Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Saccorhytus is an early ecdysozoan and not the earliest deuterostome

This article has been updated

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

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Anatomy of S. coronarius.
Fig. 2: Anatomy of S. coronarius.
Fig. 3: Anatomy of S. coronarius.
Fig. 4: Reconstruction and phylogenetic interpretation of S. coronarius.

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

  1. 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).

    Article  Google Scholar 

  2. Gee, H. On being vetulicolian. Nature 414, 407–408 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. 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).

    Article  Google Scholar 

  4. 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).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zamora, S. et al. Re-evaluating the phylogenetic position of the enigmatic early Cambrian deuterostome Yanjiahella. Nat. Commun. 11, 1286 (2020).

    Article  CAS  PubMed  Google Scholar 

  6. 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).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Rahman, I. A. Tiny fossils in the animal family tree. Nature 542, 170–171 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Gee, H. A (Very) Short History of Life on Earth: 4.6 Billion Years in 12 Pithy Chapters (Pan Macmillan, 2021).

  9. Peng, S., Babcock, L. E. & Ahlberg, P. in Geological Time Scale 2020 (eds Gradstein, F. M. et al.) 565–629 (Elsevier, 2020).

  10. 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).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Hejnol, A. & Martín-Durán, J. M. Getting to the bottom of anal evolution. Zool. Anz. 256, 61–74 (2015).

    Article  Google Scholar 

  12. 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).

    Google Scholar 

  13. 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).

  14. 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).

    Article  Google Scholar 

  15. 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).

    Article  Google Scholar 

  16. Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Xiao, S. & Schiffbauer, J. D. in From Fossils to Astrobiology (eds Seckbach, J. & Walsh, M.) 89–117 (Springer-Verlag, 2009).

  18. Nielsen, C. Animal Evolution: Interrelationships of the Living Phyla (Oxford Univ. Press, 2012).

  19. Hejnol, A. & Martindale, M. Q. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456, 382–386 (2008).

    Article  ADS  CAS  PubMed  Google Scholar 

  20. Shu, D. et al. Primitive deuterostomes from the Chengjiang Lagerstätte (Lower Cambrian, China). Nature 414, 419–424 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Shu, D., Conway Morris, S., Han, J., Zhang, Z. & Liu, J. Ancestral echinoderms from the Chengjiang deposits of China. Nature 430, 422–428 (2004).

    Article  ADS  CAS  PubMed  Google Scholar 

  22. 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).

    Article  CAS  PubMed  Google Scholar 

  23. Sun, H. et al. Hyoliths with pedicles illuminate the origin of the brachiopod body plan. Proc. R. Soc. B 285, 7 (2018).

    Article  Google Scholar 

  24. 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).

    Article  CAS  PubMed  Google Scholar 

  25. 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).

    Article  Google Scholar 

  26. 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).

    Article  Google Scholar 

  27. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kapli, P. & Telford, M. J. Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Sci. Adv. 6, 11 (2020).

    Article  Google Scholar 

  29. Kapli, P. et al. Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria. Sci. Adv. 7, eabe2741 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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).

    Article  CAS  PubMed  Google Scholar 

  31. Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009).

    Article  CAS  PubMed  Google Scholar 

  32. 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).

    Article  PubMed  Google Scholar 

  33. 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).

    Article  Google Scholar 

  34. 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).

    Article  CAS  PubMed  Google Scholar 

  35. Liu, Y. et al. New armoured scalidophorans (Ecdysozoa, Cycloneuralia) from the Cambrian Fortunian Zhangjiagou Lagerstätte, South China. Pap. Palaeontol. 5, 241–260 (2019).

    Article  Google Scholar 

  36. Shao, T. et al. New macrobenthic cycloneuralians from the Fortunian (lowermost Cambrian) of South China. Precambrian Res. 349, 105413 (2020).

    Article  ADS  CAS  Google Scholar 

  37. Zhang, H. et al. Armored kinorhynch-like scalidophoran animals from the early Cambrian. Sci Rep. 5, 16521 (2015).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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).

    Article  Google Scholar 

  39. 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).

    Article  Google Scholar 

  40. 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).

    Article  Google Scholar 

  41. 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).

    Article  Google Scholar 

  42. Lewis, P. O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50, 913–925 (2001).

    Article  CAS  PubMed  Google Scholar 

Download references

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

Authors

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

Correspondence to Huaqiao Zhang, Shuhai Xiao or Philip C. J. Donoghue.

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.

ac, UMCU2014005, with five large protuberances; a, apertural or anterior view; b, abapertural or posterior view; c, SRXTM image, virtual transverse section marked in b; dg, 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 (ae), 50 μm (f), 40 μm (g). See Fig. 1 for abbreviations.

Extended Data Fig. 3 Saccorhytus coronarius.

ac, 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; di, 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; ik, 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 (ad, f, hj), 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 (ad), 25 μm (e), 1 μm (f). See Fig. 1 for abbreviations.

Extended Data Fig. 6 Saccorhytus coronarius.

ac, 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; dg, 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.

ac, 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, dg), 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.

ad, 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

Reporting Summary

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.

NEXUS files.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • 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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing