Development Genes and Evolution

, Volume 219, Issue 1, pp 21–29 | Cite as

Morphogenetic mechanisms of coelom formation in the direct-developing sea urchin Heliocidaris erythrogramma

  • Margaret S. Smith
  • Steve Collins
  • Rudolf A. Raff
Original Article


Indirect development via a feeding pluteus larva represents the ancestral mode of sea urchin development. However, some sea urchin species exhibit a derived form of development, called direct development, in which features of the feeding larva are replaced by accelerated development of the adult. A major difference between these two developmental modes is the timing of the formation of the left coelom and initiation of adult development. These processes occur much earlier in developmental and absolute time in direct developers and may be underlain by changes in morphogenetic processes. In this study, we explore whether differences in the cellular mechanisms responsible for the development of the left coelom and adult structures are associated with the change in the timing of their formation in the direct-developing sea urchin Heliocidaris erythrogramma. We present evidence that left coelom formation in H. erythrogramma, which differs in major aspects of coelom formation in indirect developers, is not a result of cell division. Further, we demonstrate that subsequent development of adult structures requires cell division.


Sea urchin Gastrulation Morphogenetic Cell division Heliocidaris erythrogramma 


  1. Angerer LM, Angerer RC (1991) Localization of mRNAs by in situ hybridization: visualization of nucleic acids. Methods Cell Biol 35:37–71PubMedCrossRefGoogle Scholar
  2. Burke RD, Myers RK, Sexton TL, Jackson C (1991) Cell movements during the initial phase of gastrulation in the sea urchin embryo. Dev Biol 146:152–557CrossRefGoogle Scholar
  3. Chapman DM (1977) Erichrome cyanin as a substitute for haematoxylin and eosin. Can J Med Technol 39:65–66Google Scholar
  4. Dolbeare F, Gratzner H, Pallavicini MG, Gray JW (1983) Flow cytometric measurement of total DNA content and incorporated bromodeoxyuridine. Proc Natl Acad Sci U S A 80:5573–5577PubMedCrossRefGoogle Scholar
  5. Ettensohn CA (1984) Primary invagination of the vegetal plate during sea urchin gastrulation. Am Zool 24:571–588Google Scholar
  6. Ettensohn CA (1985) Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. Dev Biol 112:383–390PubMedCrossRefGoogle Scholar
  7. Ferkowicz MJ (1997) Wnt gene expression in sea urchins exhibiting two different forms of early development. PhD dissertation, Undiana University, Bloomington, pp 241Google Scholar
  8. Ferkowicz MJ, Raff RA (2001) Wnt gene expression in sea urchin development: heterochronies associated with the evolution of developmental mode. Evol Dev 3:24–33PubMedCrossRefGoogle Scholar
  9. Haag ES (1997) Modification of gene expression during the evolution of a direct-developing sea urchin. PhD dissertation, Indiana University, Bloomington, pp 178Google Scholar
  10. Hardin J (1989) Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev Biol 136:430–445PubMedCrossRefGoogle Scholar
  11. Hardin JD, Cheng LY (1986) The Mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev Biol 115:490–501CrossRefGoogle Scholar
  12. Hoegh-Guldberg O, Emlet R (1997) Energy use during the development of a lecithotrophic and a planktotrophic echinoid. Biol Bull 192:27–40CrossRefGoogle Scholar
  13. Jeffery CH, Emlet RB, Littlewood DTJ (2003) Phylogeny and evolution of developmental mode in temnopleurid echinoids. Mol Phylogenet Evol 28:99–118PubMedCrossRefGoogle Scholar
  14. Kominami T, Takata H (2004) Gastrulation in the sea urchin embryo: a model system for analyzing morphogenesis of a monolayered epithelium. Dev Growth Differ 46:309–326PubMedCrossRefGoogle Scholar
  15. McEdward L (1996) Experimental manipulation of parental investment of echinoid echinoderms. Am Zool 36:169–179Google Scholar
  16. Parks AL, Parr BA, Chin J-E, Leaf DS, Raff RA (1988) Molecular analysis of heterochronic changes in the evolution of direct developing sea urchins. J Evol Biol 1:27–44CrossRefGoogle Scholar
  17. Pehrson JR, Cohen LH (1986) The fate of the small micromeres in sea urchin development. Dev Biol 113:522–526PubMedCrossRefGoogle Scholar
  18. Smith MM, Smith LC, Cameron RA, Urry LA (2008) The larval stages of the sea urchin, Stongylocentrotus purpuratus. J Morphol 269:713–733PubMedCrossRefGoogle Scholar
  19. Snoke Smith M, Zigler KS, Raff RA (2007) Evolution of direct-developing larvae: selection vs loss. Bioessays 29:566–571CrossRefGoogle Scholar
  20. Stander MC (1999) Regulation and evolution of skeletogenesis in sea urchin development. MA thesis, Indiana University, BloomingtonGoogle Scholar
  21. Stephens L, Hardin J, Keller R, Wilt F (1986) The effects of aphidicolin on morphogenesis and differentiation in the sea urchin embryo. Dev Biol 118:64–69PubMedCrossRefGoogle Scholar
  22. Strathman R (1978) The evolution and loss of feeding larval strategies of marine invertebrates. Evolution 32:894–906CrossRefGoogle Scholar
  23. Strathman RR, Fenaux L, Strathman MF (1992) Heterochronic developmental plasticity in larval sea urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986CrossRefGoogle Scholar
  24. Tokuoka M, Setoguchi C, Kominami T (2002) Specification and differentiation processes of secondary mesenchyme-derived cells in embryos of the sea urchin Hemicentrotus pulcherrimus. Dev Growth Differ 44:239–250PubMedCrossRefGoogle Scholar
  25. Williams DHC, Anderson DT (1975) The reproductive system, embryonic development, larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Aust J Zool 23:371–403CrossRefGoogle Scholar
  26. Wray GA (1996) Parallel evolution of nonfeeding larvae in Echinoids. Syst Biol 45:308–322CrossRefGoogle Scholar
  27. Wray GA (1997) Echinoderms. In: Gilbert SF, Raunio AM (eds) Embryology, constructing the organism. Sinauer, Sunderland, pp 309–329Google Scholar
  28. Wray GA, Raff RA (1991) Rapid evolution of gastrulation mechanisms in a sea urchin with lecithotrophic larvae. Evolution 45:1741–1750CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Margaret S. Smith
    • 1
  • Steve Collins
    • 1
  • Rudolf A. Raff
    • 1
    • 2
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA
  2. 2.School of Biological SciencesUniversity of SydneySydneyAustralia

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