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Ultrastructure of the stomochord and the heart–glomerulus complex in Rhabdopleura compacta (Pterobranchia): phylogenetic implications

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Abstract

Pterobranchia and Enteropneusta traditionally form the highest ranking sister taxa within the Hemichordata. The most prominent feature of all representatives of the Hemichordata is the stomochord, which is associated with an anterior excretory complex. The stomochord has been homologized with the notochord of the Chordata species, though this hypothesis is still under debate. Recently, even the validity and position of the Pterobranchia and the Hemichordata has been doubted. These uncertainties are along with a lack of information on the Rhabdopleurida, one of the highest ranking taxa within the Pterobranchia. This study analyzes the stomochord and the heart–glomerulus complex of Rhabdopleura compacta on the ultrastructural level. The data confirm that a glomerulus exists in representatives of the Rhabdopleurida, which previously was only known from the Cephalodiscida, the second highest ranking Pterobranchia taxon. The heart–glomerulus complex is, as expected, associated with the stomochord. Consisting of monociliated, non-vacuolated cells that form a monolayered epithelium of presumed ectodermal origin in R. compacta, the stomochord belongs to the ground pattern of the Pterobranchia and Enteropneusta. Information that would support a homology hypothesis of the chordate notochord and the hemichordate stomochord was not found. Furthermore, there is some evidence that the stomochord might represent a glandular organ. Thus, differences concerning the possible ontogenetic origin, morphology, and function are assumed to result from an independent evolution of the stomochord and the notochord.

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References

  • Andersson KA (1907) Die Pterobranchier der schwedischen Südpolarexpedition 1901–1903. Wiss Ergebn Schwed Südpolar-Exp 5:1–122

    Google Scholar 

  • Ax P (1996) Multicellular animals. A new approach to the phylogenetic order in nature, vol 1. Springer, Berlin Heidelberg New York

  • Ax P (2003) Multicellular animals. Order in nature—system made by man, vol 3. Springer, Berlin Heidelberg New York

  • Balser EJ (1985) Ultrastructure and function of the proboscis complex of Saccoglossus (Enteropneusta). Am Zool 25:41A

    Google Scholar 

  • Balser EJ, Ruppert EE (1990) Structure, ultrastructure, and function of the preoral heart–kidney in Saccoglossus kowalevskii (Hemichordata, Enteropneusta) including new data on the stomochord. Acta Zool 71:235–249

    Google Scholar 

  • Bargmann W, Hehn G von (1968) Über das Axial-Organ ("mysterious gland") von Asterias rubens. Z Zellforsch 88:262–277

    CAS  Google Scholar 

  • Bateson W (1884) Note on the later stages in the development of Balanoglossus kowalevskii (Agassiz), and on the affinities of the Enteropneusta. Proc R Soc Lond 38:23–30

    Google Scholar 

  • Bateson W (1886) The ancestry of the Chordata. Q J Microsc Sci 26:535–571

    Google Scholar 

  • Benito J, Pardos F (1997) Hemichordata. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 15. Wiley-Liss, New York, pp 15–101

  • Burghel P, Cloney RA (1997) Urochordata: Ascidiacea. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 15. Wiley-Liss, New York, pp 221–347

  • Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci U S A 97:4469–4474

    Article  CAS  PubMed  Google Scholar 

  • Cloney RA (1964) Development of the ascidian notochord. Acta Embryol Morphol Exp 7:111–130

    Google Scholar 

  • Dawydoff C (1948) Conception morphologique du stomochordé. In: Grassé PP (ed) Traité de Zoologie, vol 11. Masson, Paris, pp 510–532

  • Dilly PN, Welsch U, Rehkämper G (1986a) Fine structure of heart, pericardium and glomerular vessel in Cephalodiscus gracilis M'Intosh, 1882 (Pterobranchia, Hemichordata). Acta Zool 67:173–179

    Google Scholar 

  • Dilly PN, Welsch U, Rehkämper G (1986b) On the fine structure of the alimentary tract of Cephalodiscus gracilis (Pterobranchia, Hemichordata). Acta Zool 67:87–95

    Google Scholar 

  • Halanych KM (1995) The phylogenetic position of the Pterobranch hemichordates based on 18S rDNA sequence data. Mol Phyl Evol 4:72–76

    Article  CAS  Google Scholar 

  • Halanych KM (1996) Convergence in the feeding apparatuses of lophophorates and pterobranch hemichordates revealed by 18S rDNA: an interpretation. Biol Bull 190:1–5

    Google Scholar 

  • Harmer SF (1905) The Pterobranchia of the Siboga expedition with an account on other species. In: Weber M (ed) Résultats des explorations à bord du Siboga, monographie, vol 26. Brill, Leyden, pp 1–132

  • Hyman LH (1959) Phylum Hemichordata. In: Boell EJ (ed) The invertebrates, vol 5. McGraw-Hill, New York, pp 72–207

  • Komai T (1949) Internal structure of the pterobranch Atubaria heterolopha Sato, with an appendix on the homology of the notochord. Proc Jpn Acad 25:19–24

    Google Scholar 

  • Lester SM (1988) Settlement and metamorphosis of Rhabdopleura normani (Hemichordata: Pterobranchia). Acta Zool 69:111–120

    Google Scholar 

  • Masterman AT (1897) On the notochord of Cephalodiscus. Zool Anz 20:443–450

    Google Scholar 

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

  • Olsson R (1965) Comparative morphology and physiology of the Oikopleura notochord. Isr J Zool 14:213–220

    CAS  PubMed  Google Scholar 

  • Peterson KJ, Cameron RA, Tagawa K, Satoh N, Davidson EH (1999) A comparative molecular approach to mesodermal patterning in basal deuterostomes: the expression pattern of Brachyury in the enteropneust hemichordate Ptychodera flava. Development 126:85–95

    CAS  PubMed  Google Scholar 

  • Ridewood WG (1918) Cephalodiscus. British Antarctic ("terra nova") expedition, 1910. Natural history report. Zoology 4:11–82

    Google Scholar 

  • Ruppert EE (1997a) Introduction: microscopic anatomy of the notochord, heterochrony, and chordate evolution. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 15. Wiley-Liss, New York, pp 1–13

  • Ruppert EE (1997b) Cephalochordata (Acrania). In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 15. Wiley-Liss, New York, pp 349–504

  • Ruppert EE, Balser JB (1986) Nephridia in the larvae of hemichordates and echinoderms. Biol Bull 171:188–196

    Google Scholar 

  • Ruppert EE, Smith PR (1988) The functional organisation of filtration nephridia. Biol Rev 63:231–258

    Google Scholar 

  • Schepotieff A (1907a) Die Pterobranchier. Anatomische und histologische Untersuchungen über Rhabdopleura normani Allman und Cephalodiscus dodecalophus M'Int. 1. Teil. Rhabdopleura normani. 1. Abschnitt. Die Anatomie von Rhabdopleura. Zool Jahrb 23:463–534

    Google Scholar 

  • Schepotieff A (1907b) Die Pterobranchier. Anatomische und histologische Untersuchungen über Rhabdopleura normani Allman und Cephalodiscus dodecalophus M'Int. 1. Teil. Rhabdopleura normani. 2. Abschnitt. Knospungsprozess und Gehäuse von Rhabdopleura. Zool Jahrb 24:193–238

    Google Scholar 

  • Spengel JW (1893) Die Enteropneusten des Golfes von Neapel und der angrenzenden Meeresabschnitte. Fauna und Flora des Golfes von Neapel. 18. Monographie. Friedländer, Berlin

  • Tagawa K, Humphreys T, Satoh N (1998) Gene expression pattern. Novel pattern of Brachyury gene expression in hemichordate embryos. Mech Dev 75:139–143

    CAS  PubMed  Google Scholar 

  • Takacs CM, Moy VN, Peterson KJ (2002) Testing putative hemichordate homologues of the chordate dorsal nervous system and endostyle: expression of NK2.1 (TTF-1) in the acorn worm Ptychodera flava (Hemichordata, Ptychoderidae). Evol Dev 4:405–417

    Article  CAS  PubMed  Google Scholar 

  • Welsch U, Storch V (1969) Zur Feinstruktur der Chorda dorsalis niederer Chordaten (Dendrodoa grossularia (v. Beneden) und Oikopleura dioica Fol). Z Zellforsch 93:547–559

    CAS  Google Scholar 

  • Welsch U, Storch V (1970) Fine structure of the stomochord of the enteropneusts Harrimania kupfferi and Ptychodera flava. Z Zellforsch 107:234–239

    CAS  Google Scholar 

  • Welsch U, Dilly PN, Rehkämper G (1987) The fine structure of the stomochord in Cephalodiscus gracilis M'Intosh, 1882 (Hemichordata, Pterobranchia). Zool Anz 218:209–218

    Google Scholar 

  • Wilke U (1972a) Der Eicheldarm der Enteropneusten als Stützorgan für Glomerulus und Perikardialvesikel. Verh Dtsch Zool Ges 66:93–96

    Google Scholar 

  • Wilke U (1972b) Die Feinstruktur des Glomerulus von Glossobalanus minutus Kowalewsky (Enteropneusta). Cytobiologie 5:439–447

    Google Scholar 

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Acknowledgements

We thank Dr. C. Lüter and Prof. Dr. O. Kraus for criticizing the manuscript. We are also grateful to P. Grobe for collecting the material. This work was supported by the Studienstiftung des deutschen Volkes.

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  1. Systematik und Evolution der Tiere, Institut für Biologie - Zoologie, Freie Universität Berlin, Königin-Luise-Strasse 1–3, 14195, Berlin, Germany

    Georg Mayer & Thomas Bartolomaeus

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  1. Georg Mayer
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  2. Thomas Bartolomaeus
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Correspondence to Georg Mayer.

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Mayer, G., Bartolomaeus, T. Ultrastructure of the stomochord and the heart–glomerulus complex in Rhabdopleura compacta (Pterobranchia): phylogenetic implications. Zoomorphology 122, 125–133 (2003). https://doi.org/10.1007/s00435-003-0078-z

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