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Hemichordata

  • Chapter
Evolutionary Developmental Biology of Invertebrates 6

Abstract

Hemichordata is a group of exclusively marine animals, consisting of two subgroups, the sessile and small colonial pterobranchs and the solitary, vermiform enteropneusts (acorn worms) (Fig. 2.1; van der Horst 1939; Hyman 1959; Benito and Pardos 1997). With about 130 described species, Hemichordata comprises a relatively small taxon of benthic animals (http://www.marinespecies.org/index.php; Cameron 2005). They are distributed worldwide and inhabit shallow coastal areas but are also found in the deep sea. For a long time, pterobranchs have been known only from deep waters, whereas enteropneusts were thought to burrow mainly in shallow waters. However, within the last five decades, about a dozen of different enteropneusts have been documented in the deep sea (Osborn et al. 2012). In contrast, pterobranchs have been found in intertidal zones of tropical waters only recently (Lester 1985) and might have been overlooked previously due to their minute size and superficial similarities in their gross morphology with other tube-dwelling animals, such as polychaetes and bryozoans.

Chapter vignette artwork by Brigitte Baldrian.© Brigitte Baldrian and Andreas Wanninger.

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References

  • Agassiz A (1873) The history of Balanoglossus and Tornaria. Mem Am Acad Arts Sci 9:421–436

    Google Scholar 

  • Al C, Colwin LH (1950) The developmental capacities of separated early blastomeres of an enteropneust, Saccoglossus kowalevskii. J Exp Zool 115:263–295

    Google Scholar 

  • Allman GJ (1869) Rhabdopleura normani, Allman, nov. gen. et sp. Report of the British Association for the Advancement of Science 311–312

    Google Scholar 

  • Anderson K (1907) Die Pterobranchier der schwedischen Südpolar-Expedition 1901–1903. Wiss Ergebn Schwedischen Südpolar 5:1–122

    Google Scholar 

  • Angerer LM, Oleksyn DW, Logan CY, McClay DR, Dale L, Angerer RC (2000) A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development (Cambridge, England) 127:1105–1114

    CAS  Google Scholar 

  • Angerer LM, Yaguchi S, Angerer RC, Burke RD (2011) The evolution of nervous system patterning: insights from sea urchin development. Development (Cambridge, England) 138:3613–3623

    CAS  Google Scholar 

  • Arendt D, Nübler-Jung K (1996) Common ground plans in early brain development in mice and flies. Bioessays 18:255–259

    CAS  PubMed  Google Scholar 

  • Aronowicz J, Lowe CJ (2006) Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems. Integr Comp Biol 46:890–901

    CAS  PubMed  Google Scholar 

  • Ax P (2001) Das System der Metazoa III. Ein Lehrbuch der phylogenetischen Systematik. Spektrum Akademischer Verlag, Heidelberg

    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 

  • Barrington EJ (1965) The biology of Hemichordata and Protochordata. WH Freeman, San Francisco

    Google Scholar 

  • Bateson W (1884) The early stages of the development of Balanoglossus (sp. incert.). Q J Microsc Sci NS 24:208–236, pls 18–21

    Google Scholar 

  • Bateson W (1885) The later stages in the development of Balanoglossus kowalevskii, with a suggestion on the affinities of the Enteropneusta. Q J Microsc Sci 25:81–128

    Google Scholar 

  • Bateson W (1886) Continued account of the later stages in the development of Balanoglossus kowalevskii, and the morphology of the Enteropneusta. Q J Microsc Sci 26:511–533

    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

    Google Scholar 

  • Bertrand S, Escriva H (2011) Evolutionary crossroads in developmental biology: amphioxus. Development 138:4819–4830

    CAS  PubMed  Google Scholar 

  • Bertrand S, Camasses A, Somorjai I, Belgacem MR, Chabrol O, Escande M, Pontarotti P, Escriva H (2011) Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc Natl Acad Sci 108:9160–9165

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR, Telford MJ (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85–88

    CAS  PubMed  Google Scholar 

  • Bourne GC (1889) On a Tornaria found in British seas. J Mar Biol Assoc 1:63–68, pls 7–8

    Google Scholar 

  • Brandenburger JL, Woollacott RM, Eakin RE (1973) Fine structure of the eyespots in tornaria larvae. Z Zellforsch 142:605–613

    Google Scholar 

  • Bullock TH (1946) The anatomical organization of the nervous system of enteropneusts. Q J Microsc Sci 86:55–111, pls2–8

    Google Scholar 

  • Bullock TH (1965) The nervous system of hemichordates. In: Bullock TH and Horridge GA (eds.) Structure and Function in the Nervous Systems of Invertebrates. WH Freeman and Co, San Francisco

    Google Scholar 

  • Burdon-Jones C (1952) Development and biology of the larva of Saccoglossus horsti (Enteropneusta). Phil Trans R Soc B 236:553–590

    Google Scholar 

  • Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi SS, Kiyama T, Liang S, Mu X, Agca C, Klein WH, Brandhorst BP, Rowe M, Wilson K, Churcher AM, Taylor JS, Chen N, Murray G, Wang DY, Mellott D, Hallbook F, Olinski R, Thorndyke MC (2006) A genomic view of the sea urchin nervous system. Dev Biol 300:434–460

    CAS  PubMed Central  PubMed  Google Scholar 

  • Byrne M, Cisternas P (2002) Development and distribution of the peptidergic system in larval and adult Patiriella: comparison of sea star bilateral and radial nervous systems. J Comp Neurol 451:101–114

    CAS  PubMed  Google Scholar 

  • Byrne M, Nakajima Y, Chee FC, Burke RD (2007) Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol Dev 9:432–445

    PubMed  Google Scholar 

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

    Google Scholar 

  • Cameron RA, Davidson EH (1991) Cell type specification during sea urchin development. Trends Genet 7:212–218

    CAS  PubMed  Google Scholar 

  • Cameron RA, Hough-Evans BR, Britten RJ, Davidson EH (1987) Lineage and fate of each blastomere of the eight-cell sea urchin embryo. Genes Dev 1:75–85

    CAS  PubMed  Google Scholar 

  • Cameron RA, Fraser SE, Britten RJ, Davidson EH (1989) The oral-aboral axis of a sea urchin embryo is specified by first cleavage. Development (Cambridge, England) 106:641–647

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Caron J-B, Morris SC, Cameron CB (2013) Tubicolous enteropneusts from the Cambrian period. Nature 495:503–506

    CAS  PubMed  Google Scholar 

  • Chen SH, Li KL, Lu IH, Wang YB, Tung CH, Ting HC, Lin CY, Lin CY, Su YH, Yu JK (2014) Sequencing and analysis of the transcriptome of the acorn worm Ptychodera flava, an indirect developing hemichordate. Mar Genomics 15:35–43

    PubMed  Google Scholar 

  • Cho S-J, Vallès Y, Giani VC, Seaver EC, Weisblat DA (2010) Evolutionary dynamics of the wnt gene family: a lophotrochozoan perspective. Mol Biol Evol 27:1645–1658

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cisternas P, Byrne M (2003) Peptidergic and serotonergic immunoreactivity in the metamorphosing ophiopluteus of Ophiactis resiliens (Echinodermata, Ophiuroidea). Invertebr Biol 122:177–185

    Google Scholar 

  • Colwin AL, Colwin LH (1951) Relationships between the egg and larva of Saccoglossus kowalevskii (Enteropneusta): axes and planes: general prospective significance of the early blastomeres. J Exp Zool 117:111–137

    Google Scholar 

  • Colwin AL, Colwin LH (1953) The normal embryology of Saccoglossus kowalevskii. J Morphol 92:401–453

    Google Scholar 

  • Croce J, McClay D (2006) The canonical Wnt pathway in embryonic axis polarity. Semin Cell Dev Biol 17:168–174

    CAS  PubMed  Google Scholar 

  • Cunningham D, Casey ES (2014) Spatiotemporal development of the embryonic nervous system of Saccoglossus kowalevskii. Dev Biol 386:252–263

    CAS  PubMed  Google Scholar 

  • Darras S, Gerhart J, Terasaki M, Kirschner M, Lowe CJ (2011) Beta-catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development 138:959–970

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dawydoff C (1907) Sur la morphologie des formations cardiope ‘ricardique des Enteropneusts. Zool Anz 31:352–362

    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

    PubMed Central  PubMed  Google Scholar 

  • De Robertis EM, Sasai Y (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380:37–40

    PubMed  Google Scholar 

  • De Robertis EM, Larraín J, Oelgeschläger M, Wessely O (2000) The establishment of Spemann’s organizer and patterning of the vertebrate embryo. Nat Rev Genet 1:171–181

    PubMed Central  PubMed  Google Scholar 

  • Delle Chiaje S (1829) Memorie sulla storia e notomia degli animali senza vertebre del Regno di Napoli. Napoli 4:117–120

    Google Scholar 

  • Denes AS, Jékely G, Steinmetz PRH, Raible F, Snyman H, Prud’homme B, Ferrier DEK, Balavoine G, Arendt D (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in Bilateria. Cell 129:277–288

    CAS  PubMed  Google Scholar 

  • Dilly PN (1973) The larva of Rhabdopleura compacta (Hemichordata). Mar Biol (Berlin) 18:69–86

    Google Scholar 

  • Dilly PN (1975) The pterobranch Rhabdopleura compacta: its nervous system and phylogenetic position. Symp Zool Soc Lond 36:1–16

    Google Scholar 

  • Dilly PN (2013) Cephalodiscus reproductive biology (Pterobranchia, Hemichordata). Acta Zool. doi:10.1111/azo.12015

    Google Scholar 

  • Dohle W (2004) Die Verwandtschaftsbeziehungen der Großgruppen der Deuterostomier: alternative Hypothesen und ihre Begründungen. Sber Ges Naturf Freunde Berlin 43:123–162

    Google Scholar 

  • Duboc V, Röttinger E, Besnardeau L, Lepage T (2004) Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6:397–410

    CAS  PubMed  Google Scholar 

  • Duboc V, Röttinger E, Lapraz F, Besnardeau L, Lepage T (2005) Left-right asymmetry in the sea urchin embryo regulated by nodal signaling on the right side. Dev Cell 9:147–158

    CAS  PubMed  Google Scholar 

  • Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1992) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417–1430

    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 

  • Eschscholtz F (1825) Bericht über die zoologische Ausbeute der Reise von Kronstadt bis St.-Peter und Paul. Oken’s Isis. pp 734–747

    Google Scholar 

  • Fletcher RB, Baker JC, Harland RM (2006) FGF8 splice forms mediate early mesoderm and posterior neural tissue formation in Xenopus. Development 133:1703–1714

    CAS  PubMed  Google Scholar 

  • Franz V (1927) Morphologie der Akranier. Z Anat 27:464–692

    Google Scholar 

  • Freeman R, Ikuta T, Wu M, Koyanagi R, Kawashima T, Tagawa K, Humphreys T, Fang G-C, Fujiyama A et al (2012) Identical genomic organization of two hemichordate Hox clusters. Curr Biol 22:2053–2058, 1–6

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fritzenwanker JH, Gerhart J, Freeman RM, Lowe CJ (2014) The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii. EvoDevo 5:17

    PubMed Central  PubMed  Google Scholar 

  • Gillis JA, Fritzenwanker JH, Lowe CJ (2011) A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc R Soc B Biol Sci 279:237–246

    Google Scholar 

  • Goldschmid A (2007) Hemichordata. In: Westheide W, Rieger R (eds) Spezielle Zoologie, vol 1, 2nd edn, Einzeller und wirbellose Tiere. Elsevier GmbH, Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Gonzalez P, Cameron CB (2009) The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter-feeding structures. Biol J Linn Soc Lond 98:898–906

    Google Scholar 

  • Goodrich ES (1917) ‘Proboscis pores’ in craniate vertebrates, a suggestion concerning the premandibular somites and hypophysis. Q J Microsc Sci 62:539–553

    Google Scholar 

  • Green SA, Norris RP, Terasaki M, Lowe CJ (2013) FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii. Development (Cambridge, England) 140:1024–1033

    CAS  Google Scholar 

  • Hadfield M (1975) Hemichordata. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates. Academic, New York, pp 185–240

    Google Scholar 

  • Hamada H, Meno C, Watanabe D, Saijoh Y (2002) Establishment of vertebrate left-right asymmetry. Nat Rev Genet 3:103–113

    CAS  PubMed  Google Scholar 

  • Harada Okai N, Taguchi S, Shoguchi E, Tagawa K (2001) Embryonic expression of a hemichordate distal-less gene. repository.kulib.kyoto-u.ac.jp

    Google Scholar 

  • Harada Y, Shoguchi E, Taguchi S, Okai N, Humphreys T, Tagawa K, Satoh N (2002) Conserved expression pattern of BMP-2/4 in hemichordate acorn worm and echinoderm sea cucumber embryos. Zool Sci 19:1113–1121

    CAS  PubMed  Google Scholar 

  • Harmer SF (1905) The Pterobranchia of the Siboga Expedition with an account of other species. In: Weber M (ed) Siboga-Expeditie: uitkomsten op zoölogisch, botanisch, oceanographisch en geologisch gebied verzameld in Nederlandsch Oost-Indië 1899–1900 aan boord HM Siboga onder commando van Luitenant ter Zee 1e kl GF Tydeman. E. J Brill, Leyden, p 132

    Google Scholar 

  • Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Phil Trans R Soc Lon B 267:1071–1079

    Google Scholar 

  • Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WE, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc Lond B 276:4261–4270

    Google Scholar 

  • Henry JQ, Tagawa K, Martindale M (2001) Deuterostome evolution: early development in the enteropneust hemichordate, Ptychodera flava. Evol Dev 3:375–390

    CAS  PubMed  Google Scholar 

  • Holland LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu J-K (2013) Evolution of bilaterian central nervous systems: a single origin? EvoDevo 4:27

    PubMed Central  PubMed  Google Scholar 

  • Holland ND, Clague DA, Gordon DP, Gebruk A, Pawson DL, Vecchione M (2005) ‘Lophenteropneust’ hypothesis refuted by collection and photos of new deep-sea hemichordates. Nature 434:374–376

    Google Scholar 

  • Holley SA, Ferguson EL (1997) Fish are like flies are like frogs: conservation of dorsal-ventral patterning mechanisms. Bioessays 19:281–284

    CAS  PubMed  Google Scholar 

  • Hyman LH (1955) The Invertebrates, vol 4, Echinodermata. McGraw-Hill, New York

    Google Scholar 

  • Hyman LH (1959) The invertebrates, vol 5, Smaller coelomate groups. McGraw-Hill Book Company, New York

    Google Scholar 

  • Ikuta T, Miyamoto N, Saito Y, Wada H, Satoh N, Saiga H (2009) Ambulacrarian prototypical Hox and ParaHox gene complements of the indirect-developing hemichordate Balanoglossus simodensis. Dev Genes Evol 219(7):383–389

    CAS  PubMed  Google Scholar 

  • Imai KS, Satoh N, Satou Y (2002) Early embryonic expression of FGF4/6/9 gene and its role in the induction of mesenchyme and notochord in Ciona savignyi embryos. Development 129:1729–1738

    CAS  PubMed  Google Scholar 

  • Kaul S, Stach T (2010) Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. J Morphol 271:1240–1259

    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

    Google Scholar 

  • Kaul-Strehlow S, Stach T (2013) A detailed description of the development of the hemichordate Saccoglossus kowalevskii using SEM, TEM, Histology and 3D-reconstructions. Frontiers in Zoology 10:53

    Google Scholar 

  • Kim GJ, Yamada A, Nishida H (2000) An FGF signal from endoderm and localized factors in the posterior-vegetal egg cytoplasm pattern the mesodermal tissues in the ascidian embryo. Development 127:2853–2862

    CAS  PubMed  Google Scholar 

  • Kimelman D (2006) Mesoderm induction: from caps to chips. Nat Rev Genet 7:360–372

    CAS  PubMed  Google Scholar 

  • Knight-Jones EW (1952) On the nervous system of Saccoglossus cambrensis (Enteropneusta). Philos Trans R Soc Lond B 236:315–354

    Google Scholar 

  • Kowalevsky A (1866) Anatomie des Balanoglossus Delle Chiaje. Mem Acad Imp Sc St Petersbourg 7:1–18

    Google Scholar 

  • Krohn A (1854) Beobachtungen über Echinodermenlarven. Arch Anat Physiol wiss Med 208–213

    Google Scholar 

  • Lankester ER (1884) A Contribution of the knowledge of Rhabdopleura. Q J Microsc Sci 96:622–647

    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

    PubMed Central  PubMed  Google Scholar 

  • Lee PN, Pang K, Matus DQ, Martindale MQ (2006) A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 17:157–167

    PubMed  Google Scholar 

  • Lemaire P (2011) Evolutionary crossroads in developmental biology: the tunicates. Development 138:2143–2152

    CAS  PubMed  Google Scholar 

  • Lemons D, Fritzenwanker JH, Gerhart J, Lowe CJ, Mcginnis W (2010) Co-option of an anteroposterior head axis patterning system for proximodistal patterning of appendages in early bilaterian evolution. Dev Biol 344:358–362

    CAS  PubMed Central  PubMed  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 

  • Lester SM (1988a) Ultrastructure of adult gonads and development and structure of the larva of Rhabdopleura normani (Hemichordata: Pterobranchia). Acta Zool 69:95–109

    Google Scholar 

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

    Google Scholar 

  • Lowe CJ, Wu M, Salic A, Evans L, Lander E, Stange-ThomannN GCE, Gerhart J, Kirschner M (2003) Anteroposterior patterning in hemichordates and the origin of the chordate nervous system. Cell 113:853–865

    CAS  PubMed  Google Scholar 

  • Lowe CJ, Tagawa K, Humphreys T, Kirschner M, Gerhart J (2004) Hemichordate embryos: procurement, culture, and basic methods. Methods Cell Biol 74:171–194

    Google Scholar 

  • Lowe CJ, Terasaki M, Wu M, Freeman 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

    PubMed Central  PubMed  Google Scholar 

  • Luttrell S, Konikoff C, Byrne A, Bengtsson B, Swalla BJ (2012) Ptychoderid hemichordate neurulation without a notochord. Integr Comp Biol 52:829–834

    PubMed  Google Scholar 

  • Maisey JG (1986) Heads and tails: a chordate phylogeny. Cladistics 2:201–256

    Google Scholar 

  • Martin BL, Kimelman D (2009) Wnt signaling and the evolution of embryonic posterior development. Curr Biol 19:R215–R219

    CAS  PubMed  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

    Google Scholar 

  • McClay DR (2011) Evolutionary crossroads in developmental biology: sea urchins. Development 138:2639–2648

    CAS  PubMed Central  PubMed  Google Scholar 

  • Merker S, Gruhl A, Stach T (2013) Comparative anatomy of the heart – glomerulus complex of Cephalodiscus gracilis (Pterobranchia): structure, function, and phylogenetic implications. Zoomorphology 133:83–98

    Google Scholar 

  • Metschnikoff E (1870) Untersuchungen über die Metamorphose einiger Seethiere. Z Wiss Zool 20:131–144

    Google Scholar 

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

    Google Scholar 

  • Mierzejewski P (2004) Classification of the cephalodiscoidea. iNet: Graptolite Net: http://pterobranchia.graptolite.net/Cephalodiscoidea.html

  • M’Intosh WC (1882) Preliminary notice of Cephalodiscus, a new type allied to Prof. Allman’s Rhabdopleura, dredged in H. M. S. ‘Challenger’. Ann Mag Nat Hist Ser 5:337–348

    Google Scholar 

  • Miyamoto N, Wada H (2013) Hemichordate neurulation and the origin of the neural tube. Nat Commun 4:2713

    PubMed  Google Scholar 

  • Miyamoto N, Nakajima Y, Wada H, Saito Y (2010) Development of the nervous system in the acorn worm Balanoglossus simodensis: insights into nervous system evolution. Evol Dev 12:416–424

    PubMed  Google Scholar 

  • Morgan TH (1891) The growth and metamorphosis of Tornaria. J Morphol 5:407–458

    Google Scholar 

  • Morgan TH (1894) The development of Balanoglossus. J Morphol 9:1–86

    Google Scholar 

  • Morokuma J, Ueno M, Kawanishi H, Saiga H, Nishida H (2002) HrNodal, the ascidian nodal -related gene, is expressed in the left side of the epidermis, and lies upstream of HrPitx. Dev Genes Evol 212:439–446

    CAS  PubMed  Google Scholar 

  • Müller J (1850) Ueber die Larve und die Metamorphose der Echinodermen. Akad Wiss Berlin 2:75–109

    Google Scholar 

  • Nakano H, Murabe N, Amemiya S, Nakajima Y (2006) Nervous system development in the sea cucumber Stichopus japonicus. Dev Biol 292:205–212

    CAS  PubMed  Google Scholar 

  • Nezlin LP, Yushin VV (2004) Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphology 123:1–13

    Google Scholar 

  • Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development (Cambridge, England) 137:845–857

    CAS  Google Scholar 

  • Nielsen C (2011) Animal evolution. Interrelationships of the living phyla, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Nielsen C, Hay-Schmidt A (2007) Development of the enteropneust Ptychodera flava: ciliary bands and nervous system. J Morphol 268:551–570

    PubMed  Google Scholar 

  • Nomaksteinsky M, Röttinger E, Dufour H, Chettouh Z, Lowe C, Martindale M, Brunet J (2009) Centralization of the deuterostome nervous system predates chordates. Curr Biol 19:1264–1269

    CAS  PubMed  Google Scholar 

  • Okai N, Tagawa K, Humphreys T, Satoh N, Ogasawara M (2000) Characterization of gill-specific genes of the acorn worm Ptychodera flava. Dev Dyn 217:309–319

    CAS  PubMed  Google Scholar 

  • Osborn KJ, Kuhnz LA, Priede IG, Urata M, Gebruk AV, Holland ND (2012) Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea. Proc R Soc B 279:1646–1654

    PubMed Central  PubMed  Google Scholar 

  • Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ (2012) Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483:289–294

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rao KP (1953) The development of Glandiceps (Enteropneusta; Spengelidae). J Morphol 93:1–17

    Google Scholar 

  • Rehkämper G, Welsch U, Dilly PN (1987) Fine structure of the ganglion of Cephalodiscus gracilis (pterobranchia, hemichordata). J Comp Neurol 259:308–315

    Google Scholar 

  • Röttinger E, Lowe CJ (2012) Evolutionary crossroads in developmental biology: hemichordates. Development 139:2463–2475

    PubMed  Google Scholar 

  • Röttinger E, Martindale M (2011) Ventralization of an indirect developing hemichordate by NiCl suggests a conserved mechanism of dorsoventral (D/V) patterning in Ambulacraria (hemichordates and echinoderms). Dev Biol 354:173–190

    PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Rychel AL, Swalla BJ (2007) Development and evolution of chordate cartilage. J Exp Zool 308:325–335

    Google Scholar 

  • Sato T (1936) Vorläufige Mitteilung über Atubaria heterolopha gen. nov. sp. nov., einen in freiem Zustand aufgefundenen Pterobranchier aus dem Stilen Ozean. Zool Anz 115:97–106

    Google Scholar 

  • Sato A, Holland PW (2008) Asymmetry in a pterobranch hemichordate and the evolution of left-right patterning. Dev Dyn 237:3634–3639

    PubMed  Google Scholar 

  • Sato A, Bishop JDD, Holland PWH (2008) Developmental biology of pterobranch hemichordates: history and perspectives. Genesis 46:587–591

    PubMed  Google Scholar 

  • Sato A, White-Cooper H, Doggett K, Holland PW (2009) Degenerate evolution of the hedgehog gene in a hemichordate lineage. Proc Natl Acad Sci U S A 106:7491–7494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saudemont A, Haillot E, Mekpoh F, Bessodes N, Quirin M, Lapraz F, Duboc V, Röttinger E, Range R, Oisel A et al (2010) Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. PLoS Genet 6:e1001259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schaeffer B (1987) Deuterostome monophyly and phylogeny. Evol Biol 21:179–235

    Google Scholar 

  • Schepotieff A (1907) 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 Anat 23:463–534

    Google Scholar 

  • Silén L (1950) On the nervous system of Glossobalanus marginatus Meek (Enteropneusta). Acta Zool 31:149–175

    Google Scholar 

  • Slack JM, Darlington BG, Gillespie LL, Godsave SF, Isaacs HV, Paterno GD (1989) The role of fibroblast growth factor in early Xenopus development. Development 107(Suppl):141–148

    Google Scholar 

  • Smith S, Douglas R, da Silva K, Swalla B (2003) Morphological and molecular identification of Saccoglossus species (Hemichordata: Harrimaniidae) in the Pacific Northwest. Can J Zool 81:133–141

    Google Scholar 

  • Spengel JW (1893) Die Enteropneusten des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel, vol 18. Engelmann, Leipzig

    Google Scholar 

  • Spengel JW (1901) Die Benennung der Enteropneusten–Gattungen. Zool Jahrb Abt Syst 15:209–218

    Google Scholar 

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

    Google Scholar 

  • Stach T (2013) Larval anatomy of the pterobranch Cephalodiscus gracilis supports secondarily derived sessility concordant with molecular phylogenies. Naturwiss. doi:10.1007/s00114-013-1117-3

    PubMed  Google Scholar 

  • Stach T, Kaul S (2012) The postanal tail of the enteropneust Saccoglossus kowalevskii is a ciliary creeping organ without distinct similarities to the chordate tail. Acta Zool 92:150–160

    Google Scholar 

  • Stach T, Gruhl A, Kaul-Strehlow S (2012) The central and peripheral nervous system of Cephalodiscus gracilis (Pterobranchia, Deuterostomia). Zoomorphology 131:11–24

    Google Scholar 

  • Stainier DYR (2002) A glimpse into the molecular entrails of endoderm formation. Genes Dev 16:893–907

    CAS  PubMed  Google Scholar 

  • Stebbing ARD (1970) Aspects of the reproduction and life cycle of Rhabdopleura compacta (Hemichordata). Mar Biol (Berlin) 5:205–212

    Google Scholar 

  • Stiasny G (1914a) Studium über die Entwicklung des Balanoglossus clavigerus Delle Chiaje. I. Die Entwicklung der Tornaria. Mitt Zool Stat Neapel 22:36–75

    Google Scholar 

  • Stiasny G (1914b) Studium über die Entwicklung des Balanoglossus clavigerus Delle Chiaje. II. Darstellung der weiteren Entwicklung bis zur Metamorphose. Mitt Zool Stat Neapel 22:255–290

    Google Scholar 

  • Su Y-H, Davidson EH (2009) A perturbation model of the gene regulatory network for oral and aboral ectoderm specification in the sea urchin embryo. Dev Biol 329:410–421

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tagawa K, Nishino A, Humphreys T, Satoh N (1998a) The spawning and early development of the Hawaiian acorn worm (hemichordate), Ptychodera flava. Zool Sci 15:85–91

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Taguchi S, Tagawa K, Humphreys T, Nishino A, Satoh N, Harada Y (2000) Characterization of a hemichordate fork head/HNF-3 gene expression. Dev Genes Evol 210:11–17

    CAS  PubMed  Google Scholar 

  • Technau U, Scholz CB (2003) Origin and evolution of endoderm and mesoderm. Int J Dev Biol 47:531–539

    PubMed  Google Scholar 

  • Ullrich-Lüter EM, Dupont S, Arboleda E, Hausen H, Arnone MI (2011) Unique system of photoreceptors in sea urchin tube feet. Proc Natl Acad Sci 108:8367–8372

    PubMed Central  PubMed  Google Scholar 

  • Urata M, Yamaguchi M (2004) The development of the enteropneust hemichordate Balanoglossus misakiensis Kuwano. Zool Sci 21:533–540

    PubMed  Google Scholar 

  • Urata M, Iwasaki S, Ohtsuka S, Yamaguchi M (2014) Development of the swimming acorn worm Glandiceps hacksi: similarity to holothuroids. Evol Dev 16:149–154

    PubMed  Google Scholar 

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

    Google Scholar 

  • Whitman M (2001) Nodal signaling in early vertebrate embryos themes and variations. Dev Cell 1:605–617

    CAS  PubMed  Google Scholar 

  • Willey A (1898) Spengelia, a new genus of Enteropneusta. Q.J Microsc Sci 40:623–630

    Google Scholar 

  • Worsaae K, Sterrer W, Kaul-Strehlow S, Hay-Schmidt A, Giribet G (2012) An anatomical description of a miniaturized acorn worm (hemichordata, enteropneusta) with asexual reproduction by paratomy. PLoS One 7(11):e48529. doi:10.1371/journal.pone.0048529

    CAS  PubMed Central  PubMed  Google Scholar 

  • Young JZ (1962) The life of vertebrates, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Yu J-K, Holland LZ, Holland ND (2002) An amphioxus nodal gene (AmphiNodal) with early symmetrical expression in the organizer and mesoderm and later asymmetrical expression associated with left-right axis formation. Evol Dev 4:418–425

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Integrative Zoology, University of Vienna, Althanstr. 14, Vienna, 1090, Austria

    Sabrina Kaul-Strehlow

  2. Institute for Research on Cancer and Aging, Université Nice Sophia Antipolis, IRCAN, UMR 7284, Nice, 06107, France

    Eric Röttinger

  3. CNRS, IRCAN, UMR 7284, Nice, 06107, France

    Eric Röttinger

  4. INSERM, IRCAN, U1081, Nice, 06107, France

    Eric Röttinger

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  1. Sabrina Kaul-Strehlow
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  2. Eric Röttinger
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Correspondence to Sabrina Kaul-Strehlow .

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  1. Department of Integrative Zoology, University of Vienna Faculty of Life Sciences, Wien, Austria

    Andreas Wanninger

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Kaul-Strehlow, S., Röttinger, E. (2015). Hemichordata. In: Wanninger, A. (eds) Evolutionary Developmental Biology of Invertebrates 6. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1856-6_2

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