Skip to main content
SpringerLink
Log in

Comparative anatomy of the heart–glomerulus complex of Cephalodiscus gracilis (Pterobranchia): structure, function, and phylogenetic implications

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

Abstract

Cephalodiscus gracilis Harmer, 1905 is a semi-sessile deuterostome that shares with fish-like chordates pharyngeal gill slits and a dorsally situated brain. In order to reveal structures potentially homologous among deuterostomes and to infer their functional roles, we investigated the axial complex, associated blood vessels and structures of C. gracilis using transmission electron microscopy, light microscopy, and digital 3D reconstructions. We describe the smooth, bipartite cephalic shield retractor muscles that originate as solid compact muscles and fan out to traverse the protocoel as individual muscle cells. The axial complex consists of a cap-shaped coelomic sac, the pericardium that surrounds the central heart. The pericardium is constituted of myoepithelial cells, with the cells facing the heart being thicker and richer in myofilaments. A prominent dorsal median blood vessel opens into the heart, which gives rise to a short median ventral vessel that opens into the paired glomeruli connected to the ventral side of the stomochord. The tip of the curved stomochord rests precisely above the connection of the dorsal median vessel with the heart, a position that would allow the stomochord to function as a valve facilitating unidirectional blood flow. Glomeruli are lined by podocytes of the spacious protocoel and are considered to be the site of ultrafiltration. Two pairs of blood vessels enter the median dorsal blood vessel from the tentacles. The median dorsal blood vessel is separated from the brain by a thin basement membrane. This arrangement is consistent with the hypothesis that blood vessels in the tentacles increase oxygen supply for the brain. Based on detailed similarities, the heart–glomerulus complex of C. gracilis is considered homologous with the heart–glomerulus complex in Rhabdopleura spp., and Enteropneusta, and the axial complex in Echinodermata. In addition, we hypothesize homology to the excretory complex including Hatschek’s nephridium in Cephalochordata. Thus, the heart–glomerulus complex does not support a sister-group relationship between Echinodermata and Hemichordata, whereas the organization of the cephalic shield retractor muscles is consistent with the evolution of pterobranchs within enteropneusts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36(2):199–221

    Article  Google Scholar 

  • Arendt D, Nübler-Jung K (1995) Inversion of dorsoventral axis? Nature 371:26

  • Arendt D, Nübler-Jung K (1999) Comparison of early nerve cord development in insects and vertebrates. Development 126:2309–2325

    CAS  PubMed  Google Scholar 

  • Ax P (2001) Das System der Metazoa: ein Lehrbuch der phylogenetischen Systematik. Spektrum Akademischer Verlag GmbH, Heidelberg, Berlin

  • Balser E, Ruppert E (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

    Article  Google Scholar 

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

    Google Scholar 

  • Cameron CB (2005) A phylogeny of the hemichordates based on morphological characters. Can J Zool 83:196–215

    Article  Google Scholar 

  • Cannon JT, Rychel AL, Eccleston H, Halanych KM, Swalla BJ (2009) Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Mol Phylogenet Evol 52(1):17–24

    Article  CAS  PubMed  Google Scholar 

  • Caron J-B, Conway Morris S, Shu D (2010) Tentaculate fossils from the Cambrian of Canada (British Columbia) and China (Yunnan) interpreted as primitive deuterostomes. PLoS One 5(3):e9586

    Article  PubMed Central  PubMed  Google Scholar 

  • Caron J-B, Morris SC, Cameron CB (2013) Tubicolous enteropneusts from the Cambrian period. Nature advance online publication

  • Cerfontaine P (1906) Recherches sur le développment de l’Amphioxus. Archives de Biologie 22:229–418

  • Clark RB (1964) Dynamics in the metazoan evolution. The origin of the coelom and segments. Oxford, Clarendon

    Google Scholar 

  • Conklin EG (1932) The embryology of amphioxus. J Morphol 54:69–151

    Google Scholar 

  • De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308

    Article  PubMed Central  PubMed  Google Scholar 

  • De Robertis EM, Sasai Y (2000) A common plan for dorsoventral patterning in Bilateria. Nature 380:37–40

    Google Scholar 

  • Dilly PN (1985) The habitat and behavior of Cephalodiscus gracilis (Pterobranchia: Hemichordata) from Bermuda. J Zool 230:63–67

    Google Scholar 

  • Dilly PN, Welsch U, Rehkämper G (1986) Fine structure of heart, pericardium and glomerular vessel in Cephalodiscus gracilis M’Intosh, 1882 (Pterobranchia, Hemichordata). Acta Zool 67(3):173–179

    Article  Google Scholar 

  • Dunn C, Hejnol A, Matus D, Pang K, Browne W, Smith S, Seaver E, Rouse G, Obst M, Edgecombe G, Sorensen M, Haddock S, Schmidt-Rhaesa A, Okusu A, Kristensen R, Wheeler W, Martindale M, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Google Scholar 

  • Edgecombe G, Giribet G, Dunn C, Hejnol A, Kristensen R, Neves R, Rouse G, Worsaae K, Sørensen M (2011) Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11:151–172

    Google Scholar 

  • Fauchald K (1974) Polychaete phylogeny: a problem in protostome evolution. Syst Biol 23(4):493–506

    Article  Google Scholar 

  • Franz V (1925) Morphologische und ontogenetische Akranierstudien über Darm, Trichter, Zölomderivate, Muskulatur- und Bindegewebsformationen. Jenaische Zeitschrift für Naturwissenschaft 61:407–468

  • Franz V (1927) Morphologie der Akranier. Zeitschrift für die gesamte Anatomie 27(III. Abt.):464–692

    Google Scholar 

  • Garstang W (1928) The morphology of the Tunicata, and its bearings on the phylogeny of the Chordata. Q J Microscopical Sci 72:51–187

    Google Scholar 

  • Geoffroy Saint-Hilaire E (1822) Considerations generales sur la vertebre. Mem Mus d’Hist Nat 9:89–119

    Google Scholar 

  • Gudo M, Syed T (2008) 100 years of Deuterostomia (GROBBEN, 1908): cladogenetic and anagenetic relations within the Notoneuralia domain. ArXiv Publication

  • Gutmann WF (1981) Relationships between invertebrate phyla based on functional-mechanical analysis of the hydrostatic skeleton. Am Zool 21:63–81

    Google Scholar 

  • Holland ND, Holland LZ (2006) Stage- and tissue-specific patterns of cell division in embryonic and larval tissues of amphioxus during normal development. Evol Dev 8(2):142–149

    Article  PubMed  Google Scholar 

  • Kaul-Strehlow S, Stach T (2011) The pericardium in the deuterostome Saccoglossus kowalevskii (Enteropneusta) develops from the ectoderm via schizocoely. Zoomorphology 130:107–120

    Article  Google Scholar 

  • Kriebel ME (1967) Conduction velocity and intracellular action potentials of the tunicate heart. J Gen Physiol 50(8):2097–2107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lankester ER (1877) Notes on the embryology and classification of the animal kingdom: comprising a revision of speculations relative to the origin and significance of the germ-layers. Q J Microscopic Sci 17:399–454

    Google Scholar 

  • Lapraz F, Besnardeau L, Lepage T (2009) Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network. PLoS Biol 7:e1000248

    Google Scholar 

  • Lester SM (1985) Cephalodiscus sp. (Hemichordata: Pterobranchia): observations of functional morphology, behavior and occurrence in shallow water around Bermuda. Mar Biol 85:263–268

    Google Scholar 

  • Lowe CJ, Terasaki M, Wu M, Freeman Jr. RM, Runft L, Kwan K, Haigo S, Aronowicz J, Lander E, Gruber C, Smith M, Kirschner M, Gerhart J (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4:e291

  • Malakhov VV (1977) The problem of the basic structural plan in various groups of Deuterostomia. Zhurnal Obshey Biologii 38:485–499

    Google Scholar 

  • Mayer G, Bartolomaeus T (2003) Ultrastructure of the stomochord and the heart-glomerulus complex in Rhabdopleura compacta (Pterobranchia): phylogenetic implications. Zoomorphology 122:125–133

    Article  Google Scholar 

  • Metschnikoff V (1881) Über die systematische Stellung von Balanoglossus. Zool Anz 4:139–157

    Google Scholar 

  • Nielsen C (1995) Animal evolution. Oxford University Press, New York, Tokyo

    Google Scholar 

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

    Google Scholar 

  • Nielsen C (2012) Animal evolution. Interrelationships of the living phyla. Oxford University Press, Oxford, p 402

    Google Scholar 

  • Nübler-Jung K, Arendt D (1994) Is ventral in insects dorsal in vertebrates? Roux's Arch Dev Biol 203:357–366

    Google Scholar 

  • Nübler-Jung K, Arendt D (1999) Dorsoventral axis inversion: enteropneust anatomy links invertebrates to chordates turned upside down. J Zool Syst Evol Res 37:93–100

    Google Scholar 

  • Perseke M, Hetmank J, Bernt M, Stadler P, Schlegel M, Bernhard D (2011) The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria. BMC Evol Biol 11:134

    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

    Google Scholar 

  • Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470:255–258

    Google Scholar 

  • Rähr H (1979) The circulatory system of amphioxus (Branchiostoma lanceolatum (Pallas): a light-microscopic investigation based on intravascular injection technique. Acta Zool 60:1–18

    Article  Google Scholar 

  • Ridewood WG (1907) Pterobranchia: Cephalodiscus. National Antarctic expedition 1901-4 discovery reports—natural history. British Museum, London, pp 1–67

  • Ritter WE (1902) The movements of the Enteropneusta and the mechanism by which they are accomplished. Biol Bull 3(6):255–261

    Article  Google Scholar 

  • Ruppert EE (1996) Morphology of Hatschek's nephridium in larval and juvenile stages of Branchiostoma virginiae (Cephalochordata). Isr J Zool 42:161–182

    Google Scholar 

  • Ruppert EE (1997a) Cephalochordata (Acrania). In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates Hemichordata, Chaetognatha, and the invertebrate chordates. Wiley-Liss, New York, pp 349–504

    Google Scholar 

  • Ruppert EE (1997b) Introduction: microscopic anatomy of the notochord, heterochrony, and chordate evolution. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates. Hemichordata, Chaetognatha, and the invertebrate chordates, vol 15. Willey-Liss, Incorporation, New York, Chichester, Weinheim, Brisbane, Singapore, Toronto, pp 1–13

  • Ruppert EE (2005) Key characters uniting hemichordates and chordates: homologies or homoplasies? Can J Zool 83:8–23

    Article  Google Scholar 

  • Satoh N, Tagawa K, Takahashi H (2012) How was the notochord born? Evol Dev 14(1):56–75

    CAS  PubMed  Google Scholar 

  • Schepotieff A (1907) Die Pterobranchier. Zoologische Jahrbücher Abteilung für Anatomie 23:463–534, Tafeln 425–433

    Google Scholar 

  • Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, Oxford, p 363

    Book  Google Scholar 

  • Skramlik E (1938a) Über den Kreislauf bei den niederen Chordaten. Ergebnisse der Biologie 15:166–308

    Google Scholar 

  • Skramlik Ev (1938b) Vorgänge im Kreislaufsystem von Amphioxus lanceolatus Y. Reichsstelle für den Unterrichtsfilm Film C 267, issue 3, pp 1–11

  • Stach T (1998) Coelomic cavities may function as a vascular system in amphioxus larvae. Biol Bull 195:260–263

    Google Scholar 

  • Stach T (2000) Microscopic anatomy of developmental stages of Branchiostoma lanceolatum (Cephalochordata, Chordata). Bonn Zool Monogr 47:1–111

    Google Scholar 

  • Stach T (2002) Minireview: on the homology of the protocoel in Cephalochordata and ‘lower’ Deuterostomia. Acta Zool 83:25–31

    Article  Google Scholar 

  • Stach T (2008) Chordate phylogeny and evolution: a not so simple three-taxon problem. J Zool 276:117–141

    Google Scholar 

  • Stach T (2013) Deuterorstome phylogeny—a morphological perspective. In: Wägele W, Bartolomaeus T (eds) Deep metazoan phylogeny: the backbone of the tree of life. De Gruyter, Berlin (accepted)

  • Stach T, Eisler K (1998) The ontogeny of the nephridial system of the larval amphioxus (Branchiostoma lanceolatum). Acta Zool 79(2):113–118

    Article  Google Scholar 

  • Struck TH (2011) Direction of evolution within Annelida and the definition of Pleistoannelida. J Zool Syst Evol Res 49:340–345

    Google Scholar 

  • Struck TH, Paul C, Hill N, Hartmann S, Hosel C, Kube M, Lieb B, Meyer A, Tiedemann R, Purschke G, Bleidorn C (2011) Phylogenomic analyses unravel annelid evolution. Nature 471:95–98

    Google Scholar 

  • Swalla B, Smith A (2008) Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos Trans R Soc Lond B Biol Sci 363:1557–1568

    Article  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

  • van der Horst CJ (1939). Hemichordata. In: Bronn HG (ed) Akademische Verlagsgesellschaft m. b. H, Leipzig. 737 p

  • Westheide W, Rieger RM (2007) Spezielle Zoologie. Teil 1: Einzeller und Wirbellose Tiere. Elsevier GmbH, Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Winchell C, Sullivan J, Cameron C, Swalla B, Mallatt J (2002) Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol Biol Evol 19:762–776

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the financial support of the German Research Foundation (DFG grants: Sta 655/2-1&2 (Deep Metazoan Phylogeny Priority Program) and Sta 655/4-1) and the financial support of the Biological Institute of Ocean Sciences (Grants-in-Aid Program).

Author information

Authors and Affiliations

  1. Institut für Zoologie, Technische Universität Dresden, 01062, Dresden, Germany

    Sebastian Merker

  2. Department of Zoology, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    Alexander Gruhl

  3. Vergleichende Zoologie, Humboldt-Universität zu Berlin, Philippstrasse 13, 10115, Berlin, Germany

    Thomas Stach

Authors
  1. Sebastian Merker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander Gruhl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Stach
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Stach.

Additional information

Communicated by A. Schmidt-Rhaesa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

435_2013_200_MOESM1_ESM.zip

Aligned stack of light micrographs of complete series of longitudinal sections is deposited on MorphDBase.de: MDB Acc.-No.: T_Stach_20130322-M-3.1 (ZIP 55605 kb)

Movie of light micrographs of complete series of longitudinal sections is deposited on MorphDBase.de: MDB Acc.-No.: T_Stach_EDIT-M-4.1 (AVI 52404 kb)

Movie of light micrographs of complete series of cross sections is deposited on MorphDBase.de: MDB Acc.-No.: T_Stach_EDIT-M-6.1 (AVI 66525 kb)

435_2013_200_MOESM4_ESM.pdf

3D-pdf-version of Figure 10 is also deposited on MorphDBase.de (3D-features accessible in Adobe Reader 9.0 and higher): MDB Acc.-No.: T_Stach_EDIT-M-5.1 (PDF 518 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Merker, S., Gruhl, A. & Stach, T. Comparative anatomy of the heart–glomerulus complex of Cephalodiscus gracilis (Pterobranchia): structure, function, and phylogenetic implications. Zoomorphology 133, 83–98 (2014). https://doi.org/10.1007/s00435-013-0200-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-013-0200-9

Keywords

Search

Navigation