Cited by 259Paleontology and Stratigraphy of FossilsPaleontology and Evolutionary BiologyEvolution and Paleontology Studies

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Eumetazoan fossils in terminal Proterozoic phosphorites?

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Xiao, Shuhai, Yuan, Xunlai, Knoll, Andrew H.·2000·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.250491697PMC PMC17636

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Abstract

Phosphatic sedimentary rocks preserve a record of early animal life different from and complementary to that provided by Ediacaran fossils in terminal Proterozoic sandstones and shales. Phosphorites of the Doushantuo Formation, South China, contain eggs, egg cases, and stereoblastulae that document animals of unspecified phylogenetic position; small fossils containing putative spicules may specifically record the presence of sponges. Microfossils recently interpreted as the preserved gastrulae of cnidarian and bilaterian metazoans can alternatively be interpreted as conventional algal cysts and/or egg cases modified by diagenetic processes known to have had a pervasive influence on Doushantuo phosphorites. Regardless of this interpretation, evidence for Doushantuo eumetazoans is provided by millimeter-scale tubes that display tabulation and apical budding characteristic of some Cnidaria, especially the extinct tabulates. Like some Ediacaran remains, these small, benthic, colonial fossils may represent stem-group eumetazoans or stem-group cnidarians that lived in the late Proterozoic ocean.

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The Unique Invention of the Siliceous Sponges: Their Enzymatically Made Bio-Silica Skeleton
Müller, W. E. G., Wang, X., Chen, A., Hu, S., Gan, L., Schröder, H. C., Schloßmacher, U., & Wiens, M. (2011) · Progress in molecular and subcellular biology · doi:10.1007/978-3-642-21230-7_9 · Cited by 14
“Between these two major ice ages, the multicellular animals (Knoll and Carroll 1999) evolved among which only the sponges (Porifera) developed, a genetic repertoire that allowed the survival through those adverse events until today (Xiao et al. 2000); hence, these animals were termed “living fossils” (M€uller 1998; se…”
Background
Diversification of the Metazoa: Ediacarans, colonies, and the origin of eumetazoan complexity by nested modularity
Dewel, R. A., Dewel, W. C., & McKinney, F. K. (2001) · Historical Biology · doi:10.1080/10292380109380592 · Cited by 14
Ecological constraints on the origin of neurones
Monk, T., Paulin, M. G., & Green, P. (2015) · Journal of Mathematical Biology · doi:10.1007/s00285-015-0862-7 · Cited by 12
“There is no body fossil or trace fossil evidence to support the existence of bilaterians before 560 MYa (Budd and Jensen 2000; Droser et al. 2006; Jensen 2003; Liu et al. 2010; Seilacher et al. 2005; Xiao et al. 2000; Xiao and Laflamme 2008).”
Background
Comparative taphonomy and phylogenetic signal of phosphatized Weng’an and Kuanchuanpu Biotas
Bottjer, D. J., Yin, Z., Zhao, F., & Zhu, M. (2019) · Precambrian Research · doi:10.1016/j.precamres.2019.105408 · Cited by 12
The Cambrian radiation of bilaterians: Evolutionary origins and palaeontological emergence; earth history change and biotic factors
Lieberman, B. S. (2007) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2007.05.021 · Cited by 13
“…of metazoan embryos (Xiao et al., 1998; Steiner et al., 2004; Chen et al., 2006), with recognition of their possible triploblastic character (Xiao et al., 2000; Chen et al., 2006); analyses revealing the nature of ecological changes during the early and Middle Cambrian (Bottjer et al.,…”
Deciphering deuterostome phylogeny: molecular, morphological, and palaeontological perspectives
Smith, A. B., & Swalla, B. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0009 · Cited by 13
The evolution of nervous system centralization
Arendt, D., Denes, A. S., Jékely, G., & Tessmar‐Raible, K. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0007 · Cited by 12
Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian (Ediacaran) Weng’an and Early Cambrian Maotianshan Biotas, China
Chen, J.-Y. (2012) · Earth and Life · doi:10.1007/978-90-481-3428-1_10 · Cited by 17
“1) yield diverse metazoans, including sponges (Li et al. 1998), cnidarians (Chen et al. 2000, 2002a; Xiao et al. 2000), and bilateral animals and their related embryos (Chen et al. 2004b; Chen et al. 2006)”.”
Background
A high-resolution chemostratigraphy of post-Marinoan Cap Carbonate using drill core samples in the Three Gorges area, South China
Sato, H., Tahata, M., Sawaki, Y., Maruyama, S., Yoshida, N., Shu, D., Han, J., Li, Y., & Komiya, T. (2015) · Geoscience Frontiers · doi:10.1016/j.gsf.2015.07.008 · Cited by 11
“In addition, the strata are famous for their many fossils, including animal embryos, algae, acritarchs and sponges (Xiao et al., 1998, 2000; Xiao and Knoll, 2000; Yin et al., 2007; Zhou et al., 2007; McFadden et al., 2008; Du et al., 2015; Yin et al., 2015).”
Background
New observations of the ornamented Doushantuo embryo fossils from the Ediacaran Weng’an Biota, South China
Yin, Z. J., & Zhu, M. (2012) · Bulletin of Geosciences · doi:10.3140/bull.geosci.1234 · Cited by 11
The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records
Peterson, K. J., Cotton, J. A., Gehlîng, J. G., & Pisani, D. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0002 · Cited by 12
Analysis of fluorescence from algae fossils of the Neoproterozoic Doushantuo formation of China by confocal laser scanning microscope
Chi, H., Xiao, Z., Fu, D., & Lu, Z. (2006) · Microscopy Research and Technique · doi:10.1002/jemt.20295 · Cited by 11
“This preserved biota also includes the ancient animal egg fossils, algae fossils, and adult animal fossils (Chen at al., 2000, 2002, 2004; Xiao et al., 1998b, 2000).”
Background
Internal Structure of Cambrian Fossil Embryo Markuelia Revealed in the Light of Synchrotron Radiation X‐ray Tomographic Microscopy
Gong, C., Fan, P., Duan, B., & Xiping, D. (2011) · Acta Geologica Sinica - English Edition · doi:10.1111/j.1755-6724.2011.00381.x · Cited by 11
The phosphorus cycle and biological pump in Earth’s middle age: Reappraisal of the “Boring Billion”
Huang, T., Wang, R., & Shen, B. (2022) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/tb-2021-1168 · Cited by 10
Chapter 4 Global distributional dynamics of Cambrian clades as revealed by Burgess Shale-type deposits
Hendricks, J. R. (2013) · Geological Society London Memoirs · doi:10.1144/m38.4 · Cited by 10
“The five Precambrian groups include cyanobacteria, chlorophyta, rhodophyta, porifera and cnidaria (for evidence, see Knoll 1992; Gehling & Rigby 1996; Knoll & Carroll 1999; Li et al. 1998; Xiao et al. 2000; Xiao & Dong 2006; Maloof et al. 2010).”
Background
A Web of Controversies: Complexity in the Burgess Shale Debate
Baron, C. (2010) · Journal of the History of Biology · doi:10.1007/s10739-010-9248-2 · Cited by 10
Vestiges of a beginning? Paleontological and geochemical constraints on early animal evolution
Knoll, A. H. (2003) · Annales de Paléontologie · doi:10.1016/j.annpal.2003.07.002 · Cited by 10
Self-citation
Neoproterozoic Stratigraphy, Depositional Environments and Hydrocarbon Source-Reservoir-Seal Bed Assemblage in South China
Zhu, M., Zhang, J., Yang, A., Li, G., Zhao, F., Miao, L., Yin, Z., Miao, L., & Hu, C. (2022) · Springer geology · doi:10.1007/978-981-19-5666-9_5 · Cited by 9
New Data of Phosphatized Microfossils from the Doushantuo Formation in Baizhu,Baokang County,Hubei Province,and Their Stratigraphic Implications
Yin, C., Liu, P., Gao, L., Tang, F., & Chen, S. (2009) · Acta Geoscientica Sinica · Cited by 9
Invertebrate Problematica: kinds, causes, and solutions
Jenner, R. A., Timothy, D. J., & Littlewood, D. T. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0011 · Cited by 7
Tubular microfossils from the Ediacaran Weng’an Biota (Doushantuo Formation, South China) are not early animals
Sun, W., Yin, Z., Donoghue, P. C. J., Liu, P., Shang, X., & Zhu, M. (2019) · Palaeoworld · doi:10.1016/j.palwor.2019.04.004 · Cited by 8
Geobiological Events in the Ediacaran Period
Xiao, S. (2008) · The Paleontological Society Papers · doi:10.1017/s1089332600001625 · Cited by 8
Self-citation
Are the new Ediacaran Doushantuo Megasphaera -like acritarchs early metazoans?
Tang, B. L. (2015) · Palaeoworld · doi:10.1016/j.palwor.2015.06.005 · Cited by 8
Localization and Characterization of Ferritin in Demospongiae: A Possible Role on Spiculogenesis
Natálio, F., Wiese, S., Friedrich, N., Werner, P., & Tahir, M. N. (2014) · Marine Drugs · doi:10.3390/md12084659 · Cited by 7
Microtubular metazoan fossils with multi-branches in Weng’an biota
Liu, P., Yin, C., & Tang, F. (2006) · Chinese Science Bulletin · doi:10.1007/s11434-006-0630-6 · Cited by 7
The Evolutionary Origin of Nervous Systems and Implications for Neural Computation
Monk, T. (2014) · Otago University Research Archive (University of Otago) · Cited by 7
Symbiogeny and the Evolution of Tissues: The Hypothesis
Shostak, S. (2015) · Biological Systems Open Access · doi:10.4172/2329-6577.1000127 · Cited by 6
“The obvious interpretation of the spheroids, namely, that they were the eggs and embryos of metazoans had its supporters [21, 23-29] and detractors [22, 30–33].”
Background
Genesis of Silica‐phosphatic Nodules with Small Shelly Fossils Preserved in the Lowermost Cambrian of South China
Qiu, H., Feng, L., Chu, X., Li, L., Zhang, X., & Li, J. (2022) · Acta Geologica Sinica - English Edition · doi:10.1111/1755-6724.14924 · Cited by 6
“…great interest not only because of their economic value, but also because they provide an unusually clear window on Ediacaran-Cambrian life and environments (Zhang et al., 1998; Xiao et al., 2000, 2010, 2014; Yin et al., 2007; Jiang et al., 2007; Muscente et al., 2015; Bottjer et al., 2020).”
Background
Animal Evolution
(2009) · doi:10.1093/acprof:oso/9780199549429.001.0001 · Cited by 7
The earliest fossil record of the animals and its significance
Budd, G. E. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0001 · Cited by 6
Problematic tubular fossils from the Portfjeld Formation (Ediacaran) of North Greenland
Willman, S., & Peel, J. S. (2022) · Journal of Paleontology · doi:10.1017/jpa.2022.43 · Cited by 5
“Some Sinocyclocyclicus (Xiao et al., 2000, ﬁ g. 2 H, I) are morphologically similar to the fossils described herein.”
The rise of bilaterians: a reply
Xiao, S., Kowalewski, M., Shen, B., Dong, L., & Laflamme, M. (2009) · Historical Biology · doi:10.1080/08912960903471659 · Cited by 5
“However, Doushantuo sponges (Li et al. 1998), cnidarians (Chen et al. 2000) and bilaterians (Chen et al. 2004) have been called into question (Xiao et al. 2000; Yin et al. 2001; Bengtson and Budd 2004; Hagadorn et al. 2006), an issue that will be further examined in the following section.”
BackgroundSelf-citation
Life on Mars: Clues, Evidence or Proof?
Rizzo, V., Armstrong, R. A., Hua, H., Cantasano, N., Nicolò, T., & Bianciardi, G. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.95531 · Cited by 4
Research Progress of Ediacaran (Sinian) Biostratigraphy in South China
Liu, P., Yin, C., & Tang, F. (2022) · Springer geology · doi:10.1007/978-981-19-5666-9_4 · Cited by 4
A simulation experiment on phosphatized spherical microfossils
Zhang, J., & Hua, H. (2013) · Chinese Science Bulletin · doi:10.1007/s11434-013-0002-y · Cited by 4
Application of Atomic Force Microscopy on Observing the Ultra‐Fine Structure of the Neoproterozoic Microfossils from China
Chi, H., Xiao, Z., Chen, J., & Lu, Z. (2007) · Scanning · doi:10.1002/sca.20008 · Cited by 4
The evolution of developmental gene networks: lessons from comparative studies on holometabolous insects
Peel, A. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0016 · Cited by 4
Caracterização tafonômica e estratigráfica de Cloudina lucianoi (Beurlen & Sommer, 1957) Zaine & Faircild, 1985, no Grupo Corumbá, ediacarano do sudeste do Brasil
Meira, F. V. E. (2011) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.44.2011.tde-28092012-153037 · Cited by 4
Phosphatized embryo-like fossils from the Chang 73 sub-member, middle-upper Triassic Yanchang Formation, Ordos Basin, northwest China: Affinity, preservation and paleoecological implications
Gan, D., Dong, J., Yang, W., Liu, W., Gao, T., Wang, J., Bian, C., Xie, L., Li, Y., Liu, J., et al. (2025) · Marine and Petroleum Geology · doi:10.1016/j.marpetgeo.2025.107531 · Cited by 3
Characterization and Biological Performance of Marine Sponge Collagen
Fernandes, K. R., Parisi, J. R., Cruz, M. D. A., Gabbai‐Armelin, P. R., de Araújo, T. A. T., Santana, A. D. F., Avanzi, I. R., Silva‐Freitas, F. R., Ribeiro, A. M., do Vale, G. C. A., et al. (2021) · Brazilian Archives of Biology and Technology · doi:10.1590/1678-4324-2021200592 · Cited by 3
Diversity of organic-walled microfossils in the phosphates of the ca. 1-Ga Diabaig Formation, Torridon Group, NW Scotland
Dzul, E. R., Loron, C., Agić, H., Donaldson, S., Knoll, P., & McMahon, S. (2025) · Journal of Paleontology · doi:10.1017/jpa.2025.10119 · Cited by 3
“…the Ediacaran Weng ’ an biota from the lower Doushantuo Formation of South China (ca. 600 – 582 Ma) contains exceptionally preserved examples of complex organisms such as multicellular algae, tubular microfossils of putative metazoans, and possibly early-stage embryos (Xiao et al., 2000, 2014).”
The Nano Membrane-Like Structure of the Precambrian Microfossils under Atomic Force Microscope (AFM)
Chi, H., Xiao, Z., & Xiao, X. X. (2007) · Diffusion and defect data, solid state data. Part B, Solid state phenomena/Solid state phenomena · doi:10.4028/www.scientific.net/ssp.121-123.739 · Cited by 3
The rise of bilaterians: a few closing comments
Xiao, S., Kowalewski, M., Shen, B., Dong, L., & Laflamme, M. (2010) · Historical Biology · doi:10.1080/08912961003784207 · Cited by 3
“The problems are the same: lack of taphonomic consideration and the lack of threedimensional information (Zhang et al. 1998; Xiao et al. 2000; Yin et al. 2001; Bengtson and Budd 2004).”
BackgroundSelf-citation
Preservation and fluorescence of the microfossils from Neoproterozoic Doushantuo formation
Chi, H., Feng, M., Xiao, Z., & Lu, Z. (2007) · Microscopy Research and Technique · doi:10.1002/jemt.20547 · Cited by 3
“However, there are still discussions about the interpretation of some fossils such as fossil embryos and small bilateral animal fossils (Bengtson and Budd, 2004; Chen et al., 2000, 2004a,b; Xiao et al., 2000).”
BackgroundInfluential
The origins and evolution of the Ecdysozoa
Telford, M. J., Bourlat, S. J., Economou, A. D., Papillon, D., & Rota‐Stabelli, O. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0008 · Cited by 4
Origins of metazoan body plans: the larval revolution
Raff, R. A. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0005 · Cited by 3
The Long March of Corals
Martin‐Garin, B., & Montaggioni, L. F. (2023) · Coral reefs of the world · doi:10.1007/978-3-031-16887-1_4 · Cited by 2
磷循环及磷组分在古海洋环境重建中的应用
Li, T., Zhu, G., Zhang, Y., & Chen, Z. (2025) · Earth Science-Journal of China University of Geosciences · doi:10.3799/dqkx.2023.202 · Cited by 2

Authors: Xiao, S., Yuan, X., & Knoll, A. H.
Affiliations: Tulane University (US)
Corresponding author: Knoll, Andrew H.
ORCID: Xiao, Shuhai
Yuan, Xunlai
Knoll, Andrew H.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2000-11-28
Volume: 97
Issue: 25
Pages: 13684-13689
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.250491697
PMC: PMC17636
OpenAlex: W2004614425
Cited by: 259
References: 31
Citations by year: 2025: 7 · 2024: 2 · 2023: 4 · 2022: 8 · 2021: 2 · 2020: 2 · 2019: 8 · 2018: 3 · 2017: 4 · 2016: 9 · 2015: 16 · 2014: 15 · 2013: 11 · 2012: 13
FWCI: 7.02
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
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, phosphate rock, early animal evolution, Ediacaran, sponge spicules, egg cases, diagenesis, tabulate corals, South China
MeSH terms: Animals, Cnidaria, Fossils, Gastrula, Minerals, Phosphates, Geologic Sediments

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