Abstract
Early coelomic development in the abbreviated development of the sea urchin Holopneustes purpurescens is described and then used in a comparison with coelomic development in chordate embryos to support homology between a single arm of the five-armed radial body plan of an echinoderm and the single bilateral axis of a chordate. The homology depends on a positional similarity between the origin of the hydrocoele in echinoderm development and the origin of the notochord in chordate development, and a positional similarity between the respective origins of the coelomic mesoderm and chordate mesoderm in echinoderm and chordate development. The hydrocoele is homologous with the notochord and the secondary podia are homologous with the somites. The homology between a single echinoderm arm and the chordate axis becomes clear when the aboral to oral growth from the archenteron in the echinoderm larva is turned anteriorly, more in line with the anterior–posterior axis of the early zygote. A dorsoventral axis inversion in chordates is not required in the proposed homology.
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Arenas-Mena C, Martinez P, Cameron RA, Davidson EH (1998) Expression of the Hox gene complex in the indirect development of a sea urchin. Proc Natl Acad Sci USA 95:13062–13067
Arenas-Mena C, Cameron AR, Davidson EH (2000) Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. Development 127:4631–4643
Aulehla A, Pourquié O (2010) Signaling gradients during paraxial mesoderm development. Cold Spring Harb Perspect Biol 2:a000869
Bellairs R, Osmond M (2005) The atlas of chick development, 2nd edn. Elsevier, Amsterdam
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 USA 97:4469–4474
Cisternas P, Byrne M (2009) Expression of Hox4 during development of the pentamerous juvenile sea star, Parvulastra exigua. Dev Genes Evol 219:613–618
Cox G (2007) Optical imaging techniques in cell biology. CRC, Boca Raton
David B, Mooi R (1996) Embryology supports a new theory of skeletal homologies for the phylum Echinodermata. C R Acad Sci Paris 319:577–584
De Robertis EM, Sasai Y (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380:37–40
Ferkowicz MJ, Raff RA (2001) Wnt gene expression in sea urchin development: heterochronies associated with the evolution of developmental mode. Evol Dev 3:24–33
Gilbert SF (2010) Developmental biology, 9th edn. Sinauer Associates, Sunderland
Hara Y, Yamaguchi M, Akasaka K, Nakano H, Nonaka M, Amemiya S (2006) Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus. Dev Genes Evol 216:797–809
Heinzeller Th, Welsch U (1999) The complex of notochord/neural plate in chordates and the complex of hydrocoel/ectoneural cord in echinoderms—analogous or homologous? In: Candia Carnevali MD, Bonasoro F (eds) Echinoderm research 1998. Balkema, Rotterdam, pp 285–290
Hibino T, Harada Y, Minokawa T, Nonaka M, Amemiya S (2004) Molecular heterotopy in the expression of Brachyury orthologs in order Clypeasteroida (irregular sea urchins) and order Echinoida (regular sea urchins). Dev Genes Evol 214:546–558
Holland LZ, Kene M, Williams NA, Holland ND (1997) Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): the metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development 124:1723–1732
Hotchkiss FHC (1998) A “rays-as-appendages” model for the origin of pentamerism in echinoderms. Paleobiology 24:200–214
Hyman LH (1955) The invertebrates: Echinodermata IV. McGraw-Hill, New York
Jefferies RPS (1990) The solute Dendrocystoides scoticus from the Upper Ordovician of Scotland and the ancestry of chordates and echinoderms. Palaeontology 33:631–679
Lacalli TC (2005) Protochordate body plan and the evolutionary role of larvae: old controversies resolved? Can J. Zool 83:216–224
Lawson KA, Meneses JJ, Pedersen RA (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113:891–911
Lowe CJ, Wray GA (1997) Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718–721
Mooi R, David B, Marchand D (1994) Echinoderm skeletal homologies: classical morphology meets modern phylogenetics. In: David B, Guille A, Féral JP, Roux M (eds) Echinoderms through time. Balkema, Rotterdam, pp 87–95
Mooi R, David B, Wray GA (2005) Arrays in rays: terminal addition in echinoderms and its correlation with gene expression. Evol Dev 7:542–555
Morris VB (1995) Apluteal development of the sea urchin Holopneustes purpurescens Agassiz (Echinodermata: Echinoidea: Euechinoidea). Zool J Linnean Soc Lond 114:349–364
Morris VB (2007) Origins of radial symmetry identified in an echinoderm during adult development and the inferred axes of ancestral bilateral symmetry. Proc R Soc B 274:1511–1516
Morris VB (2009) On the sites of secondary podia formation in a juvenile echinoid: growth of the body types in echinoderms. Dev Genes Evol 219:597–608
Morris VB (2011) Coelomogenesis during the abbreviated development of the echinoid Heliocidaris erythrogramma and the developmental origin of the echinoderm pentameral body plan. Evol Dev 13:370–381
Morris VB, Byrne M (2005) Involvement of two Hox genes and Otx in echinoderm body-plan morphogenesis in the sea urchin Holopneustes purpurescens. J Exp Zool (Mol Dev Evol) 304B:456–467
Nishida H (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev Biol 121:526–541
Peterson KJ, Harada Y, Cameron RA, Davidson EH (1999a) Expression pattern of Brachyury and Not in the sea urchin: comparative implications for the origins of mesoderm in the basal deuterostomes. Dev Biol 207:419–431
Peterson KJ, Cameron RA, Tagawa K, Satoh N, Davidson EH (1999b) 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
Poustka AJ, Kühn A, Groth D, Weise V, Yaguchi S, Burke RD, Herwig R, Lehrach H, Panopoulou G (2007) A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. Genome Biol 8:R85
Putnam NH, Butts T, Ferrier DEK, Furlong RF, Hellsten U et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071
Raff RA, Popodi EM (1996) Evolutionary approaches to analyzing development. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies, and protocols. Wiley, New York, pp 245–265
Ruppert EE (2005) Key characters uniting hemichordates and chordates: homologies or homoplasies? Can J Zool 83:8–23
Selleck MAJ, Stern CD (1991) Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112:615–626
Smith AB (2005) The pre-radial history of echinoderms. Geol J 40:255–280
Swalla BJ, Smith AB (2008) Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Phil Trans R Soc B 363:1557–1568
Turner RL (1998) The metameric echinoderm. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Balkema, Rotterdam, p 89
Ubaghs G (1967) General characters of Echinodermata. In: Moore RC (ed) Treatise on invertebrate paleontology, part S, Echinodermata 1. The University of Kansas and the Geological Society of America, Inc, Lawrence, pp S3–S60
von Ubisch L (1913) Die Entwicklung von Strongylocentrotus lividus. (Echinus microtuberculatus, Arbacia pustulosa.). Zeit f wiss Zool 106:409–448
Zamora S, Rahman IA, Smith AB (2012) Plated Cambrian bilaterians reveal the earliest stages of echinoderm evolution. PLoS ONE 7(6):e38296
Acknowledgments
I thank Eleanor Kable and acknowledge the facilities and the scientific and technical assistance of staff of the Australian Microscopy and Microanalysis Facility at the Electron Microscope Unit, The University of Sydney.
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Communicated by Hiroki Nishida
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Morris, V.B. Early development of coelomic structures in an echinoderm larva and a similarity with coelomic structures in a chordate embryo. Dev Genes Evol 222, 313–323 (2012). https://doi.org/10.1007/s00427-012-0415-7
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DOI: https://doi.org/10.1007/s00427-012-0415-7