Theory in Biosciences

, Volume 137, Issue 1, pp 1–16 | Cite as

The evolutionary origin of chordate segmentation: revisiting the enterocoel theory

Review
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Abstract

One of the definitive characteristics of chordates (cephalochordates, vertebrates) is the somites, which are a series of paraxial mesodermal blocks exhibiting segmentation. The presence of somites in the basal chordate amphioxus and in vertebrates, but not in tunicates (the sister group of vertebrates), suggests that the tunicates lost the somites secondarily. Somites are patterned from anterior to posterior during embryogenesis. How such a segmental pattern evolved from deuterostome ancestors is mysterious. The classic enterocoel theory claims that chordate mesoderm evolved from the ancestral deuterostome mesoderm that organizes the trimeric body parts seen in extant hemichordates. Recent progress in molecular embryology has been tremendous, which has enabled us to test this classic theory. In this review, the history of the study on the evolution of the chordate mesoderm is summarized. This is followed by a review of the current understanding of genetic mapping on anterior/posterior (A/P) mesodermal patterning between chordates (cephalochordates, vertebrates) and a direct developing hemichordate (Saccoglossus kowalevskii). Finally, a possible scenario about the evolution of the chordate mesoderm from deuterostome ancestors is discussed.

Keywords

Metamerism Chordates Deuterostomes Somites Mesoderm 

Notes

Acknowledgements

The author thanks Dr. Y. Henmi, H. Shimasaki, A. Maenaka and K. Shimohira of Kumamoto University for the collection of adult amphioxus in Amakusa, Kumamoto, Japan, and Dr. M. Okauchi of National Research Institute of Aquaculture for the algal culture. The author also thanks Dr. N. D. Holland, Dr. L. Z. Holland of UCSD and Dr. S. Green of Caltech for critically reading of the manuscript and for providing many suggestions for improvement, and Dr. S. Kuratani, Dr. Y. Oisi of RIKEN, Dr. C. J. Lowe of Stanford University, Dr. R. Cherny of Charles University and Dr. G. P. Wagner of Yale University for discussion. The author also thanks the reviewer for constructive comments on the manuscript. This research was supported by University of Fukui, Life Science Innovation Center.

Authors’ contributions

TO wrote the paper and performed all the experiments.

Compliance with ethical standards

Conflict of interest

I declare I have no conflict of interests.

Supplementary material

12064_2018_260_MOESM1_ESM.docx (576 kb)
Supplementary material 1 (DOCX 576 kb)
12064_2018_260_MOESM2_ESM.docx (1018 kb)
Supplementary material 2 (DOCX 1017 kb)

References

  1. Adachi N, Kuratani S (2012) Development of head and trunk mesoderm in the dogfish, Scyliorhinus torazame: I. Embryology and morphology of the head cavities and related structures. Evol Dev 14:234–256.  https://doi.org/10.1111/j.1525-142X.2012.00542.x CrossRefPubMedGoogle Scholar
  2. Adachi N, Takechi M, Hirai T, Kuratani S (2012) Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head. Evol Dev 14:257–276.  https://doi.org/10.1111/j.1525-142X.2012.00543.x CrossRefPubMedGoogle Scholar
  3. 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.  https://doi.org/10.1093/icb/icl045 CrossRefPubMedGoogle Scholar
  4. Balfour FM (1877) The development of elasmobranch fishes. J Anat Physiol 11:406–490PubMedPubMedCentralGoogle Scholar
  5. Balfour FM (1878) A monograph on the development of elasmobranch fishes. Macmillan, LondonCrossRefGoogle Scholar
  6. Bateson W (1885) The later stages in the development of Balanoglossus kowalevskii, with a suggestion as to the affinities of the Enteropneusta. Q J Microsc Sci 2:81–122Google Scholar
  7. Bateson W (1886) The ancestry of the chordata. Q J Microsc Sci 26:535–571Google Scholar
  8. Beaster-Jones L, Kaltenbach SL, Koop D, Yuan S, Chastain R, Holland LZ (2008) Expression of somite segmentation genes in amphioxus: a clock without a wavefront? Dev Genes Evol 218:599–611.  https://doi.org/10.1007/s00427-008-0257-5 CrossRefPubMedGoogle Scholar
  9. Candiani S, Holland ND, Oliveri D, Parodi M, Pestarino M (2008) Expression of the amphioxus Pit-1 gene (AmphiPOU1F1/Pit-1) exclusively in the developing preoral organ, a putative homolog of the vertebrate adenohypophysis. Brain Res Bull 75:324–330.  https://doi.org/10.1016/j.brainresbull.2007.10.023 CrossRefPubMedGoogle Scholar
  10. Conway Morris S, Caron JB (2014) A primitive fish from the Cambrian of North America. Nature 512:419–422.  https://doi.org/10.1038/nature13414 CrossRefGoogle Scholar
  11. 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 (Cambridge, England) 138:959–970.  https://doi.org/10.1242/dev.059493 CrossRefGoogle Scholar
  12. de Beer GR (1937) The development of the vertebrate skull. Oxford University Press, Oxford, pp 1–552Google Scholar
  13. Dean B (1899) On the embryology of Bdellostoma stouti. In: Dean B (ed) Festschrift zum siebenzigsten Geburtstag von Carl von Kupffer. Gustav Fischer, Jena, pp 221–276Google Scholar
  14. Foucault M (1966) Les Mots et les choses—Une Archéologie des sciences humaines. GallimardGoogle Scholar
  15. Fritzenwanker JH, Gerhart J, Freeman RM Jr, Lowe CJ (2014) The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii. EvoDevo 5:17.  https://doi.org/10.1186/2041-9139-5-17 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Froriep A (1892) Entwickelungsgeschichte des Kopfes. Anatomische Hefte; Zweite Abteilung, Ergebnisse der Anatomie und Entwickelungsgeschichte 1:521–605Google Scholar
  17. Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220:268–274CrossRefPubMedGoogle Scholar
  18. Gillis JA, Fritzenwanker JH, Lowe CJ (2012) A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc Biol Sci/R Soc 279:237–246.  https://doi.org/10.1098/rspb.2011.0599 CrossRefGoogle Scholar
  19. Goethe JW (1790) Das Schädelgrüt aus sechs Wirbelknochen aufgebaut. zur naturwissenschaft überhaupt, besonders zur morphologie II 2 (cited in Gaupp 1898)Google Scholar
  20. Goette A (1890) Entwickelungsgeschichte des Flussneunauges (Petromyzon fluviatilis). Theil I. Hamburg u und Leipzig:1–95, Table 91–99Google Scholar
  21. Goodrich ES (1918) On the development of the segments of the head in Scyllium. Q J Micr Sci 63:1–30Google Scholar
  22. Goodrich ES (1930) Studies on the structure and development of vertebrates. Macmillan, LondonCrossRefGoogle Scholar
  23. Gould SJ (1992) Ontogeny and phylogeny–revisited and reunited. BioEssays 14:275–279CrossRefPubMedGoogle Scholar
  24. Green SA, Norris RP, Terasaki M, Lowe CJ (2013) FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii. Development (Cambridge, England) 140:1024–1033.  https://doi.org/10.1242/dev.083790 CrossRefGoogle Scholar
  25. Gruhl A, Grobe P, Bartolomaeus T (2005) Fine structure of the epistome in Phoronis ovalis: significance for the coelomic organization in Phoronida. Invert Biol 124:332–342CrossRefGoogle Scholar
  26. Haeckel E (1876) The evolution of man (English translation of third edition of Anthropogenie), 3rd edn. Fowle, New YorkGoogle Scholar
  27. Hammerschmidt M, Wedlich D (2008) Regulated adhesion as a driving force of gastrulation movements. Development (Cambridge, England) 135:3625–3641.  https://doi.org/10.1242/dev.015701 CrossRefGoogle Scholar
  28. Hatschek B (1881) Studien über entwicklung des Amphioxus. A Hölder, WienGoogle Scholar
  29. Holland LZ (2009) Chordate roots of the vertebrate nervous system: expanding the molecular toolkit Nature reviews. Neuroscience 10:736–746.  https://doi.org/10.1038/nrn2703 PubMedGoogle Scholar
  30. Holland LZ (2016a) Tunicates current biology. CB 26:R146–R152.  https://doi.org/10.1016/j.cub.2015.12.024 PubMedGoogle Scholar
  31. Holland ND (2016b) Nervous systems and scenarios for the invertebrate-to-vertebrate transition. Philos Trans R Soc Lond Ser B Biol Sci 371:20150047.  https://doi.org/10.1098/rstb.2015.0047 CrossRefGoogle Scholar
  32. Holland LZ, Holland ND (1996) Expression of AmphiHox-1 and AmphiPax-1 in amphioxus embryos treated with retinoic acid: insights into evolution and patterning of the chordate nerve cord and pharynx. Development (Cambridge, England) 122:1829–1838Google Scholar
  33. Holland LZ, Onai T (2011) Early development of cephalochordate (amphioxus). WIREs Dev Biol 1:167–183.  https://doi.org/10.1002/wdev.11 CrossRefGoogle Scholar
  34. Holland LZ, Pace DA, Blink ML, Kene M, Holland ND (1995a) Sequence and expression of amphioxus alkali myosin light chain (AmphiMLC-alk) throughout development: implications for vertebrate myogenesis. Dev Biol 171:665–676.  https://doi.org/10.1006/dbio.1995.1313 CrossRefPubMedGoogle Scholar
  35. Holland PW, Koschorz B, Holland LZ, Herrmann BG (1995b) Conservation of Brachyury (T) genes in amphioxus and vertebrates: developmental and evolutionary implications. Development (Cambridge, England) 121:4283–4291Google Scholar
  36. 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 124:1723–1732PubMedGoogle Scholar
  37. Holland LZ, Holland ND, Gilland E (2008) Amphioxus and the evolution of head segmentation. Integr Comp Biol 48:630–646.  https://doi.org/10.1093/icb/icn060 CrossRefPubMedGoogle Scholar
  38. Holland ND, Holland LZ, Holland PW (2015) Scenarios for the making of vertebrates. Nature 520:450–455.  https://doi.org/10.1038/nature14433 CrossRefPubMedGoogle Scholar
  39. Huxley TH (1858) The croonian lecture: on the theory of the vertebrate skull. Proc Zool Soc London 9:381–457Google Scholar
  40. Jacobson AG (1988) Somitomeres: mesodermal segments of vertebrate embryos. Development (Cambridge, England) 104:209–220Google Scholar
  41. Jandzik D, Garnett AT, Square TA, Cattell MV, Yu JK, Medeiros DM (2015) Evolution of the new vertebrate head by co-option of an ancient chordate skeletal tissue. Nature 518:534–537.  https://doi.org/10.1038/nature14000 CrossRefPubMedGoogle Scholar
  42. Janvier P (2015) Facts and fancies about early fossil chordates and vertebrates. Nature 520:483–489.  https://doi.org/10.1038/nature14437 CrossRefPubMedGoogle Scholar
  43. Jefferies RPS (1986) The ancestry of the vertebrates. British Museum (Natural History), LondonGoogle Scholar
  44. Kaul-Strehlow S, Stach T (2013) A detailed description of the development of the hemichordate Saccoglossus kowalevskii using SEM, TEM, Histology and 3D-reconstructions. Front Zool 10:53.  https://doi.org/10.1186/1742-9994-10-53 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kingsbury BF, Adelmann HB (1924) The morphological plan of the head. Q J Microsc Sci 68:239–285Google Scholar
  46. Kirschner MW. The origin of vertebrates iBiology. https://www.ibiology.org/development-and-stem-cells/hemichordates/. Accessed 16 Feb 2018
  47. Koltzoff NK (1902) Entwickelungsgeschichte des Kopfes von Petromyzon planeri; ein Beitrag zur Lehre über Metamerie des Wirbelthierkopfes. Bulletin de la Societe Imperiale des Naturalistes de Moscou 16:259–589Google Scholar
  48. Kozmik Z et al (2007) Pax-Six-Eya-Dach network during amphioxus development: conservation in vitro but context specificity in vivo. Dev Biol 306:143–159.  https://doi.org/10.1016/j.ydbio.2007.03.009 CrossRefPubMedGoogle Scholar
  49. Kupffer C (1895) Die Entwickelung der Kopfnerven von Ammocoetes Planeri. Studien zur vergl. Entwg. d. Kopfes d. Kranioten. Heft 3 München 1–80Google Scholar
  50. Kuratani S (2008) Is the vertebrate head segmented?-evolutionary and developmental considerations. Integr Comp Biol 48:647–657.  https://doi.org/10.1093/icb/icn015 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kuratani S, Adachi N (2016) What are head cavities?—a history of studies on vertebrate head segmentation. Zool Sci 33:213–228.  https://doi.org/10.2108/zs150181 CrossRefPubMedGoogle Scholar
  52. Kuratani S, Horigome N, Hirano S (1999) Developmental morphology of the head mesoderm and reevaluation of segmental theories of the vertebrate head: evidence from embryos of an agnathan vertebrate, Lampetra Japonica. Dev Biol 210:381–400CrossRefPubMedGoogle Scholar
  53. Lowe CJ et al (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113:853–865CrossRefPubMedGoogle Scholar
  54. Lowe CJ et al (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4:e291.  https://doi.org/10.1371/journal.pbio.0040291 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lowe CJ, Clarke DN, Medeiros DM, Rokhsar DS, Gerhart J (2015) The deuterostome context of chordate origins. Nature 520:456–465.  https://doi.org/10.1038/nature14434 CrossRefPubMedGoogle Scholar
  56. MacBride EW (1897) The relationship of amphioxus to Balanoglossus. Proc Camb Philos Soc 9:309–313Google Scholar
  57. Mallatt J, Holland N (2013) Pikaia gracilens Walcott: stem chordate, or already specialized in the Cambrian? J Exp Zoology Part B Mol Dev Evol 320:247–271.  https://doi.org/10.1002/jez.b.22500 CrossRefGoogle Scholar
  58. Masterman AT (1898) On the theory of archimeric segmentation and its bearing upon the phyletic classification of the coelomata. Proc R Soc Edinb 22:270–310Google Scholar
  59. Matsuura M et al (2008) Identification of four Engrailed genes in the Japanese lamprey, Lethenteron japonicum. Dev Dyn 237:1581–1589.  https://doi.org/10.1002/dvdy.21552 CrossRefPubMedGoogle Scholar
  60. Meier S, Packard DS Jr (1984) Morphogenesis of the cranial segments and distribution of neural crest in the embryos of the snapping turtle, Chelydra serpentina. Dev Biol 102:309–323CrossRefPubMedGoogle Scholar
  61. Minguillon C, Jimenez-Delgado S, Panopoulou G, Garcia-Fernandez J (2003) The amphioxus hairy family: differential fate after duplication. Development (Cambridge, England) 130:5903–5914.  https://doi.org/10.1242/dev.00811 CrossRefGoogle Scholar
  62. Müller GB, Newman SA (2005) Editorial: evolutionary innovation and morphological novelty Journal of experimental zoology Part B. Mol Dev Evol 304:485–486.  https://doi.org/10.1002/jez.b.21080 Google Scholar
  63. Newman SA (2014) Physico-genetics of morphogenesis: the hybrid nature of developmental mechanisms: towards a theory of development. Oxford University Press, Oxford, pp 95–113Google Scholar
  64. Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207:575–601.  https://doi.org/10.1111/j.1469-7580.2005.00473.x CrossRefPubMedPubMedCentralGoogle Scholar
  65. Northcutt RG (2008) Historical hypotheses regarding segmentation of the vertebrate head. Integr Comp Biol 48:611–619.  https://doi.org/10.1093/icb/icn065 CrossRefPubMedGoogle Scholar
  66. Ogata S, Morokuma J, Hayata T, Kolle G, Niehrs C, Ueno N, Cho KW (2007) TGF-beta signaling-mediated morphogenesis: modulation of cell adhesion via cadherin endocytosis. Genes Dev 21:1817–1831.  https://doi.org/10.1101/gad.1541807 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Oisi Y, Ota KG, Kuraku S, Fujimoto S, Kuratani S (2013) Craniofacial development of hagfishes and the evolution of vertebrates. Nature 493:175–180.  https://doi.org/10.1038/nature11794 CrossRefPubMedGoogle Scholar
  68. Oken L (1807) Über die Bedeutung der Schädelknochen. Göbhardt, BambergGoogle Scholar
  69. Olsson L, Ericsson R, Cerny R (2005) Vertebrate head development: segmentation, novelties, and homology. Theory Biosci 124:145–163.  https://doi.org/10.1016/j.thbio.2005.06.001 CrossRefPubMedGoogle Scholar
  70. Onai T, Irie N, Kuratani S (2014) The evolutionary origin of the vertebrate body plan: the problem of head segmentation. Annu Rev Genomics Hum Genet 15:443–459.  https://doi.org/10.1146/annurev-genom-091212-153404 CrossRefPubMedGoogle Scholar
  71. Onai T, Aramaki T, Inomata H, Hirai T, Kuratani S (2015a) Ancestral mesodermal reorganization and evolution of the vertebrate head. Zool Lett 1:29.  https://doi.org/10.1186/s40851-015-0030-3 CrossRefGoogle Scholar
  72. Onai T, Aramaki T, Inomata H, Hirai T, Kuratani S (2015b) On the origin of vertebrate somites. Zool Lett 1:33.  https://doi.org/10.1186/s40851-015-0033-0 CrossRefGoogle Scholar
  73. Onai T, Adachi N, Kuratani S (2017) Metamerism in cephalochordates and the problem of the vertebrate head. Int J Dev Biol 61:621–632.  https://doi.org/10.1387/ijdb.170121to CrossRefPubMedGoogle Scholar
  74. Owen R (1848) On the archetype and homologies of the vertebrate skeleton. John van Voorst, LondonCrossRefGoogle Scholar
  75. Owen R (1849) On the nature of limbs. Voorst, LondonCrossRefGoogle Scholar
  76. 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.  https://doi.org/10.1038/nature10838 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Patterson C (1982) Morphological characters and homology. In: Joysey KA, Friday AE (eds) Problems of phylogenetic reconstruction. Academic Press, New York, pp 21–74Google Scholar
  78. Putnam NH et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071.  https://doi.org/10.1038/nature06967 CrossRefPubMedGoogle Scholar
  79. Rasmussen SL, Holland LZ, Schubert M, Beaster-Jones L, Holland ND (2007) Amphioxus AmphiDelta: evolution of Delta protein structure, segmentation, and neurogenesis. Genesis (New York, NY: 2000) 45:113–122.  https://doi.org/10.1002/dvg.20278 CrossRefGoogle Scholar
  80. Remane A (1963a) The enterocelic origin of the celom. The lower metazoa. Comparative biology and physiology. University of California Press, Berkelry, pp 78–90Google Scholar
  81. Remane A (1963b) Zur Metamerie, Metamerismen und Metamerisation bei Wirbeltieren. Zoologischer Anzeiger 170:489–502Google Scholar
  82. Rottinger E, Lowe CJ (2012) Evolutionary crossroads in developmental biology: hemichordates. Development (Cambridge, England) 139:2463–2475.  https://doi.org/10.1242/dev.066712 CrossRefGoogle Scholar
  83. Schubert M, Holland LZ, Panopoulou GD, Lehrach H, Holland ND (2000) Characterization of amphioxus AmphiWnt8: insights into the evolution of patterning of the embryonic dorsoventral axis. Evol Dev 2:85–92CrossRefPubMedGoogle Scholar
  84. Sedgwick A (1884) On the origin of metameric segmentation and some other morphological questions. Q J Microsc Sci 24:43–82Google Scholar
  85. Shu DG et al (2003) Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature 421:526–529.  https://doi.org/10.1038/nature01264 CrossRefPubMedGoogle Scholar
  86. Simakov O et al (2015) Hemichordate genomes and deuterostome origins. Nature 527:459–465.  https://doi.org/10.1038/nature16150 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Simpson GG (1961) Principles of animal taxonomy New York. Columbia University Press, New YorkGoogle Scholar
  88. Standring S (2015) Gray’s anatomy: the anatomical basis of clinical practice, 41st edn. Elsevier, AmsterdamGoogle Scholar
  89. Tada M, Kai M (2012) Planar cell polarity in coordinated and directed movements. Curr Top Dev Biol 101:77–110.  https://doi.org/10.1016/b978-0-12-394592-1.00004-1 CrossRefPubMedGoogle Scholar
  90. Temereva EN (2015) Organization of the coelomic system in Phoronis australis (Lophotrochozoa: Phoronida) and consideration of the coelom in the lophophorates. J Zool 296:79–94CrossRefGoogle Scholar
  91. Temereva EN, Gebruk AA, Malakhov VV (2015) Demonstration of the preoral coelom in the brachiopod Lingula anatina with consideration of its phylogenetic significance. Zoologischer Anzeiger 256:22–27CrossRefGoogle Scholar
  92. Thompson JR, Chen SW, Ho L, Langston AW, Gudas LJ (1998) An evolutionary conserved element is essential for somite and adjacent mesenchymal expression of the Hoxa1 gene. Dev Dyn 211:97–108.  https://doi.org/10.1002/(sici)1097-0177(199801)211:1<97::aid-aja9>3.0.co;2-2 CrossRefPubMedGoogle Scholar
  93. Van Wijhe JW (1882) Über die Mesodermsegmente und die Entwicklung der Nerven des Selachierkopfes. Ver Akad Wiss Amsterdam, Groningen, pp 1–50Google Scholar
  94. Wagner GP (2014) Homology, genes, and evolutionary innovation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  95. Zhang S, Holland ND, Holland LZ (1997) Topographic changes in nascent and early mesoderm in amphioxus embryos studied by DiI labeling and by in situ hybridization for a Brachyury gene. Dev Genes Evol 206:532–535CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Anatomy, School of Medical SciencesUniversity of FukuiEiheiji-cho, Yoshida-gunJapan
  2. 2.Life Science Innovation CenterUniversity of FukuiEiheiji-cho, Yoshida-gunJapan

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