catecholaminergic neurons in the brain of rotifers. Hydrobiologia 387(388):135–140
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
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
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
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
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
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
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
Monks S, Richardson DJ (2011) Phylum Acanthocephala. Zootaxa 3148:234–237
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
Ricci C (2017) Bdelloid rotifers: ‘sleeping beauties’ and ‘evolutionary scandals’, but not only. Hydrobiologia 796:277–285
Ricci C, Melone C, Sotgia C (1993) Old and new data on Seisonidea (Rotifera). Hydrobiologia 255(256):495–511
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
Rieger RM, Tyler S (1995) Sister-group relationship of Gnathostomulida and Rotifera-Acanthocephala. Invertebr Biol 114:186–188
Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, Oxford
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
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
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
von Haffner K (1950) Organisation und systematische Stellung der Acanthocephalen. Zool Anz 145:243–274
Welch DBM (2000) Evidence from a protein-coding gene that acanthocephalans are rotifers. Invertebr Biol 119:17–26
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
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
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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DOI: https://doi.org/10.1007/s00435-017-0369-4