Skip to main content

Germ Layer Evolution: Using Novel Approaches to Address a Classic Evolutionary Embryological Problem

  • Chapter
  • First Online:
Old Questions and Young Approaches to Animal Evolution

Part of the book series: Fascinating Life Sciences ((FLS))

  • 1088 Accesses

Abstract

The genesis of gastrulation, the embryological process that results in the segregation of primary germ layers, was arguably a key evolutionary innovation that enabled metazoan diversification. The developmental mechanisms that induced germ layer specification during gastrulation are not fully understood, but this process has fascinated embryologists for centuries. The early attempts by descriptive embryologists to understand germ layer specification and to put it into an evolutionary framework resulted in the inception of the germ layer theory. Over the years, the germ layer theory was modified to accommodate new knowledge generated through embryological studies on a variety of different animals. However, with new empirical data, certain limitations of the germ layer theory were identified, and based on these limitations, the validity of the theory was put into question. Despite its limitations, the ideas put forward by the early embryologists who came up with the germ layer theory are still being investigated using a variety of animal models and novel experimental approaches. This chapter attempts to provide a historical overview of the idea of germ layer evolution and to discuss how novel experimental approaches can shed light onto these old ideas and build on them to improve our understanding of germ layer evolution in particular and animal evolution in general.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 119.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Angerer LM, Angerer RC (2003) Patterning the sea urchin embryo: gene regulatory networks, signaling pathways, and cellular interactions. Curr Top Dev Biol 53:159–198

    Article  CAS  Google Scholar 

  • Balfour FM (1880–1881) A treatise on comparative embryology. Macmillan, London

    Google Scholar 

  • Barnes ME (2014) Karl Ernst von Baer’s laws of embryology. Embryo project encyclopedia (2014-04-15). ISSN: 1940-5030. http://embryo.asu.edu/handle/10776/7821

  • Baxter AL (1977) E. B. Wilson’s “destruction” of the germ-layer theory. Isis 68:243

    Article  Google Scholar 

  • Blochmann F (1882) Uber die Entwicklung der Neritina fluratilis Mull. Z Wiss Zool 36:125–174

    Google Scholar 

  • Bodmer R (1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118(3):719–729

    CAS  PubMed  Google Scholar 

  • Boyden A (1947) Homology and analogy: a critical review of the meanings and implications of these concepts in biology. Am Midl Nat 37:648–649

    Article  Google Scholar 

  • Brand T (2003) Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol 258(1):1–19

    Article  CAS  Google Scholar 

  • Brauckmann S, Gilbert SF (2004) Sucking in the gut: a brief history of early studies on gastrulation. In: Stern CD (ed) Gastrulation. From cells to embryo. Cold Spring harbor Lab Press, New York

    Google Scholar 

  • Briggs JA, Weinreb C, Wagner DE, Megason S, Peshkin L, Kirschner MW, Klein AM (2018) The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution. Science 360(6392):eaar5780. https://doi.org/10.1126/science.aar5780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cameron RA, Davidson EH (1991) Cell type specification during sea urchin development. Trends Genet 7:212–218

    Article  CAS  Google Scholar 

  • Cusanovich DA, Reddington JP, Garfield DA, Daza RM, Aghamirzaie D, Marco-Ferreres R, Pilner HA, Christiansen L, Qui X, Steemers FJ, Trapnell C, Shendure J, Furlong EEM (2018) The cis-regulatory dynamics of embryonic development at single-cell resolution. Nature 555(7679):538–542

    Article  CAS  Google Scholar 

  • Davidson EH (2001) Genomic regulatory systems. Academic Press, London

    Google Scholar 

  • Davidson EH (2006) The regulatory genome. Academic Press, Burlington, MA

    Google Scholar 

  • Davidson EH, Erwin DH (2006) Gene regulatory networks and the evolution of animal body plans. Science 311(5762):796–800

    Article  CAS  Google Scholar 

  • Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh C et al (2002) A genomic regulatory network for development. Science 295:1669

    Article  CAS  Google Scholar 

  • de Beer GR (1958) Embryos and ancestors, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Article  CAS  Google Scholar 

  • Farrell JA, Wang Y, Riesenfeld SJ, Shekhar K, Regev A, Schier AF (2018) Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis. Science 360(6392):eaar3131. https://doi.org/10.1126/science.aar3131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haeckel E (1866) Generelle Morphologie der Organismen, vol 1 & 2. Georg Reimer, Berlin

    Book  Google Scholar 

  • Haeckel E (1874) Die Gastrrea-Theorie. die phylogenetische Klassification des Tierreiches und Homologie der Kimblätter. Jena Z. Naturwiss 8:1–55

    Google Scholar 

  • Haeckel E (1875) Die Gastraea und die Eifurchung der Thiere. Jena Z. Natllrwiss 9:402–508

    Google Scholar 

  • Hall BK (1995) Homology and embryonic development. Evol Biol 28:1–37

    CAS  Google Scholar 

  • Hall BK (1996) Baupläne. Phylotypic stages and constraint: why there are so few types of animals. Evol Biol 29:215–261

    Google Scholar 

  • Hall BK (1998) Germ layers and the germ layer theory revisited: primary and secondary germ layers, neural crest as a fourth germ layer, homology, and demise of the germ layer theory. In: Hecht MK, Macintyre RJ, Clegg MT (eds) Evolutionary biology, vol 30. Springer Science + Business Media, New York

    Google Scholar 

  • Hall BK (2018) Germ layers, the neural crest and emergent organization in development and evolution. Genesis 56(6–7):e23103. https://doi.org/10.1002/dvg.23103

    Article  PubMed  Google Scholar 

  • Hayward DC, Miller DJ, Ball EE (2004) Snail expression during embryonic development of the coral Acropora: blurring the diploblast/triploblast divide? Dev Genes Evol 214:257–260

    Article  Google Scholar 

  • Hayward DC, Grasso LC, Saint R, Miller DJ, Ball EE (2015) 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

    Article  CAS  Google Scholar 

  • Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Muller WE, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci 276:4261–4270

    Article  Google Scholar 

  • Hinman VF, Davidson EH (2007) Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci U S A 104(49):19404–19409

    Article  CAS  Google Scholar 

  • Housden BE, Perrimon N (2014) Spatial and temporal organization of signaling pathways. Trends Biochem Sci 39(10):457–464. https://doi.org/10.1016/j.tibs.2014.07.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huxley TH (1849) On the anatomy and the affinities of the family of the Medusae. Philos Trans R Soc Lond 139:413–434

    Article  Google Scholar 

  • Huxley TH (1853) Fragments relating to philosophical zoology. In: Von Baer KE (ed) Scientific memoirs. Taylor and Francis, London, pp 176–238. http://www.biodiversitylibrary.org/item/70597#page/186/mode/1up

    Google Scholar 

  • Ip YT, Maggert K, Levine M (1994) Uncoupling gastrulation and mesoderm differentiation in the Drosophila embryo. EMBO J 13(24):5826–5834

    Article  CAS  Google Scholar 

  • King N (2004) The unicellular ancestry of animal development. Dev Cell 7:313–325

    Article  CAS  Google Scholar 

  • Kleinenberg N (1886) Die Entstehung des Annelids aus der Larve von Lopaderhynchus. Zeitschriftifur Wissenschaftliche Zoologie 44:3

    Google Scholar 

  • Knoll AH (2011) The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39:217–239

    Article  CAS  Google Scholar 

  • Kowalevsky AO (1866) Entwickelungsgeschichte der einfachen Ascidien. Mem Acad Sei St Petersbol/rg 7(15):19

    Google Scholar 

  • Kowalevsky AO (1867) Entwickelungsgeschichte des Amphioxl/s lanceolatl/s. Mem Acad Sei St Petersbol/rg 11(4):17

    Google Scholar 

  • Kowalevsky AO (1871) Weitere Studien über die Entwicklung der einfachen Ascidien. Arch Mikrosk Anat 7:101–130

    Article  Google Scholar 

  • Kowalevsky AO (1877) Weitere Studien über die Entwickelungsgeschichte des Amphioxus lanceolatus. Arch Mikrosk Anat 13:181–204

    Article  Google Scholar 

  • Kumburegama S, Wijesena N, Xu R, Wikramanayake AH (2011) Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/beta-catenin-dependent endoderm cell-fate specification in Nematostella vectensis (Anthozoa, Cnidaria): implications for the evolution of gastrulation. Evo Devo 2:2

    CAS  Google Scholar 

  • Lang A (1884) Die Polycladen. Fauna und Flora der Golfes von Neapel, Monographie 11:331–334

    Google Scholar 

  • Levine M, Davidson EH (2005) Gene regulatory networks for development. Proc Natl Acad Sci U S A 102(14):4936–4942

    Article  CAS  Google Scholar 

  • Lillie F (1944) The woods hole marine biological laboratory. University of Chicago Press, Chicago

    Google Scholar 

  • Lints TJ, Parsons LM, Hartley L, Lyons I, Harvey RP (1993) Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119(2):419–431

    CAS  PubMed  Google Scholar 

  • Liu Z, Woo S, Weiner OD (2018) Nodal signaling has dual roles in fate specification and directed migration during germ layer segregation. Development 145(17):dev163535. https://doi.org/10.1242/dev.163535

    Article  CAS  PubMed  Google Scholar 

  • Logan CY, Miller JR, Ferkowicz MJ, McClay DR (1999) Nuclear beta-catenin s required to specify vegetal cell fates in the sea urchin embryo. Development 126:345–357

    CAS  PubMed  Google Scholar 

  • Loose M, Patient R (2004) A genetic regulatory network for Xenopus mesendoderm formation. Dev Biol 271(2):467–478

    Article  CAS  Google Scholar 

  • Maduro MF (2006) Endomesoderm specification in Caenorhabditis elegans and other nematodes. BioEssays 28(10):1010–1022

    Article  CAS  Google Scholar 

  • Martindale MQ (2005) The evolution of metazoan axial properties. Nat Rev Genet 6:917–927

    Article  CAS  Google Scholar 

  • Martindale MQ, Hejnol A (2009) A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Dev Cell 17:1–13

    Article  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: mesodermal gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131(10):2463

    Article  CAS  Google Scholar 

  • Momose T, Houliston E (2007) Two oppositely localized frizzled determinants in a cnidarian embryo. PLoS Biol 5:889–899

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Oppenheimer J (1967) The non-specificity of the germ layers in essays in the history of embryology. MIT Press, Cambridge

    Google Scholar 

  • Pander CH (1817) Dissertatio Inauguralis. Sistens Historiam Metamorphoseos quam Ovum InC/lbatum Prioribus quinque Dieblls Subit. Würzburg

    Google Scholar 

  • Pang K, Martindale MQ (2008) Ctenophores. Curr Biol 18(24):R1119–R1120

    Article  CAS  Google Scholar 

  • Pang K, Ryan JF, Comparative Sequencing Program NISC, Mullikin JC, Baxevanis AD, Martindale MQ (2010) Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. EvoDevo 1:10

    Article  CAS  Google Scholar 

  • Perrimon N, Pitsouli C, Shilo BZ (2012) Signaling mechanisms controlling cell fate and embryonic patterning. Cold Spring Harb Perspect Biol 4(8):a005975

    Article  Google Scholar 

  • Perry KJ, Lyons DC, Truchado-Garcia M, Fischer AH, Helfrich LW, Johansson KB et al (2015) Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusk Crepidula. Dev Dyn 244:1215–1248

    Article  CAS  Google Scholar 

  • Peter IS, Davidson EH (2009) Modularity and design principles in the sea urchin embryo gene regulatory network. FEBS Lett 583:3948–3958

    Article  CAS  Google Scholar 

  • Peter IS, Davidson EH (2011) Evolution of gene regulatory networks controlling body plan development. Cell 144(6):970–985

    Article  CAS  Google Scholar 

  • Price AL, Patel NH (2004) The evolution of gastrulation: cellular and molecular aspects. In: Stern CD (ed) Gastrulation. From cells to embryo. Cold Spring harbor Lab Press, New York

    Google Scholar 

  • Rathke MH (1825) Flusskrebs. Isis von Oken, iahrg 2:1093–1100

    Google Scholar 

  • Rathke MH (1829) Untersuchungen über die Bildung und Entwickelung des Flusskrebes Leipzig

    Google Scholar 

  • Remak R (1850–1855) Untersuchungen über die Entwickelung der Wirbelthiere. Georg Reimer, Berlin

    Google Scholar 

  • Rodway A, Patient R (2001) Mesendoderm: an ancient germ layer? Cell 105:169–172

    Article  Google Scholar 

  • Röttinger E, Dahlin P, Martindale MQ (2012) A framework for the establishment of a cnidarian gene regulatory network for “endomesoderm” specification: the inputs of ß-catenin/TCF signaling. PLoS Genet 8(12):e1003164

    Article  Google Scholar 

  • Russell ES (1916) Form and function: a contribution to the history of animal morphology. John Murray, London

    Google Scholar 

  • Sebe-Pedros A, Chomsky E, Pang K, Lara-Astiaso D, Gaiti F, Mukamel Z, Amit I, Hejnol A, Degnan BM, Tanay A (2018a) Early metazoan cell type diversity and the evolution of multicellular gene regulation. Nat Ecol Evol 2:1176–1188

    Article  Google Scholar 

  • Sebe-Pedros A, Saudemont B, Chomsky E, Plessier F, Mailhe MP, Renno J, Loe-Mie Y, Lifshitz A, Mukamel Z, Schmutz S, Steinmetz P, Spitz F, Tanay A, Marlow H (2018b) Cnidarian cell type diversity and regulation revealed by whole-organism single-cellRNA-seq. Cell 173:1520–1534

    Article  CAS  Google Scholar 

  • Sethi AJ, Wikramanayake RM, Angerer RC, Range RC, Angerer LM (2012) Sequential signaling crosstalk regulates endomesoderm segregation in sea urchin embryos. Science 335(6068):590–593

    Article  CAS  Google Scholar 

  • Srivastava D, Cserjesi P, Olsen EN (1995) A subclass of bHLH proteins required for cardiac morphogenesis. Science 270:1995–1999

    Article  CAS  Google Scholar 

  • von Baer KE (1828) Über Entwicklungsgeschichte der Thiere. Beobachtung und Reflexion, Gebrüder, Bornträger, Königsberg

    Google Scholar 

  • Wagner DE, Weinreb C, Collins ZM, Briggs JA, Megason SG, Klein AM (2018) Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo. Science 360(6392):981–987. https://doi.org/10.1126/science.aar4362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijesena NM, Simmons DK, Martindale MQ (2017) Antagonistic BMP-cWNT signaling in the cnidarian Nematostella vectensis reveals insight into the evolution of mesoderm. PNAS 114(28):E5608–E5615

    Article  CAS  Google Scholar 

  • Wikramanayake AH, Huang L, Klein WH (1998) β-catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo. Proc Natl Acad Sci U S A 95:9343–9348

    Article  CAS  Google Scholar 

  • Wilmer P (1990) Invertebrate relationships. In: Patterns in animal evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Wilson EB (1892) The cell lineage of Nereis: a contribution to the cytogeny of the annelid body. J Morphol 6:365

    Article  Google Scholar 

  • Wilson EB (1894) The embryological criterion of homology. Bio Lects Woods Hole 3:101

    Google Scholar 

  • Yasuoka Y, Shinzato C, Satoh N (2016) The mesoderm-forming gene Brachyury regulates ectoderm-endoderm demarcation in the coral Acropora digitifera. Curr Biol 26:2885–2892

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I would like to thank the editors, José María Martín-Durán and Bruno C. Vellutini for the invitation to write this chapter and for the comments given by them and the reviewer, which helped to improve the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Naveen Wijesena .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Wijesena, N. (2019). Germ Layer Evolution: Using Novel Approaches to Address a Classic Evolutionary Embryological Problem. In: Martín-Durán, J., Vellutini, B. (eds) Old Questions and Young Approaches to Animal Evolution. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-18202-1_7

Download citation

Publish with us

Policies and ethics