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Doushantuo embryos preserved inside diapause egg cysts

Nature volume 446, pages 661–663 (2007)Cite this article

Abstract

Phosphatized microfossils in the Ediacaran (635–542 Myr ago) Doushantuo Formation, south China, have been interpreted as the embryos of early animals1,2,3,4. Despite experimental demonstration that embryos can be preserved5, microstructural evidence that the Doushantuo remains are embryonic6 and an unambiguous record of fossil embryos in Lower Cambrian rocks7, questions about the phylogenetic relationships of these fossils remain. Most recently, some researchers have proposed8 that Doushantuo microfossils may be giant sulphur-oxidizing bacteria comparable to extant Thiomargarita sp. Here we report new observations that provide a test of the bacterial hypothesis. The discovery of embryo-like Doushantuo fossils inside large, highly ornamented organic vesicles (acritarchs) indicates that these organisms were eukaryotic, and most probably early cleavage stage embryos preserved within diapause egg cysts. Large acanthomorphic microfossils of the type observed to contain fossil embryos first appear in rocks just above a 632.5 ± 0.5-Myr-old ash bed9, suggesting that at least stem-group animals6 inhabited shallow seas in the immediate aftermath of global Neoproterozoic glaciation.

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Figure 1: Large acanthomorphic acritarchs, some containing preserved embryos, in the Ediacaran Doushantuo Formation, Xiaofenghe section, western Hubei Province, China.
Figure 2: Xiaofenghe section of the Doushantuo Formation, showing the stratigraphic distribution of large acanthomorph acritarchs.

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References

  1. Xiao, S., Zhang, Y. & Knoll, A. H. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391, 553–558 (1998)

    Article  ADS  CAS  Google Scholar 

  2. Xiao, S. & Knoll, A. H. Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng’an, Guizhou, South China. J. Paleontol. 74, 767–788 (2000)

    Article  Google Scholar 

  3. Chen, J. et al. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science 305, 218–222 (2006)

    Article  ADS  Google Scholar 

  4. Dornbos, S. Q. et al. Environmental controls on the taphonomy of phosphatized animals and animal embryos from the Neoproterozoic Doushantuo Formation, southwest China. Palaios 21, 3–14 (2006)

    Article  ADS  Google Scholar 

  5. Raff, E. C., Villinski, J. T., Turner, F. R., Donoghue, P. C. J. & Raff, R. A. Experimental taphonomy shows the feasibility of fossil embryos. Proc. Natl Acad. Sci. USA 103, 5846–5851 (2006)

    Article  ADS  CAS  Google Scholar 

  6. Hagadorn, J. W. et al. Cellular and subcellular structure of Neoproterozoic animal embryos. Science 314, 291–294 (2006)

    Article  ADS  CAS  Google Scholar 

  7. Donoghue, P. C. J. et al. Fossilized embryos are widespread but the record is temporally and taxonomically biased. Evol. Dev. 8, 232–238 (2006)

    Article  Google Scholar 

  8. Bailey, J. V., Joye, S. B., Kalanetra, K. M., Flood, B. E. & Corsetti, F. A. Evidence of giant sulfur bacteria in Neoproterozoic phosphorites. Nature 445, 198–201 (2007)

    Article  ADS  CAS  Google Scholar 

  9. Condon, D. et al. U-Pb ages from the Neoproterozoic Doushantuo Formation, China. Science 308, 95–98 (2005)

    Article  ADS  CAS  Google Scholar 

  10. Donoghue, P. C. J. Embryonic identity crisis. Nature 445, 155–156 (2007)

    Article  ADS  CAS  Google Scholar 

  11. Xiao, S., Hagadorn, J. W., Zhou, C. & Yuan, X. Rare helical spheroidal fossils from the Doushantuo Lagerstätte: Ediacaran animal embryos come of age? Geology 35, 115–118 (2007)

    Article  ADS  Google Scholar 

  12. Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Phil. Trans. Roy. Soc. B 361, 1023–1038 (2006)

    Article  CAS  Google Scholar 

  13. Zhang, Y., Yin, L., Xiao, S. & Knoll, A. H. Permineralized fossils from the terminal Proterozoic Doushantuo Formation, south China. J. Paleontol. 72 (Suppl. to no. 4) 1–52 (1998)

    Article  Google Scholar 

  14. Yuan, X. & Hofmann, H. J. New micropaleontological data from Neoproterozoic Sinica Doushantuo phosphorite rocks, Weng’an, Guizhou Province, southwestern China. Alcheringa 22, 189–222 (1998)

    Article  Google Scholar 

  15. Van Waveren, I. & Marcus, N. H. Morphology of recent copepod egg envelopes from Turkey Point, Gulf of Mexico, and their implications for acritarch affinity. Spec. Pap. Paleontol. 48, 111–124 (1993)

    Google Scholar 

  16. Buckland-Nicks, J. Hull cupules of chiton eggs: parachute structures and sperm focusing devices? Biol. Bull. 184, 269–276 (1993)

    Article  CAS  Google Scholar 

  17. Yin, C., Bengtson, S. & Yue, Z. Silicified and phosphatized Tianzhushania, spheroidal microfossils of possible animal origin from the Neoproterozoic of South China. Acta Palaeontol. Pol. 49, 1–12 (2004)

    Google Scholar 

  18. Grey, K. Ediacaran palynology of Australia. Mem. Assoc. Australas. Palaeontologists 31, 1–439 (2005)

    Google Scholar 

  19. Marcus, N. H. & Boero, F. Minireview: The importance of benthic–pelagic coupling and the forgotten role of life cycles in coastal aquatic systems. Limnol. Oceanogr. 43, 763–768 (1998)

    Article  ADS  Google Scholar 

  20. Zhu, M., Zhang, J. & Yang, A. Integrated Ediacaran (Sinian) chronostratigraphy of South China. Palaeogeogr. Palaeoclimatol. Palaeoecol. (in the press).

  21. Barfod, G. H. et al. New Lu-Hf and Pb-Pb age constraints on the earliest animal fossils. Earth Planet. Sci. Lett. 201, 203–212 (2002)

    Article  ADS  CAS  Google Scholar 

  22. Chen, D., Dong, W. Q., Qi, L., Chen, G. Q. & Chen, X. P. Pb-Pb ages of Neproterozoic Doushantuo phosphorites in South China: constraints on early metazoan evolution and glaciation events. Precambr. Res. 132, 123–222 (2004)

    Article  ADS  CAS  Google Scholar 

  23. Zhou, C., Xie, G., Mcfadden, K., Xiao, S. & Yuan, X. The diversification and extinction of Doushantuo–Pertatataka acritarchs in South China: causes and biostratigraphic significance. Geol. J. 41, 1–34 (2006)

    Article  Google Scholar 

  24. Hoffman, P. F., Kaufman, A. J., Halverson, G. P. & Schrag, D. P. A Neoproterozoic snowball earth. Science 281, 1342–1346 (1998)

    Article  ADS  CAS  Google Scholar 

  25. Voreb’eva, N. G., Sergeev, V. N. & Knoll, A. H. Diverse Ediacaran acritarchs from the margin of the East European Platform. Geology (submitted).

  26. Canfield, D. E., Poulton, S. W. & Narbonne, G. M. Late Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 10.1126/science.1135013. (2006)

  27. Fike, D. A., Grotzinger, J. P., Pratt, L. M. & Summons, R. E. Oxidation of the Ediacaran ocean. Nature 444, 744–747 (2006)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Chinese Academy of Sciences, the National Natural Science Foundation of China, the Major Basic Research Projects of MST of China, and an NSF Grant. We thank S. Xiao and P. Cohen for discussions.

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Authors and Affiliations

  1. State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China,

    Leiming Yin, Maoyan Zhu, Xunlai Yuan, Junming Zhang & Jie Hu

  2. Botanical Museum, Harvard University, Cambridge, Massachusetts 02138, USA,

    Andrew H. Knoll

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  1. Leiming Yin
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  3. Andrew H. Knoll
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Correspondence to Leiming Yin.

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Yin, L., Zhu, M., Knoll, A. et al. Doushantuo embryos preserved inside diapause egg cysts. Nature 446, 661–663 (2007). https://doi.org/10.1038/nature05682

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