Doushantuo embryos preserved inside diapause egg cysts
Open accessAbstract
Phosphatized microfossils in the Ediacaran (635-542 Myr ago) Doushantuo Formation, south China, have been interpreted as the embryos of early animals. Despite experimental demonstration that embryos can be preserved, microstructural evidence that the Doushantuo remains are embryonic and an unambiguous record of fossil embryos in Lower Cambrian rocks, questions about the phylogenetic relationships of these fossils remain. Most recently, some researchers have proposed 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 bed, suggesting that at least stem-group animals inhabited shallow seas in the immediate aftermath of global Neoproterozoic glaciation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The oldest described probable metazoan embryo is Tianzhushania, found just above the Marinoan glaciation but continuing through most of the younger parts of the Doushantuo formation.
“The oldest described probable metazoan embryo is Tianzhushania , found just above the Marinoan glaciation but continuing through most of the younger parts of the Doushantuo formation (Yin et al. 2007).”
From An integrated view of precambrian eumetazoan evolution (2009) · cites this paper as Yin et al. 2007
Cites
A Neoproterozoic Snowball Earth
Hoffman, P. F., Kaufman, A. J., Halverson, G. P., & Schrag, D. P. (1998) · Science · doi:10.1126/science.281.5381.1342 · Cited by 2,693 · see citing works
U-Pb Ages from the Neoproterozoic Doushantuo Formation, China
Condon, D., Zhu, M., Bowring, S., Wang, W., Yang, A., & Jin, Y. (2005) · Science · doi:10.1126/science.1107765 · Cited by 1,329 · see citing works
Self-citationLate-Neoproterozoic Deep-Ocean Oxygenation and the Rise of Animal Life
Canfield, D. E., Poulton, S. W., & Narbonne, G. M. (2007) · Science · doi:10.1126/science.1135013 · Cited by 1,000 · see citing works
Oxidation of the Ediacaran Ocean
Fike, D. A., Grotzinger, J. P., Pratt, L. M., & Summons, R. E. (2006) · Nature · doi:10.1038/nature05345 · Cited by 989 · see citing works
Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian
Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W., & Davidson, E. H. (2004) · Science · doi:10.1126/science.1099213 · Cited by 284 · see citing works
New Lu–Hf and Pb–Pb age constraints on the earliest animal fossils
Barfod, G. H., Albarède, F., Knoll, A. H., Xiao, S., Télouk, P., Frei, R., & Baker, J. (2002) · Earth and Planetary Science Letters · doi:10.1016/s0012-821x(02)00687-8 · Cited by 251 · see citing works
Self-citationXunlai, Y., & Hofmann, H. J. (1998) · Alcheringa: An Australasian Journal of Palaeontology · doi:10.1080/03115519808619200 · Cited by 90 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Partitioning heritability by functional annotation using genome-wide association summary statistics
ReproGen Consortium, Finucane, H. K., Schizophrenia Working Group of the Psychiatric Genomics Consortium, The RACI Consortium, Bulik-Sullivan, B., Gusev, A., Trynka, G., Reshef, Y., Loh, P.-R., Anttila, V., et al. (2015) · Nature Genetics · doi:10.1038/ng.3404 · Cited by 2,604 · see citing works
Fossil steroids record the appearance of Demospongiae during the Cryogenian period
Love, G. D., Grosjean, E., Stalvies, C., Fike, D. A., Grotzinger, J. P., Bradley, A. S., Kelly, A. E., Bhatia, M., Meredith, W., Snape, C. E., et al. (2009) · Nature · doi:10.1038/nature07673 · Cited by 731 · see citing works
A Stratified Redox Model for the Ediacaran Ocean
Li, C., Love, G. D., Lyons, T. W., Fike, D. A., Sessions, A. L., & Chu, X. (2010) · Science · doi:10.1126/science.1182369 · Cited by 673 · see citing works
The Neoproterozoic oxygenation event: Environmental perturbations and biogeochemical cycling
Och, L. M., & Shields-Zhou, G. A. (2012) · Earth-Science Reviews · doi:10.1016/j.earscirev.2011.09.004 · Cited by 646 · see citing works
Stratigraphy and paleogeography of the Ediacaran Doushantuo Formation (ca. 635–551Ma) in South China
Jiang, G., Shi, X., Zhang, S., Wang, Y., & Xiao, S. (2011) · Gondwana Research · doi:10.1016/j.gr.2011.01.006 · Cited by 624 · see citing works
Pulsed oxidation and biological evolution in the Ediacaran Doushantuo Formation
McFadden, K. A., Huang, J., Chu, X., Jiang, G., Kaufman, A. J., Zhou, C., Yuan, X., & Xiao, S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708336105 · Cited by 617 · see citing works
Self-citationThe Multiple Origins of Complex Multicellularity
Knoll, A. H. (2011) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.031208.100209 · Cited by 562 · see citing works
Self-citationOcean oxygenation in the wake of the Marinoan glaciation
Sahoo, S. K., Planavsky, N. J., Kendall, B., Wang, X., Shi, X., Scott, C., Anbar, A. D., Lyons, T. W., & Jiang, G. (2012) · Nature · doi:10.1038/nature11445 · Cited by 544 · see citing works
Animal phylogeny and its evolutionary implications
Dunn, C. W., Giribet, G., Edgecombe, G. D., & Hejnol, A. (2014) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev-ecolsys-120213-091627 · Cited by 401 · see citing works
The earliest Cambrian record of animals and ocean geochemical change
Maloof, A. C., Porter, S. M., Moore, J. L., Dudas, F. O., Bowring, S. A., Higgins, J. A., Fike, D. A., & Eddy, M. P. (2010) · Geological Society of America Bulletin · doi:10.1130/b30346.1 · Cited by 419 · see citing works
Oceanic oxygenation events in the anoxic Ediacaran ocean
Sahoo, S. K., Planavsky, N. J., Jiang, G., Kendall, B., Owens, J. D., Wang, X., Shi, X., Anbar, A. D., & Lyons, T. W. (2016) · Geobiology · doi:10.1111/gbi.12182 · Cited by 352 · see citing works
Kendall, B., Komiya, T., Lyons, T. W., Bates, S. M., Gordon, G. W., Romaniello, S. J., Jiang, G., Creaser, R. A., Xiao, S., McFadden, K., et al. (2015) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2015.02.025 · Cited by 286 · see citing works
The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s
Nelson, D. R., Goldstone, J. V., & Stegeman, J. J. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0474 · Cited by 193 · see citing works
Ader, M., Sansjofre, P., Halverson, G. P., Busigny, V., Trindade, R. I. F., Kunzmann, M., & Nogueira, A. C. R. (2014) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2014.03.042 · Cited by 180 · see citing works
The Weng'an biota and the Ediacaran radiation of multicellular eukaryotes
Xiao, S., Muscente, A. D., Chen, L., Zhou, C., Schiffbauer, J. D., Wood, A. D., Polys, N. F., & Yuan, X. (2014) · National Science Review · doi:10.1093/nsr/nwu061 · Cited by 172 · see citing works
Self-citationHuldtgren, T., Cunningham, J. A., Yin, C., Stampanoni, M., Marone, F., Donoghue, P. C. J., & Bengtson, S. (2011) · Science · doi:10.1126/science.1209537 · Cited by 171 · see citing works
The Proterozoic Record of Eukaryotes
Cohen, P. A., & Macdonald, F. A. (2015) · Paleobiology · doi:10.1017/pab.2015.25 · Cited by 173 · see citing works
Large spinose microfossils in Ediacaran rocks as resting stages of early animals
Cohen, P. A., Knoll, A. H., & Kodner, R. B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902322106 · Cited by 166 · see citing works
Self-citationUncovering the spatial heterogeneity of Ediacaran carbon cycling
Li, C., Hardisty, D. S., Luo, G., Huang, J., Algeo, T. J., Cheng, M., Shi, W., An, Z., Tong, J., Xie, S., et al. (2017) · Geobiology · doi:10.1111/gbi.12222 · Cited by 152 · see citing works
Late Ediacaran redox stability and metazoan evolution
Johnston, D. T., Poulton, S. W., Goldberg, T., Sergeev, V. N., Podkovyrov, V., Vorob'eva, N. G., Bekker, A., & Knoll, A. H. (2012) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2012.05.010 · Cited by 146 · see citing works
Self-citationCambrian explosion: Birth of tree of animals
Shu, D. (2008) · Gondwana Research · doi:10.1016/j.gr.2007.08.004 · Cited by 143 · see citing works
The earliest fossil record of the animals and its significance
Budd, G. E. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2232 · Cited by 140 · see citing works
Cell differentiation and germ–soma separation in Ediacaran animal embryo-like fossils
Chen, L., Xiao, S., Pang, K., Zhou, C., & Yuan, X. (2014) · Nature · doi:10.1038/nature13766 · Cited by 113 · see citing works
Self-citationThe role of microbes in the formation of modern and ancient phosphatic mineral deposits
Crosby, C. H., & Bailey, J. V. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00241 · Cited by 107 · see citing works
Liu, P., Yin, C., Gao, L., Tang, F., & Chen, S. (2009) · Science Bulletin · doi:10.1007/s11434-008-0589-6 · Cited by 98 · see citing works
Riedman, L. A., & Sadler, P. M. (2018) · Precambrian Research · doi:10.1016/j.precamres.2017.10.008 · Cited by 92 · see citing works
The Burgess Shale paleocommunity with new insights from Marble Canyon, British Columbia
Nanglu, K., Caron, J.-B., & Gaines, R. R. (2020) · Paleobiology · doi:10.1017/pab.2019.42 · Cited by 81 · see citing works
Chernikova, D., Motamedi, S., Csürös, M., Koonin, E. V., & Rogozin, I. B. (2011) · Biology Direct · doi:10.1186/1745-6150-6-26 · Cited by 72 · see citing works
Octoradiate spiral organisms in the Ediacaran of South China
Feng, T., Chongyu, Y., BENGTSON, S., Pengju, L., Ziqiang, W., & Linzhi, G. (2008) · Acta Geologica Sinica - English Edition · doi:10.1111/j.1755-6724.2008.tb00321.x · Cited by 66 · see citing works
Causes and consequences of the Cambrian explosion
Zhang, X., & Shu, D. (2014) · Science China Earth Sciences · doi:10.1007/s11430-013-4751-x · Cited by 50 · see citing works
An integrated view of precambrian eumetazoan evolution
Davidson, E. H., & Erwin, D. H. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.042 · Cited by 48 · see citing works
Derkowski, A., Bristow, T. F., Wampler, J. M., Środoń, J., Marynowski, L., Elliott, W. C., & Chamberlain, C. P. (2013) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2013.01.015 · Cited by 46 · see citing works
The mouth, the anus, and the blastopore—open questions about questionable openings
Hejnol, A., & Martindale, M. Q. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0004 · Cited by 37 · see citing works
Terminal Developments in Ediacaran Embryology
Butterfield, N. J. (2011) · Science · doi:10.1126/science.1216125 · Cited by 37 · see citing works
Chen, Y., Chu, X., Zhang, X., & Zhai, M. (2015) · Science China Earth Sciences · doi:10.1007/s11430-015-5071-0 · Cited by 35 · see citing works
Oxygen and Early Animal Evolution
Xiao, S. (2014) · Treatise on Geochemistry · doi:10.1016/b978-0-08-095975-7.01310-3 · Cited by 31 · see citing works
Genomic, phylogenetic, and cell biological insights into metazoan origins
Nichols, S. A., Dayel, M. J., & King, N. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0003 · Cited by 24 · see citing works
- Authors
- Yin, L., Zhu, M., Knoll, A. H., Yuan, X., Zhang, J., & Hu, J.
- Affiliations
- Chinese Academy of Sciences (CN)
- Harvard University (US)
- Corresponding author
- Yin, Leiming
- Venue
- Nature
- Published
- 2007-04
- Volume
- 446
- Issue
- 7136
- Pages
- 661-663
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2164367600
- Cited by
- 347
- References
- 7
- Citations by year
- 2026: 3 · 2025: 10 · 2024: 11 · 2023: 9 · 2022: 15 · 2021: 19 · 2020: 12 · 2019: 8 · 2018: 18 · 2017: 12 · 2016: 18 · 2015: 20 · 2014: 24 · 2013: 24 · 2012: 27
- FWCI
- 22.16
- Type
- journal article
- Language
- en
- Open access
- green
- nrs.harvard.edu
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Natural Science Foundation of China
- Chinese Academy of Sciences
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Evolutionary Biology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- Doushantuo Formation, acritarchs, delayed implantation, eukaryotic origin, phosphatization, fossil preservation, Neoproterozoic glaciation
- MeSH terms
- Animals, China, Embryo, Nonmammalian, Eukaryotic Cells, Fossils, Models, Biological, Ovum, Time Factors, Reproducibility of Results, Gammaproteobacteria, Blastula, History, Ancient
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
