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Evo-Devo Lessons Learned from Hemichordates

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Abstract

Hemichordates are exclusively marine animals related to vertebrate chordates, like ourselves, and to non-vertebrate chordates, such as lancelets and ascidians; therefore, they are useful to understand our ancestral state. Hemichordates are also associated with the radially symmetrical echinoderms, organisms such as sea stars and sea urchins, because of similarities in embryogenesis and larval form. Hemichordate larvae are believed to resemble the hypothetical dipleurula larva, which is thought to have been a crucial stage in metazoan evolution. Hemichordates include about 130 described species and are divided into two classes: the free-living Enteropneusta and the sessile Pterobranchia. Enteropneusts are commonly called giboshi mushi in Japanese and acorn worms in English, since the enteropneust proboscis resembles a traditional ornament on the tops of posts or balustrades of bridges, shrines or temples, and acorns. Pterobranchs are small animals that form colonies of clones connected via stalks. This chapter reviews recent studies on hemichordates, focusing on phylogeny, paleontology, molecular developmental biology, and genomics, to review what we have learned about animal evolution and development from these obscure organisms.

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References

  • Agassiz AE (1872) Tornaria, the young stage of Balanoglossus. Amer Natural 6:636–637

    Google Scholar 

  • Agassiz AE (1873) The history of Balanoglossus and Tornaria. Mem Amer Acad Arts Sci 9:421–436

    Google Scholar 

  • Allman GJ (1869) Rhabdopleura normani, Allman, nov. gen. et sp. In: Norman AM (ed) Shetland final dredging report. Part II. Crustacea, Tunicata, Polyzoa, Echinodermata, Actinozoa, Hydrozoa and Porifera. Reports of the British Association of the Advancement of Science 1868:311–312

    Google Scholar 

  • Arimoto A, Tagawa K (2018) Regeneration in the enteropneust hemichordate Ptychodera flava and its evolutionary implication. Develop Growth Differ 60:400–408

    Article  Google Scholar 

  • Bateson W (1885) The later stages in the development of Balanoglossus kowalevskii, with a suggestion as to the affinities of the Enteropneusta. Q J Microsc Sci 25(Suppl):81–122

    Google Scholar 

  • Cannon JT, Rychel AL, Eccleston H, Halanych KM, Swalla BJ (2009) Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Mol Phylogenet Evol 52:17–24

    Article  CAS  Google Scholar 

  • Cannon JT, Kocot KM, Waits DS, Weese DA, Swalla BJ, Santos SR, Halanych KM (2014) Phylogenomic resolution of the hemichordate and echinoderm clade. Curr Biol 24:2827–2832

    Article  CAS  Google Scholar 

  • Caron JB, Conway Morris S, Cameron CB (2013) Tubicolous enteropneusts from the Cambrian period. Nature 495:503–506

    Article  CAS  Google Scholar 

  • Darras S, Gerhart J, Terasaki M, Kirschner M, Lowe CJ (2011) β-catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development 138:959–970

    Article  CAS  Google Scholar 

  • Darras S, Fritzenwanker JH, Uhlinger KR, Farrelly E, Pani AM, Hurley IA, Norris RP, Osovitz M, Terasaki M, Wu M, Aronowic ZJ, Kirshner M, Gerhart JC, Lowe CJ (2018) Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development. PLoS Biol 16(1):e2003698. https://doi.org/10.1371/journal.pbio.2003698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eschscholtz JF (1825) Bericht über die zoologische Ausbeute während der Reise von Kronstadt bis St. Peter und Paul. Oken’s Isis for 1825, (6): 733–747.

    Google Scholar 

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

    Google Scholar 

  • Gegenbaur C (1870) Grundzüge der vergleichenden Anatomie. Zweite. umgearbeitete Auflage. Wilhelm Engelmann, Leipzig, 892 p

    Google Scholar 

  • Gonzalez P, Uhlinger KR, Lowe CJ (2017) The adult body plan of indirect developing hemichordates develops by adding a Hox-patterned trunk to an anterior larval territory. Curr Biol 27:87–95

    Article  CAS  Google Scholar 

  • Grobben K (1908) Die systematische einteilung des tierreiches. Verh Zool Bot Ges Wien 58:491–511

    Google Scholar 

  • Harmer SF (1887) Appendix to Report on Cephalodiscus dodecalophus. In C. Wyville Thompson and J. Murray (eds.), Rep. scient. results voy. H.M.S. Challenger during the years 1873-76. Zool. 20(52):39–47

    Google Scholar 

  • Holland ND, Clague DA, Gordon DP, Gebruk A, Pawson DL, Vecchione M (2005) Lophenteropneust’ hypothesis refuted by collection and photos of new deep-sea hemichordates. Nature 434:374–376

    Article  CAS  Google Scholar 

  • Holland ND, Holland LZ, Holland PW (2015) Scenarios for the making of vertebrates. Nature 520:450–455

    Article  CAS  Google Scholar 

  • Kowalevsky AO (1866) Anatomie des Balanoglossus delle Chiaje. Mem Acad Imp Sci St Petersbourg 7:1–18

    Google Scholar 

  • Lankester ER (1877) Notes on the embryology and classification of the animal kingdom: comprising a revision of speculations relative to the origin and significance of the germ-layers. Q J Microsc Sci 17:399–454

    Google Scholar 

  • Lowe CJ (2008) Molecular genetic insights into deuterostome evolution from the direct-developing hemichordate Saccoglossus kowalevskii. Philos Trans R Soc B 363:1569–1578

    Article  Google Scholar 

  • Lowe CJ, Terasaki M, Wu M, Freeman RM Jr, Runft L, Kwan K, Haigo S, Aronowics J, Lander E, Gruber C, Smith M, Kirshner M, Gerhart J (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4(9):e291. https://doi.org/10.1371/journal.pbio.0040291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowe CJ, Clarke DN, Medeiros DM, Rokhsar DS, Gerhart J (2015) The deuterostome context of chordate origins. Nature 520:456–465

    Article  CAS  Google Scholar 

  • Maletz J (2014) Hemichordata (Pterobranchia, Enteropneusta) and the fossil record. Palaeogeogr Palaeoclimatol Palaeoecol 398:16–27

    Article  Google Scholar 

  • McIntosh WC (1882) Preliminary notice of Cephalodiscus, a new type allied to Prof. Allman’s Rhabdopleura, dredged in H M S “Challenger”. Ann Mag Nat Hist, (5)10:337–348

    Google Scholar 

  • Metchnikoff E (1869) Ueber Tornaria. Nachr K Ges. Wiss Univ Göttingen 15:287–292

    Google Scholar 

  • Metchnikoff E (1870) Untersuchungen über die Metamorphose einiger Seethiere. I. Ueber Tornaria. Z Wiss Zool 20:131–144

    Google Scholar 

  • Mitchell CE, Melchin MJ, Cameron CB, Maletz J (2013) Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia 46:34–56

    Article  Google Scholar 

  • Müller JP (1850) Über die Larven und die Metamorphose der Echinodermen. Abh Akad Wiss Berlin, 1848, Physiology, 75–110

    Google Scholar 

  • Raff RA (2008) Origins of the other metazoan body plans: the evolution of larval forms. Philos Trans R Soc B 363:1473–1479

    Article  Google Scholar 

  • Sars M (1868) Remarks on the distribution of animal life in the depths of the sea (in Norwegian). Forh. VidenskSelsk. Krist., 1868, pp. 246–75

    Google Scholar 

  • Sars GO (1872) On some remarkable forms of animal life from the great deep off the Norwegian coast. 1. Christiana Univ Program for the 1st half-year, 1869, Pt 1.

    Google Scholar 

  • Sars GO (1874) On Rhabdpleura mirabilis (M. Sars). Quart J Micr Sci 14:23–44

    Google Scholar 

  • Satoh N (2016) Chordate origins and evolution. Academic, Boston

    Google Scholar 

  • Simakov O, Kawashima T, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, Bredeson J, Shoguchi E, Gyoja F, Yue JX, Chen YC, Freeman RM, Sasaki A, Tomoe Hikosaka-Katayama T, Sato A, Fujie M, Baughman KW, Levine J, Gonzalez P, Cameron C, Fritzenwanker JH, Pani AM, Goto H, Kanda M, Arakaki N, Yamasaki S, Qu J, Cree A, Ding Y, Dinh HH, Dugan S, Holder M, Jhangiani SN, Kovar CL, Lee SL, Lewis LR, Morton D, Nazareth LV, Okwuonu G, Santibanez J, Chen R, Richards S, Muzny DM, Gillis A, Peshkin L, Wu M, Tom Humphreys T, Su YH, Putnam NH, Schmutz J, Fujiyama A, Yu JK, Tagawa K, Worley KC, Gibbs RA, Kirschner MW, Lowe CJ, Satoh N, Rokhsar DS, Gerhart J (2015) Hemichordate genomes and deuterostome origins. Nature 527:459–465

    Article  CAS  Google Scholar 

  • Spengel JW (1893) Die Enteropneusten des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel, Monographie, Engelmann, Lipzig, vol 18, pp 1–758

    Google Scholar 

  • Tagawa K (2016) Hemichordate models. Curr Opin Genet Dev 39:71–78

    Article  CAS  Google Scholar 

  • Tagawa K, Satoh N, Humphreys T (2001) Molecular studies of hemichordate development: a key to understanding the evolution of bilateral animals and chordates. Evol Dev 3:443–454

    Article  CAS  Google Scholar 

  • Willey A (1899) Remarks on some recent works on the protochordata, with a condensed account of some fresh observations on the enteropneusta. Q J Microsc Sci 42:223–244

    Google Scholar 

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Acknowledgments

I would like to thank the editor, Dr. Ehab Abouheif, for inviting me to write this chapter. I also would like to express my gratitude to the outstanding investigators in the hemichordate research field, who have always stimulated me in both positive and negative ways. I wish to express my sincere thanks to Springer Nature and the Royal Society for allowing me to reproduce their data as Figs. 1, 4, 5, 7, 8, 9, and 6, respectively, in this chapter. Special thanks to Professor Nori Satoh and Dr. Steven D. Aird, who checked my poor Japanese English carefully and gave me many useful comments and suggestions. Finally, I would like to acknowledge all members of my lab, past and present, who have always been supportive. I apologize that I could not fully quote sources due to limitations imposed upon the number of citations.

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Correspondence to Kuni Tagawa .

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Tagawa, K. (2019). Evo-Devo Lessons Learned from Hemichordates. In: Nuno de la Rosa, L., Müller, G. (eds) Evolutionary Developmental Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-33038-9_183-1

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  • DOI: https://doi.org/10.1007/978-3-319-33038-9_183-1

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