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Saccorhytus is an early ecdysozoan and not the earliest deuterostome

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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.

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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.

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.

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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.

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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.

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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

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