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Cell differentiation and germ–soma separation in Ediacaran animal embryo-like fossils

Abstract

Phosphorites of the Ediacaran Doushantuo Formation (600 million years old) yield spheroidal microfossils with a palintomic cell cleavage pattern1,2. These fossils have been variously interpreted as sulphur-oxidizing bacteria3, unicellular protists4, mesomycetozoean-like holozoans5, green algae akin to Volvox6,7, and blastula embryos of early metazoans1,2,8,9,10 or bilaterian animals11,12. However, their complete life cycle is unknown and it is uncertain whether they had a cellularly differentiated ontogenetic stage, making it difficult to test their various phylogenetic interpretations. Here we describe new spheroidal fossils from black phosphorites of the Doushantuo Formation that have been overlooked in previous studies. These fossils represent later developmental stages of previously published blastula-like fossils, and they show evidence for cell differentiation, germ–soma separation, and programmed cell death. Their complex multicellularity is inconsistent with a phylogenetic affinity with bacteria, unicellular protists, or mesomycetozoean-like holozoans. Available evidence also indicates that the Doushantuo fossils are unlikely crown-group animals or volvocine green algae. We conclude that an affinity with cellularly differentiated multicellular eukaryotes, including stem-group animals or algae, is likely but more data are needed to constrain further the exact phylogenetic affinity of the Doushantuo fossils.

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Figure 1: Early developmental stages of Megasphaera.
Figure 2: Megaclonophycus-like fossils with dividing cell packets.
Figure 3: Megaclonophycus-like fossils with matryoshkas.

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Acknowledgements

This work was supported by the Ministry of Science and Technology of China, National Natural Science Foundation of China, Chinese Academy of Sciences, and the US National Science Foundation. We thank Q. Fu, S. Golubic, F. Meng, and D. Wang for discussion.

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Authors

Contributions

L.C. and K.P. performed the research under the guidance of S.X. and X.Y. S.X. developed the interpretation and prepared the manuscript with the assistance of C.Z. and X.Y.

Corresponding authors

Correspondence to Shuhai Xiao or Xunlai Yuan.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Measurements of Megaclonophycus-like fossils with cell packets and matryoshkas.

a, b, Cross-plots of specimen size (that is, diameter of spheroidal fossils), cell number, and diameter of blastomere-like cells, showing the constancy of spheroidal size, independency of spheroidal size on cell size, and power relationship between cell number and cell diameter, as predicted from palintomic cell division. The relationship confirms that the Megaclonophycus-like fossils with cell packets and matryoshkas follow an ontogenetic trajectory established by Parapandorina- and Megaclonophycus-stage fossils. Measurements were made on thin-section specimens in our collection as well as on extracted specimens from published material1,2,31,32,33,34,35. Each data point represents a single specimen, with its diameter averaged between maximum and minimum dimensions. Cell diameter is averaged among all observable cells, excluding cell packets and matryoshkas. In Parapandorina-stage specimens, cell number was determined from actual count whenever possible. In Megaclonophycus-stage specimens, cell number was estimated from random close packing of spherical cells (64% packing density36). In Megaclonophycus-like specimens with cell packets and matryoshkas, cell number was also estimated from random close packing of spherical cells, but assuming that the volumes of cell packets or matryoshkas were occupied by spherical blastomere-like cells. c, d, Cross-plots of matryoshka diameter, cell number in matryoshkas, and average cell size in matryoshkas, showing constancy of cell size, independency of matryoshka size on cell size, and power relationship between matryoshka diameter and cell number, as predicted from the continuing growth of matryoshkas. Each data point represents a single matryoshka, with its diameter averaged between its maximum and minimum dimensions. Cell diameter is averaged among all observable cells encountered in thin sections. Cell number was estimated from tight packing of polyhedral cells (100% packing density). See Source Data for measurements.

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Chen, L., Xiao, S., Pang, K. et al. Cell differentiation and germ–soma separation in Ediacaran animal embryo-like fossils. Nature 516, 238–241 (2014). https://doi.org/10.1038/nature13766

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