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How to build a larval body with less than a hundred cells? Insights from the early development of a stalked jellyfish (Staurozoa, Cnidaria)

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Abstract

The stalked jellyfish (Staurozoa) is an extraordinary clade within medusozoan cnidarians in which the medusa is attached to the substrate unlike the pelagic jellyfishes which compose the rest of the medusozoans. Along with this remarkable feature, staurozoans are characterized by an extremely low number of cells (< 100) in the embryos and larvae. The aim of the present study is to explore early development of the staurozoan Lucernaria quadricornis and to elucidate morphogenetic events evolved to overcome the constraints imposed by low cell number. Using bright field, confocal, and electron microscopy, we create a normal table of development of Lucernaria, describe cell number dynamics, and visualize organization of embryos and larvae. From these data, we infer a crosstalk between cell reshaping, cell rearrangement, and mechanical stress, involved in gastrulation, anterior-posterior axis differentiation, and even locomotion of the larva. Our work also demonstrates that staurozoans convergently developed morphogenetic pathways similar to other very distant animals with low cell number in the early development. We consider Lucernaria as an EvoDevo model with potential for further research to answer the question of how evolutionary forces act on developmental trajectories.

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all data generated or analyzed during this study are included in this published article; original images generated in the course of light, confocal, and electron microscopy studies are available by request.

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Acknowledgments

We thank N.A. Pertsov White Sea Biological Station of Moscow State University for the help and support in obtaining samples and providing access to all required facilities and equipment of the “Center of Microscopy WSBS MSU”. We are very grateful to the Shared Facilities center “Electron Microscopy for Life Sciences” of the Lomonosov Moscow State University for the possibility to perform TEM. We want to express special gratitude to Catriona Munro (Collège de France, Center for Interdisciplinary Research in Biology) and members of the Villefranche-sur-mer Developmental Biology Laboratory for manuscript critical reading and advice. The authors thank Brigit Shea Sullivan, NIH Library Editing Service, for manuscript editing assistance.

Funding

This study was funded by the Russian Foundation for Basic Research (grant # 15-04-08214-а) and by the Governmental Basic Research Program for the Koltzov Institute of Developmental Biology of the Russian Academy of Sciences (0108-2019-0003).

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Y.K. and T.M. designed the research; T.M., B.O., and Y.K. performed the in vivo and TEM studies; T.M. and Y.K. performed confocal microscopy; T.M. and Y.K. analyzed the data and wrote the paper.

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Correspondence to Tatiana D. Mayorova or Yulia Kraus.

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Mayorova, T.D., Osadchenko, B. & Kraus, Y. How to build a larval body with less than a hundred cells? Insights from the early development of a stalked jellyfish (Staurozoa, Cnidaria). Org Divers Evol 20, 681–699 (2020). https://doi.org/10.1007/s13127-020-00459-8

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  • DOI: https://doi.org/10.1007/s13127-020-00459-8

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