Abstract
The early history of deuterostomes, the group composed of the chordates, echinoderms and hemichordates1, is still controversial, not least because of a paucity of stem representatives of these clades2,3,4,5. The early Cambrian microscopic animal Saccorhytus coronarius was interpreted as an early deuterostome on the basis of purported pharyngeal openings, providing evidence for a meiofaunal ancestry6 and an explanation for the temporal mismatch between palaeontological and molecular clock timescales of animal evolution6,7,8. Here we report new material of S. coronarius, which is reconstructed as a millimetric and ellipsoidal meiobenthic animal with spinose armour and a terminal mouth but no anus. Purported pharyngeal openings in support of the deuterostome hypothesis6 are shown to be taphonomic artefacts. Phylogenetic analyses indicate that S. coronarius belongs to total-group Ecdysozoa, expanding the morphological disparity and ecological diversity of early Cambrian ecdysozoans.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The data that support the findings of this study are available in the paper and its Supplementary Information, or from the corresponding authors upon reasonable request. All specimens illustrated in this paper are deposited at the University Museum of Chang’an University (accession numbers UMCU2014001–2014005, 2016006–2016010, 2018011–2018015, 2019016–2019020 and 2020021–2020025), and at the Department of Earth Sciences, Freie Universität Berlin (accession numbers He22-45, He22-57, He22-94, KYuan26, KYuan55 and KYuan102). Tomographic data are freely available from the University of Bristol data repository, data.bris, at https://doi.org/10.5523/bris.2iha22zobeher2leh936xrktqx.
Code availability
The phylogenetic dataset, commands, and topological constraints necessary to run the MrBayes analyses are included as NEXUS formatted files in the Supplementary Information.
Change history
01 September 2022
In the version of this article initially published, the NEXUS files necessary to run the MrBayes analyses were omitted and have now been amended to the online version of the article.
References
Peterson, K. J. & Eernisse, D. J. The phylogeny, evolutionary developmental biology, and paleobiology of the Deuterostomia: 25 years of new techniques, new discoveries, and new ideas. Org. Divers. Evol. 16, 401–418 (2016).
Gee, H. On being vetulicolian. Nature 414, 407–408 (2001).
Aldridge, R. J., Hou, X., Siveter, D. J., Siveter, D. J. & Gabbott, S. E. The systematics and phylogenetic relationships of vetulicolians. Palaeontology 50, 131–168 (2007).
Topper, T. P., Guo, J., Clausen, S., Skovsted, C. & Zhang, Z. A stem group echinoderm from the basal Cambrian of China and the origins of Ambulacraria. Nat. Commun. 10, 1366 (2019).
Zamora, S. et al. Re-evaluating the phylogenetic position of the enigmatic early Cambrian deuterostome Yanjiahella. Nat. Commun. 11, 1286 (2020).
Han, J., Conway Morris, S., Ou, Q., Shu, D. & Huang, H. Meiofaunal deuterostomes from the basal Cambrian of Shaanxi (China). Nature 542, 228–231 (2017).
Rahman, I. A. Tiny fossils in the animal family tree. Nature 542, 170–171 (2017).
Gee, H. A (Very) Short History of Life on Earth: 4.6 Billion Years in 12 Pithy Chapters (Pan Macmillan, 2021).
Peng, S., Babcock, L. E. & Ahlberg, P. in Geological Time Scale 2020 (eds Gradstein, F. M. et al.) 565–629 (Elsevier, 2020).
Lowe, C. J., Clarke, D. N., Medeiros, D. M., Rokhsar, D. S. & Gerhart, J. The deuterostome context of chordate origins. Nature 520, 456–465 (2015).
Hejnol, A. & Martín-Durán, J. M. Getting to the bottom of anal evolution. Zool. Anz. 256, 61–74 (2015).
Shu, D. & Han, J. The core value of Chengjiang fauna: the formation of the animal kingdom and the birth of basic human organs. Earth Sci. Front. 27, 382–412 (2020).
Liu, Y., Zhang, H., Xiao, S., Shao, T. & Duan, B. An early Cambrian ecdysozoan with a terminal mouth but no anus. Preprint at bioRxiv https://doi.org/10.1101/2020.09.04.283960 (2020).
Shao, T. et al. Diversity of cnidarians and cycloneuralians in the Fortunian (early Cambrian) Kuanchuanpu Formation at Zhangjiagou, South China. J. Paleontol. 92, 115–129 (2018).
Steiner, M., Li, G., Qian, Y. & Zhu, M. Lower Cambrian small shelly fossils of northern Sichuan and southern Shaanxi (China), and their biostratigraphic importance. Geobios 37, 259–275 (2004).
Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006).
Xiao, S. & Schiffbauer, J. D. in From Fossils to Astrobiology (eds Seckbach, J. & Walsh, M.) 89–117 (Springer-Verlag, 2009).
Nielsen, C. Animal Evolution: Interrelationships of the Living Phyla (Oxford Univ. Press, 2012).
Hejnol, A. & Martindale, M. Q. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456, 382–386 (2008).
Shu, D. et al. Primitive deuterostomes from the Chengjiang Lagerstätte (Lower Cambrian, China). Nature 414, 419–424 (2001).
Shu, D., Conway Morris, S., Han, J., Zhang, Z. & Liu, J. Ancestral echinoderms from the Chengjiang deposits of China. Nature 430, 422–428 (2004).
Zhao, Y. et al. Cambrian sessile, suspension feeding stem-group ctenophores and evolution of the comb jelly body plan. Curr. Biol. 29, 1112–1125 (2019).
Sun, H. et al. Hyoliths with pedicles illuminate the origin of the brachiopod body plan. Proc. R. Soc. B 285, 7 (2018).
Vinther, J. & Parry, L. A. Bilateral jaw elements in Amiskwia sagittiformis bridge the morphological gap between gnathiferans and chaetognaths. Curr. Biol. 29, 881–888 (2019).
Bekkouche, N. & Worsaae, K. Nervous system and ciliary structures of Micrognathozoa (Gnathifera): evolutionary insight from an early branch in Spiralia. R. Soc. Open Sci. 3, 17 (2016).
Hejnol, A. & Lowe, C. J. Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution. Phil. Trans. R. Soc. B 370, 16 (2015).
Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
Kapli, P. & Telford, M. J. Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Sci. Adv. 6, 11 (2020).
Kapli, P. et al. Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria. Sci. Adv. 7, eabe2741 (2021).
Peterson, K. J. & Eernisse, D. J. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol. Dev. 3, 170–205 (2001).
Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009).
Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P. & Nieves-Aldrey, J. L. Bayesian phylogenetic analysis of combined data. Syst. Biol. 53, 47–67 (2004).
Gostling, N. J., Dong, X.-P. & Donoghue, P. C. J. Ontogeny and taphonomy: An experimental taphonomy study of the development of the brine shrimp Artemia salina. Palaeontology 52, 169–186 (2009).
Liu, Y., Xiao, S., Shao, T., Broce, J. & Zhang, H. The oldest known priapulid-like scalidophoran animal and its implications for the early evolution of cycloneuralians and ecdysozoans. Evol. Dev. 16, 155–165 (2014).
Liu, Y. et al. New armoured scalidophorans (Ecdysozoa, Cycloneuralia) from the Cambrian Fortunian Zhangjiagou Lagerstätte, South China. Pap. Palaeontol. 5, 241–260 (2019).
Shao, T. et al. New macrobenthic cycloneuralians from the Fortunian (lowermost Cambrian) of South China. Precambrian Res. 349, 105413 (2020).
Zhang, H. et al. Armored kinorhynch-like scalidophoran animals from the early Cambrian. Sci Rep. 5, 16521 (2015).
Zhang, H., Maas, A. & Waloszek, D. New material of scalidophoran worms in Orsten-type preservation from the Cambrian Fortunian Stage of South China. J. Paleontol. 92, 14–25 (2018).
Steiner, M., Qian, Y., Li, G., Hagadorn, J. W. & Zhu, M. The developmental cycles of early Cambrian Olivooidae fam. nov. (?Cycloneuralia) from the Yangtze Platform (China). Palaeogeogr. Palaeoclimatol. Palaeoecol. 398, 97–124 (2014).
Steiner, M., Li, G., Qian, Y., Zhu, M. & Erdtmann, B.-D. Neoproterozoic to early Cambrian small shelly fossil assemblages and a revised biostratigraphic correlation of the Yangtze Platform (China). Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 67–99 (2007).
Marone, F., Studer, A., Billich, H., Sala, L. & Stampanoni, M. Towards on-the-fly data post-processing for real-time tomographic imaging at TOMCAT. Adv. Structural Chem. Imaging 3, 1 (2017).
Lewis, P. O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50, 913–925 (2001).
Acknowledgements
This work was supported by National Natural Science Foundation of China (nos. 41872014, 42172020 and 41972026, Research Fund for International Senior Scientists 2021), Strategic Priority Research Program of Chinese Academy of Sciences (no. XDB26000000), State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences (no. 20191104). E.C. was supported by a University of Bristol Scholarship; M.S. was funded by Deutsche Forschungsgesellschaft (STE814/5-1); S.X. was supported by the U.S. National Science Foundation (EAR-2021207); P.C.J.D. was funded by Natural Environment Research Council (NERC) grant (NE/P013678/1), part of the Biosphere Evolution, Transitions and Resilience (BETR) programme, which is co-funded by the Natural Science Foundation of China (NSFC), as well as the Leverhulme Trust (RF-2022-167). We acknowledge the Paul Scherrer Institut, Villigen, Switzerland for provision of synchrotron radiation beamtime at the TOMCAT beamline of the SLS. We thank D. Yang for assistance with artistic reconstructions and F. Dunn for data that contributed to our phylogenetic analyses.
Author information
Authors and Affiliations
Contributions
H.Z. and P.C.J.D. designed the research. Y.L., T.S., B.Y. and M.S. obtained the fossils. H.Z. and M.S. carried out SEM work. E.C., F.M. and P.C.J.D. collected SRXTM data. E.C. and B.D. analysed SRXTM data. E.C. and P.C.J.D. conducted phylogenetic analyses. H.Z., E.C., S.X., M.S. and P.C.J.D. developed the interpretation. H.Z. wrote the first draft of the manuscript, with contributions from all other authors.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature thanks the anonymous reviewers for their contribution to the peer review of this work.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
Extended Data Fig. 1 Location map and stratigraphic column.
a, map of Shaanxi Province, South China, with star marking Zhangjiagou section and hexagon marking Shizhonggou section where fossils of Saccorhytus coronarius were collected; b, detailed map of southern Shaanxi Province showing Zhangjiagou section (star) and Shizhonggou section (hexagon); c, stratigraphic column of Zhangjiagou section showing key horizon (arrow) where fossils of Saccorhytus coronarius were collected.
Extended Data Fig. 2 Saccorhytus coronarius.
a–c, UMCU2014005, with five large protuberances; a, apertural or anterior view; b, abapertural or posterior view; c, SRXTM image, virtual transverse section marked in b; d–g, UMCU2014001, with three large protuberances; d, apertural or anterior view; e, abapertural or posterior view; f, g, detail of circumapertural protuberances. Scale bar: 200 μm (a–e), 50 μm (f), 40 μm (g). See Fig. 1 for abbreviations.
Extended Data Fig. 3 Saccorhytus coronarius.
a–c, UMCU2014001, same specimen as in Extended Data Fig. 2d; a, dorso-anterior view (assuming an anterior mouth and dorsal large protuberances); b, ventral view (assuming an anterior mouth and dorsal large protuberances); c, SRXTM image, virtual longitudinal section marked in a, with arrows marking boundary between two integument layers; d–i, UMCU2014002; d, left view; e, right view; f, SRXTM image, virtual tangential coronal section marked in d; g, close-up of sixth left body cone in central right of d; h, detail of small abapertural spines and chevron patterns in lower right of d; i, detail of fourth, fifth, and sixth right body cones in upper central of e. Scale bar: 200 μm (a, b, d, e); 100 μm (c, f); 40 μm (g, h), 60 μm (i). See Fig. 1 for abbreviations.
Extended Data Fig. 4 Saccorhytus coronarius.
a, b, UMCU2019017, with two large protuberances; a, apertural or anterior view; b, abapertural or posterior view; c, UMCU2016006, with four large protuberances, antero-left view; d, e, UMCU2020022; d, left view; e, detail of seventh right body cone and chevron pattern in central right of d; f, g, UMCU2020023; f, left view; g, detail of circumapertural protuberances in central left of f; h, UMCU2018013, with two large protuberances, antero-left view; i–k, UMCU2020024; i, right ventral view (assuming an anterior mouth and dorsal large protuberances); j, left dorsal view (assuming an anterior mouth and dorsal large protuberances); k, detail of fourth left body cone in central of j. Scale bar: 200 μm (a–d, f, h–j), 40 μm (e, g, k). See Fig. 1 for abbreviations.
Extended Data Fig. 5 Saccorhytus coronarius.
a, b, UMCU2014004, with only one large protuberance; a, anterior dorsal view (assuming an anterior mouth and dorsal large protuberances); b, abapertural or posterior view; c, d, UMCU2018014, with four large protuberances; c, right view; d, left view; e, f, same specimen as shown in Fig. 1a–e, UMCU2016009; e, close-up view of central right of Fig. 1d, with arrow indicating the two tightly adpressed integument layers and rectangle marking area enlarged in f, which illustrates randomly oriented nanometer-scale apatite crystals. Scale bar: 200 μm (a–d), 25 μm (e), 1 μm (f). See Fig. 1 for abbreviations.
Extended Data Fig. 6 Saccorhytus coronarius.
a–c, UMCU2016007, with two large protuberances; a, apertural or anterior view; b, abapertural or posterior view; c, detail of circumapertural protuberances in central right of a; d–g, UMCU2019019, with two large protuberances; d, apertural or anterior view; e, abapertural or posterior view; f, g, detail of fourth and fifth right body cones in central upper and upper right of e; h, i, UMCU2018012, same specimen as in Fig. 3j; h, left view; i, detail of fourth, fifth, and sixth left body cones in upper left of h. Scale bar: 200 μm (a, b, d, e, h), 20 μm (c, f, g, i). See Fig. 1 for abbreviations.
Extended Data Fig. 7 Saccorhytus coronarius.
a–c, UMCU2016008, same specimen as in Fig. 3f, with three large protuberances; a, detail of fourth, fifth, and sixth left body cones in central upper of Fig. 3f; b, right view; c, detail of fifth and sixth right body cones in upper left of b; d, UMCU2019020, a fragment with five large protuberances, dorsal anterior view (assuming an anterior mouth and dorsal large protuberances); e, h, UMCU2020025; e, left view; h, detail of fourth and fifth left body cones, exhibiting round conical bases with longitudinal folds; f, g, UMCU2018015, with two large protuberances; f, apertural or anterior view; g, abapertural or posterior view. Scale bar: 60 μm (a), 200 μm (b, d–g), 50 μm (c, h). See Fig. 1 for abbreviations.
Extended Data Fig. 8 Saccorhytus coronarius.
a, UMCU2018015, same specimen as in Extended Data Fig. 7f, exhibiting radial folds and large protuberances; b, d, UMCU2019018, same specimen as in Fig. 3l, with two large protuberances; b, ventral anterior view (assuming an anterior mouth and dorsal large protuberances); d, detail of fourth and fifth right body cones in central upper of Fig. 3l; c, e, f, UMCU2014003, a fragment with two large protuberances; c, apertural or anterior view; e, detail of circumapertural protuberances and large protuberances; f, abapertural or posterior view. Scale bar represents 100 μm in all images. See Fig. 1 for abbreviations.
Extended Data Fig. 9 Saccorhytus coronarius from Kuanchuanpu Formation at Shizhonggou section.
a–d, body surface with regular rows of small abapertural spines; a, b, KYuanH102; a, abapertural or posterior view; b, virtual section through a body cone as denoted in surface model, showing inner and outer integument layers; c, d, KYuan26; c, lateral view; d, virtual section through a body cone as denoted in surface model; e, f, KYuan55; e, anterior ventral view (assuming an anterior mouth and dorsal large protuberances); f, close-up view, showing small abapertural spines and chevron patterns. Scale bar: 200 μm (a, c, e), 50 μm (b), 100 μm (d), 40 μm (f). See Fig. 1 for abbreviations.
Extended Data Fig. 10 Phylogenetic positioning of Saccorhytus.
a, partially constrained tree where constraint is compatible with monophyletic Lophotrochozoa; b, partially constrained tree where constraints are compatible with monophyletic Lophotrochozoa, paraphyletic Coelenterata and monophyletic Deuterostomia + Xenacoelomorpha; c, partially constrained tree where constraints are compatible with monophyletic Lophotrochozoa, paraphyletic Coelenterata and paraphyletic Deuterostomia. Nodal supports are posterior probabilities. In all trees, Saccorhytus is resolved as part of a polytomy at the base of Ecdysozoa. Animal icons from phylopic.org.
Supplementary information
Supplementary Information
This file contains supplementary sections including systematic palaeontology, supplementary phylogenetic analyses, descriptions of characters used in the phylogenetic analysis, supplementary animations, Table 1 and references
Supplementary Video 1
SRXTM video based on volume rendition of specimen UMCU2014005 (Extended Data Fig. 2a).
Supplementary Video 2
Three-dimensional animation showing the general morphology of S. coronarius.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, Y., Carlisle, E., Zhang, H. et al. Saccorhytus is an early ecdysozoan and not the earliest deuterostome. Nature 609, 541–546 (2022). https://doi.org/10.1038/s41586-022-05107-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41586-022-05107-z
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.