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Embryonic origins of hull cells in the flatworm Macrostomum lignano through cell lineage analysis: developmental and phylogenetic implications

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Abstract

The development of macrostomid flatworms is of interest for evolutionary developmental biology research because these taxa combine characteristics of the canonical spiral cleavage pattern with significant deviations from this pattern. One such deviation is the formation of hull cells, which surround the remaining embryonic primordium during early development. Using live observations with a 4D microscope system, histology, and 3D reconstructions, we analyzed the ontogeny of these hull cells in the macrostomid model organism Macrostomum lignano. Our cell lineage analysis allowed us to find the precursors of the hull cells in this species. We discuss the relation between macrostomid development and the development of other spiralians and the question of whether hull cells are homologous within rhabditophoran flatworms.

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Acknowledgments

M.W. would like to thank Prof. Dr. Dominique Adriaens for the use of the Amira software and Dr. David Weisblat for the help in improving the manuscript. This work was supported by IWT doctoral grants to M.W. and S.M. (by the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen)) and a FWO postdoctoral fellowship to W.H. B.E. was supported by a postdoctoral fellowship from the Francqui Fondation, and a Sparkling Science grant funded by the Austrian Ministry of Science and Research. C. W. would like to thank Volker Hartenstein for the opportunity to work on flatworms.

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Authors and Affiliations

  1. Department of Biology, Ghent University, K. L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Maxime Willems, Stijn Mouton, Wouter Houthoofd, Pamela Fonderie, Marjolein Couvreur & Gaëtan Borgonie

  2. Institute of Zoology, University of Innsbruck, Technikerstrasse 25, 6020, Innsbruck, Austria

    Bernhard Egger

  3. Institut für Biologie, Humboldt-Universität zu Berlin,Vergleichende Zoologie, Philippstr. 13, 10115, Berlin, Germany

    Carsten Wolff

  4. Center for Environmental Sciences, Research Group Biodiversity Phylogeny and Population Studies, Hasselt University, Agoralaan, Gebouw D, 3590, Belgium

    Tom Artois

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  1. Maxime Willems
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Correspondence to Maxime Willems.

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Communicated by D.A. Weisblat

Maxime Willems, Bernhard Egger, and Carsten Wolff equally contributed to this work.

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Hull cell formation. Movie of the first 12 h of development. Blastomeres become less recognizable because hull cells start to surround them (AVI 8,879 kb)

Hull cell degeneration. The process starts approximately 51 h after egg laying. The movie covers 6 h of development. Arrows indicate areas of cellular immigration (AVI 0 kb)

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Willems, M., Egger, B., Wolff, C. et al. Embryonic origins of hull cells in the flatworm Macrostomum lignano through cell lineage analysis: developmental and phylogenetic implications. Dev Genes Evol 219, 409–417 (2009). https://doi.org/10.1007/s00427-009-0304-x

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