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bioRxiv · 10.1101/068783

Conserved traits of spiralian development in the bryozoan Membranipora membranacea

Bruno Cossermelli Vellutini·Jose M Martin-Duran·Andreas Hejnol
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Abstract

BackgroundSpiral cleavage is a remarkably conserved pattern of embryogenesis present in animals of the clade Spiralia, such as annelids, molluscs, flatworms and nemerteans. However, not all spiralians display spiral cleavage. Recent phylogenies suggest that the spiral arrangement of embryonic blastomeres is an ancestral trait for the Spiralia and that it was secondarily modified in several spiralian lineages, such as gastrotrichs, brachiopods and bryozoans. To better understand the evolution of cleavage patterns in relation to blastomere fate maps and embryonic gene expression, we describe the cell lineage and molecular patterning in the embryogenesis of the bryozoan Membranipora membranacea.\n\nResultsM. membranacea develops through a unique stereotypic cleavage pattern with biradial symmetry and an embryo organized in identical quadrants with synchronous cell divisions. The quadrant identities are established as early as the 28-cell stage, when one vegetal blastomere (3D) activates the MAPK pathway, marking the future posterior region of the larva. Cells from this posterior quadrant divide asynchronously in subsequent stages leading to the morphological differentiation between quadrants. The first quartet of M. membranacea gives rise to the apical organ and ciliated band, the second and third quartet forms the oral/anal ectoderm, the fourth quartet the mesoderm and the vegetal blastomeres form the endoderm. We found that the early embryonic organization and the fate map of these early blastomeres in the bryozoan embryo are similar to a typical spiral-cleaving embryo. Furthermore we observe that correspondent blastomeres between the bryozoan and spiral-cleaving embryos share similar molecular identities, as revealed by the activity of MAPK and the expression of otx and foxa. The development of M. membranacea mainly differs from spiral-cleaving embryos in the downstream portions of the cell lineage, and in the origin of the mesoderm, which is formed by multiple fourth quartet blastomeres.\n\nConclusionsThe similarity between the fate map of M. membranacea and spiral-cleaving embryos indicates that the cleavage geometry of the bryozoan evolved decoupled from other spiralian developmental traits. In this case, the blastomere fates remained evolutionarily conserved despite the drastic modification in the cleavage pattern from spiral to biradial. These findings suggest that blastomere fates of spiral-cleaving embryos might not be linked to the stereotypic spiral cleavage pattern, but depend on other factors, such as the underlying molecular patterning. Our comparative analysis on the bryozoan reveals yet another facet of how early development evolves and helps to shed some light into the developmental diversity of spiralians.

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Bruno Cossermelli Vellutini, Jose M Martin-Duran, Andreas Hejnol. 2016-08-11. Conserved traits of spiralian development in the bryozoan Membranipora membranacea. https://doi.org/10.1101/068783

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