Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Scenarios for the making of vertebrates

Nature volume 520, pages 450–455 (2015)Cite this article

Subjects

Abstract

Over the past 200 years, almost every invertebrate phylum has been proposed as a starting point for evolving vertebrates. Most of these scenarios are outdated, but several are still seriously considered. The short-range transition from ancestral invertebrate chordates (similar to amphioxus and tunicates) to vertebrates is well accepted. However, longer-range transitions leading up to the invertebrate chordates themselves are more controversial. Opinion is divided between the annelid and the enteropneust scenarios, predicting, respectively, a complex or a simple ancestor for bilaterian animals. Deciding between these ideas will be facilitated by further comparative studies of multicellular animals, including enigmatic taxa such as xenacoelomorphs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Scenarios for the invertebrate-to-vertebrate transition.
Figure 2: Simplified trees of metazoan animal life.
Figure 3: Annelid and enteropneust theories.

Similar content being viewed by others

References

  1. Lamarck, J. B. Philosophie Zoologique [in French] Vol. 2 (Dentu, 1809). The first explicitly evolutionary derivation of vertebrates from invertebrates.

    Google Scholar 

  2. Geoffroy St-Hilaire, E. Considérations générales sur la vertèbre [in French]. Mém. Mus. Hist. Nat. 9, 89–119 (1822).

    Google Scholar 

  3. Patten, W. The Evolution of the Vertebrates and Their Kin (Blakiston's Son, 1912).

    Book  Google Scholar 

  4. Gislén, T. Affinities between the Echinodermata, Enteropneusta, and Chordania. Zool. Bidr. Uppsala 12, 199–304 (1930).

    Google Scholar 

  5. Jefferies, R. P. S. The Ancestry of the Vertebrates (British Museum Natural History, 1986). This scholarly work, even if no longer accepted in its broad outline, was centrally important for reawakening interest in the invertebrate-to-vertebrate transition in the latter part of the twentieth century.

    Google Scholar 

  6. Satoh, N. An aboral-dorsalization hypothesis for chordate origin. Genesis 46, 614–622 (2008).

    Article  PubMed  Google Scholar 

  7. Gans, C. & Northcut, R. G. Neural crest and the origin of the vertebrates: a new head. Science 220, 268–274 (1983). This influential scenario did much to focus the attention of vertebrate biologists back on questions about the evolutionary origin of their group.

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Northcutt, R. G. The new head hypothesis revisited. J. Exp. Zool. 304B, 274–297 (2005).

    Article  Google Scholar 

  9. Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064–1071 (2008).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Dohrn, A. Der Ursprung der Wirbelthiere und das Princip des Functionswechsels: genealogische Skizzen [in German] (Engelmann, 1875). This is the original annelid theory.

    Google Scholar 

  12. Semper, C. Die Stammesverwandtschaft der Wirbelthiere und Wirbellosen [in German]. Arb. Zool.-Zootom. Inst. Würzburg 2, 25–76 (1875).

    Google Scholar 

  13. Balavoine, G. & Adoutte, A. The segmented urbilateria: a testable scenario. Integr. Comp. Biol. 43, 137–147 (2003).

    Article  PubMed  Google Scholar 

  14. Eisig, H. Der Nebendarm der Capitelliden und seine Homologa [in German]. Zool. Anz. 1, 148–152 (1878).

    Google Scholar 

  15. Kleinenberg, N. Die Entstehung des Annelids aus der Larve von Lopadorhynchus, nebst Bemerkungen über die Entwicklung anderer Polychaeten [in German]. Z. Wiss. Zool. 44, 1–227 (1886).

    Google Scholar 

  16. Van Beneden, E. & Julin, C. Recherches sur la morphologie des tuniciers [in French]. Arch. Biol. (Liege) 6, 237–476 (1886).

    Google Scholar 

  17. Koehler, R. Sur la parenté du Balanoglossus [in French]. Zool. Anz. 9, 506–507 (1886).

    Google Scholar 

  18. Beard, J. Some annelidan affinities in the ontogeny of the vertebrate nervous system. Nature 39, 259–261 (1889).

    Article  ADS  Google Scholar 

  19. Kennel, J. Ueber die Ableitung der Vertebratenaugen von den Augen der Anneliden [in German]. Sitzungsber. Naturforsch. Ges. Univ. Dorpat. 9, 408–411 (1892).

    Google Scholar 

  20. Minot, C. S. Cephalic homologies. A contribution to the determination of the ancestry of the vertebrates. Am. Nat. 31, 927–943 (1897).

    Article  Google Scholar 

  21. Bernard, H. M. A new reading for the annulate ancestry of the Vertebrata. Nat. Sci. 13, 17–30 (1898).

    Google Scholar 

  22. Jones, C. M., Lyons, K. M., Lapan, P. M., Wright, C. V. E. & Hogan, B. L. M. DVR-4 (bone morphogenetic protein-4) as a posteriorventralizing factor in Xenopus mesoderm induction. Development 115, 639–647 (1992).

    Article  CAS  PubMed  Google Scholar 

  23. Arendt, D. & Nübler-Jung, K. Inversion of dorsoventral axis? Nature 371, 26 (1994). This publication launched the current revival of the annelid theory.

    Article  ADS  CAS  PubMed  Google Scholar 

  24. Holley, S. A. et al. A conserved system for dorso-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249–253 (1995). This application of developmental genetic data to classic questions of animal phylogeny attracted much attention to the young field of evolutionary developmental biology.

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  26. Kulakova, M. et al. Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Dev. Genes Evol. 217, 39–54 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. Denes, A. S. et al. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in Bilateria. Cell 129, 277–288 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Tomer, R., Denes, A. S., Tessmar-Raible, K. & Arendt, D. Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142, 800–809 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Lauri, A. et al. Development of the annelid axochord: insights into notochord evolution. Science 345, 1365–1368 (2014).

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Halanych, K. M. The new view of animal phylogeny. Annu. Rev. Ecol. Evol. Syst. 35, 229–256 (2004).

    Article  Google Scholar 

  31. Philippe, H. et al. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470, 255–260 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bateson, W. The ancestry of the Chordata. Q. J. Microsc. Sci. 26, 535–571 (1886). This article is the original enteropneust theory.

    Google Scholar 

  33. Masterman, A. T. On the Diplochorda. I. The structure of Actinotrocha. Q. J. Microsc. Sci. 40, 281–338 (1897).

    Google Scholar 

  34. Nübler-Jung, K. & Arendt, D. Enteropneusts and chordate evolution. Curr. Biol. 6, 352–353 (1996).

    Article  PubMed  Google Scholar 

  35. Lowe, C. J. et al. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113, 853–865 (2003). This publication launched the current revival of the enteropneust theory.

    Article  CAS  PubMed  Google Scholar 

  36. Puelles, L. & Ferran, J. L. Concept of neural genoarchitecture and its genomic fundament. Front. Neuroanat. 6, 47 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Lowe, C. J. Molecular genetic insights into deuterostome evolution from the direct-developing hemichordate Saccoglossus kowalevskii. Phil. Trans. R. Soc. B 363, 1569–1578 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Nomaksteinsky, M. et al. Centralization of the deuterostome nervous system predates chordates. Curr. Biol. 19, 1264–1269 (2009).

    Article  CAS  PubMed  Google Scholar 

  39. Cunningham, D. & Casey, E. S. Spatiotemporal development of the embryonic nervous system of Saccoglossus kowalevskii. Dev. Biol. 386, 252–263 (2014).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  41. Wlizla, M. Evolution of Nodal signaling in Deuterostomes: insights from Saccoglossus kowalevskii. PhD thesis, Univ. Chicago (2011).

  42. Röttinger, E., Duboc, T. & Martindale, M. Q. Investigating the role of the Nodal signaling pathway in a indirect developing hemichordate, Ptychodera flava. Integr. Comp. Biol. 50, abstract, e144 (2010).

    Article  Google Scholar 

  43. Miyamoto, N. & Wada, H. Hemichordate neurulation and the origin of the neural tube. Nature Commun. 4, 2713 (2013).

    Article  ADS  CAS  Google Scholar 

  44. Gaskell, W. H. et al. Origin of vertebrates. Proc. Linn. Soc. Lond. 122, 9–50 (1910).

    Google Scholar 

  45. Ota, K. G., Fujimoto, S., Oisi, Y. & Kuratani, S. Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish. Nature Commun. 2, 373 (2011).

    Article  ADS  CAS  Google Scholar 

  46. Furlong, R. F. & Holland, P. W. H. Bayesian phylogenetic analysis supports monophyly of ambulacraria and of cyclostomes. Zoolog. Sci. 19, 593–599 (2002).

    Article  PubMed  Google Scholar 

  47. Achatz, J. G., Chiodin, M., Salvenmoser, W., Tyler, S. & Martinez, P. The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis). Org. Divers. Evol. 13, 267–286 (2013).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  49. Graham, A., Butts, T., Lumsden, A. & Kiecker, C. What can vertebrates tell us about segmentation? EvoDevo 5, 24 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  50. De Robertis, E. M. The molecular ancestry of segmentation mechanisms. Proc. Natl Acad. Sci. USA 105, 16411–16412 (2008).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  51. Dray, N. et al. Hedgehog signaling regulates segment formation in the annelid Platynereis. Science 329, 339–342 (2010).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  52. Beaster-Jones, L. et al. Expression of somite segmentation genes in amphioxus: a clock without a wavefront? Dev. Genes Evol. 218, 599–611 (2008).

    Article  CAS  PubMed  Google Scholar 

  53. Wagner, G. P. The developmental genetics of homology. Nature Rev. Genet. 8, 473–479 (2007).

    Article  CAS  PubMed  Google Scholar 

  54. Northcutt, R. G. Evolution of centralized nervous systems: two schools of evolu-tionary thought. Proc. Natl Acad. Sci. USA 109 (Suppl. 1), 10626–10633 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. van Wijhe, J. W. Über den vorderen neuroporus und die phylogenetische function des canalis neurentericus der wirbelthiere [in German]. Zool. Anz. 7, 683–687 (1884).

    Google Scholar 

  56. Ziegler, H. E. Die phylogenetische entstehung des kopfes der wirbeltiere [in German]. Jena. Zeitschr. Naturwiss. 43, 653–684 (1908).

    Google Scholar 

  57. Bjerring, H. C. Major anatomical steps toward craniotedness: a heterodox view based largely on embryological data. J. Vert. Paleontol. 4, 17–29 (1984).

    Article  Google Scholar 

  58. Hatschek, B. Studien über Entwicklungsgeschichte der Anneliden. Ein beitrag zur morphologie der Bilaterien [in German]. Arb. Zool. Inst. Wien 11, 1–128 (1878).

    Google Scholar 

  59. Roule, L. Étude sur les forms premièrs de la notochorde et sur les affinitiés naturelles des cordés [in French]. Arch. Zool. Exp. Gén. (Sér.4) 10, 447–547 (1909)

    Google Scholar 

  60. Delsman, H. C. The Ancestry of Vertebrates (Valkoff, 1922). Feelings ran high about vertebrate-origin scenarios, for instance, J. W. van Wijhe thought this work “ought to be confiscated and consigned to the flames”.

    Google Scholar 

  61. Marlow, H. et al. Larval body patterning and apical organs are conserved in animal evolution. BMC Biol. 12, 7 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Garstang, W. Preliminary note on a new theory of the phylogeny of the Chordata. Zool. Anz. 17, 122–125 (1894).

    Google Scholar 

  63. Jollie, M. The origin of chordates. Acta Zool. Stockh. 54, 81–100 (1973).

    Article  Google Scholar 

  64. Ivanova-Kazas, O. M. On the ancestry of Chordata and Deuterostomia as a whole. Russ. J. Mar. Biol. 23, 219–226 (1997).

    Google Scholar 

  65. Nielsen, C. Animal Evolution: Interrelationships of the Living Phyla (Oxford Univ. Press, 2001).

    Google Scholar 

  66. Kupffer, C. v. Die stammverwandtschaft zwischen Ascidien und wirbelthieren [in German]. Ark. Mik. Anat. 6, 115–172 (1870).

    Article  Google Scholar 

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

    Google Scholar 

  68. Berrill, N. J. The Origin of Vertebrates (Clarendon, 1955).

    Google Scholar 

  69. Whitear, M. Some remarks on the ascidian affinities of vertebrates. Ann. Mag. Nat. Hist. (Ser. 12) 10, 338–348 (1957).

    Article  Google Scholar 

  70. Romer, A. S. The Vertebrate Body 3rd Edn (Saunders, 1962). The scenario of Romer became well known because his book was read attentively by generations of American premedical students cramming for medical school acceptance.

    Google Scholar 

  71. Berg, L. S. Nomogenesis or Evolution Determined by Law (Constable, 1926).

    Google Scholar 

  72. Clark, A. H. The New Evolution: Zoogenesis (Williams & Wilkins, 1930).

    Book  Google Scholar 

  73. Nursall, J. R. On the origin of the major groups of animals. Evolution 16, 118–123 (1962).

    Article  Google Scholar 

  74. Anderson, D. T. Origins and relationships among animal phyla. Proc. Linn. Soc. N. S. W. 106, 151–166 (1982).

    Google Scholar 

  75. Sedgwick, A. On the origin of metameric segmentation and some other morphological questions. Q. J. Microsc. Sci. 24, 43–82 (1884).

    Google Scholar 

  76. Lameere, A. L'origine des vertébrés [in French]. Bull. Séanc. Soc. Belge Micros. 17, 91–121 (1891).

    Google Scholar 

  77. Inglis, W. G. Evolutionary waves: patterns in the origins of animal phyla. Aust. J. Zool. 33, 153–178 (1985).

    Article  Google Scholar 

  78. Dewel, R. A. Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity. J. Morphol. 243, 35–74 (2000).

    Article  CAS  PubMed  Google Scholar 

  79. Tretjakoff, D. Ursprung der Chordaten [in German]. Z. Wiss. Zool. 134, 558–640 (1929).

    Google Scholar 

  80. Christofersen, M. L. & Araujo-de-Almeida, E. A phylogenetic framework of the Enterocoela (Metameria: Coelomata). Rev. Nordest. Biol. 9, 173–208 (1994).

    Google Scholar 

  81. Gerhart, J. & Kirschner, M. Cells, Embryos and Evolution: Toward a Cellular and Developmental Understanding of Phenotypic Variation and Evolutionary Adaptability (Blackwell, 1997).

    Google Scholar 

  82. Leydig, F. Vom Bau des thierischen Körpers. Handbuch der vergleichenden Anatomie, Vol. 1 [in German] (Laupp & Siebeck, Tübingen, 1864). This is the first scenario for an invertebrate-to-vertebrate transition to appear after On the Origin of Species and to be written from a Darwinian point of view.

    Google Scholar 

  83. Gaudry, A. Les Enchaînments du Monde Animal dans les Temps Géologiques [in French] (Savy, 1883).

    Google Scholar 

  84. Jaeckel, O. Über die Stammform der Wirbelthiere [in German]. Sitzungsber. Ges. Naturforsch. Freunde Berlin 1896, 107–129 (1896).

    Google Scholar 

  85. Gaskell, W. H. The Origin of Vertebrates (Longmans Green, 1908).

    Book  Google Scholar 

  86. Raw, F. Outline of a theory of origin of the Vertebrata. J. Paleontol. 34, 497–539 (1960).

    Google Scholar 

  87. Sillman, L. R. The origin of the vertebrates. J. Paleontol. 34, 540–544 (1960).

    Google Scholar 

  88. Hoffhaus, C. E. A homogeneous theory of the origin of vertebrates. J. Paleontol. 37, 458–471 (1963).

    Google Scholar 

  89. Løvtrup, S. The Phylogeny of Vertebrata (Wiley, 1977).

    Google Scholar 

  90. Bergström, J. The origin of animal phyla and the new phylum Procoelomata. Lethaia 22, 259–269 (1989).

    Article  Google Scholar 

  91. Hesse, R. Tierbau und Tierleben in Ihrem Zusammenhang Betrachtet. Vol. I. Der Tierkörper als Selbständiger Organismus [in German] (Teubner, 1910).

    Google Scholar 

  92. Naef, A. Notizen zur morphologie und stammgeschichte der wirbeltiere. 7. Das verhältnis der chordaten zu niederen tierformen und der typische verlauf ihrer frühen entwicklung [in German]. Biol. Zentralbl. 46, 39–50 (1926).

    Google Scholar 

  93. Sepp, E. K. Developmental History of the Nervous System of Vertebrates [in Russian] (Medgiz, 1959).

    Google Scholar 

  94. Engelbrecht, D. V. Z. The annelid ancestry of the chordates and the origin of the chordate central nervous system and the notochord. J. Zool. Syst. Evol. Res. 7, 18–30 (1969).

    Article  Google Scholar 

  95. Gutmann, W. F. Relationships between invertebrate phyla based on functional-mechanical analysis of the hydrostatic skeleton. Am. Zool. 21, 63–81 (1981).

    Article  Google Scholar 

  96. Hubrecht, A. A. W. The relation of the Nemertea to the Vertebrata. Q. J. Microsc. Sci. 27, 605–644 (1887).

    Google Scholar 

  97. Macfarlane, J. M. The Causes and Course of Organic Evolution. A Study in Bioenergetics (Macmillan, 1918).

    Google Scholar 

  98. Jensen, D. D. Hoplonemertines, myxinoids and deuterostome origins. Nature 188, 649–650 (1960).

    Article  ADS  Google Scholar 

  99. Willmer, E. N. Nemertines as possible ancestors of the vertebrates. Biol. Rev. Camb. Philos. Soc. 49, 321–363 (1974).

    Article  CAS  PubMed  Google Scholar 

  100. Dzik, J. The origin of the mineral skeleton in chordates. Evol. Biol. 31, 105–154 (2000).

    Google Scholar 

  101. Goette, A. Über den Ursprung der Wirbelthiere [in German]. Verh. Dtsch. Zool. Ges. 5, 12–30 (1895).

    Google Scholar 

  102. Plate, L. Über den Ursprung der Wirbelthiere; eine kritische Besprechung [in German]. Anat. Anz. 58, 39–46 (1924).

    Google Scholar 

  103. Salvini-Plawen, L. The urochordate larva and archicoelomate organization: chordate origin and anagenesis revisited. J. Zool. Syst. Evol. Res. 36, 129–145 (1998).

    Article  Google Scholar 

  104. Gregory, W. K. The transformation of organic design: a review of the origin and deployment of the earlier vertebrates. Biol. Rev. 11, 311–344 (1936).

    Article  Google Scholar 

  105. Dillon, L. S. The hydrocoel and the ancestry of the chordates. Evolution 19, 436–446 (1965).

    Article  Google Scholar 

  106. Eaton, T. H. The stem-tail problem and the ancestry of the chordates. J. Paleontol. 44, 969–979 (1970).

    Google Scholar 

  107. Kuznetsov, A. N. Five longitudes in chordate body. Theor. Biol. Forum 105, 21–35 (2012).

    PubMed  Google Scholar 

  108. Béraneck, M. E. Théories Récentes Sur la Descendance des Vertébrés [in French] (Attinger, 1892).

    Google Scholar 

  109. Theophiloff, S. Zur Phylogenie der Tunicaten: Eine Kritische Studie [in German]. PhD thesis, Univ. Jena (1892).

    Google Scholar 

  110. MacBride, E. W. A review of Professor Spengel's monograph on Balanoglossus. Q. J. Microsc. Sci. 36, 385–420 (1894).

    Google Scholar 

  111. Kemna, A. L'origine de la corde dorsale [in French]. Ann. Soc. Roy. Zool. Malacol. Belg. 39, lxxxv–clvii (1904).

    Google Scholar 

  112. van der Horst, C. J. Hemichordata in Dr H. G. Bronn's Klassen und Ordnungen des Tierreichs [in German]. Vol. 4, Part 4, Book 2, Section 2, Installments 1–5 (Akademische Verlagsgesellschaft, 1939).

    Google Scholar 

  113. Tokioka, T. Phylogenetic speculation of the Tunicata. Publ. Seto Mar. Biol. Lab. 19, 43–63 (1971).

    Article  Google Scholar 

  114. Cameron, C. B., Garey, J. R. & Swalla, B. J. Evolution of the chordate body plan: new insights from phylogenetic analysis of deuterostome phyla. Proc. Natl Acad. Sci. USA 97, 4469–4474 (2000).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  115. Röttinger, E. & Lowe, C. J. Evolutionary crossroads in developmental biology: hemichordates. Development 139, 2463–2475 (2012).

    Article  PubMed  CAS  Google Scholar 

  116. Ayers, H. Concerning vertebrate cephalogenesis. J. Morphol. 4, 221–245 (1890).

    Article  Google Scholar 

  117. Willey, A. Amphioxus and the Ancestry of the Vertebrates (Macmillan, 1894).

    Book  Google Scholar 

  118. Perrier, E. L'origine des vertébrés. C. R. Acad. Sci. Paris 126, 1479–1486 (1898).

    Google Scholar 

  119. Manzanares, M. & Nieto, M. A. A celebration of the new head and an evaluation of the new mouth. Neuron 37, 895–898 (2003).

    Article  CAS  PubMed  Google Scholar 

  120. Todaro, F. Sur l'origine phylogénétique des yeux des vertébrés et sur la signification des épiphises et des hypophyses de leur cerveau [in French]. Arch. Ital. Biol. 9, 55–57 (1888).

    Google Scholar 

  121. Brooks, W. K. The genus Salpa. Mem. Biol. Lab. Johns Hopkins Univ. 2, 1–303 (1893).

    Google Scholar 

  122. Delage, Y. & Hérouard, E. Traité de Zoologie Concrète. Vol VII. Les Procordés [in French] (Schleicher, 1898).

    Google Scholar 

  123. Sewertzoff, A. N. Directions of evolution. Acta Zool. 10, 59–141 (1929).

    Article  Google Scholar 

  124. Wada, H. Evolutionary history of free-swimming and sessile lifestyles in urochordates as deduced from 18S rDNA molecular phylogeny. Mol. Biol. Evol. 15, 1189–1194 (1998).

    Article  CAS  PubMed  Google Scholar 

  125. Halanych, K. M. et al. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267, 1641–1643 (1995). This pioneering study in molecular phylogenetics indicated that the greater part of the animal kingdom is divisible into three major super-phyletic groups.

    Article  ADS  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to R. Jenner and T. Lacalli for their criticisms during preparation of our manuscript. We dedicate this Review to the memory of Yoshiki Sasai, whose elucidation of the genetic control of dorsoventral patterning will endure as a landmark in the field of evolutionary developmental biology.

Author information

Authors and Affiliations

  1. Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California 92093, USA.,

    Nicholas D. Holland & Linda Z. Holland

  2. Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK

    Peter W. H. Holland

Authors
  1. Nicholas D. Holland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Linda Z. Holland
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter W. H. Holland
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicholas D. Holland.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reprints and permissions information is available at www.nature.com/reprints.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Holland, N., Holland, L. & Holland, P. Scenarios for the making of vertebrates. Nature 520, 450–455 (2015). https://doi.org/10.1038/nature14433

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature14433

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing