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Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite

Abstract

Phosphorites of the late Neoproterozoic (570 ± 20 Myr BP) Doushantuo Formation, southern China, preserve an exceptional record of multicellular life from just before the Ediacaran radiation of macroscopic animals. Abundant thalli with cellular structures preserved in three-dimensional detail show that latest-Proterozoic algae already possessed many of the anatomical and reproductive features seen in the modern marine flora. Embryos preserved in early cleavage stages indicate that the divergence of lineages leading to bilaterians may have occurred well before their macroscopic traces or body fossils appear in the geological record. Discovery of these fossils shows that the early evolution of multicellular organisms is amenable to direct palaeontological inquiry.

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Figure 1: Location and generalized stratigraphy of the fossiliferous Weng'an section in Guizhou Province, South China.
Figure 2: Algal thalli from the Doushantuo phosphorite and the modern bangiophyte red alga, Prophyra suborbiculata.
Figure 3: Parenchymatous and pseudoparenchymatous thalli from the Doushantuo phosphorite.
Figure 4: Reproductive structures in Doushantuo thalli and a modern red alga.
Figure 5: Fossil embryos preserving different stages of cleavage from the Doushantuo phosphorite.

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References

  1. Buss, L. W. The Evolution of Individuality (Princeton Univ. Press, NJ, 1987).

    Google Scholar 

  2. Han, T.-M. & Runnegar, B. Megascopic eukaryotic algae from the 2.1 billion-year-old Negaunee Iron-Formation, Michigan. Science 257, 232–235 (1992).

    Article  ADS  CAS  Google Scholar 

  3. Knoll, A. H. The early evolution of eukaryotes: a geological perspective. Science 256, 622–627 (1992).

    Article  ADS  CAS  Google Scholar 

  4. Whittington, H. B. The Burgess Shale (Yale Univ. Press, New Haven, CT, 1985).

    Google Scholar 

  5. Briggs, D. E. G., Erwin, D. H. & Collier, F. J. The Fossils of the Burgess Shale (Smithsonian Institution Press, Washington DC, 1994).

    Google Scholar 

  6. Kidston, R. & Lang, W. H. On Old Red Sandstone plants showing structure from the Rhynie chert bed, Aberdeenshire. Parts I–Iv. Trans. R. Soc. Edinb. 51, 761–784; 52, 603–627; 62, 643–680; 52, 831–854 (1917–1921).

    Article  Google Scholar 

  7. Remy, W., Gensel, P. J. & Hass, H. The gametophyte generation of some early Devonian land plants. Int. J. Plant Sci. 154, 35–58 (1993).

    Article  Google Scholar 

  8. Zhao, Z., Xing, Y., Ma, G. & Chen, Y. Biostratigraphy of the Yangtze Gorge Area, (1) Sinian (Geological Publishing House, Beijing, 1985).

    Google Scholar 

  9. Zhao, Z. et al. The Sinian System of Hubei (China University of Geosciences Press, Wuhan, 1988).

    Google Scholar 

  10. Sun, W. Late Precambrian pennatulids (sea pens) from the eastern Yangtze Gorge, China: Paracharnia gen. nov. Precambrian Res. 31, 361–375 (1986).

    Article  ADS  Google Scholar 

  11. Qian, Y., Chen, M. & Chen, Y. Hyolithids and other small shelly fossils from the Lower Cambrian Huangshandong Formation in the eastern part of the Yangtze Gorge. Acta Palaeontol. Sinica 18(3), 207–232 (1979).

    Google Scholar 

  12. Compston, W., Williams, I. S., Kirchvink, J. L., Zhang, Z. & Ma, G. Zircon U-Pb ages for the Early Cambrian time-scale. J. Geol. Soc. Lond. 149, 171–184 (1992).

    Article  CAS  Google Scholar 

  13. Zhang, Y., Ying, L., Xiao, S. & Knoll, A. H. Permineralized fossils from the Terminal Proterozoic Doushantuo Formation, South China. Paleontol. Soc. Mem. (in the press).

  14. Grotzinger, J. P., Bowring, S. A., Saylor, B. Z. & Kaufman, A. J. Biostratigraphic and geochronologic constraints on early animal evolution. Science 270, 598–604 (1995).

    Article  ADS  CAS  Google Scholar 

  15. Kaufman, A. J., Knoll, A. H. & Narbonne, G. M. Isotopes, ice ages, and terminal Proterozoic earth history. Proc. Natl Acad. Sci. USA 94, 6600–6605 (1997).

    Article  ADS  CAS  Google Scholar 

  16. Benus, A. P. Sedimentologic context of a deep-water Ediacaran fauna (Mistaken Point Formation, Avalon zone, eastern Newfoundland). Bull. N. Y. State Mus. 463, 8–9 (1988).

    Google Scholar 

  17. Hofmann, H. J., Narbonne, G. M. & Aitken, J. D. Ediacaran remains from intertillite beds in northwestern Canada. Geology 18, 1199–1202 (1990).

    Article  ADS  Google Scholar 

  18. Briggs, D. E. G., Kear, A. J., Martill, D. M. & Wilby, P. R. Phosphatization of soft-tissue in experiments and fossils. J. Geol. Soc. Lond. 150, 1035–1038 (1993).

    Article  Google Scholar 

  19. Krajewski, K. P. et al. Biological processes and apatite formation in sedimentary environments. Ecolog. Geol. Helvet. 87, 701–745 (1994).

    Google Scholar 

  20. Glenn, C. R. et al. Phosphorus and phosphorites: Sedimentology and environments of formation. Eclog. Geol. Helvet. 87, 747–788 (1994).

    Google Scholar 

  21. Föllmi, K. B. The phosphorus cycle, phosphogenesis and marine phosphate-rich deposits. Earth Sci. Rev. 40, 55–124 (1996).

    Article  ADS  Google Scholar 

  22. Zhu, S. & Wang, Y. in The Upper Precambrian and Sinian-Cambrian Boundary in Guizhou (eds Wang, Y. et al.) 93–103 (People's Publishing House of Ghizhou, Guiyang, 1984).

    Google Scholar 

  23. Zhang, Y. Multicellular thallophytes with differentiated tissues from Late Proterozoic phosphate rocks of South China. Lethaia 22, 113–132 (1989).

    Article  CAS  Google Scholar 

  24. Zhang, Y. & Yuan, X. New data on multicellular thallophytes and fragments of cellular tissues from Late Proterozoic phosphate rocks, South China. Lethaia 25, 1–18 (1992).

    Article  Google Scholar 

  25. Awramik, S. M. et al. Prokaryotic and eukaryotic microfossils from a Proterozoic/Phanerozoic transition in China. Nature 315, 655–658 (1985).

    Article  ADS  Google Scholar 

  26. Bold, H. C. & Wynne, M. J. Introduction to the Algae (Prentice-Hall, Englewood Cliffs, NJ, 1985).

    Google Scholar 

  27. Fritsch, F. E. The Structure and Reproduction of the Algae Vols 1 2,(Cambridge Univ. Press, 1965).

    Google Scholar 

  28. van den Hoek, C., Mann, D. G. & Jahns, H. M. Algae: An Introduction to Phycology (Cambridge Univ. Press, 1995).

    Google Scholar 

  29. Butterfield, N. J., Knoll, A. H. & Swett, K. Abangiophyte red alga from the Proterozoic of Arctic Canada. Science 250, 104–107 (1990).

    Article  ADS  CAS  Google Scholar 

  30. Xiao, S., Knoll, A. H. & Yuan, X. Morphological reconstruction of Miaohephyton bifurcatum, a possible brown alga from the Terminal Proterozoic Doushantuo Formation, South China. J. Paleontol. (in the press).

  31. Hermann, T. N. Organic World Billion Year Ago (Nauka, Leningrad, 1990).

    Google Scholar 

  32. Chen, M. & Xiao, Z. Discovery of the macrofossils in the Upper Sinain Doushantuo Formation at Miaohe, eastern Yangtze Gorges. Sci. Geol. Sinica 4, 317–324 (1991).

    Google Scholar 

  33. Butterfield, N. J., Knoll, A. H. & Swett, K. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils Strata 34, 1–84 (1994).

    Google Scholar 

  34. Haeckel, E. The gastrea theory, the phylogenetic classification of the animal kingdom and the homology of the germ-lamellae. Q. J. Microsc. Soc. 14, 142–165 (1874).

    Google Scholar 

  35. Davidson, E. H., Peterson, K. J. & Cameron, R. A. Origin of bilaterian body plans: Evolution of develpmental regulatory mechanisms. Science 270, 1319–1325 (1995).

    Article  ADS  CAS  Google Scholar 

  36. Wray, G. A., Levinton, J. S. & Shapiro, L. H. Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274, 568–573 (1996).

    Article  ADS  CAS  Google Scholar 

  37. Sogin, M. L. in Early Life on Earth (ed. Bengtson, S.) 181–192 (Columbia Univ. Press, NY, 1994).

    Google Scholar 

  38. Vermeij, G. J. Animal Origins. Science 274, 525–526 (1996).

    Article  ADS  CAS  Google Scholar 

  39. Fortey, R. A., Briggs, D. E. G. & Wills, M. A. The Cambrian evolutionary ‘explosion’: decoupling cladogenesis from morphological disparity. Biol. J. Linn. Soc. 57, 13–33 (1996).

    Google Scholar 

  40. Zhang, X. & Pratt, B. R. Middle Cambrian Arthropod embryos with blastomeres. Science 266, 627–639 (1994).

    ADS  Google Scholar 

  41. Bengtson, S. & Yue, Z. Fossilized metazoan embryos from the earliest Cambrian. Science 277, 1645–1648 (1997).

    Article  Google Scholar 

  42. Xue, Y., Tang, T., Yu, C. & Zhou, C. Large Spheroidal Chlorophyta fossils from the Doushantuo Formation phosphoric sequence (late Sinian), central Guizhou, South China. Acta Palaeontol. Sinica 34, 688–706 (1995).

    Google Scholar 

  43. Kumé, M. & Dan, K. Invertebrate Embryology.(NOLIT, Belgrade, 1968).

  44. Anderson, D. T. Embryology and Phylogeny in Annelids and Arthropods (International Series of Monographs in Pure and Applied Biology, Vol. 50) (Pergamon, Oxford, 1973).

  45. Brusca, R. C. & Brusca, G. J. Invertebrates (Sinauer, Sunderland, MA, 1990).

    Google Scholar 

  46. Nielsen, C. Animal Evolution: Interrelationships of the Living Phyla (Oxford Univ. Press, 1995).

    Google Scholar 

  47. Agassiz, L. Essay on Classification (reprinted from Contributions to the Natural History of the United States, vol. 1,(1857) (Harvard Univ. Press, Cambridge, MA, 1962).

    Google Scholar 

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Acknowledgements

We thank Y. Leiming for field assistance, E. Seling for technical help and S. Bengtson, D. McHugh, R. M. Woollacott, S. J. Gould, C. Nielsen, E. Ruppert, E. Davidson, A. Cameron and J. Henry for discussions and comments. This work was partly supported by grants from NSFC (to Y.Z.) and NSF (to A.H.K.).

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Xiao, S., Zhang, Y. & Knoll, A. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391, 553–558 (1998). https://doi.org/10.1038/35318

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