Hemichordates: Development

Abstract

Hemichordates are marine invertebrates consisting of two distinct groups: the solitary enteropneusts, or acorn worms (comprising a few hundred species), and the colonial and tube‐dwelling pterobranchs (comprising 20 or so species). Phylogenetically, hemichordates are the sister group to echinoderms, together composing the Ambulacraria, and share some features with chordates. Hemichordates are thus considered key organisms for addressing the origins of deuterostome and chordate body plans. Unlike the other deuterostome models including echinoderms and chordates, however, information about the developmental biology of this group is limited. Recent improvements in the accessibility of embryos, functional tool development and genomic resources from several model organisms have yielded important information on the cellular and genetic mechanisms of embryogenesis and organogenesis in hemichordates. Comparisons of hemichordates and other deuterostomes permit identification of the common ancestor of deuterostomes and help elucidate the origin of the chordate body plan.

Key Concepts

  • Hemichordate developmental biology is key to elucidating the origin of chordates and the early evolution of deuterostomes.
  • Descriptive and comparative studies using novel model species provide new insights into hemichordate evolution and diversity.
  • Establishment of genetic resources and experimental methods drive the molecular developmental biology of hemichordates.
  • Hemichordates and chordates show a conserved anteroposterior patterning mechanism.
  • Hemichordate research indicates that inversion of the dorsoventral axis occurred in the chordate lineage.
  • Gill slits of hemichordates and chordates are almost certainly homologous.
  • The stomochord of hemichordates and the notochord of chordates share some genetic features, but are unlikely to be homologous.
  • The origin of the tubular nervous system predates the diversification of hemichordates and chordates, but the homology of the collar nerve cord and neural tube still requires resolution.

Keywords: hemichordate; development; chordate evolution; body plan; nervous system

Figure 1. General morphology of an enteropneust (a) and a pterobranch (b) showing tripartite body plans. (c) Phylogeny of bilaterians showing the hemichordate relationship based on recent molecular phylogenies (Cannon ., , ; Peterson ., ).
Figure 2. Embryonic development of a direct developer, . (a–c) side views, (d–h) sections. (a) Fertilised egg. (b) Fertilised egg after the vegetal contraction. (c) Eight‐cell stage. (d) Blastula. Arrows indicate signalling by the endomesoderm that posteriorises the ectoderm. (e) Gastrula. (f) Longitudinal section of gastrula showing expression of the dorsoventral axis patterning genes. (g) enterocoely. (h) Neurula. (i) Neurula showing three signalling centres. The signalling molecules are expressed in the ectoderm. p, c and t are presumptive proboscis, collar and trunk, respectively. vc, ventral contraction.
Figure 3. (a) Diagram of an enteropneust indicating the positions of the sections in (b)–(d). (b) A longitudinal section of the proboscis stem and collar showing the position of the stomochord. (c) A cross‐section of the dorsal portion of the collar showing the collar nerve cord and stomochord. (d) A cross‐section of the posterior part of the trunk. (e) A high magnification of the boxed area in (d) indicating the topological relationship among the gut, pygochord, blood vessel and ventral nerve cord. (f) Diagram showing a cross‐section of an enteropneust. (g), (h) Cross‐sections of the dorsal portion of the collar (g) and the ventral portion of the posterior trunk (h). bv, blood vessel; cc, collar nerve cord; g, gut; ps, proboscis skeleton; py, pygochord; st, stomochord; vnc, ventral nerve cord. Scale bars: (b), (d) = 200 µm; (c), (e) = 50 µm.
Figure 4. Schematic illustration of chordate and hemichordate neurulation. The hemichordate neurulation takes place in the collar region.
Figure 5. Predicted bilaterian evolutionary scenario. A dorsoventral patterning process predates the diversification of deuterostomes and protostomes. The tubular nervous system evolved in the deuterostome ancestor. Inversion of the dorsoventral axis (BMP/chordin gradients) occurred in the chordate lineage. Illustration of the protostome is based on annelid worms (Denes ., ; Lauri ., ). Note that the gene has not yet been found in annelids. D, dorsal; V, ventral.
close

References

Aronowicz J and Lowe CJ (2006) Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous system. Integrative and Comparative Biology. 46: 890–901.

Bateson W (1886) The ancestry of the chordate. Quarterly Journal of Microscopical Science 26: 535–571.

Brown FD, Prendergast A and Swalla BJ (2008) Man is but a worm: chordate origins. Genesis 46: 605–613.

Bullock TH (1945) The anatomical organization of the nervous system of enteropneusta. Quarterly Journal of Microscopical Science 86: 55–111.

Cannon JT, Rychel AL, Eccleston H, et al. (2009) Molecular phylogeny of hemichordata, with updated status of deep‐sea enteropneusts. Molecular Phylogenetics and Evolution 52: 17–24.

Cannon JT, Kocot KM, Waits DS, et al. (2014) Phylogenomic resolution of the hemichordate and echinoderm clade. Current Biology 24: 2827–2832.

Chen SH, Li KL, Lu IH, et al. (2014) Sequencing and analysis of the transcriptome of the acorn worm Ptychodera flava, an indirect developing hemichordate. Marine Genomics 15: 35–43.

Cunningham D and Casey ES (2014) Spatiotemporal development of the embryonic nervous system of Saccoglossus kowalevskii. Developmental Biology 386: 252–263.

Darras S, Gerhart J, Terasaki M, et al. (2011) beta‐catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowakevskii. Development 138: 959–970.

Denes A, Jékely G, Steinmetz PRH, et al. (2007) Molecular architecture of annelid nervous cord supports common origin of nervous system centralization in bilateria. Cell 129: 277–288.

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

Dilly P (2014) Cephalodiscus reproductive biology (Pterobranchia, Hemichordata). Acta Zoologica (Stockholm) 95: 111–124.

Dominguez P, Jacobson AG and Jefferies RPS (2002) Paired gill slits in a fossil with a calcite skeleton. Nature 417: 841–844.

Freeman RM Jr Wu M, Cordonnier‐Pratt MM, et al. (2008) cDNA sequences for transcription factors and signaling proteinas of the hemichordate Saccoglossus kowalevskii: efficacy of the expressed sequence tag (EST) approach for evolutionary and developmental studies of a new organism. Biological Bulletin 214: 284–302.

Gerhart J, Lowe C and Kirschner M (2005) Hemichordates and the origin of chordates. Current Opinion in Genetics and Development 15: 461–467.

Gillis JA, Fritzenwanker JH and Lowe CJ (2011) A stem‐deuterostome origin of the vertebrate pharyngeal transcriptional network. Proceedings of the Royal Society B 279: 237–246.

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

Harada Y, Shoguchi E, Taguchi S, et al. (2002) Conserved expression pattern of BMP‐2/4 in hemichordate acorn worm and echinoderm sea cucumber embryos. Zoological Science 19: 1113–1121.

Hardin J, Coffman JA, Black SD and McClay DR (1992) Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development 116: 671–685.

Humphreys T, Sasaki A, Uenishi G, et al. (2010) Regeneration in the hemichordate Ptychodera flava. Zoological Science 27: 91–95.

Kaul S and Stach T (2010) Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. Journal of Morphology 271: 1240–1259.

Kaul‐Strehlow S and 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.

Lauri A, Brunet T, Handberg‐Thorsager M, et al. (2014) Development of the annelid axochord: insights into notochord evolution. Science 345: 1365–1368.

Lemons D, Fritzenwanker JH, Gerhart J, et al. (2010) Co‐option of an anteroposterior head axis patterning system for proximodistal patterning of appendages in early bilaterian evolution. Developmental Biology 344: 358–362.

Lowe CJ, Wu M, Salic A, et al. (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113: 853–965.

Lowe CJ, Terasaki M, Wu M, et al. (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biology 4: e291.

Luttrell S, Konikoff C, Byrne A, et al. (2012) Ptychoderid hemichordate neurulation without a notochord. Integrative and Comparative Biology 52: 829–834.

Miyamoto N and Saito Y (2007) Morphology and development of a new species of Balanoglossus (Hemichordata: Enteropneusta: Ptychoderidae) from Shimoda, Japan. Zoological Science 24: 1278–1285.

Miyamoto N and Saito Y (2010) Morphological characterization of the asexual reproduction in the acorn worm Balanoglossus simodensis. Development, Growth & Differentiation 52: 615–627.

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

Miyamoto N and Wada H (2013) Hemichordate neurulation and the origin of the neural tube. Nature Communications 4: 2713.

Nakano H, Lundin K, Bourlat SJ, et al. (2013) Xenoturbella bocki exhibits direct development with similarities to Acoelomorpha. Nature Communications 4: 1537.

Neilsen C and Hay‐Schmidt A (2007) Development of the enteropneust Ptychodera flava: ciliary bands and nervous system. Journal of Morphology 268: 551–570.

Nomaksteinsky M, Röttinger E, Dufour HD, et al. (2009) Centralization of the deuterostome nervous system predates chordates. Current Biology 19: 1264–1269.

Nübler‐Jung K and Arendt D (1999) Dorsoventral axis inversion: enteropneust anatomy links invertebrates to chordate turned upside down. Journal of Zoological Systematics and Evolutionary Research 37: 93–100.

Ogasawara M, Wada H, Peters H and Satoh N (1999) Developmental expression of Pax1/9 genes in urochordate and hemichordate gills: insight into function and evolution of the pharyngeal epithelium. Development 126: 2539–2550.

Pani AM, Mullarkey EE, Aronowicz J, et al. (2012) Deep deuterostome origins of vertebrate brain signalling centres. Nature 483: 289–294.

Peterson KJ, Cameron RA, Tagawa K, Satoh N and 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.

Peterson KJ, Su YH, Arnone MI, et al. (2013) MicroRNAs support the monophyly of enteropneust hemichordates. Journal of Experimental Zoology Part B Molecular and Developmental Evolution 320: 368–374.

Philippe H, Brinkmann H, Copley RR, et al. (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470: 255–258.

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

Ruppert EE (2005) Key characters uniting hemichordates and chordates: homologies and homoplasies? Canadian Journal of Zoology 83: 8–23.

Rychel AL, Smith SE, Shimamoto HT and Swalla BJ (2006) Evolution and development of the chordates: collagen and pharyngeal cartilage. Molecular Biology and Evolution 23: 541–549.

Rychel AL and Swalla BJ (2007) Development and evolution of chordate cartilage. Journal of Experimental Zoology B Molecular and Developmental Evolution 308: 325–335.

Rychel AL and Swalla BJ (2008) Anterior regeneration in the hemichordate Ptychodera flava. Developmental Dynamics 237: 3222–3232.

Sato A and Holland PWH (2008) Asymmetry in a pterobranch hemichordate and the evolution of left‐right patterning. Developmental Dynamics 237: 3634–3639.

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

Sato A, White‐Cooper H, Doggett K and Holland PWH (2009) Degenerate evolution of the hedgehog gene in a hemichordate lineage. Proceedings of the National Academy of Science USA 106: 7491–7494.

Satoh N, Tagawa K, Lowe CJ, et al. (2014) On a possible evolutionary link of the stomochord of hemichordate to pharyngeal organs of chordates. Genesis 52: 925–934.

Stach T (2013) Larval anatomy of the pterobranch Cephalodiscus gracilis supports secondarily derived sessility concordant with molecular phylogenies. Naturwissenschaften 100: 1187–1191.

Takacs CM, Moy VN and 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). Evolution & Development 6: 405–417.

Urata M, Iwasaki S, Ohtsuma S and Yamaguchi M (2014) Development of the swimming acorn worm Glandiceps hacksi: similarity to holothuroids. Evolution & Development 16: 149–154.

Worsaae K, Sterrer W, Kaul‐Strehlow S, Hay‐Schmidt A and Giribet G (2012) An anatomical description of a miniaturized acorn wotm (Hemichordata, Enteropneusta) with asexual reproduction by paratomy. PLoS One 7: e48529.

Further Reading

Arendt D and Nuubler‐Jung K (1994) Inversion of dorsoventral axis? Nature 371: 26.

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

Holland ND (2003) Early central nervous system evolution: an era of skin brains? Nature Reviews Neuroscience 4: 1–11.

Ikuta T, Chen YC, Annunziata R, et al. (2013) Identification of an intact ParaHox cluster with temporal colinearity but altered spatial colinearity in the hemichordate Ptychodera flava. BMC Evolutionary Biology 13: 129.

Knight‐Jones E (1952) On the nervous system of Saccoglossus cambriensis (Enteropneusta). Philosophical Transaxtions of the Royal Society of London B. Biological Science 236: 315–354.

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

Lowe CJ (2008) Molecular genetic insights into deuterostomes evolution from the direct‐developing hemichordate Saccoglossus kowalevskii. Philosophical Transactions of the Royal Society B 363: 1569–1578.

Nübler‐Jung K and Arendt D (1996) Enteropneusts and chordate evolution. Current Biology 6: 352–353.

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

Satoh N (2008) An aboral‐dorsalization hypothesis for chordate origin. Genesis 46: 614–622.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Miyamoto, Norio, and Wada, Hiroshi(Apr 2015) Hemichordates: Development. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0004110.pub2]