Death march of a segmented and trilobate bilaterian elucidates early animal evolution

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Abstract

The origin of motility in bilaterian animals represents an evolutionary innovation that transformed the Earth system. This innovation probably occurred in the late Ediacaran period—as evidenced by an abundance of trace fossils (ichnofossils) dating to this time, which include trails, trackways and burrows1,2,3. However, with few exceptions4,5,6,7,8, the producers of most of the late Ediacaran ichnofossils are unknown, which has resulted in a disconnection between the body- and trace-fossil records. Here we describe the fossil of a bilaterian of the terminal Ediacaran period (dating to 551–539 million years ago), which we name Yilingia spiciformis (gen. et sp. nov). This body fossil is preserved along with the trail that the animal produced during a death march. Yilingia is an elongate and segmented bilaterian with repetitive and trilobate body units, each of which consists of a central lobe and two posteriorly pointing lateral lobes, indicating body and segment polarity. Yilingia is possibly related to panarthropods or annelids, and sheds light on the origin of segmentation in bilaterians. As one of the few Ediacaran animals demonstrated to have produced long and continuous trails, Yilingia provides insights into the identity of the animals that were responsible for Ediacaran trace fossils.

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Fig. 1: Body fossils and associated mortichnium of Y. spiciformis.
Fig. 2: Trace fossils produced by Y. spiciformis.
Fig. 3: Reconstruction of Y. spiciformis and its traces.

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 in Nanjing Institute of Geology and Palaeontology (accession numbers NIGP-166252 to NIGP-166258, NIGP-169870), with the exception of NIGP-169869, which is currently left on the outcrop (30° 47′ 9.5′′ N, 111° 02′ 57.6′′ E) at Wuhe village (Yichang, Hubei province, China).

References

  1. 1.

    Jensen, S., Droser, M. L. & Gehling, J. G. in Neoproterozoic Geobiology (eds Xiao, S. & Kaufman, A. J.) 115–157 (Springer, 2006).

  2. 2.

    Buatois, L. A. & Mángano, M. G. in The Trace-Fossil Record of Major Evolutionary Events, Volume 1: Precambrian and Paleozoic (eds Gabriela Mángano, M. & Buatois, L. A.) 27–72 (Springer, 2016).

  3. 3.

    Chen, Z., Chen, X., Zhou, C., Yuan, X. & Xiao, S. Late Ediacaran trackways produced by bilaterian animals with paired appendages. Sci. Adv. 4, eaao6691 (2018).

  4. 4.

    Gehling, J. G., Droser, M. L., Jensen, S. R. & Runnegar, B. N. in Evolving Form and Function: Fossils and Development (ed. Briggs, D. E. G.) 43–66 (Yale Peabody Museum, 2005).

  5. 5.

    Evans, S. D., Gehling, J. G. & Droser, M. L. Slime travelers: early evidence of animal mobility and feeding in an organic mat world. Geobiology https://doi.org/10.1111/gbi.12351 (2019).

  6. 6.

    Gehling, J. G., Runnegar, B. N. & Droser, M. L. Scratch traces of large Ediacara bilaterian animals. J. Paleontol. 88, 284–298 (2014).

  7. 7.

    Ivantsov, A. Y. Trace fossils of precambrian metazoans “Vendobionta” and “Mollusks”. Stratigr. Geol. Correl. 21, 252–264 (2013).

  8. 8.

    Ivantsov, A. Feeding traces of Proarticulata—the Vendian metazoa. Paleontol. J. 45, 237–248 (2011).

  9. 9.

    Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

  10. 10.

    dos Reis, M. et al. Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. Curr. Biol. 25, 2939–2950 (2015).

  11. 11.

    Seilacher, A. Trace Fossil Analysis (Springer, 2007).

  12. 12.

    Fedonkin, M. A., Simonetta, A. & Ivantsov, A. Y. in The Rise and Fall of the Ediacaran Biota (eds Vickers-Rich, P. & Komarower, P.) 157–179 (Geological Society of London, 2007).

  13. 13.

    Bottjer, D. J., Hagadorn, J. W. & Dornbos, S. Q. The Cambrian substrate revolution. GSA Today 10, 1–7 (2000).

  14. 14.

    Seilacher, A. & Pflüger, F. in Biostabilization of Sediments (eds Krumbein, W. E. et al.) 97–105 (Bibliotheks und Informationssystem der Carl von Ossietzky Universität, Odenburg, 1994).

  15. 15.

    Canfield, D. E. & Farquhar, J. Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proc. Natl Acad. Sci. USA 106, 8123–8127 (2009).

  16. 16.

    Tarhan, L. G. The early Paleozoic development of bioturbation—evolutionary and geobiological consequences. Earth Sci. Rev. 178, 177–207 (2018).

  17. 17.

    Condon, D. et al. U–Pb ages from the neoproterozoic Doushantuo Formation, China. Science 308, 95–98 (2005).

  18. 18.

    Okada, Y. et al. New chronological constraints for Cryogenian to Cambrian rocks in the Three Gorges, Weng’an and Chengjiang areas, South China. Gondwana Res. 25, 1027–1044 (2014).

  19. 19.

    Ekdale, A. A., Bromley, R. G. & Pemberton, S. G. Ichnology: The Use of Trace Fossils in Sedimentology and Stratigraphy (SEPM Short Course 15) (SEPM Society for Sedimentary Geology, 1984).

  20. 20.

    Droser, M. L., Gehling, J. G. & Jensen, S. in Evolving Form and Function: Fossils and Development (ed. Briggs, D. E. G.) 125–138 (Yale Peabody Museum, 2005).

  21. 21.

    Mángano, M. G. & Buatois, L. A. The Trace-Fossil Record of Major Evolutionary Events, Volume 1: Precambrian and Paleozoic (Springer, 2016).

  22. 22.

    Davis, G. K. & Patel, N. H. The origin and evolution of segmentation. Trends Cell Biol. 9, M68–M72 (1999).

  23. 23.

    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).

  24. 24.

    Budd, G. E. Why are arthropods segmented? Evol. Dev. 3, 332–342 (2001).

  25. 25.

    Minelli, A., Boxshall, G. & Fusco, G. Arthropod Biology and Evolution (Springer, 2013).

  26. 26.

    Chipman, A. D. Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. BioEssays 32, 60–70 (2010).

  27. 27.

    Dunn, F. S., Liu, A. G. & Donoghue, P. C. J. Ediacaran developmental biology. Biol. Rev. Camb. Philos. Soc. 93, 914–932 (2018).

  28. 28.

    Couso, J. P. Segmentation, metamerism and the Cambrian explosion. Int. J. Dev. Biol. 53, 1305–1316 (2009).

  29. 29.

    Gold, D. A., Runnegar, B., Gehling, J. G. & Jacobs, D. K. Ancestral state reconstruction of ontogeny supports a bilaterian affinity for Dickinsonia. Evol. Dev. 17, 315–324 (2015).

  30. 30.

    Zhao, F. et al. Orthrozanclus elongata n. sp. and the significance of sclerite-covered taxa for early trochozoan evolution. Sci. Rep. 7, 16232 (2017).

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Acknowledgements

This research was supported by Chinese Academy of Sciences (XDB26000000, XDB18000000 and QYZDJ-SSW-DQC009), National Key Research and Development Program of China (2017YFC0603101), National Natural Science Foundation of China (41372009), National Science Foundation (EAR-1528553) and National Geographic Society (9564-14).

Author information

All authors participated in field work and fossil analysis. Z.C. photographed specimens. S.X. and Z.C. prepared figures and wrote manuscript with input from X.Y. and C.Z.

Correspondence to Xunlai Yuan or Shuhai Xiao.

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Competing interests

The authors declare no competing interests.

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Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Peer review information Nature thanks Marc Laflamme, Rachel Wood and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Fig. 1 Geological map and stratigraphic column.

a, Generalized geological map of the Yangtze Gorges area, showing the distribution of Ediacaran strata and the fossil location at Wuhe village (triangle). b, Stratigraphic column of the Ediacaran Doushantuo and Dengying Formations, showing stratigraphic occurrences of fossils (including Yilingia (triangle)). Fm, Formation; HMJ, Hamajing Member; Mbr, Member; SSF, small shelly fossil. Radiometric dates have previously been published17,18.

Extended Data Fig. 2 Descriptive terminology for Y. spiciformis.

Anterior and posterior designations are inferred from association with a mortichnium (Fig. 1f).

Extended Data Fig. 3 Measurements.

a, Maximum width versus preserved length of body fossils and associated trace fossils of Y. spiciformis. b, Trunk width versus segment length of body fossils of Y. spiciformis (n = 29). Trunk width and segment length of each specimen are averaged over multiple measurements made along the length of the specimen. Nt, number of trace fossil specimens (13); Nb, number of body fossil specimens (35); R, Pearson’s correlation coefficient between segment length and trunk width. Source data

Extended Data Fig. 4 Body fossils of Y. spiciformis showing dorsoventral differentiation.

a, Convex cast on bed top, showing dorsal characters (specimen NIGP-166252). Note the possible podomere-like segments (white arrows) in lateral lobes. b, Specimen (NIGP-166254) collected as a float with unknown stratigraphic orientation. Note the possible podomere-like segments (white arrows) in lateral lobes and lateral levee (bottom right) probably produced by the animal. c, Convex cast on bed sole (specimen NIGP-166258), showing ventral characters with posterior end on the right end. d, Convex cast on bed sole (specimen NIGP-166253), showing ventral characters with posterior end on the left end. The illustrated specimens were selected from a total of 48 specimens in the collection. Scale bars, 2 cm.

Extended Data Fig. 5 Nearly complete specimens of Y. spiciformis.

a, b, Part and counterpart (specimen NIGP-169869), preserving dorsal features with anterior end to the left in a. c, Specimen (NIGP-169870) preserved as convex relief, and tapering gradually towards the anterior end to the right. Specimen was collected as a float with unknown stratigraphic orientation. The illustrated specimens were selected from a total of 48 specimens in the collection. Scale bars, 2 cm.

Extended Data Fig. 6 Key specimens that support the morphological reconstruction of Y. spiciformis.

a, A nearly complete specimen (NIGP-169869), preserving dorsal features as concave relief on bed sole, anterior end to the right. b, Posterior end preserving ventral features as convex relief on bed sole (specimen NIGP-166258). Note the narrow central lobes and rod-like structures at terminus. c, Dorsal features preserved as convex relief on bed top (specimen NIGP-166252), showing details of central and lateral lobe. d, Specimen that gradually tapers towards the anterior end to the right (NIGP-169870). e, Reconstruction, dorsal view. f, Detail of central and lateral lobes, dorsal view. g, Details of central and lateral lobes, ventral view. Note that the lateral lobes are tucked beneath the central lobes, and that the central lobes therefore appear narrower on the ventral side than on the dorsal side. h, Hypothesized transverse cross-section. The illustrated specimens were selected from a total of 48 specimens in the collection. Scale bars, 2 cm.

Extended Data Fig. 7 Y. spiciformis and mortichnium.

a, A body fossil (specimen NIGP-166253) preserved as convex relief on bed sole (thus preserving ventral features) and associated with a mortichnium. Note the presence of smaller Helminthoidichnites-like trace fossils (Ht, white arrowheads) preserved as negative hyporeliefs, as well as two poorly preserved specimens of Y. spiciformis (white arrows). b, Enlargement of white rectangle in a, showing body fossil (BF), trace fossil (TF), lateral grooves (arrow) and Helminthoidichnites-like trace fossil. c, Counterpart of b on bed top. d, Close-up of yellow rectangle in a, showing the truncation of primary sediment structures and Helminthoidichnites-like trace fossil. The illustrated specimens were selected from a total of 48 specimens in the collection. Scale bars, 5 cm.

Extended Data Fig. 8 Additional trace fossil produced by Y. spiciformis (specimen NIGP-166256).

a, b, Part and counterpart, with lateral grooves in a (inferred bed sole) and corresponding levees in b (arrows; inferred to be bed top). This specimen was collected in situ, but stratigraphic orientation was not marked at the time of collection. Stratigraphic orientation was inferred on the basis that bed top was exposed (and thus more weathered than the bed sole). c, d, Enlargements of the white rectangles in a, showing lateral grooves (white arrows, c), impression of trilobate segments (c, possibly a resting trace) similar to those of Y. spiciformis, and truncation of a poorly preserved fossil (white arrow, d). The illustrated specimens were selected from a total of 48 specimens in the collection. Scale bars, 2 cm (a, b), 1 cm (c, d).

Supplementary information

Supplementary Information

This file contains the geological setting and detailed fossil description.

Reporting Summary

Supplementary Table

This file contains the measurment of Yilingia and related trace fossils (specimen number = 48).

Source data

Source Data Extended Data Fig. 3

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