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Evolution of the bilaterian mouth and anus

Abstract

It is widely held that the bilaterian tubular gut with mouth and anus evolved from a simple gut with one major gastric opening. However, there is no consensus on how this happened. Did the single gastric opening evolve into a mouth, with the anus forming elsewhere in the body (protostomy), or did it evolve into an anus, with the mouth forming elsewhere (deuterostomy), or did it evolve into both mouth and anus (amphistomy)? These questions are addressed by the comparison of developmental fates of the blastopore, the opening of the embryonic gut, in diverse animals that live today. Here we review comparative data on the identity and fate of blastoporal tissue, investigate how the formation of the through-gut relates to the major body axes, and discuss to what extent evolutionary scenarios are consistent with these data. Available evidence indicates that stem bilaterians had a slit-like gastric opening that was partially closed in subsequent evolution, leaving open the anus and most likely also the mouth, which would favour amphistomy. We discuss remaining difficulties, and outline directions for future research.

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Fig. 1: Theories for the evolutionary origin of mouth and anus in the bilaterians.
Fig. 2: Two conflicting possibilities of how the body axes in cnidarians and bilaterians are related, based on different interpretations of axial Hox, canonical Wnt and Bmp activity.
Fig. 3: Fates of the blastoporal opening and of the periblastoporal tissue.
Fig. 4: Ancestral state reconstruction of the fate of blastoporal tissue.
Fig. 5: Gene expression in the circumblastoporal tissue.
Fig. 6: Morphology of the central nervous system in bilaterians and the evolution of a bilaterian ancestor from the trochaea.

References

  1. 1.

    Grobben, K. Die systematische Einteilung des Tierreichs. Verh. Zool. Bot. Ges. Wien 58, 491–511 (1908).

    Google Scholar 

  2. 2.

    Haeckel, E. Generelle Morphologie der Organismen (Georg Reimer, Berlin, 1866).

  3. 3.

    Haeckel, E. Die Gastraea-Theorie, die phylogenetische Classification des Thierreichs und die Homologie der Keimblätter. Jena Z. Naturwiss. 8, 1–55 (1874).

    Google Scholar 

  4. 4.

    Nielsen, C. Animal Evolution: Interrelationships of the Living Phyla 3rd edn, (Oxford Univ. Press, Oxford, 2012).

    Google Scholar 

  5. 5.

    Brusca, R. C., Moore, W. & Schuster, S. M. Invertebrates 3rd edn (Sinauer, Sunderland, MA, 2016).

  6. 6.

    Rieger, R., Haszprunar, G. & Hobmayer, B. in Spezielle Zoologie. Teil 1: Einzeller und Wirbellose (eds Westheide, W. & Rieger, G.) 164–179 (Springer, Heidelberg 2013).

  7. 7.

    Dunn, C. W., Giribet, G., Edgecombe, G. E. & Hejnol, A. Animal phylogeny and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 45, 371–395 (2014).

    Article  Google Scholar 

  8. 8.

    Telford, M. J., Budd, G. E. & Philippe, H. Phylogenomic insights into animal evolution. Curr. Biol. 25, R876–R887 (2015).

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Arendt, D. & Nübler-Jung, K. Inversion of dorsoventral axis? Nature 371, 26 (1994).

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Slack, J. M. W., Holland, P. W. H. & Graham, C. F. The zootype and the phylotypic stage. Nature 361, 490–492 (1993).

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Hejnol, A. & Martín-Durán, J. M. Getting to the bottom of anal evolution. Zool. Anz. 256, 61–74 (2015).

    Article  Google Scholar 

  12. 12.

    Arendt, D., Technau, U. & Wittbrodt, J. Evolution of the bilaterian larval foregut. Nature 409, 81–85 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Martín-Durán, J. M. & Hejnol, A. The study of Priapulus caudatus reveals conserved molecular patterning underlying different gut morphogenesis in the Ecdysozoa. BMC Biol. 13, 29 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Kaji, T., Reimer, J. D., Morov, A. R., Kuratani, S. & Yasui, K. Amphioxus mouth after dorso-ventral inversion. Zool. Lett. 2, 2 (2016).

    Article  Google Scholar 

  15. 15.

    Arendt, D. & Nübler-Jung, K. Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech. Dev. 61, 7–21 (1997).

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Hejnol, A. & Martindale, M. Q. Acoel development supports a simple planula-like urbilaterian. Phil. Trans. R. Soc. B 363, 1493–1501 (2008).

    Article  PubMed  Google Scholar 

  17. 17.

    Martín-Durán, J. M., Janssen, R., Wennberg, S., Budd, G. E. & Hejnol, A. Deuterostomic development in the protostome Priapulus caudatus. Curr. Biol. 22, 2161–2166 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. 18.

    Martindale, M. Q. & Hejnol, A. A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Dev. Cell 17, 162–174 (2009).

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    Nielsen, C. Larval ciliary bands and metazoan phylogeny. Fortschr. Zool. Syst. Evolutionsforsch. 1, 178–184 (1979).

    Google Scholar 

  20. 20.

    Nielsen, C. Evolution of deuterostomy - and origin of the chordates. Biol. Rev. Camb. Philos. Soc. 92, 316–325 (2017).

    Article  PubMed  Google Scholar 

  21. 21.

    Presnell, J. S. et al. The presence of a functionally tripartite through-gut in Ctenophora has implications for metazoan character trait evolution. Curr. Biol. 26, 2814–2820 (2016).

    Article  CAS  PubMed  Google Scholar 

  22. 22.

    Arendt, D., Tosches, M. A. & Marlow, H. From nerve net to nerve ring, nerve cord and brain—evolution of the nervous system. Nat. Rev. Neurosci. 17, 61–72 (2016).

    Article  CAS  PubMed  Google Scholar 

  23. 23.

    Hyman, L. H. The Invertebrates: Platyhelminthes and Rhynchocoela. The Acoelomate Bilateria Vol. 2 (McGraw-Hill, New York, NY, 1951).

  24. 24.

    Holstein, T. W. The evolution of the Wnt pathway. Cold Spring Harb. Perspect. Biol. 4, a007922 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Meinhardt, H. Different strategies for midline formation in bilaterians. Nat. Rev. Neurosci. 5, 502–510 (2004).

    Article  CAS  PubMed  Google Scholar 

  26. 26.

    Shimizu, H., Takaku, Y., Zhang, X. & Fujisawa, T. The aboral pore of hydra: evidence that the digestive tract of hydra is a tube not a sac. Dev. Genes Evol. 217, 563–568 (2007).

    Article  PubMed  Google Scholar 

  27. 27.

    Amiel, A. R. et al. Characterization of morphological and cellular events underlying oral regeneration in the sea anemone, Nematostella vectensis. Int. J. Mol. Sci. 16, 28449–28471 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Hyman, L. H. The Invertebrates: Protozoa through Ctenophora Vol. 1 (McGraw-Hill, New York, NY, 1940).

  29. 29.

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

    Google Scholar 

  30. 30.

    Finnerty, J. R. Did internal transport, rather than directed locomotion, favor the evolution of bilateral symmetry in animals? BioEssays 27, 1174–1180 (2005).

    Article  PubMed  Google Scholar 

  31. 31.

    Merabet, N. et al. Selective heart rate reduction improves metabolic syndrome-related left ventricular diastolic dysfunction. J. Cardiovasc. Pharmacol. 66, 399–408 (2015).

    Article  CAS  PubMed  Google Scholar 

  32. 32.

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

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Kusserow, A. et al. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156–160 (2005).

    Article  CAS  PubMed  Google Scholar 

  34. 34.

    Rentzsch, F. & Technau, U. Genomics and development of Nematostella vectensis and other anthozoans. Curr. Opin. Genet. Dev. 39, 63–70 (2016).

    Article  CAS  PubMed  Google Scholar 

  35. 35.

    Finnerty, J. R., Pang, K., Burton, P., Paulson, D. & Martindale, M. Q. Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304, 1335–1337 (2004).

    Article  CAS  PubMed  Google Scholar 

  36. 36.

    Marlow, H., Matus, D. Q. & Martindale, M. Q. Ectopic activation of the canonical wnt signaling pathway affects ectodermal patterning along the primary axis during larval development in the anthozoan Nematostella vectensis. Dev. Biol. 380, 324–334 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Trevino, M., Stefanik, D. J., Rodriguez, R., Harmon, S. & Burton, P. M. Induction of canonical Wnt signaling by alsterpaullone is sufficient for oral tissue fate during regeneration and embryogenesis in Nematostella vectensis. Dev. Dyn. 240, 2673–2679 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Genikhovich, G. et al. Axis patterning by BMPs: Cnidarian network reveals evolutionary constraints. Cell Rep. 10, 1646–1654 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    DuBuc, T. Q., Stephenson, T. B., Rock, A. Q. & Martindale, M. Q. Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation. Nat. Commun. 9, 2007 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Arendt, D., Benito-Gutierrez, E., Brunet, T. & Marlow, H. Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution. Phil. Trans. R. Soc. B 370, 20150286 (2015).

    Article  CAS  PubMed  Google Scholar 

  41. 41.

    Genikhovich, G. & Technau, U. On the evolution of bilaterality. Development 144, 3392–3404 (2017).

    Article  CAS  PubMed  Google Scholar 

  42. 42.

    Hoppler, S. & Moon, R. T. BMP-2/-4 and Wnt-8 cooperatively pattern the Xenopus mesoderm. Mech. Dev. 71, 119–129 (1998).

    Article  CAS  PubMed  Google Scholar 

  43. 43.

    Yamaguchi, T. P. Heads or tails: Wnts and anterior–posterior patterning. Curr. Biol. 11, R713–R724 (2001).

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    Wacker, S. A., Jansen, H. J., McNulty, C. L., Houtzager, E. & Durston, A. J. Timed interactions between the Hox expressing non-organiser mesoderm and the Spemann organiser generate positional information during vertebrate gastrulation. Dev. Biol. 268, 207–219 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    DuBuc, T. Q., Ryan, J. F., Shinzato, C., Satoh, N. & Martindale, M. Q. Coral comparative genomics reveal expanded Hox cluster in the cnidarian–bilaterian ancestor. Integr. Comp. Biol. 52, 835–841 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Ryan, J. F. et al. Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS ONE 2, e153 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Treadwell, A. L. The cytogeny of Podarke obscura Verrill. J. Morphol. 17, 399–486 (1901).

    Article  Google Scholar 

  48. 48.

    Malakhov, V. V. Embryological and histological peculiarities of the order Enoplida, a primitive group of nematodes. Russ. J. Nematol. 6, 41–46 (1998).

    Google Scholar 

  49. 49.

    Janssen, R., Jörgensen, M., Lagebro, L. & Budd, G. E. Fate and nature of the onychophoran mouth–anus furrow and its contribution to the blastopore. Proc. R. Soc. B 282, 20142628 (2015).

    Article  PubMed  Google Scholar 

  50. 50.

    Heath, H. The development of Ischnochiton. Zool. Jahrb. Abt. Anat. Ontogenie Tiere 12, 567–656 (1899).

    Google Scholar 

  51. 51.

    Kowalevsky, A. Étude sur l’embryogénie du Dentale. Ann. Mus. Hist. Nat. Marseille Zool. 1, 1–54 (1883).

    Google Scholar 

  52. 52.

    Dautert, E. Die Bildung der Keimblätter von Paludina vivipara. Zool. Jahrb. Abt. Anat. Ontogenie Tiere 50, 433–496 (1929).

    Google Scholar 

  53. 53.

    Åkesson, B. The embryology of the polychaete Eunice kobiensis. Acta Zool. 48, 142–192 (1967).

    Article  Google Scholar 

  54. 54.

    Lebedinsky, J. Beobachtungen über die Entwicklungsgeschichte der Nemertinen. Arch. Mikrosk. Anat. 49, 503–556 (1897).

    Article  Google Scholar 

  55. 55.

    Hertzler, P. L. Cleavage and gastrulation in the shrimp Penaeus (Litopenaeus) vannamei (Malacostraca, Decapoda, Dendrobranchiata). Arthropod Struct. Dev. 34, 455–469 (2005).

    Article  Google Scholar 

  56. 56.

    Hertzler, P. L. & Clark, W. H. Jr. Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116, 127–140 (1992).

    CAS  PubMed  Google Scholar 

  57. 57.

    Burfield, S. T. Memoir 28: Sagitta. Proc. Trans. Liverpool Biol. Soc. 41(App. 2), 1–101 (1927).

    Google Scholar 

  58. 58.

    Arendt, D. & Nübler-Jung, K. Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs. Mech. Dev. 81, 3–22 (1999).

    Article  CAS  PubMed  Google Scholar 

  59. 59.

    Brusca, G. J., Brusca, R. C. & Gilbert, S. E. in Embryology: Constructing the Organism (eds Gilbert, S. E. & Raunio, A. M.) 3–19 (Sinauer, Sunderland, MA, 1997).

  60. 60.

    Lyons, D. C., Perry, K. J. & Henry, J. Q. Spiralian gastrulation: germ layer formation, morphogenesis, and fate of the blastopore in the slipper snail Crepidula fornicata. EvoDevo 6, 24 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Anderson, D. T. Embryology and Phylogeny of Annelids and Arthropods (Pergamon, Oxford, 1973).

  62. 62.

    Martín-Durán, J. M., Passamaneck, Y. J., Martindale, M. Q. & Hejnol, A. The developmental basis for the recurrent evolution of deuterostomy and protostomy. Nat. Ecol. Evol. 1, 0005 (2016).

    Article  Google Scholar 

  63. 63.

    Lyons, D. C. & Henry, J. Q. Ins and outs of Spiralian gastrulation. Int. J. Dev. Biol. 58, 413–428 (2014).

    Article  PubMed  Google Scholar 

  64. 64.

    Morgan, T. H. in Studies from the Biological Laboratory Vol. 4 (eds Newell Martin, H. & Brooks, W. K.) 355–377 (John Hopkins Univ., Baltimore, 1890).

  65. 65.

    Pasteels, J. Fermeture du blastopore, anus et intestin caudal chez les Amphibiens Anoures. Acta Neerl. Morphol. Norm. Pathol. 5, 11–25 (1943).

    Google Scholar 

  66. 66.

    Martindale, M. Q. Evolution of development: the details are in the entrails. Curr. Biol. 23, R25–R28 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Technau, U. Brachyury, the blastopore and the evolution of the mesoderm. BioEssays 23, 788–794 (2001).

    Article  CAS  PubMed  Google Scholar 

  68. 68.

    Woltereck, R. Beiträge zur praktischen Analyse der Polygordius-Entwicklung nach dem »Nordsee-« und dem »Mittelmeertypus«. Arch. Entwicklungsmech. Org. 18, 377–403 (1904).

    Article  Google Scholar 

  69. 69.

    Lyons, D. C., Perry, K. J. & Henry, J. Q. Morphogenesis along the animal–vegetal axis: fates of primary quartet micromere daughters in the gastropod Crepidula fornicata. BMC Evol. Biol. 17, 217 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Moroz, L. L. et al. The ctenophore genome and the evolutionary origins of neural systems. Nature 510, 109–114 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Moroz, L. L. & Kohn, A. B. Independent origins of neurons and synapses: insights from ctenophores. Phil. Trans. R. Soc. B 371, 20150041 (2016).

    Article  CAS  PubMed  Google Scholar 

  72. 72.

    Ryan, J. F. et al. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342, 1242592 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Pisani, D. et al. Genomic data do not support comb jellies as the sister group to all other animals. Proc. Natl Acad. Sci. USA 112, 15402–15407 (2015).

    Article  CAS  PubMed  Google Scholar 

  74. 74.

    Simion, P. et al. A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr. Biol. 27, 958–967 (2017).

    Article  CAS  Google Scholar 

  75. 75.

    Jékely, G., Paps, J. & Nielsen, C. The phylogenetic position of ctenophores and the origin(s) of nervous systems. EvoDevo 6, 1 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Marlow, H. & Arendt, D. Evolution: ctenophore genomes and the origin of neurons. Curr. Biol. 24, R757–R761 (2014).

    Article  CAS  Google Scholar 

  77. 77.

    Ryan, J. F. Did the ctenophore nervous system evolve independently? Zoology 117, 225–226 (2014).

    Article  PubMed  Google Scholar 

  78. 78.

    Chun, C. Die Ctenophoren des Golfes von Neapel und der Angrenzenden Meeres-Abschnitte (Fauna und Flora des Golfes von Neapel Vol. 1, W. Engelmann, Leipzig, 1880).

  79. 79.

    Tamm, S. L. Cilia and the life of ctenophores. Invertebr. Biol. 133, 1–46 (2014).

    Article  Google Scholar 

  80. 80.

    Collins, A. G. et al. Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst. Biol. 55, 97–115 (2006).

    Article  PubMed  Google Scholar 

  81. 81.

    Putnam, N. H. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94 (2007).

    Article  CAS  Google Scholar 

  82. 82.

    Pick, K. S. et al. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol. Biol. Evol. 27, 1983–1987 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Kayal, E., Roure, B., Philippe, H., Collins, A. G. & Lavrov, D. V. Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol. Biol. 13, 5 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Bridge, D., Cunningham, C. W., DeSalle, R. & Buss, L. W. Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. Mol. Biol. Evol. 12, 679–689 (1995).

    CAS  PubMed  Google Scholar 

  85. 85.

    David, C. N. et al. Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet. 24, 431–438 (2008).

    Article  CAS  PubMed  Google Scholar 

  86. 86.

    Sinigaglia, C., Busengdal, H., Leclère, L., Technau, U. & Rentzsch, F. The bilaterian head patterning gene six3/6 controls aboral domain development in a cnidarian. PLoS Biol. 11, e1001488 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Nakanishi, N., Yuan, D., Jacobs, D. K. & Hartenstein, V. Early development, pattern, and reorganization of the planula nervous system in Aurelia (Cnidaria, Scyphozoa). Dev. Genes Evol. 218, 511–524 (2008).

    Article  PubMed  Google Scholar 

  88. 88.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Koizumi, O. & Bode, H. R. Plasticity in the nervous system of adult hydra. III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J. Neurosci. 11, 2011–2020 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Watanabe, H., Fujisawa, T. & Holstein, T. W. Cnidarians and the evolutionary origin of the nervous system. Dev. Growth Differ. 51, 167–183 (2009).

    Article  CAS  PubMed  Google Scholar 

  91. 91.

    Nakanishi, N., Renfer, E., Technau, U. & Rentzsch, F. Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139, 347–357 (2012).

    Article  CAS  PubMed  Google Scholar 

  92. 92.

    Kelava, I., Rentzsch, F. & Technau, U. Evolution of eumetazoan nervous systems: insights from cnidarians. Phil. Trans. R. Soc. B 370, 20150065 (2015).

    Article  CAS  PubMed  Google Scholar 

  93. 93.

    Hayward, D. C., Grasso, L. C., Saint, R., Miller, D. J. & Ball, E. E. The organizer in evolution–gastrulation and organizer gene expression highlight the importance of Brachyury during development of the coral, Acropora millepora. Dev. Biol. 399, 337–347 (2015).

    Article  CAS  PubMed  Google Scholar 

  94. 94.

    Martindale, M. Q., Pang, K. & Finnerty, J. R. Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131, 2463–2474 (2004).

    Article  CAS  PubMed  Google Scholar 

  95. 95.

    Scholz, C. B. & Technau, U. The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 212, 563–570 (2003).

    CAS  PubMed  Google Scholar 

  96. 96.

    Bielen, H. et al. Divergent functions of two ancient Hydra Brachyury paralogues suggest specific roles for their C-terminal domains in tissue fate induction. Development 134, 4187–4197 (2007).

    Article  CAS  PubMed  Google Scholar 

  97. 97.

    Momose, T., Derelle, R. & Houliston, E. A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135, 2105–2113 (2008).

    Article  CAS  PubMed  Google Scholar 

  98. 98.

    Spring, J. et al. Conservation of Brachyury, Mef2, and Snail in the myogenic lineage of jellyfish: a connection to the mesoderm of bilateria. Dev. Biol. 244, 372–384 (2002).

    Article  CAS  PubMed  Google Scholar 

  99. 99.

    Matus, D. Q. et al. Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc. Natl Acad. Sci. USA 103, 11195–11200 (2006).

    Article  CAS  PubMed  Google Scholar 

  100. 100.

    Haszprunar, G. Review of data for a morphological look on Xenacoelomorpha (Bilateria incertae sedis). Org. Divers. Evol. 16, 363–389 (2016).

    Article  Google Scholar 

  101. 101.

    Rouse, G. W., Wilson, N. G., Carvajal, J. I. & Vrijenhoek, R. C. New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature 530, 94–97 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. 102.

    Perea-Atienza, E. et al. The nervous system of Xenacoelomorpha: a genomic perspective. J. Exp. Biol. 218, 618–628 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  103. 103.

    Westblad, E. Xenoturbella bocki ng, n. sp., a peculiar, primitive turbellarian type. Ark. Zool. 2nd Ser. 1, 11–29 (1950).

    Google Scholar 

  104. 104.

    Raikova, O. I., Reuter, M., Jondelius, U. & Gustafsson, M. K. S. An immunocytochemical and ultrastructural study of the nervous and muscular systems of Xenoturbella westbladi (Bilateria inc. sed.). Zoomorphology 120, 107–118 (2000).

    Article  Google Scholar 

  105. 105.

    Nakano, H. et al. Xenoturbella bocki exhibits direct development with similarities to Acoelomorpha. Nat. Commun. 4, 1537 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. 106.

    Stach, T. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 62–66 (Oxford Univ. Press, Oxford, 2016).

  107. 107.

    Gavilán, B., Perea-Atienza, E. & Martínez, P. Xenacoelomorpha: a case of independent nervous system centralization? Phil. Trans. R. Soc. B 371, 20150039 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Børve, A. & Hejnol, A. Development and juvenile anatomy of the nemertodermatid Meara stichopi (Bock) Westblad 1949 (Acoelomorpha). Front. Zool. 11, 50 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  109. 109.

    Fritzenwanker, J. H., Saina, M. & Technau, U. Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev. Biol. 275, 389–402 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Rentzsch, F. et al. Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev. Biol. 296, 375–387 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Martinez, D. E. et al. Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in Hydra. Dev. Biol. 192, 523–536 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. 112.

    Technau, U. & Bode, H. R. HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development 126, 999–1010 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Raikova, O. I. et al. Basiepidermal nervous system in Nemertoderma westbladi (Nemertodermatida): GYIRFamide immunoreactivity. Zoology 107, 75–86 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  114. 114.

    Hejnol, A. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 56–61 (Oxford Univ. Press, Oxford, 2016).

  115. 115.

    Henry, J. Q., Martindale, M. Q. & Boyer, B. C. The unique developmental program of the acoel flatworm. Neochildia fusca. Dev. Biol. 220, 285–295 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. 116.

    Smith, J. P. S. III & Tyler, S. in The Origins and Relationships of Lower Invertebrates (ed. Conway Morris, S.) 123–142 (Oxford Univ. Press, Oxford, 1985).

  117. 117.

    Achatz, J. G. & Martinez, P. The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications. Front. Zool. 9, 27 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  118. 118.

    Bery, A., Cardona, A., Martinez, P. & Hartenstein, V. Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev. Genes Evol. 220, 61–76 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  119. 119.

    Semmler, H., Chiodin, M., Bailly, X., Martinez, P. & Wanninger, A. Steps towards a centralized nervous system in basal bilaterians: insights from neurogenesis of the acoel Symsagittifera roscoffensis. Dev. Growth Differ. 52, 701–713 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. 120.

    Weigert, A. et al. Illuminating the base of the annelid tree using transcriptomics. Mol. Biol. Evol. 31, 1391–1401 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. 121.

    Laumer, C. E. et al. Spiralian phylogeny informs the evolution of microscopic lineages. Curr. Biol. 25, 2000–2006 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. 122.

    Struck, T. H. et al. The evolution of annelids reveals two adaptive routes to the interstitial realm. Curr. Biol. 25, 1993–1999 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Woltereck, R. Wurm”kopf”, Wurmrumpf und Trochophora. Zool. Anz. 28, 273–322 (1904).

    Google Scholar 

  124. 124.

    Conn, H. W. Note from the Chesapeake Zoological Laboratory. Development of Serpula. Zool. Anz. 7, 669–672 (1884).

    Google Scholar 

  125. 125.

    Balfour, F. M. The anatomy and development of Peripatus capensis. Q. J. Microsc. Sci. 23, 213–259 (1883).

    Google Scholar 

  126. 126.

    Hatschek, B. Entwicklung der Trochophora von Eupomatus uncinatus, Philippi (Serpula uncinatus). Arb. Zool. Inst. Univ. Wien 6, 121–148 (1885).

    Google Scholar 

  127. 127.

    Arenas-Mena, C. Embryonic expression of HeFoxA1 and HeFoxA2 in an indirectly developing polychaete. Dev. Genes Evol. 216, 727–736 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. 128.

    Torrey, J. C. The early embryology of Thalassema mellita (Conn). Ann. NY Acad. Sci. 14, 165–246 (1903).

    Article  Google Scholar 

  129. 129.

    Wilson, E. B. The cell-lineage of Nereis. A contribution to the cytogeny of the annelid body. J. Morphol. 6, 361–480 (1892).

    Article  Google Scholar 

  130. 130.

    Child, C. M. The early development of Arenicola and Sternaspis. Arch. Entwicklungsmech. Org. 9, 587–723 (1900).

    Article  Google Scholar 

  131. 131.

    Delsman, H. C. Eifurchung und Keimblattbildung bei Scoloplos armiger O. F. Müller. Tijdschr. Ned. Dierkd. Ver. 14, 383–498 (1916).

    Google Scholar 

  132. 132.

    Smart, T. I. & Von Dassow, G. Unusual development of the mitraria larva in the polychaete Owenia collaris. Biol. Bull. 217, 253–268 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  133. 133.

    Gline, S. E., Nakamoto, A., Cho, S.-J., Chi, C. & Weisblat, D. A. Lineage analysis of micromere 4d, a super-phylotypic cell for Lophotrochozoa, in the leech Helobdella and the sludgeworm Tubifex. Dev. Biol. 353, 120–133 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. 134.

    Weisblat, D. A. & Kuo, D.-H. Developmental biology of the leech. Helobdella. Int. J. Dev. Biol. 58, 429–443 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Weisblat, D. A., Kim, S. Y. & Stent, G. S. Embryonic origins of cells in the leech Helobdella triserialis. Dev. Biol. 104, 65–85 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. 136.

    Nardelli-Haefliger, D. & Shankland, M. Lox10, a member of the NK-2 homeobox gene class, is expressed in a segmental pattern in the endoderm and in the cephalic nervous system of the leech Helobdella. Development 118, 877–892 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Westheide, W. & Purschke, G. in Spezielle Zoologie Teil 1: Einzeller und Wirbellose Tiere 3rd edn (eds Westheide, W. & Rieger, G.) 357–415 (Springer, Heidelberg, 2013).

  138. 138.

    Dorresteijn, A. W. Quantitative analysis of cellular differentiation during early embryogenesis ofPlatynereis dumerilii. Rouxs Arch. Dev. Biol. 199, 14–30 (1990).

    Article  PubMed  PubMed Central  Google Scholar 

  139. 139.

    Brinkmann, N. & Wanninger, A. Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol. Dev. 10, 606–618 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  140. 140.

    Westheide, W. Monographie der Gattungen Hesionides Friedrich und Microphthalmus Mecznikow (Polychaeta, Hesionidae). Z. Morphol. Tiere 61, 1–159 (1967).

    Article  Google Scholar 

  141. 141.

    Pilgrim, M. The anatomy and histology of the nervous system and excretory system of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi. J. Morphol. 155, 311–325 (1978).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. 142.

    Coulon, J. & Bessone, R. Autoradiographic detection of indolamine and catecholamine neurons in the nervous system of Owenia fusiformis (Polychaeta, Annelida). Cell Tissue Res. 198, 95–104 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. 143.

    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  PubMed Central  Google Scholar 

  144. 144.

    Arenas-Mena, C. Brachyury, Tbx2/3 and sall expression during embryogenesis of the indirectly developing polychaete Hydroides elegans. Int. J. Dev. Biol. 57, 73–83 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. 145.

    Boyle, M. J. & Seaver, E. C. Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). EvoDevo 1, 2 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. 146.

    Kitakoshi, T. & Shimizu, T. An oligochaete homologue of the Brachyury gene is expressed transiently in the third quartette of micromeres. Gene Expr. Patterns 10, 306–313 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. 147.

    Brunet, T., Lauri, A. & Arendt, D. Did the notochord evolve from an ancient axial muscle? The axochord hypothesis. BioEssays 37, 836–850 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  148. 148.

    Nielsen, C., Haszprunar, G., Ruthensteiner, B. & Wanninger, A. Early development of the aplacophoran mollusc. Chaetoderma. Acta Zool. 88, 231–247 (2007).

    Article  Google Scholar 

  149. 149.

    Okusu, A. Embryogenesis and development of Epimenia babai (Mollusca Neomeniomorpha). Biol. Bull. 203, 87–103 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  150. 150.

    Thompson, T. E. The development of Neomenia carinata Tullberg (Mollusca Aplacophora). Proc. R. Soc. B 153, 263–278 (1960).

    Article  Google Scholar 

  151. 151.

    Todt, C. & Wanninger, A. Of tests, trochs, shells, and spicules: development of the basal mollusk Wirenia argentea (Solenogastres) and its bearing on the evolution of trochozoan larval key features. Front. Zool. 7, 6 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  152. 152.

    Henry, J. Q., Okusu, A. & Martindale, M. Q. The cell lineage of the polyplacophoran, Chaetopleura apiculata: variation in the spiralian program and implications for molluscan evolution. Dev. Biol. 272, 145–160 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. 153.

    Hejnol, A., Martindale, M. Q. & Henry, J. Q. High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. Dev. Biol. 305, 63–76 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. 154.

    Conklin, E. G. The embryology of Crepidula, a contribution to the cell lineage and early development of some marine gasteropods. J. Morphol. 13, 1–226 (1897).

    Article  Google Scholar 

  155. 155.

    Chan, X. Y. & Lambert, J. D. Development of blastomere clones in the Ilyanassa embryo: transformation of the spiralian blastula into the larval body plan. Dev. Genes Evol. 224, 159–174 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  156. 156.

    Delsman, H. C. Entwicklungsgeschichte von Littorina obtusata. Tijdschr. Ned. Dierkd. Ver. 13, 170–340 (1914).

    Google Scholar 

  157. 157.

    Dictus, W. J. A. G. & Damen, P. Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (mollusca). Mech. Dev. 62, 213–226 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. 158.

    Bullock, T. H. & Horridge, G. A. Structure and Function in the Nervous Systems of Invertebrates (Freemann, San Francisco, CA, 1965).

  159. 159.

    Sigwart, J. D. & Sumner-Rooney, L. H. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 172–189 (Oxford Univ. Press, Oxford, 2016).

  160. 160.

    Voronezhskaya, E. E. & Croll, R. P. in Structure and Evolution of Invertebrate Nervous Syatems (eds Schmidt-Rhaesa, A. et al.) 196–221 (Oxford Univ. Press, Oxford, 2016).

  161. 161.

    Todt, C., Büchinger, T. & Wanninger, A. The nervous system of the basal mollusk Wirenia argentea (Solenogastres): a study employing immunocytochemical and 3D reconstruction techniques. Mar. Biol. Res. 4, 290–303 (2008).

    Article  Google Scholar 

  162. 162.

    Shigeno, S., Sasaki, T. & Haszprunar, G. Central nervous system of Chaetoderma japonicum (Caudofoveata, Aplacophora): implications for diversified ganglionic plans in early molluscan evolution. Biol. Bull. 213, 122–134 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  163. 163.

    Faller, S., Rothe, B. H., Todt, C., Schmidt-Rhaesa, A. & Loesel, R. Comparative neuroanatomy of Caudofoveata, Solenogastres, Polyplacophora, and Scaphopoda (Mollusca) and its phylogenetic implications. Zoomorphology 131, 149–170 (2012).

    Article  Google Scholar 

  164. 164.

    Wollesen, T. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 222–240 (Oxford Univ. Press, Oxford, 2016).

  165. 165.

    Redl, E., Scherholz, M., Todt, C., Wollesen, T. & Wanninger, A. Development of the nervous system in Solenogastres (Mollusca) reveals putative ancestral spiralian features. EvoDevo 5, 48 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  166. 166.

    Friedrich, S., Wanninger, A., Brückner, M. & Haszprunar, G. Neurogenesis in the mossy chiton, Mopalia muscosa (Gould) (Polyplacophora): evidence against molluscan metamerism. J. Morphol. 253, 109–117 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  167. 167.

    Hinman, V. F., O’Brien, E. K., Richards, G. S. & Degnan, B. M. Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. Evol. Dev. 5, 508–521 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. 168.

    Raineri, M. Is a mollusc an evolved bent metatrochophore? A histochemical investigation of neurogenesis in Mytilus (Mollusca: Bivalvia). J. Mar. Biol. Assoc. UK 75, 571–592 (1995).

    Article  Google Scholar 

  169. 169.

    Koolakovsky, E. E. & Phlyachinskaya, L. P. Formation of elements of the regulatory systems during larval development of Mytilus edulis. Zool. Zh. 72, 20–28 (1993).

    Google Scholar 

  170. 170.

    Voronezhskaya, E. E., Nezlin, L. P., Odintsova, N. A., Plummer, J. T. & Croll, R. P. Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphology 127, 97–110 (2008).

    Article  Google Scholar 

  171. 171.

    Ellis, I. & Kempf, S. C. Characterization of the central nervous system and various peripheral innervations during larval development of the oyster Crassostrea virginica. Invertebr. Biol. 130, 236–250 (2011).

    Article  Google Scholar 

  172. 172.

    Wanninger, A. & Haszprunar, G. The development of the serotonergic and FMRF-amidergic nervous system in Antalis entalis (Mollusca, Scaphopoda). Zoomorphology 122, 77–85 (2003).

    Google Scholar 

  173. 173.

    Kin, K., Kakoi, S. & Wada, H. A novel role for dpp in the shaping of bivalve shells revealed in a conserved molluscan developmental program. Dev. Biol. 329, 152–166 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. 174.

    Perry, K. J. et al. Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusc. Crepidula. Dev. Dyn. 244, 1215–1248 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. 175.

    Andrade, S. C. S. et al. A transcriptomic approach to ribbon worm systematics (Nemertea): resolving the Pilidiophora problem. Mol. Biol. Evol. 31, 3206–3215 (2014).

    Article  CAS  PubMed  Google Scholar 

  176. 176.

    Beckers, P. The nervous systems of Pilidiophora (Nemertea). Zoomorphology 134, 1–24 (2015).

    Article  Google Scholar 

  177. 177.

    Kvist, S., Laumer, C. E., Junoy, J. & Giribet, G. New insights into the phylogeny, systematics and DNA barcoding of Nemertea. Invertebr. Syst. 28, 287–308 (2014).

    Article  CAS  Google Scholar 

  178. 178.

    Nielsen, C. Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. J. Exp. Zool. 304B, 401–447 (2005).

    Article  Google Scholar 

  179. 179.

    Hiebert, L. S. & Maslakova, S. A. Hox genes pattern the anterior–posterior axis of the juvenile but not the larva in a maximally indirect developing invertebrate, Micrura alaskensis (Nemertea). BMC Biol. 13, 23 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  180. 180.

    Jägersten, G. Evolution of the Metazoan Life Cycle (Academic, London, 1972).

  181. 181.

    Maslakova, S. A. Development to metamorphosis of the nemertean pilidium larva. Front. Zool. 7, 30 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  182. 182.

    von Dassow, G. & Maslakova, S. A. The trochoblasts in the pilidium larva break an ancient spiralian constraint to enable continuous larval growth and maximally indirect development. EvoDevo 8, 19 (2017).

    Article  CAS  Google Scholar 

  183. 183.

    Cantell, C. E. The devouring of the larval tissue during metamorphosis of pilidium larvae (Nemertini). Ark. Zool. 2nd Ser. 18, 489–492 (1966).

    Google Scholar 

  184. 184.

    Martín-Durán, J. M., Vellutini, B. C. & Hejnol, A. Evolution and development of the adelphophagic, intracapsular Schmidt’s larva of the nemertean Lineus ruber. EvoDevo 6, 28 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. 185.

    Hickman, V. V. The occurrence in Tasmania of the land nemertine, Geonemertes australiensis Dendy, with some account of its distribution, habits, variations and development. Pap. Proc. R. Soc. Tasmania 97, 63–75 (1963).

    Google Scholar 

  186. 186.

    Maslakova, S. A., Martindale, M. Q. & Norenburg, J. L. Vestigial prototroch in a basal nemertean, Carinoma tremaphoros (Nemertea; Palaeonemertea). Evol. Dev. 6, 219–226 (2004).

    Article  CAS  PubMed  Google Scholar 

  187. 187.

    Maslakova, S. A., Martindale, M. Q. & Norenburg, J. L. Fundamental properties of the spiralian developmental program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea). Dev. Biol. 267, 342–360 (2004).

    Article  CAS  PubMed  Google Scholar 

  188. 188.

    Maslakova, S. A. & von Döhren, J. Larval development with transitory epidermis in Paranemertes peregrina and other hoplonemerteans. Biol. Bull. 216, 273–292 (2009).

    Article  PubMed  Google Scholar 

  189. 189.

    Hiebert, L. S. & Maslakova, S. A. Expression of Hox, Cdx, and Six3/6 genes in the hoplonemertean Pantinonemertes californiensis offers insight into the evolution of maximally indirect development in the phylum Nemertea. EvoDevo 6, 26 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. 190.

    Turbeville, J. M. in Microscopic Anatomy of Invertebrates Vol. 3 (ed. Harrison, F. W.) 285–328 (Wiley, New York, NY, 1991).

  191. 191.

    Beckers, P., Faller, S. & Loesel, R. Lophotrochozoan neuroanatomy: an analysis of the brain and nervous system of Lineus viridis(Nemertea) using different staining techniques. Front. Zool. 8, 17 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  192. 192.

    Hindinger, S., Schwaha, T. & Wanninger, A. Immunocytochemical studies reveal novel neural structures in nemertean pilidium larvae and provide evidence for incorporation of larval components into the juvenile nervous system. Front. Zool. 10, 31 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  193. 193.

    Nielsen, C. in Evolving Pathways: Key Themes in Evolutionary Developmental Biology (eds Minelli, A. & Fusco, G.) 399–416 (Cambridge Univ. Press, Cambridge, 2008).

  194. 194.

    Iwata, F. Studies on the comparative embryology of nemerteans with special reference to their interrelationships. Publ. Akkeshi Mar. Biol. Stn 10, 2–51 (1960).

    Google Scholar 

  195. 195.

    von Döhren, J. Development of the nervous system of Carinina ochracea (Palaeonemertea, Nemertea). PLoS ONE 11, e0165649 (2016).

    Article  CAS  Google Scholar 

  196. 196.

    Littlewood, D. T. J. & Waeschenbach, A. Evolution: a turn up for the worms. Curr. Biol. 25, R457–R460 (2015).

    Article  CAS  PubMed  Google Scholar 

  197. 197.

    Egger, B. et al. A transcriptomic–phylogenomic analysis of the evolutionary relationships of flatworms. Curr. Biol. 25, 1347–1353 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. 198.

    Ax, P. Multicellular Animals: A New Approach to the Phylogenetic Order in Nature Vol. 1 (Springer, Heidelberg, 1996).

  199. 199.

    Rawlinson, K. A. Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits. Front. Zool. 7, 12 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  200. 200.

    Rawlinson, K. A. The diversity, development and evolution of polyclad flatworm larvae. EvoDevo 5, 9 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  201. 201.

    Morris, J. et al. The embryonic development of the flatworm Macrostomum sp. Dev. Genes Evol. 214, 220–239 (2004).

    Article  Google Scholar 

  202. 202.

    Ellis, C. H. J. & Fausto-Sterling, A. in Embryology: Constructing the Organism (eds Gilbert, S. F. & Raunio, A. M.) 115–130 (Sinauer, Sunderland, MA, 1997).

  203. 203.

    Surface, F. M. The early development of a polyclad, Planocera inquilina Wh. Proc. Acad. Nat. Sci. Phila. 59, 514–559 (1907).

    Google Scholar 

  204. 204.

    Boyer, B. C., Henry, J. J. & Martindale, M. Q. The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev. Biol. 204, 111–123 (1998).

    Article  CAS  Google Scholar 

  205. 205.

    Ruppert, E. E. in Settlement and Metamorphosis of Marine Invertebrate Larvae (eds Chia, F. S. & Rice, M. E.) 65–81 (Elsevier, Toronto, 1978).

  206. 206.

    Halton, D. W. & Gustafsson, M. K. S. Functional morphology of the platyhelminth nervous system. Parasitology 113, S47–S72 (1996).

    Article  Google Scholar 

  207. 207.

    Reuter, M. & Halton, D. W. in Interrelationships of the Platyhelminthes Vol. 60 (eds Littlewood, D. T. J. & Bray, R. A.) 239–249 (Taylor and Francis, London, 2001).

  208. 208.

    Richter, S. et al. Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front. Zool. 7, 29 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  209. 209.

    Reisinger, E. Untersuchungen am Nernvensystem der Bothrioplana semperi Braun. Z. Morphol. Ökol. Tiere 5, 119–149 (1925).

    Article  Google Scholar 

  210. 210.

    Reisinger, E. Die Evolution des Orthogons der Spiralier und das Archicölomatenproblem. J. Zool. Syst. Evol. Res. 10, 1–43 (1972).

    Article  Google Scholar 

  211. 211.

    Lacalli, T. C. The nervous system and ciliary band of Müller’s larva. Proc. R. Soc. Lond. B 217, 37–58 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. 212.

    Lacalli, T. C. The brain and central nervous system of Müller’s larva. Can. J. Zool. 61, 39–51 (1983).

    Article  Google Scholar 

  213. 213.

    Martín-Durán, J. M. & Romero, R. Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev. Biol. 352, 164–176 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. 214.

    Adler, C. E., Seidel, C. W., McKinney, S. A. & Sánchez Alvarado, A. Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. eLife 3, e02238 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. 215.

    Currie, K. W. et al. HOX gene complement and expression in the planarian Schmidtea mediterranea. EvoDevo 7, 7 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. 216.

    de Beauchamp, P. Le développement des Gastrotriches. Bull. Soc. Zool. Fr. 54, 549–558 (1929).

    Google Scholar 

  217. 217.

    Sacks, M. Observations on the embryology of an aquatic gastrotrich, Lepidodermella squammata (Dujardin, 1841). J. Morphol. 96, 473–495 (1955).

    Article  Google Scholar 

  218. 218.

    Teuchert, G. Zur Fortpflanzung und Entwicklung der Macrodasyoidea (Gastrotricha). Z. Morphol. Tiere 63, 343–418 (1968).

    Article  Google Scholar 

  219. 219.

    Rothe, B. H., Schmidt-Rhaesa, A. & Kieneke, A. The nervous system of Neodasys chaetonotoideus (Gastrotricha: Neodasys) revealed by combining confocal laserscanning and transmission electron miocroscopy: evolutionary comparison of neuroanatomy within Gastrotricha and basal Protostomia. Zoomorphology 130, 51–84 (2011).

    Article  Google Scholar 

  220. 220.

    Teuchert, G. The ultrastructure of the marine gastrotrich Turbanella cornuta Remane (Macrodasyoidea) and its functional and phylogenetical importance. Zoomorphologie 88, 189–246 (1977).

    Article  Google Scholar 

  221. 221.

    Wiedermann, A. Zur Ultrastruktur des Nervensystems bei Cephalodasys maximus (Macrodasyoida, Gastrotricha). Microfauna Mar. 10, 173–233 (1995).

    Google Scholar 

  222. 222.

    Sørensen, M. V. Further structures in the jaw apparatus of Limnognathia maerski (Micrognathozoa), with notes on the phylogeny of the Gnathifera. J. Morphol. 255, 131–145 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  223. 223.

    Riedl, R. J. Gnathostomulida from America. Science 163, 445–452 (1969).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. 224.

    Sterrer, W. & Sørensen, M. V. in Handbook of Zoology, Gastrotricha, Cycliophora and Gnathifera: Gastrotricha and Gnathifera Vol. 3 (ed. Schmidt-Rhaesa, A.) 135–196 (de Gruyter, Berlin, 2015).

  225. 225.

    Sørensen, M. V. & Kristensen, R. M. in Handbook of Zoology, Gastrotricha, Cycliophora and Gnathifera: Gastrotricha and Gnathifera Vol. 3 (ed. Schmidt-Rhaesa, A.) 197–216 (de Gruyter, Berlin, 2015).

  226. 226.

    Bekkouche, N. & Worsaae, K. Nervous system and ciliary structures of Micrognathozoa (Gnathifera): evolutionary insight from an early branch in Spiralia. R. Soc. Open Sci. 3, 160289 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. 227.

    Sielaff, M. et al. Phylogeny of Syndermata (syn. Rotifera): mitochondrial gene order verifies epizoic Seisonidea as sister to endoparasitic Acanthocephala within monophyletic Hemirotifera. Mol. Phylogenet. Evol. 96, 79–92 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. 228.

    Wey-Fabrizius, A. R. et al. Transcriptome data reveal Syndermatan relationships and suggest the evolution of endoparasitism in Acanthocephala via an epizoic stage. PLoS ONE 9, e88618 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  229. 229.

    Lechner, M. Untersuchungen zur Embryonalentwicklung des Rädertieres Asplanchna girodi De Guerne. Wilhelm Roux Arch. Entwickl. Mech. Org. 157, 117–173 (1966).

    Article  PubMed  PubMed Central  Google Scholar 

  230. 230.

    Remane, A. in Bronn’s Klassen und Ordnungen des Tierreichs (Akademische Verlagsgesellschaft, Leipzig, 1929–1933).

  231. 231.

    Clément, P. & Wurdak, E. in Microscopic Anatomy of Invertebrates Vol. 4 (ed. Harrison, F. W.) 219–297 (Wiley, New York, NY, 1991).

  232. 232.

    Leasi, F., Pennati, R. & Ricci, C. First description of the serotonergic nervous system in a bdelloid rotifer: Macrotrachela quadricornifera Milne 1886 (Philodinidae). Zool. Anz. 248, 47–55 (2009).

    Article  Google Scholar 

  233. 233.

    Hochberg, R. Three-dimensional reconstruction and neural map of the serotonergic brain of Asplanchna brightwellii (Rotifera, Monogononta). J. Morphol. 270, 430–441 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  234. 234.

    Hochberg, R. On the serotonergic nervous system of two planktonic rotifers, Conochilus coenobasis and C. dossuarius (Monogononta, Flosculariacea, Conochilidae). Zool. Anz. 245, 53–62 (2006).

    Article  Google Scholar 

  235. 235.

    Struck, T. H. et al. Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia. Mol. Biol. Evol. 31, 1833–1849 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  236. 236.

    Kocot, K. M. et al. Phylogenomics of Lophotrochozoa with consideration of systematic error. Syst. Biol. 66, 256–282 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  237. 237.

    Malakhov, V. V. Description of the development of Ascopodaria discreta (Coloniales, Barentsiidae) and discussion of the Kamptozoa status in the animal kingdom. Zool. Zh. 69, 20–30 (1990).

    Google Scholar 

  238. 238.

    Marcus, E. Briozoários marinhos brasileiros III. Bol. Fac. Filos. Cienc. Let. Univ. S. Paulo. Zool. 3, 111–354 (1939).

    Google Scholar 

  239. 239.

    Nielsen, C. On the life-cycle of some loxosomatidae (Entoprocta). Ophelia 3, 221–247 (1966).

    Article  Google Scholar 

  240. 240.

    Fuchs, J., Bright, M., Funch, P. & Wanninger, A. Immunocytochemistry of the neuromuscular systems of Loxosomella vivipara and L. parguerensis (Entoprocta: Loxosomatidae). J. Morphol. 267, 866–883 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  241. 241.

    Schwaha, T., Wood, T. S. & Wanninger, A. Trapped in freshwater: the internal anatomy of the entoproct Loxosomatoides sirindhornae. Front. Zool. 7, 7 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  242. 242.

    Nielsen, C. Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9, 209–341 (1971).

    Article  Google Scholar 

  243. 243.

    Wanninger, A. Fuchs, J. & Haszprunar, G. Anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications. Invertebr. Biol. 126, 268–278 (2007).

    Article  Google Scholar 

  244. 244.

    Wanninger, A. Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the tetraneuralia concept. Biol. Bull. 216, 293–306 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  245. 245.

    Funch, P. & Kristensen, R. M. in Microscopic Anatomy of Invertebrates Vol. 13 (ed. Harrison, F. W.) 409–474 (Wiley, New York, NY, 1997).

  246. 246.

    Obst, M. & Funch, P. Dwarf male of Symbion pandora (cycliophora). J. Morphol. 255, 261–278 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  247. 247.

    Neves, R. C. in Structure and Development of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 360–367 (Oxford Univ. Press, Oxford, 2016).

  248. 248.

    Reed, C. G. in Reproduction of Marine Invertebrates Vol. 6 (eds Giese, A. C. et al.) 85–245 (Boxwood, Pacfici Grove, CA, 1991).

  249. 249.

    Nielsen, C. & Worsaae, K. Structure and occurrence of cyphonautes larvae (Bryozoa, Ectoprocta). J. Morphol. 271, 1094–1109 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  250. 250.

    Gruhl, A. Ultrastructure of mesoderm formation and development in Membranipora membranacea (Bryozoa: Gymnolaemata). Zoomorphology 129, 45–60 (2010).

    Article  Google Scholar 

  251. 251.

    Schwaha, T. F. & Wanninger, A. The serotonin-lir nervous system of the Bryozoa (Lophotrochozoa): a general pattern in the Gymnolaemata and implications for lophophore evolution of the phylum. BMC Evol. Biol. 15, 223 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  252. 252.

    Shunkina, K. V., Zaytseva, O. V., Starunov, V. V. & Ostrovsky, A. N. Comparative morphology of the nervous system in three phylactolaemate bryozoans. Front. Zool. 12, 28 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. 253.

    Gruhl, A. & Schwaha, T. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 325–340 (Oxford Univ. Press, Oxford, 2016).

  254. 254.

    Gruhl, A. Serotonergic and FMRFamidergic nervous systems in gymnolaemate bryozoan larvae. Zoomorphology 128, 135–156 (2009).

    Article  Google Scholar 

  255. 255.

    Hausdorf, B., Helmkampf, M., Nesnidal, M. P. & Bruchhaus, I. Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida). Mol. Phylogenet. Evol. 55, 1121–1127 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  256. 256.

    Sperling, E. A., Pisani, D. & Peterson, K. J. Molecular paleobiological insights into the origin of the Brachiopoda. Evol. Dev. 13, 290–303 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  257. 257.

    Silén, L. Developmental biology of Phoronidea of the Gullmar Fiord area (west coast of Sweden). Acta Zool. 35, 215–257 (1954).

    Article  Google Scholar 

  258. 258.

    Freeman, G. & Martindale, M. Q. The origin of mesoderm in phoronids. Dev. Biol. 252, 301–311 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  259. 259.

    Temereva, E. N. & Malakhov, V. V. Embryogenesis in phoronids. Invertebr. Zool. 9, 1–39 (2012).

    Article  Google Scholar 

  260. 260.

    Zimmer, R. L. in Reproduction of Marine Invertebrates Vol. 6 (eds Giese, A. C. et al.) 1–45 (Boxwood, Pacfici Grove, CA, 1991).

  261. 261.

    Temereva, E. N. The digestive tract of actinotroch larvae (Lophotrochozoa, Phoronida): anatomy, ultrastructure, innervations, and some observations of metamorphosis. Can. J. Zool. 88, 1149–1168 (2010).

    Article  Google Scholar 

  262. 262.

    Herrmann, K. Dokumentation des Metamorphoseablaufs bei Actinotrocha branchiata (Phoronidea). Helgoländer Wiss. Meeresunters. 25, 473–485 (1973).

    Article  Google Scholar 

  263. 263.

    Herrmann, K. in Microscopic Anatomy of Invertebrates Vol. 13 (ed. Harrison, F. W.) 207–235 (Wiley, Pacific Grove, CA, 1997).

  264. 264.

    Temereva, E. & Wanninger, A. Development of the nervous system in Phoronopsis harmeri (Lophotrochozoa, Phoronida) reveals both deuterostome- and trochozoan-like features. BMC Evol. Biol. 12, 121 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  265. 265.

    Temereva, E. N. Ventral nerve cord in Phoronopsis harmeri larvae. J. Exp. Zool. 318B, 26–34 (2012).

    Article  Google Scholar 

  266. 266.

    Temereva, E. N. & Tsitrin, E. B. Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny. Front. Zool. 11, 3 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  267. 267.

    Temereva, E. N. & Malakhov, V. V. Embryogenesis and larval development of Phoronopsis harmeri Pixell, 1912 (Phoronida): dual origin of the coelomic mesoderm. Invertebr. Reprod. Dev. 50, 57–66 (2007).

    Article  Google Scholar 

  268. 268.

    Temereva, E. N. & Tsitrin, E. B. Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system. Front. Zool. 11, 35 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  269. 269.

    Temereva, E. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 351–359 (Oxford Univ. Press, Oxford, 2016).

  270. 270.

    Silén, L. On the nervous system of Phoronis. Ark. Zool. 2nd Ser. 6, 1–40 (1954).

    Google Scholar 

  271. 271.

    Long, J. A. & Stricker, S. A. in Reproduction of Marine Invertebrates Vol. 6 (eds A. C. Giese, J. S. Pearse, & V. B. Pearse) 47–84 (Boxwood, Pacfici Grove, CA, 1991).

  272. 272.

    Santagata, S. in Evolutionary Developmental Biology of Invertebrates 2: Lophotrochozoa (Spiralia) (ed. Wanninger, A.) 263–277 (Springer, Vienna, 2015).

  273. 273.

    Yatsu, N. On the development of Lingula anatina. J. Coll. Sci. Imp. Univ. Tokyo 17, 1–112 (1902).

    Google Scholar 

  274. 274.

    Freeman, G. Regional specification during embryogenesis in the inarticulate brachiopod Glottidia. Dev. Biol. 172, 15–36 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  275. 275.

    Freeman, G. Regional specification during embryogenesis in Rhynchonelliform brachiopods. Dev. Biol. 261, 268–287 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  276. 276.

    Freeman, G. Regional specification during embryogenesis in the craniiform brachiopod Crania anomala. Dev. Biol. 227, 219–238 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  277. 277.

    Lüter, C. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 341–359 (Oxford Univ. Press, Oxford, 2016).

  278. 278.

    James, M. A. in Microscopic Anatomy of Invertebrates Vol. 13 (ed. Harrison, F. W.) 297–407 (Wiley, New York, NY, 1997).

  279. 279.

    van Bemmelen, J. F. Untersuchungen über den anatomischen und histologischen Bau der Brachiopoda Testicardinia. Jena Z. Naturw. 16, 88–161 (1883).

    Google Scholar 

  280. 280.

    Temereva, E. N. & Tsitrin, E. B. Modern data on the innervation of the lophophore in Lingula anatina (Brachiopoda) support the monophyly of the lophophorates. PLoS ONE 10, e0123040 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. 281.

    Altenburger, A. & Wanninger, A. Neuromuscular development in Novocrania anomala: evidence for the presence of serotonin and a spiralian-like apical organ in lecithotrophic brachiopod larvae. Evol. Dev. 12, 16–24 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  282. 282.

    Robertson, H. E., Lapraz, F., Egger, B., Telford, M. J. & Schiffer, P. H. The mitochondrial genomes of the acoelomorph worms Paratomella rubra, Isodiametra pulchra and Archaphanostoma ylvae. Sci. Rep. 7, 1847 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  283. 283.

    Bourlat, S. J., Nielsen, C., Lockyer, A. E., Littlewood, D. T. & Telford, M. J. Xenoturbella is a deuterostome that eats molluscs. Nature 424, 925–928 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. 284.

    Mao, Q. & Lecuit, T. Evo-devo: universal toll pass for the extension highway? Curr. Biol. 26, R680–R683 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  285. 285.

    Jägersten, G. On the early phylogeny of the Metazoa: the bilaterogastraea theory. Zoologiska Bidrag Uppsala 30, 321–354 (1955).

    Google Scholar 

  286. 286.

    Passamaneck, Y. J., Furchheim, N., Hejnol, A., Martindale, M. Q. & Lüter, C. Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo 2, 6 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  287. 287.

    Santagata, S. Evaluating neurophylogenetic patterns in the larval nervous systems of brachiopods and their evolutionary significance to other bilaterian phyla. J. Morphol. 272, 1153–1169 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  288. 288.

    Hay-Schmidt, A. Ultrastructure and immunocytochemistry of the nervous system of the larvae of Lingula anatina and Glottidia sp. (Brachiopoda). Zoomorphology 112, 189–205 (1992).

    Article  Google Scholar 

  289. 289.

    Altenburger, A., Martinez, P. & Wanninger, A. Homeobox gene expression in Brachiopoda: the role of Not and Cdx in bodyplan patterning, neurogenesis, and germ layer specification. Gene Expr. Patterns 11, 427–436 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  290. 290.

    Hejnol, A. & Schnabel, R. The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132, 1349–1361 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  291. 291.

    Hejnol, A. & Schnabel, R. What a couple of dimensions can do for you: comparative developmental studies using 4D microscopy—examples from tardigrade development. Integr. Comp. Biol. 46, 151–161 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  292. 292.

    Persson, D. K., Halberg, K. A., Jørgensen, A., Møbjerg, N. & Kristensen, R. M. Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): tardigrade brain structure supports the clade Panarthropoda. J. Morphol. 273, 1227–1245 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  293. 293.

    Persson, D. K., Halberg, K. A., Jørgensen, A., Møbjerg, N. & Kristensen, R. M. Brain anatomy of the marine tardigrade Actinarctus doryphorus (Arthrotardigrada). J. Morphol. 275, 173–190 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  294. 294.

    Zantke, J., Wolff, C. & Scholtz, G. Three-dimensional reconstruction of the central nervous system of Macrobiotus hufelandi (Eutardigrada, Parachela): implications for the phylogenetic position of Tardigrada. Zoomorphology 127, 21–36 (2008).

    Article  Google Scholar 

  295. 295.

    Anderson, D. T. & Manton, S. M. Studies on the Onychophora VIII. The relationship between the embryos and the oviduct in the viviparous placental onychophorans Epiperipatus trinidadensis Bouvier and Macroperipatus torquatus (Kennel) from Trinidad. Phil. Trans. R. Soc. Lond. B 264, 161–189 (1972).

    Article  Google Scholar 

  296. 296.

    Sedgwick, A. The development of the Cape species of Peripatus. Part III. On the changes from stage A to stage F. Q. J. Microsc. Sci. 27, 467–550 (1887).

    Google Scholar 

  297. 297.

    Manton, S. M. Studies on the Onychophora. VII. The early embryonic stages of Peripatopsis, and some general considerations concerning the morphology and phylogeny of the Arthropoda. Phil. Trans. R. Soc. Lond. B 233, 483–580 (1949).

    Article  Google Scholar 

  298. 298.

    Eriksson, B. J. & Tait, N. N. Early development in the velvet worm Euperipatoides kanangrensis Reid 1996 (Onychophora: Peripatopsidae). Arthropod Struct. Dev. 41, 483–493 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  299. 299.

    Eriksson, B. J., Tait, N. N. & Budd, G. E. Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J. Morphol. 255, 1–23 (2003).

    Article  PubMed  Google Scholar 

  300. 300.

    Mayer, G. & Whitington, P. M. Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda. Dev. Biol. 335, 263–275 (2009).

    Article  CAS  Google Scholar 

  301. 301.

    Strausfeld, N. J., Strausfeld, C. M., Loesel, R., Rowell, D. & Stowe, S. Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc. R. Soc. B 273, 1857–1866 (2006).

    Article  Google Scholar 

  302. 302.

    Henson, H. The theoretical aspect of insect metamorphosis. Biol. Rev. Camb. Philos. Soc. 21, 1–14 (1946).

    Article  CAS  Google Scholar 

  303. 303.

    Janssen, R. & Budd, G. E. Investigation of endoderm marker-genes during gastrulation and gut-development in the velvet worm Euperipatoides kanangrensis. Dev. Biol. 427, 155–164 (2017).

    Article  CAS  Google Scholar 

  304. 304.

    Yasuo, H. & Satoh, N. An ascidian homolog of the mouse Brachyury (T) gene is expressed exclusively in notochord cells at the fate restricted stage. Dev. Growth Differ. 36, 9–18 (1994).

    Article  CAS  Google Scholar 

  305. 305.

    Rota-Stabelli, O., Daley, A. C. & Pisani, D. Molecular timetrees reveal a Cambrian colonization of land and a new scenario for Ecdysozoan evolution. Curr. Biol. 23, 392–398 (2013).

    Article  CAS  PubMed  Google Scholar 

  306. 306.

    Regier, J. C. et al. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079–1083 (2010).

    Article  CAS  PubMed  Google Scholar 

  307. 307.

    Akiyama-Oda, Y. & Oda, H. Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development 130, 1735–1747 (2003).

    Article  CAS  PubMed  Google Scholar 

  308. 308.

    Scholtz, G. & Wolff, C. in Arthropod Biology and Evolution Ch. 4 (eds Minelli, A. et al.) 63–89 (Springer, Berlin, Heidelberg, 2013).

  309. 309.

    Gerberding, M., Browne, W. E. & Patel, N. H. Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129, 5789–5801 (2002).

    Article  CAS  PubMed  Google Scholar 

  310. 310.

    Hertzler, P. L. Development of the mesendoderm in the dendrobranchiate shrimp Sicyonia ingentis. Arthropod Struct. Dev. 31, 33–49 (2002).

    Article  Google Scholar 

  311. 311.

    Weygoldt, P. Embryologische Untersuchungen an Ostrakoden: die Entwicklung von Cyprideis litoralis (GS Brady) (Ostracoda, Podocopa, Cytheridae). Zool. Jahrb. Abt. Anat. Ontogenie Tiere 78, 369–426 (1960).

    Google Scholar 

  312. 312.

    Fioroni, P. Die organogenetische und transitorische Rolle der Vitellophagen in der Darmentwicklung von Galathea (Crustacea, Anomura). Z. Morphol. Tiere 67, 263–306 (1970).

    Article  Google Scholar 

  313. 313.

    Hanström, B. Vergleichende Anatomie des Nervensystems der wirbellosen Tiere (Springer, Berlin, 1928).

  314. 314.

    Heuer, C. M., Müller, C. H., Todt, C. & Loesel, R. Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida. Front. Zool. 7, 13 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  315. 315.

    Steinmetz, P. R. et al. Six3 demarcates the anterior-most developing brain region in bilaterian animals. EvoDevo 1, 14 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  316. 316.

    Harzsch, S. Ontogeny of the ventral nerve cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Struct. Dev. 32, 17–37 (2003).

    Article  Google Scholar 

  317. 317.

    Anderson, D. T. On the embryology of the cirripede custaceans Tetraclita rosea (Krauss), Tetraclita purpurascens (Wood), Chthamalus antennatus (Darwin) and Chamaesipho columna (Spengler) and some considerations of custacean pylogenetic relationships. Phil. Trans. R. Soc. Lond. B 256, 183–235 (1969).

    Article  Google Scholar 

  318. 318.

    Vilpoux, K., Sandeman, R. & Harzsch, S. Early embryonic development of the central nervous system in the Australian crayfish and the Marbled crayfish (Marmorkrebs). Dev. Genes Evol. 216, 209–223 (2006).

    Article  CAS  Google Scholar 

  319. 319.

    Kanayama, M. et al. Travelling and splitting of a wave of hedgehog expression involved in spider-head segmentation. Nat. Commun. 2, 500 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  320. 320.

    Edgar, A., Bates, C., Larkin, K. & Black, S. Gastrulation occurs in multiple phases at two distinct sites in Latrodectus and Cheiracanthium spiders. EvoDevo 6, 33 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  321. 321.

    Yamazaki, K., Akiyama-Oda, Y. & Oda, H. Expression patterns of a twist-related gene in embryos of the spider Achaearanea tepidariorum reveal divergent aspects of mesoderm development in the fly and spider. Zool. Sci. 22, 177–185 (2005).

    Article  CAS  Google Scholar 

  322. 322.

    Holm, Å. Experimentelle Untersuchungen über die Entwicklung und Entwicklungsphysiologie des Spinnenembryos (Almqvist & Wiksell, Stockholm, 1952).

  323. 323.

    Green, J. E. & Akam, M. Germ cells of the centipede Strigamia maritima are specified early in embryonic development. Dev. Biol. 392, 419–430 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  324. 324.

    Heymons, R. Die Entwicklungsgeschichte der Scolopender. Zoologica 13, 1–224 (1901).

    Google Scholar 

  325. 325.

    Brena, C. in Evolutionary Developmental Biology of Invertebrates: Ecdysozoa I. Non-tetraconata Vol. 3 (ed. Wanninger, A.) 141–189 (Springer, Vienna, 2015).

  326. 326.

    Browne, W. E., Schmid, B. G., Wimmer, E. A. & Martindale, M. Q. Expression of otd orthologs in the amphipod crustacean. Parhyale hawaiensis. Dev. Genes Evol. 216, 581–595 (2006).

    Article  Google Scholar 

  327. 327.

    Alwes, F., Hinchen, B. & Extavour, C. G. Patterns of cell lineage, movement, and migration from germ layer specification to gastrulation in the amphipod crustacean Parhyale hawaiensis. Dev. Biol. 359, 110–123 (2011).

    Article  CAS  Google Scholar 

  328. 328.

    Copf, T., Rabet, N., Celniker, S. E. & Averof, M. Posterior patterning genes and the identification of a unique body region in the brine shrimp Artemia franciscana. Development 130, 5915–5927 (2003).

    Article  CAS  Google Scholar 

  329. 329.

    Copf, T., Schröder, R. & Averof, M. Ancestral role of caudal genes in axis elongation and segmentation. Proc. Natl Acad. Sci. USA 101, 17711–17715 (2004).

    Article  CAS  Google Scholar 

  330. 330.

    Rabet, N., Gibert, J.-M., Quéinnec, E., Deutsch, J. S. & Mouchel-Vielh, E. The caudal gene of the barnacle Sacculina carcini is not expressed in its vestigial abdomen. Dev. Genes Evol. 211, 172–178 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  331. 331.

    Campos-Ortega, J. & Hartenstein, V. The Embryonic Development of Drosophila melanogaster 2nd edn (Springer, Heidelberg, 1997).

  332. 332.

    Hartenstein, V., Technau, G. M. & Campos-Ortega, J. A. Fate-mapping in wild-type. III. A fate map of the blastoderm. Wilhelm Roux Arch. Entwickl. Mech. Org. 194, 213–216 (1985).

    Article  Google Scholar 

  333. 333.

    Supatto, W. et al. In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proc. Natl Acad. Sci. USA 102, 1047–1052 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  334. 334.

    Wallingford, J. B., Fraser, S. E. & Harland, R. M. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2, 695–706 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  335. 335.

    Mlodzik, M. Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet. 18, 564–571 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  336. 336.

    Singer, J. B., Harbecke, R., Kusch, T., Reuter, R. & Lengyel, J. A. Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development 122, 3707–3718 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  337. 337.

    Weigel, D., Jürgens, G., Küttner, F., Seifert, E. & Jäckle, H. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645–658 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  338. 338.

    Schröder, R., Eckert, C., Wolff, C. & Tautz, D. Conserved and divergent aspects of terminal patterning in the beetle Tribolium castaneum. Proc. Natl Acad. Sci. USA 97, 6591–6596 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  339. 339.

    Goriely, A. et al. A functional homologue of goosecoid in Drosophila. Development 122, 1641–1650 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  340. 340.

    Hahn, M. & Jäckle, H. Drosophila goosecoid participates in neural development but not in body axis formation. EMBO J. 15, 3077–3084 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  341. 341.

    Mlodzik, M., Fjose, A. & Gehring, W. J. Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J. 4, 2961–2969 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  342. 342.

    Schierenberg, E. & Sommer, R. J. in Handbook of Zoology: Gastrotricha, Cycliophora and Gnathifera: Nematoda Vol. 2 (ed. Schmidt-Rhaesa, A.) 61–108 (de Gruyter, Berlin, 2013).

  343. 343.

    Schierenberg, E. Unusual cleavage and gastrulation in a freshwater nematode: developmental and phylogenetic implications. Dev. Genes Evol. 215, 103–108 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  344. 344.

    Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64–119 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  345. 345.

    Decraemer, W., Coomans, A. & Baldwin, J. in Handbook of Zoology, Gastrotricha, Cycliophora and Gnathifera: Nematoda Vol. 2 (ed. Schmidt-Rhaesa, A.) 1–60 (de Gruyter, Berlin, 2013).

  346. 346.

    Sithigorngul, P., Jarecki, J. L. & Stretton, A. O. W. A specific antibody to neuropeptide AF1 (KNEFIRFamide) recognizes a small subset of neurons in Ascaris suum: differences from Caenorhabditis elegans. J. Comp. Neurol. 519, 1546–1561 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  347. 347.

    Horner, M. A. et al. pha-4, an HNF-3 homolog, specifies pharyngeal organ identity in Caenorhabditis elegans. Genes Dev. 12, 1947–1952 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  348. 348.

    Kalb, J. M. et al. pha-4 is Ce-fkh-1, a fork head/HNF-α,β,γ homolog that functions in organogenesis of the C. elegans pharynx. Development 125, 2171–2180 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  349. 349.

    Mango, S. E., Lambie, E. J. & Kimble, J. The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans. Development 120, 3019–3031 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  350. 350.

    Gaudet, J. & Mango, S. E. Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295, 821–825 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  351. 351.

    Ahringer, J. Posterior patterning by the Caenorhabditis elegans even-skipped homolog vab-7. Genes Dev. 10, 1120–1130 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  352. 352.

    Edgecombe, G. D. et al. Higher-level metazoan relationships: recent progress and remaining questions. Org. Divers. Evol. 11, 151–172 (2011).

    Article  Google Scholar 

  353. 353.

    Martín-Durán, J. M., Wolff, G. H., Strausfeld, N. J. & Hejnol, A. The larval nervous system of the penis worm Priapulus caudatus (Ecdysozoa). Phil. Trans. R. Soc. B 371, 20150050 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  354. 354.

    Kozloff, E. N. Stages of development, from first cleavage to hatching, of an Echinoderes (Phylum Kinorhyncha: Class Cyclorhagida). Cah. Biol. Mar. 48, 199–206 (2007).

    Google Scholar 

  355. 355.

    Wennberg, S. A., Janssen, R. & Budd, G. E. Hatching and earliest larval stages of the priapulid worm Priapulus caudatus. Invertebr. Biol. 128, 157–171 (2009).

    Article  Google Scholar 

  356. 356.

    Doncaster, L. On the development of Sagitta; with notes on the anatomy of the adult. Q. J. Microsc. Sci. 46, 351–395 (1902).

    Google Scholar 

  357. 357.

    John, C. C. Habits structure, and development of Spadella cephaloptera. Q. J. Microsc. Sci. 75, 625–696 (1933).

    Google Scholar 

  358. 358.

    Shinn, G. L. & Roberts, M. E. Ultrastructure of hatchling chaetognaths (Ferosagitta hispida): epithelial arrangement of the mesoderm and its phylogenetic implications. J. Morphol. 219, 143–163 (1994).

    Article  PubMed  PubMed Central  Google Scholar 

  359. 359.

    Shimotori, T. & Goto, T. Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: relationship to protostomes. Dev. Growth Differ. 43, 371–382 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  360. 360.

    Rieger, V. et al. Immunohistochemical analysis and 3D reconstruction of the cephalic nervous system in Chaetognatha: insights into the evolution of an early bilaterian brain? Invertebr. Biol. 129, 77–104 (2010).

    Article  Google Scholar 

  361. 361.

    Harzsch, S., Perez, Y. & Müller, C. H. G. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 652–664 (Oxford Univ. Press, Oxford, 2016).

  362. 362.

    Harzsch, S. & Müller, C. H. G. A new look at the ventral nerve centre of Sagitta: implications for the phylogenetic position of Chaetognatha (arrow worms) and the evolution of the bilaterian nervous system. Front. Zool. 4, 14 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  363. 363.

    Rieger, V. et al. Development of the nervous system in hatchlings of Spadella cephaloptera (Chaetognatha), and implications for nervous system evolution in Bilateria. Dev. Growth Differ. 53, 740–759 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  364. 364.

    Harzsch, S., Müller, C. H. G. & Perez, Y. in Evolutionary Developmental Biology of Invertebrates Vol. 1 (ed. Wanninger, A.) 215–240 (Springer, Heidelberg, 2015).

  365. 365.

    Takada, N., Goto, T. & Satoh, N. Expression pattern of the Brachyury gene in the arrow worm Paraspadella gotoi (Chaetognatha). Genesis 32, 240–245 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  366. 366.

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

    Article  PubMed  PubMed Central  Google Scholar 

  367. 367.

    Ruppert, E. E. & Balser, E. J. Nephridia in the larvae of hemichordates and echinoderms. Biol. Bull. 171, 188–196 (1986).

    Article  Google Scholar 

  368. 368.

    Stach, T. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 689–698 (Oxford Univ. Press, Oxford, 2016).

  369. 369.

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

    Article  PubMed  PubMed Central  Google Scholar 

  370. 370.

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

    Article  PubMed  PubMed Central  Google Scholar 

  371. 371.

    Nübler-Jung, K. & Arendt, D. Dorsoventral axis inversion: enteropneust anatomy links invertebrates to chordates turned upside down. J. Zool. Syst. Evol. Res. 37, 93–100 (1999).

    Article  Google Scholar 

  372. 372.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  373. 373.

    Kaul-Strehlow, S., Urata, M., Minokawa, T., Stach, T. & Wanninger, A. Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords. Org. Divers. Evol. 15, 405–422 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  374. 374.

    Peterson, K. J., Cameron, R. A., Tagawa, K., Satoh, N. & Davidson, E. H. 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 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  375. 375.

    Röttinger, E. & Martindale, M. Q. Ventralization of an indirect developing hemichordate by NiCl2 suggests a conserved mechanism of dorso-ventral (D/V) patterning in Ambulacraria (hemichordates and echinoderms). Dev. Biol. 354, 173–190 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  376. 376.

    Taguchi, S. et al. Characterization of a hemichordate fork head/HNF-3 gene expression. Dev. Genes Evol. 210, 11–17 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  377. 377.

    Ikuta, T. et al. Identification of an intact ParaHox cluster with temporal colinearity but altered spatial colinearity in the hemichordate Ptychodera flava. BMC Evol. Biol. 13, 129 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  378. 378.

    Fritzenwanker, J. H., Gerhart, J., Freeman, R. M. Jr & Lowe, C. J. The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii. EvoDevo 5, 17 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  379. 379.

    Dilly, P. N. The larva of Rhabdopleura compacta (Hemichordata). Mar. Biol. 18, 69–86 (1973).

    Article  Google Scholar 

  380. 380.

    Sato, A., Bishop, J. D. D. & Holland, P. W. H. Developmental biology of pterobranch hemichordates: history and perspectives. Genesis 46, 587–591 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  381. 381.

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

    Article  Google Scholar 

  382. 382.

    Ruppert, E. E., Fox, R. S. & Barnes, R. D. Invertebrate Zoology: A Functional Evolutionary Approach 7th edn (Brooks/Cole, Belmont, CA, 2004).

  383. 383.

    Dilly, P. N. Cephalodiscus reproductive biology (Pterobranchia, Hemichordata). Acta Zool. 95, 111–124 (2014).

    Article  Google Scholar 

  384. 384.

    Gilchrist, J. D. F. On the development of the Cape Cephalodiscus (C. gilchristi, Ridewood). Q. J. Microsc. Sci. 62, 189–211 (1917).

    Google Scholar 

  385. 385.

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

    Article  Google Scholar 

  386. 386.

    David, B. & Mooi, R. How Hox genes can shed light on the place of echinoderms among the deuterostomes. EvoDevo 5, 22 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  387. 387.

    Mortensen, T. Studies in the Development of Crinoids. Pap. Dep. Mar. Biol. Carnegie Inst. Wash. 16, 1–94 (1920)

  388. 388.

    Wray, G. A. in Embryology: Constructing the Organism (eds Gilbert, S. F. & Raunio, A. M.) 309–329 (Sinauer, Sunderland, MA, 1997).

  389. 389.

    Davidson, E. H. The Regulatory Genome: Gene Regulatory Networks in Development and Evolution (Academic, Amsterdam, 2006).

  390. 390.

    Wray, G. A. & Raff, R. A. Evolutionary modification of cell lineage in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 132, 458–470 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  391. 391.

    Cameron, R. A., Hough-Evans, B. R., Britten, R. J. & Davidson, E. H. Lineage and fate of each blastomere of the eight-cell sea urchin embryo. Genes Dev. 1, 75–85 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  392. 392.

    Davidson, E. H., Cameron, R. A. & Ransick, A. Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125, 3269–3290 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  393. 393.

    Morris, V. B. & Byrne, M. Oral–aboral identity displayed in the expression of HpHox3 and HpHox11/13 in the adult rudiment of the sea urchin Holopneustes purpurescens. Dev. Genes Evol. 224, 1–11 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  394. 394.

    Wray, G. A. & Raff, R. A. Novel origins of lineage founder cells in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 141, 41–54 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  395. 395.

    McEdward, L., Jaeckle, W. B. & Komatsu, M. in Atlas of Marine Invertebrate Larvae (ed. Young, C. M.) 499–512 (Academic, San Diego, CA, 2002).

  396. 396.

    Byrne, M. & Selvakumaraswamy, P. in Atlas of Marine Invertebrate Larvae (ed. Young, C. M.) 483–498 (Academic, San Diego, 2002).

  397. 397.

    MacBride, E. W. The development of Ophiothrix fragilis. Q. J. Microsc. Sci. 51, 557–606 (1907).

    Google Scholar 

  398. 398.

    Sewell, M. A. & McEuen, F. S. in Atlas of Marine Invertebrate Larvae (ed. Young, C. M.) 513–530 (Academic, San Diego, CA, 2002).

  399. 399.

    Bury, H. The early stages in the development of Antedon rosacea. Phil. Trans. R. Soc. Lond. B 179, 257–301 (1888).

    Google Scholar 

  400. 400.

    Amemiya, S. et al. Development of ciliary bands in larvae of the living isocrinid sea lily Metacrinus rotundus. Acta Zool. 96, 36–43 (2015).

    Article  PubMed  Google Scholar 

  401. 401.

    Heinzeller, T. & Welsch, U. in Brain Evolution and Cognition (eds Roth, G. & Wullimann, M. F.) 41–75 (Wiley, New York, NY, 2001).

  402. 402.

    Mashanov, V., Zueva, O., Rubilar, T., Epherra, L. & García-Arrás, J. E. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 665–688 (Oxford Univ. Press, Oxford, 2016).

  403. 403.

    Ubisch, L. Die Entwicklung von Strongylocentrotus lividus (Echinus microtuberculatus, Arbacia pustulosa). Z. Wiss. Zool. 106, 409–448 (1913).

    Google Scholar 

  404. 404.

    Nakajima, Y., Kaneko, H., Murray, G. & Burke, R. D. Divergent patterns of neural development in larval echinoids and asteroids. Evol. Dev. 6, 95–104 (2004).

    Article  PubMed  Google Scholar 

  405. 405.

    Byrne, M., Nakajima, Y., Chee, F. C. & Burke, R. D. Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol. Dev. 9, 432–445 (2007).

    Article  PubMed  Google Scholar 

  406. 406.

    Katow, H., Elia, L. & Byrne, M. Development of nervous systems to metamorphosis in feeding and non-feeding echinoid larvae, the transition from bilateral to radial symmetry. Dev. Genes Evol. 219, 67–77 (2009).

    Article  PubMed  Google Scholar 

  407. 407.

    Dupont, S., Thorndyke, W., Thorndyke, M. C. & Burke, R. D. Neural development of the brittlestar Amphiura filiformis. Dev. Genes Evol. 219, 159–166 (2009).

    Article  PubMed  Google Scholar 

  408. 408.

    Shoguchi, E., Satoh, N. & Maruyama, Y. K. Pattern of Brachyury gene expression in starfish embryos resembles that of hemichordate embryos but not of sea urchin embryos. Mech. Dev. 82, 185–189 (1999).

    Article  CAS  PubMed  Google Scholar 

  409. 409.

    Croce, J., Lhomond, G. & Gache, C. Expression pattern of Brachyury in the embryo of the sea urchin Paracentrotus lividus. Dev. Genes Evol. 211, 617–619 (2001).

    Article  CAS  PubMed  Google Scholar 

  410. 410.

    Gross, J. M. & McClay, D. R. The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev. Biol. 239, 132–147 (2001).

    Article  CAS  Google Scholar 

  411. 411.

    Rast, J. P., Cameron, R. A., Poustka, A. J. & Davidson, E. H. brachyury target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev. Biol. 246, 191–208 (2002).

    Article  CAS  Google Scholar 

  412. 412.

    Oliveri, P., Walton, K. D., Davidson, E. H. & McClay, D. R. Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133, 4173–4181 (2006).

    Article  CAS  Google Scholar 

  413. 413.

    Angerer, L. M. et al. Sea urchin goosecoid function links fate specification along the animal–vegetal and oral–aboral embryonic axes. Development 128, 4393–4404 (2001).

    CAS  PubMed  Google Scholar 

  414. 414.

    Annunziata, R. et al. Pattern and process during sea urchin gut morphogenesis: the regulatory landscape. Genesis 52, 251–268 (2014).

    Article  Google Scholar 

  415. 415.

    Arnone, M. I. et al. Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: insights into the relationship between clustering and colinearity. Dev. Biol. 300, 63–73 (2006).

    Article  CAS  Google Scholar 

  416. 416.

    Ransick, A., Rast, J. P., Minokawa, T., Calestani, C. & Davidson, E. H. New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev. Biol. 246, 132–147 (2002).

    Article  CAS  Google Scholar 

  417. 417.

    De Robertis, E. M. & Sasai, Y. A common plan for dorsoventral patterning in Bilateria. Nature 380, 37–40 (1996).

    Article  Google Scholar 

  418. 418.

    Hirakow, R. & Kajita, N. Electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: the gastrula. J. Morphol. 207, 37–52 (1991).

    Article  CAS  Google Scholar 

  419. 419.

    Hatschek, B. Studien über Entwicklung des Amphioxus. Arb. Zool. Inst. Univ. Wien 4, 1–88 (1881).

    Google Scholar 

  420. 420.

    Holland, L. Z. Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat. Rev. Neurosci. 10, 736–746 (2009).

    Article  CAS  PubMed  Google Scholar 

  421. 421.

    Wicht, H. & Lacalli, T. C. The nervous system of amphioxus: structure, development, and evolutionary significance. Can. J. Zool. 83, 122–150 (2005).

    Article  Google Scholar 

  422. 422.

    Vallet, P. G., Ody, M. G. & Huggel, H. Étude ultrastructurale du neuropore d’amphioxus adulte (Branchiostoma lanceolatum Pallas). Rev. Suisse Zool. 92, 845–849 (1985).

    Article  Google Scholar 

  423. 423.

    Ruppert, E. E. in Microscopic Anatomy of Invertebrates Vol. 15 (ed. Harrison, F. W.) 349–504 (Wiley, New York, NY, 1997).

  424. 424.

    Lacalli, T. C., Holland, N. D. & West, J. E. Landmarks in the anterior central nervous system of amphioxus larvae. Phil. Trans. R. Soc. Lond. B 344, 165–185 (1994).

    Article  Google Scholar 

  425. 425.

    Lacalli, T. C., Gilmour, T. H. J. & Kelly, S. J. The oral nerve plexus in amphioxus larvae: Function, cell types and phylogenetic significance. Proc. R. Soc. Lond. B 266, 1461–1470 (1999).

    Article  Google Scholar 

  426. 426.

    Ruppert, E. E. Morphology of Hatschek’s nephridium in larval and juvenile stages of Branchiostoma virginiae (Cephalochordata). Isr. J. Zool. 42, S161–S182 (1996).

    Google Scholar 

  427. 427.

    Yasui, K. & Kaji, T. The lancelet and ammocoete mouths. Zool. Sci. 25, 1012–1019 (2008).

    Article  PubMed  Google Scholar 

  428. 428.

    Holland, P. W., Koschorz, B., Holland, L. Z. & Herrmann, B. G. Conservation of Brachyury (T) genes in amphioxus and vertebrates: developmental and evolutionary implications. Development 121, 4283–4291 (1995).

    CAS  PubMed  Google Scholar 

  429. 429.

    Terazawa, K. & Satoh, N. Spatial expression of the amphioxus homologue of Brachyury (T) gene during early embryogenesis of Branchiostoma belcheri. Dev. Growth Differ. 37, 395–401 (1995).

    Article  CAS  Google Scholar 

  430. 430.

    Terazawa, K. & Satoh, N. Formation of the chordamesoderm in the amphioxus embryo: analysis with Brachyury and fork head/HNF-3 genes. Dev. Genes Evol. 207, 1–11 (1997).

    Article  CAS  Google Scholar 

  431. 431.

    Zhang, S. C., Holland, N. D. & Holland, L. Z. 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, 532–535 (1997).

    Article  Google Scholar 

  432. 432.

    Onai, T. et al. Retinoic acid and Wnt/β-catenin have complementary roles in anterior/posterior patterning embryos of the basal chordate amphioxus. Dev. Biol. 332, 223–233 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  433. 433.

    Ferrier, D. E. K., Minguillón, C., Cebrián, C. & Garcia-Fernàndez, J. Amphioxus Evx genes: implications for the evolution of the midbrain–hindbrain boundary and the chordate tailbud. Dev. Biol. 237, 270–281 (2001).

    Article  CAS  Google Scholar 

  434. 434.

    Neidert, A. H., Panopoulou, G. & Langeland, J. A. Amphioxus goosecoid and the evolution of the head organizer and prechordal plate. Evol. Dev. 2, 303–310 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  435. 435.

    Conklin, E. G. The organization and cell-lineage of the ascidian egg. Proc. Acad. Nat. Sci. Phila. 13, 1–119 (1905).

    Google Scholar 

  436. 436.

    Satoh, N. Developmental Biology of Ascidians. (Cambridge Univ. Press, Cambridge, 1994).

    Google Scholar 

  437. 437.

    Lemaire, P., Smith, W. C. & Nishida, H. Ascidians and the plasticity of the chordate developmental program. Curr. Biol. 18, R620–R631 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  438. 438.

    Satoh, N. Cellular morphology and architecture during early morphogenesis of the ascidian egg: an SEM study. Biol. Bull. 155, 608–614 (1978).

    Article  CAS  Google Scholar 

  439. 439.

    Van Beneden, E. & Julin, C. Recherches sur la morphologie des Tuniciers. Arch. Biol. 6, 237–476 (1887).

    Google Scholar 

  440. 440.

    Nielsen, C. Evolution of deuterostomy — and origin of the chordates. Biol. Rev. 92, 316–325 (2017).

    Article  Google Scholar 

  441. 441.

    Veeman, M. T., Newman-Smith, E., El-Nachef, D. & Smith, W. C. The ascidian mouth opening is derived from the anterior neuropore: reassessing the mouth/neural tube relationship in chordate evolution. Dev. Biol. 344, 138–149 (2010).

    Article  CAS  Google Scholar 

  442. 442.

    Manni, L. & Pennati, R. in Structure and Evolution of Invertebrate Nervous Systems (eds Schmidt-Rhaesa, A. et al.) 699–718 (Oxford Univ. Press, Oxford, 2016).

  443. 443.

    Nicol, D. & Meinertzhagen, I. A. Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. I. The early lineages of the neural plate. Dev. Biol. 130, 721–736 (1988).

    Article  CAS  Google Scholar 

  444. 444.

    Nicol, D. & Meinertzhagen, I. A. Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. II. Neural plate morphogenesis and cell lineages during neurulation. Dev. Biol. 130, 737–766 (1988).

    Article  CAS  Google Scholar 

  445. 445.

    Meinertzhagen, I. A. & Okamura, Y. The larval ascidian nervous system: the chordate brain from its small beginnings. Trends Neurosci. 24, 401–410 (2001).

    Article  CAS  Google Scholar 

  446. 446.

    Meinertzhagen, I. A. Eutely, cell lineage, and fate within the ascidian larval nervous system: determinacy or to be determined? Can. J. Zool. 83, 184–195 (2005).

    Article  Google Scholar 

  447. 447.

    Chiba, S., Sasaki, A., Nakayama, A., Takamura, K. & Satoh, N. Development of Ciona intestinalis juveniles (through 2nd ascidian stage). Zool. Sci. 21, 285–298 (2004).

    Article  Google Scholar 

  448. 448.

    Imai, K. S., Hino, K., Yagi, K., Satoh, N. & Satou, Y. Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 131, 4047–4058 (2004).

    Article  CAS  Google Scholar 

  449. 449.

    Tassy, O. et al. The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. Genome Res. 20, 1459–1468 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  450. 450.

    Imai, K. S., Levine, M., Satoh, N. & Satou, Y. Regulatory blueprint for a chordate embryo. Science 312, 1183–1187 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  451. 451.

    Takahashi, H. et al. Brachyury downstream notochord differentiation in the ascidian embryo. Genes Dev. 13, 1519–1523 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  452. 452.

    Corbo, J. C., Erives, A., Di Gregorio, A., Chang, A. & Levine, M. Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. Development 124, 2335–2344 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  453. 453.

    Passamaneck, Y. J. et al. Direct activation of a notochord cis-regulatory module by Brachyury and FoxA in the ascidian Ciona intestinalis. Development 136, 3679–3689 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  454. 454.

    Kumano, G., Yamaguchi, S. & Nishida, H. Overlapping expression of FoxA and Zic confers responsiveness to FGF signaling to specify notochord in ascidian embryos. Dev. Biol. 300, 770–784 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  455. 455.

    Imai, K. S., Stolfi, A., Levine, M. & Satou, Y. Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. Development 136, 285–293 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  456. 456.

    Hinman, V. F., Becker, E. & Degnan, B. M. Neuroectodermal and endodermal expression of the ascidian Cdx gene is separated by metamorphosis. Dev. Genes Evol. 210, 212–216 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  457. 457.

    Ikuta, T., Yoshida, N., Satoh, N. & Saiga, H. Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc. Natl Acad. Sci. USA 101, 15118–15123 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  458. 458.

    Elinson, R. in Embryology: Constructing the Organism (eds Gilbert, S. E. & Raunio, A. M.) 409–436 (Sinauer, Sunderland, MA, 1997).

  459. 459.

    Eagleson, G. W. & Harris, W. A. Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. J. Neurobiol. 21, 427–440 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  460. 460.

    Drysdale, T. A. & Elinson, R. P. Development of the Xenopus laevis hatching gland and its relationship to surface ectoderm patterning. Development 111, 469–478 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  461. 461.

    Gont, L. K., Steinbeisser, H., Blumberg, B. & de Robertis, E. M. Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip. Development 119, 991–1004 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  462. 462.

    Vogt, W. Gestaltungsanalyse am Amphibienkeim mit Örtlicher Vitalfärbung. W. Roux’ Archiv Entwicklungsmechanik 120, 384–706 (1929).

    Article  Google Scholar 

  463. 463.

    Gilbert, S. F. & Barresi, J. F. Developmental Biology 11th edn (Sinauer, Sunderland, MA, 2016).

  464. 464.

    Davidson, A. J. et al. cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature 425, 300–306 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  465. 465.

    Reece-Hoyes, J. S., Keenan, I. D. & Isaacs, H. V. Cloning and expression of the Cdx family from the frog Xenopus tropicalis. Dev. Dyn. 223, 134–140 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  466. 466.

    Smith, J. C., Price, B. M. J., Green, J. B. A., Weigel, D. & Herrmann, B. G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  467. 467.

    Dirksen, M. L. & Jamrich, M. A novel, activin-inducible, blastopore lip-specific gene of Xenopus laevis contains a fork head DNA-binding domain. Genes Dev. 6, 599–608 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  468. 468.

    Schulte-Merker, S., Ho, R. K., Herrmann, B. G. & Nüsslein-Volhard, C. The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116, 1021–1032 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  469. 469.

    Odenthal, J. & Nüsslein-Volhard, C. fork head domain genes in zebrafish. Dev. Genes Evol. 208, 245–258 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  470. 470.

    Talbot, W. S. et al. A homeobox gene essential for zebrafish notochord development. Nature 378, 150–157 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  471. 471.

    Lemaire, L., Roeser, T., Izpisúa-Belmonte, J. C. & Kessel, M. Segregating expression domains of two goosecoid genes during the transition from gastrulation to neurulation in chick embryos. Development 124, 1443–1452 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  472. 472.

    Marom, K., Shapira, E. & Fainsod, A. The chicken caudal genes establish an anterior–posterior gradient by partially overlapping temporal and spatial patterns of expression. Mech. Dev. 64, 41–52 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  473. 473.

    Meyer, B. I. & Gruss, P. Mouse Cdx-1 expression during gastrulation. Development 117, 191–203 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  474. 474.

    Ang, S.-L. & Rossant, J. HNF-3β is essential for node and notochord formation in mouse development. Cell 78, 561–574 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  475. 475.

    Chapman, S. C., Schubert, F. R., Schoenwolf, G. C. & Lumsden, A. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev. Biol. 245, 187–199 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  476. 476.

    Wheeler, S. R., Carrico, M. L., Wilson, B. A. & Skeath, J. B. The Tribolium columnar genes reveal conservation and plasticity in neural precursor patterning along the embryonic dorsal–ventral axis. Dev. Biol. 279, 491–500 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  477. 477.

    Yang, X. et al. Probing the Drosophila retinal determination gene network in Tribolium (II): The Pax6 genes eyeless and twin of eyeless. Dev. Biol. 333, 215–227 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  478. 478.

    Vellutini, B. C., Martín-Durán, J. M. & Hejnol, A. Cleavage modification did not alter blastomere fates during bryozoan evolution. BMC Biol. 15, 33 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  479. 479.

    Hejnol, A. & Martindale, M. Q. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456, 382–386 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  480. 480.

    Keller, R. E., Danilchik, M., Gimlich, R. & Shih, J. The function and mechanism of convergent extension during gastrulation of Xenopus laevis. J. Embryol. Exp. Morphol. 89, 185–209 (1985).

    PubMed  PubMed Central  Google Scholar 

  481. 481.

    Vogt, W. Die Einrollung und Streckung der Urmundlippen bei Triton nach Versuchen mit einer neuen Methode embryonaler Transplantation. Verh. Dtsch. Zool. Ges. 27, 49–51 (1922).

    Google Scholar 

  482. 482.

    Elul, T., Koehl, M. A. & Keller, R. Cellular mechanism underlying neural convergent extension in Xenopus laevis embryos. Dev. Biol. 191, 243–258 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  483. 483.

    Keller, R., Shook, D. & Skoglund, P. The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Phys. Biol. 5, 015007 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  484. 484.

    Steinmetz, P. R. H., Zelada-Gonzáles, F., Burgtorf, C., Wittbrodt, J. & Arendt, D. Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation. Proc. Natl Acad. Sci. USA 104, 2727–2732 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  485. 485.

    Akiyama-Oda, Y. & Oda, H. Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 133, 2347–2357 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  486. 486.

    Benton, M. A. et al. Toll genes have an ancestral role in axis elongation. Curr. Biol. 26, 1609–1615 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  487. 487.

    Irvine, K. D. & Wieschaus, E. Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120, 827–841 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  488. 488.

    Sarrazin, A. F., Peel, A. D. & Averof, M. A segmentation clock with two-segment periodicity in insects. Science 336, 338–341 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  489. 489.

    Lowe, C. J. et al. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113, 853–865 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  490. 490.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  491. 491.

    Christiaen, L. et al. Evolutionary modification of mouth position in deuterostomes. Semin. Cell Dev. Biol. 18, 502–511 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  492. 492.

    Cannon, J. T. et al. Xenacoelomorpha is the sister group to Nephrozoa. Nature 530, 89–93 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  493. 493.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  494. 494.

    Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D. & Martindale, M. Q. Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev. Neurobiol. 69, 235–254 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  495. 495.

    Balfour, F. M. A Treatise on Comparative Embryology Vol. 2 (Macmillan, London, 1881).

  496. 496.

    Martín-Durán, J. M. et al. Convergent evolution of bilaterian nerve cords. Nature 553, 45–50 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  497. 497.

    Arendt, D. Animal evolution: convergent nerve cords? Curr. Biol. 28, R225–R227 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  498. 498.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  499. 499.

    Kaul-Strehlow, S., Urata, M., Praher, D. & Wanninger, A. Neuronal patterning of the tubular collar cord is highly conserved among enteropneusts but dissimilar to the chordate neural tube. Sci. Rep. 7, 7003 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  500. 500.

    Lowe, C. J. et al. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 4, e291 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  501. 501.

    Henry, J. Q., Hejnol, A., Perry, K. J. & Martindale, M. Q. Homology of ciliary bands in Spiralian Trochophores. Integr. Comp. Biol. 47, 865–871 (2007).

    Article  PubMed  Google Scholar 

  502. 502.

    Nielsen, C. Trochophora larvae: cell-lineages, ciliary bands, and body regions. 1. Annelida and Mollusca. J. Exp. Zool. 302B, 35–68 (2004).

    Article  Google Scholar 

  503. 503.

    Riisgård, H. U., Nielsen, C. & Larsen, P. S. Downstream collecting in ciliary suspension feeders: the catch-up principle. Mar. Ecol. Prog. Ser. 207, 33–51 (2000).

    Article  Google Scholar 

  504. 504.

    Nielsen, C. Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea? BMC Evol. Biol. 13, 171 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  505. 505.

    Nielsen, C. How to make a protostome. Invertebr. Syst. 26, 25–40 (2012).

    Article  Google Scholar 

  506. 506.

    Anderson, D. T. Presidential address. The comparative early embryology of the Oligochaeta, Hirudinea and Onychophora. Proc. Linn. Soc. NSW 91, 10–43 (1966).

    Google Scholar 

  507. 507.

    Meyer, N. P., Boyle, M. J., Martindale, M. Q. & Seaver, E. C. A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta. EvoDevo 1, 8 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  508. 508.

    Lartillot, N., Lespinet, O., Vervoort, M. & Adoutte, A. Expression pattern of Brachyury in the mollusc Patella vulgata suggests a conserved role in the establishment of the AP axis in Bilateria. Development 129, 1411–1421 (2002).

    CAS  PubMed  Google Scholar 

  509. 509.

    Lartillot, N., Le Gouar, M. & Adoutte, A. Expression patterns of fork head and goosecoid homologues in the mollusc Patella vulgata supports the ancestry of the anterior mesendoderm across Bilateria. Dev. Genes Evol. 212, 551–561 (2002).

    Article  PubMed  Google Scholar 

  510. 510.

    Le Gouar, M., Lartillot, N., Adoutte, A. & Vervoort, M. The expression of a caudal homologue in a mollusc, Patella vulgata. Gene Expr. Patterns 3, 35–37 (2003).

    Article  PubMed  Google Scholar 

  511. 511.

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

    Article  CAS  PubMed  Google Scholar 

  512. 512.

    de Rosa, R., Prud’homme, B. & Balavoine, G. caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol. Dev. 7, 574–587 (2005).

    Article  PubMed  Google Scholar 

  513. 513.

    Boyle, M. J., Yamaguchi, E. & Seaver, E. C. Molecular conservation of metazoan gut formation: evidence from expression of endomesoderm genes in Capitella teleta (Annelida). EvoDevo 5, 39 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  514. 514.

    Boyle, M. J. & Seaver, E. C. Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I. Evol. Dev. 10, 89–105 (2008).

    Article  CAS  PubMed  Google Scholar 

  515. 515.

    Fröbius, A. C. & Seaver, E. C. ParaHox gene expression in the polychaete annelid Capitella sp. I. Dev. Genes Evol. 216, 81–88 (2006).

    Article  CAS  PubMed  Google Scholar 

  516. 516.

    Seaver, E. C., Yamaguchi, E., Richards, G. S. & Meyer, N. P. Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation. EvoDevo 3, 8 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  517. 517.

    Davidson, A. J. & Zon, L. I. The caudal-related homeobox genes cdx1a and cdx4 act redundantly to regulate hox gene expression and the formation of putative hematopoietic stem cells during zebrafish embryogenesis. Dev. Biol. 292, 506–518 (2006).

    Article  CAS  PubMed  Google Scholar 

  518. 518.

    Joly, J. S., Joly, C., Schulte-Merker, S., Boulekbache, H. & Condamine, H. The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos. Development 119, 1261–1275 (1993).

    CAS  PubMed  Google Scholar 

  519. 519.

    Schulte-Merker, S. et al. Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 120, 843–852 (1994).

    CAS  PubMed  Google Scholar 

  520. 520.

    Thisse, C., Thisse, B., Halpern, M. E. & Postlethwait, J. H. Goosecoid expression in neurectoderm and mesendoderm is disrupted in zebrafish cyclops gastrulas. Dev. Biol. 164, 420–429 (1994).

    Article  CAS  PubMed  Google Scholar 

  521. 521.

    Mudumana, S. P., Hentschel, D., Liu, Y., Vasilyev, A. & Drummond, I. A. odd skipped related1 reveals a novel role for endoderm in regulating kidney versus vascular cell fate. Development 135, 3355–3367 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  522. 522.

    Fischer, A. H. L., Henrich, T. & Arendt, D. The normal development of Platynereis dumerilii (Nereididae, Annelida). Front. Zool. 7, 31 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  523. 523.

    Shimeld, S. M. et al. Clustered Fox genes in lophotrochozoans and the evolution of the bilaterian Fox gene cluster. Dev. Biol. 340, 234–248 (2008).

    Article  CAS  Google Scholar 

  524. 524.

    Ackermann, C., Dorresteijn, A. & Fischer, A. Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). J. Morphol. 266, 258–280 (2005).

    Article  PubMed  Google Scholar 

  525. 525.

    Starunov, V. V. et al. A metameric origin for the annelid pygidium? BMC Evol. Biol. 15, 25 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  526. 526.

    Salvini-Plawen, L. v. Zur Morphologie und Phylogenie der Mollusken: Die Beziehungen der Caudofoveata und der Solenogastres als Aculifera, als Mollusca und als Spiralia. Z. Wiss. Zool. 184, 205–394 (1972).

    Google Scholar 

  527. 527.

    Russell-Hunter, W. D. A Life of Invertebrates (Macmillan, London, 1979).

  528. 528.

    Henry, J. J. & Martindale, M. Q. Conservation of the spiralian developmental program: cell lineage of the nemertean. Cerebratulus lacteus. Dev. Biol. 201, 253–269 (1998).

    Article  CAS  PubMed  Google Scholar 

  529. 529.

    Hiebert, L. S., Gavelis, G., von Dassow, G. & Maslakova, S. A. Five invaginations and shedding of the larval epidermis during development of the hoplonemertean Pantinonemertes californiensis (Nemertea: Hoplonemertea). J. Nat. Hist. 44, 2331–2347 (2010).

    Article  Google Scholar 

  530. 530.

    Todaro, M. A., Dal Zotto, M. & Leasi, F. An integrated morphological and molecular approach to the description and systematisation of a novel genus and species of Macrodasyida (Gastrotricha). PLoS ONE 10, e0130278 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  531. 531.

    White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1–340 (1986).

    Article  CAS  Google Scholar 

  532. 532.

    Rothe, B. H. & Schmidt-Rhaesa, A. Structure of the nervous system in Tubiluchus troglodytes (Priapulida). Invertebr. Biol. 129, 39–58 (2010).

    Article  Google Scholar 

  533. 533.

    Neuhaus, B. & Higgins, R. P. Ultrastructure, biology, and phylogenetic relationships of kinorhyncha. Integr. Comp. Biol. 42, 619–632 (2002).

    Article  Google Scholar 

  534. 534.

    Benito-Gutiérrez, E. & Arendt, D. CNS evolution: new insight from the mud. Curr. Biol. 19, R640–R642 (2009).

    Article  CAS  Google Scholar 

  535. 535.

    Gross, V. & Mayer, G. Neural development in the tardigrade Hypsibius dujardini based on anti-acetylated α-tubulin immunolabeling. EvoDevo 6, 12 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  536. 536.

    Cuénot, L. in Traité de Zoologie Vol. 6 (ed. Grassé, P.-P.) 39–59 (Masson, Paris, 1949).

  537. 537.

    Harzsch, S. The tritocerebrum of Euarthropoda: a “non-drosophilocentric” perspective. Evol. Dev. 6, 303–309 (2004).

    Article  Google Scholar 

  538. 538.

    Nielsen, C. Origin of the trochophora larva. R. Soc. Open Sci. 5, 180042 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank R. Schnabel (TU Braunschweig, Germany) for new information about Caenorhabditis embryology.

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C.N. conceived the paper and wrote the sections on morphology and embryology in the Supplementary Information. T.B. wrote the sections gene expression and performed ancestral state reconstructions. D.A. elaborated and illustrated options for mouth and anus evolution. All three authors wrote the main paper and discussed the whole manuscript.

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Correspondence to Claus Nielsen or Thibaut Brunet or Detlev Arendt.

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Nielsen, C., Brunet, T. & Arendt, D. Evolution of the bilaterian mouth and anus. Nat Ecol Evol 2, 1358–1376 (2018). https://doi.org/10.1038/s41559-018-0641-0

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