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Integrative and Comparative Biology Advance Access first published online on February 16, 2006
This version published online on February 17, 2006

Integrative and Comparative Biology, doi:10.1093/icb/icj016
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© The Society for Integrative and Comparative Biology 2006. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org.

The New Microscopy: Toward a Phylogenetic Synthesis

Embryogenesis in the glass sponge Oopsacas minuta: Formation of syncytia by fusion of blastomeres

S. P. Leys 1 *, E. Cheung 1, and N. Boury-Esnault 2
1 Department of Biological Sciences CW405, University of Alberta, Edmonton, Alberta, Canada T6G 2E9
2 Centre d'Océanologie de Marseille, Université de la Méditerranée, Station marine d'Endoume, UMR-CNRS DIMAR, 6540 rue de la Batterie des Lions, 13007 Marseille, France

* To whom correspondence should be addressed.
S. P. Leys, E-mail: sleys{at}ualberta.ca


   Abstract

Synopsis Sponges (Porifera) are unusual animals whose body plans make interpreting phylogenetic relationships within the group and with other basal metazoan taxa a difficult task. Although molecular approaches have offered new insights, some questions require a morphological approach using detailed ultrastructural or light microscopical studies of developing embryos and larvae. Glass sponges (Hexactinellida) have perhaps the most unusual body plan within the Metazoa because the majority of the tissue of the adult consists of a single giant multinucleated syncytium that forms the inner and outer layers of the sponge and is joined by cytoplasmic bridges to uninucleate cellular regions. Here we have used serial section transmission and high-resolution scanning electron microscopy to examine when syncytia first form in the cave-dwelling glass sponge Oopsacas minuta. We confirm that in O. minuta blastomeres are separate until the 32-cell stage; cleavage is equal but asynchronous until a hollow blastula is formed. The sixth division yields a collection of variously sized micromeres at the surface of the embryo and large yolk- and lipid-filled macromeres lining the blastocoel. Syncytia then form by the fusion of micromeres to form cytoplasmic bridges with each other and the fusion of macromeres to form the future multinucleated trabecular tissue of the larva and adult sponge. The multinucleated trabecular tissue envelops and forms cytoplasmic bridges with all uninucleate cells, covering the developing larva with a continuous syncytial epithelium. Differentiation of tissues occurs very early during embryogenesis with the separation of uninucleate and multinucleate lineages, but all cells and syncytia are joined by cytoplasmic bridges such that there is cytoplasmic continuity throughout the entire larva. Although glass sponges begin life as a cellular embryo, the unusual mechanism of syncytia formation at such an early stage in development distinguishes this group of animals from their closest multicellular relatives, the Demospongiae. Most important, however, these data lend support to the hypothesis that the original metazoans were cellular, not syncytial.


From the symposium "The New Microscopy: Toward a Phylogenetic Synthesis" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4-8, 2005, at San Diego, California.
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