Development Genes and Evolution

, Volume 226, Issue 6, pp 383–387 | Cite as

Cell tracking supports secondary gastrulation in the moon jellyfish Aurelia

  • David A. Gold
  • Nagayasu Nakanishi
  • Nicholai M. Hensley
  • Volker Hartenstein
  • David K. JacobsEmail author
Original Article


The moon jellyfish Aurelia exhibits a dramatic reorganization of tissue during its metamorphosis from planula larva to polyp. There are currently two competing hypotheses regarding the fate of embryonic germ layers during this metamorphosis. In one scenario, the original endoderm undergoes apoptosis and is replaced by a secondary endoderm derived from ectodermal cells. In the second scenario, both ectoderm and endoderm remain intact through development. In this study, we performed a pulse-chase experiment to trace the fate of larval ectodermal cells. We observed that prior to metamorphosis, ectodermal cells that proliferated early in larval development concentrate at the future oral end of the polyp. During metamorphosis, these cells migrate into the endoderm, extending all the way to the aboral portion of the gut. We therefore reject the hypothesis that larval endoderm remains intact during metamorphosis and provide additional support for the “secondary gastrulation” hypothesis. Aurelia appears to offer the first and only described case where a cnidarian derives its endoderm twice during normal development, adding to a growing body of evidence that germ layers can be dramatically reorganized in cnidarian life cycles.


Aurelia Gastrulation Cnidaria Moon jellyfish 



This work was supported by funding from the NASA Astrobiology Institute (NNA13AA90A) Foundations of Complex Life, Evolution, Preservation, and Detection on Earth and Beyond.


  1. Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270:1319–1325CrossRefPubMedGoogle Scholar
  2. Dawson MN, Jacobs DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull 200:92–96CrossRefPubMedGoogle Scholar
  3. De Velasco B, Shen J, Go S, Hartenstein V (2004) Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Dev Biol 274:280–294CrossRefPubMedGoogle Scholar
  4. Fioroni V (1979) Abändarungen des Gastrulationsverlaufs und ihre phylogenetische Bedeutung. In: Suewing R (ed) Erlanger Symp. Ontogenie Evolutionsforsch: Ontogenie unid Phylogenie. Parey, Hamburg, pp 100–119Google Scholar
  5. Fritzenwanker JH, Genikhovich G, Kraus Y, Technau U (2007) Early development and axis specification in the sea anemone Nematostella vectensis. Dev Biol 310:264–279CrossRefPubMedGoogle Scholar
  6. Fuchs J, Martindale MQ, Hejnol A (2011) Gene expression in bryozoan larvae suggest a fundamental importance of pre-patterned blastemic cells in the bryozoan life-cycle. EvoDevo 2:1CrossRefGoogle Scholar
  7. Gold DA, Nakanishi N, Hensley NM et al (2015) Structural and developmental disparity in the tentacles of the moon jellyfish Aurelia sp.1. PLoS ONE 10:e0134741CrossRefPubMedPubMedCentralGoogle Scholar
  8. Gold DA, Jacobs DK (2013) Stem cell dynamics in Cnidaria: are there unifying principles? Dev Genes Evol 223(1-2):53–66CrossRefPubMedGoogle Scholar
  9. Helm RR, Tiozzo S, Lilley MKS et al (2015) Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles. EvoDevo 6:11CrossRefPubMedPubMedCentralGoogle Scholar
  10. Hyde JH (1894) Entwicklungsgeschichte einiger Scyphomedusen. Z Wiss Zool 58:531–565Google Scholar
  11. Kraus JEM, Fredman D, Wang W et al (2015) Adoption of conserved developmental genes in development and origin of the medusa body plan. EvoDevo 56:753–777Google Scholar
  12. Maslakova SA (2010) Development to metamorphosis of the nemertean pilidium larva. Front Zool 7:30CrossRefPubMedPubMedCentralGoogle Scholar
  13. Mayorova TD, Kosevich IA, Melekhova OP (2012) On some features of embryonic development and metamorphosis of Aurelia aurita (Cnidaria, Scyphozoa). Russ J Dev Biol 43:271–285CrossRefGoogle Scholar
  14. Martín-Durán JM, Egger B (2012) Developmental diversity in free-living flatworms. EvoDevo 3:1CrossRefGoogle Scholar
  15. Martindale M, Hejnol A (2009) A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Dev Cell 17:162–174CrossRefPubMedGoogle Scholar
  16. Mergner H (1971) Chapter 1: cnidaria. In: Reverberi G (ed) Experimental embryology of marine and fresh-water invertebrates. North Holland, Amsterdam, pp 1–84Google Scholar
  17. Morris J, Nallur R, Ladurner P, Egger B, Rieger R, Hartenstein V (2004) The embryonic development of the flatworm Macrostomum sp. Dev Genes Evol 214:220–239CrossRefPubMedGoogle Scholar
  18. Nakanishi N, Yuan D, Jacobs DK, Hartenstein V (2008) Early development, pattern, and reorganization of the planula nervous system in Aurelia (Cnidaria, Scyphozoa). Dev Genes Evol 218:511–524CrossRefPubMedGoogle Scholar
  19. Pennati R, Dell’Anna A, Pagliara P et al (2013) Neural system reorganization during metamorphosis in the planula larva of Clava multicornis (Hydrozoa, Cnidaria). Zoomorphology 132:227–237CrossRefGoogle Scholar
  20. Seipp S, Schmich J, Leitz T (2001) Apoptosis—a death-inducing mechanism tightly linked with morphogenesis in Hydractina echinata (Cnidaria, Hydrozoa). Development 128:4891–4898PubMedGoogle Scholar
  21. Seipp S, Schmich J, Will B et al (2010) Neuronal cell death during metamorphosis of Hydractina echinata (Cnidaria, Hydrozoa). Invert Neurosci 10:77–91CrossRefPubMedGoogle Scholar
  22. Smith F (1891) The gastrulation of Aurelia flavidula, Pér. & Les. Bull Museum Comparat Zool Harvard College 22:115–125Google Scholar
  23. Takashima S, Gold D, Hartenstein V (2013) Stem cells and lineages of the intestine: a developmental and evolutionary perspective. Dev Genes Evol 223:85–102CrossRefPubMedGoogle Scholar
  24. Temereva EN, Malakhov VV (2015) Metamorphic remodeling of morphology and the body cavity in Phoronopsis harmeri (Lophotrochozoa, Phoronida): the evolution of the phoronid body plan and life cycle. BMC Evol Biol 15:1CrossRefGoogle Scholar
  25. Yuan D, Nakanishi N, Jacobs DK, Hartenstein V (2008) Embryonic development and metamorphosis of the scyphozoan Aurelia. Dev Genes Evol 218:525–539CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • David A. Gold
    • 1
    • 2
  • Nagayasu Nakanishi
    • 1
    • 3
  • Nicholai M. Hensley
    • 1
    • 4
  • Volker Hartenstein
    • 5
  • David K. Jacobs
    • 1
    Email author
  1. 1.Department of Ecology and EvolutionUniversity of California, Los AngelesLos AngelesUSA
  2. 2.Division of Biology and Biological EngineeringCalifornia Institute of TechnologyPasadenaUSA
  3. 3.Whitney Laboratory for Marine BioscienceUniversity of FloridaSt. AugustineUSA
  4. 4.Department of Ecology, Evolution, and Marine BiologyUniversity of California, Santa BarbaraSanta BarbaraUSA
  5. 5.Department of Molecular, Cell, and Developmental BiologyUniversity of California, Los AngelesLos AngelesUSA

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