Integrated records of environmental change and evolution challenge the Cambrian Explosion

An Author Correction to this article was published on 12 April 2019

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Abstract

The ‘Cambrian Explosion’ describes the rapid increase in animal diversity and abundance, as manifest in the fossil record, between ~540 and 520 million years ago (Ma). This event, however, is nested within a far more ancient record of macrofossils extending at least into the late Ediacaran at ~571 Ma. The evolutionary events documented during the Ediacaran–Cambrian interval coincide with geochemical evidence for the modernisation of Earth’s biogeochemical cycles. Holistic integration of fossil and geochemical records leads us to challenge the notion that the Ediacaran and Cambrian worlds were markedly distinct, and places biotic and environmental change within a longer-term narrative. We propose that the evolution of metazoans may have been facilitated by a series of dynamic and global changes in redox conditions and nutrient supply, which, potentially together with biotic feedbacks, enabled turnover events that sustained multiple phases of radiation. We argue that early metazoan diversification should be recast as a series of successive, transitional radiations that extended from the late Ediacaran and continued through the early Palaeozoic. We conclude that while the Cambrian Explosion represents a radiation of crown-group bilaterians, it was simply one phase amongst several metazoan radiations, some older and some younger.

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Fig. 1: Integrated geochemical and biotic record between 670 and 480 million years ago.
Fig. 2: Key transitional Ediacaran and Cambrian taxa.

A. Fedorov (d); S. Xiao (e)

Fig. 3: Ediacaran ecosystem dioramas.
Fig. 4: Biotic evolution across the Ediacaran–Cambrian.

Change history

  • 12 April 2019

    In the version of this article initially published, the reference “Mitchell, E. G., & Kenchington, C. G. The utility of height for the Ediacaran organisms of Mistaken Point. Nat. Ecol. Evol. 2, 1218–1222 (2018).” was missing. A callout to the reference should have been placed at the end of this sentence: “For biotic replacement to occur, taxa must be both spatially collocated and have similar resource requirements, yet spatial analyses of contemporary communities find only very limited instances of resource competition.” The reference has been added to the list, and the error has been corrected in the PDF and HTML versions of the article.

References

  1. 1.

    Erwin, D.H. & Valentine, J.W. The Cambrian Explosion: The Construction of Animal Biodiversity (Roberts and Company Publishers Inc., Greenwood Village, CO, USA 2013).

  2. 2.

    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).

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Droser, M. L., Tarhan, L. G. & Gehling, J. G. The rise of animals in a changing environment: global ecological innovation in the late Ediacaran. Annu. Rev. Earth Planet. Sci. 45, 593–617 (2017).

    CAS  Google Scholar 

  4. 4.

    Budd, G. E. & Jensen, S. The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution. Biol. Rev. Camb. Philos. Soc. 92, 446–473 (2017).

    PubMed  Google Scholar 

  5. 5.

    Budd, G. E. The Cambrian fossil record and the origin of the phyla. Integr. Comp. Biol. 43, 157–165 (2003).

    PubMed  Google Scholar 

  6. 6.

    Zhu, M., Zhuravlev, A., Yu., Wood, R., Zhao, F. & Sukhov, S. S. A deep root for the Cambrian Explosion: implications of new bio- and chemostratigraphy from the Siberian Platform. Geology 45, 459–462 (2016).

    Google Scholar 

  7. 7.

    Darroch, S. A. F., Smith, E. F., Laflamme, M. & Erwin, D. H. Ediacaran extinction and Cambrian Explosion. Trends Ecol. Evol. 33, 653–663 (2018).

    PubMed  Google Scholar 

  8. 8.

    Tarhan, L. G., Droser, M. L., Cole, D. B. & Gehling, J. G. Ecological expansion and extinction in the late Ediacaran: weighing the evidence for environmental and biotic drivers. Integr. Comp. Biol. 58, 688–702 (2018).

    PubMed  PubMed Central  Google Scholar 

  9. 9.

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

    CAS  Google Scholar 

  10. 10.

    Servais, T., Owen, A. W., Harper, D. A. T., Kröger, B. & Munnecke, A. The great Ordovician biodiversification event (GOBE): the palaeoecological dimension. Palaeogeogr. Palaeoclimatol. Palaeoecol. 294, 99–119 (2010).

    Google Scholar 

  11. 11.

    Zhuravlev, A. Y. & Wood, R. A. Anoxia as the cause of the mid-Early Cambrian (Botomian) extinction event. Geology 24, 311–314 (1996).

    CAS  Google Scholar 

  12. 12.

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

    CAS  PubMed  Google Scholar 

  13. 13.

    Li, C. et al. Ediacaran marine redox heterogeneity and early animal ecosystems. Sci. Rep. 5, 17097 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Tostevin, R. et al. Low-oxygen waters limited habitable space for early animals. Nat. Commun. 7, 12818 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Lenton, T.M. & Daines, S.J. The effects of marine eukaryote evolution on phosphorus, carbon and oxygen cycling across the Proterozoic–Phanerozoic transition. Emerg. Top. Life Sci. ETLS20170156 (2018).

  16. 16.

    van de Velde, S., Mills, B. J. W., Meysman, F. J. R., Lenton, T. M. & Poulton, S. W. Early Palaeozoic ocean anoxia and global warming driven by the evolution of shallow burrowing. Nat. Commun. 9, 2554 (2018).

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Schiffbauer, J. D. et al. The latest Ediacaran Wormworld fauna: setting the ecological stage for the Cambrian Explosion. GSA Today 26, 4–11 (2016).

    Google Scholar 

  18. 18.

    Butterfield, N. J. Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7, 1–7 (2009).

    CAS  PubMed  Google Scholar 

  19. 19.

    Wood, R. & Erwin, D. H. Innovation not recovery: dynamic redox promotes metazoan radiations. Biol. Rev. Camb. Philos. Soc. 93, 863–873 (2018).

    PubMed  Google Scholar 

  20. 20.

    Sperling, E. A. & Stockey, R. G. The temporal and environmental context of early animal evolution: considering all the ingredients of an ‘explosion’. Integr. Comp. Biol. 58, 605–622 (2018).

    CAS  PubMed  Google Scholar 

  21. 21.

    Planavsky, N. J. et al. Late Proterozoic transitions in climate, oxygen, and tectonics, and the rise ofcomplex life. Paleontol. Soc. Papers (Earth-life transitions: paleobiology in the context of Earth system evolution) 21, 47–82 (2015).

    Google Scholar 

  22. 22.

    Grotzinger, J. P., Fike, D. A. & Fischer, W. W. Enigmatic origin of the largest-known carbon isotope excursion in Earth’s history. Nat. Geosci. 4, 285–292 (2011).

    CAS  Google Scholar 

  23. 23.

    Sperling, E. A. et al. Oxygen, ecology, and the Cambrian radiation of animals. Proc. Natl Acad. Sci. USA 110, 13446–13451 (2013).

    CAS  PubMed  Google Scholar 

  24. 24.

    Cloud, P. E. Jr. Atmospheric and hydrospheric evolution on the primitive earth. Both secular accretion and biological and geochemical processes have affected earth’s volatile envelope. Science 160, 729–736 (1968).

    CAS  PubMed  Google Scholar 

  25. 25.

    Knoll, A. H. & Sperling, E. A. Oxygen and animals in Earth history. Proc. Natl Acad. Sci. USA 111, 3907–3908 (2014).

    CAS  PubMed  Google Scholar 

  26. 26.

    Lenton, T. M., Boyle, R. A., Poulton, S. W., Shields-Zhou, G. A. & Butterfield, N. J. Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265 (2014).

    CAS  Google Scholar 

  27. 27.

    Sperling, E. A. et al. Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, 451–454 (2015).

    CAS  PubMed  Google Scholar 

  28. 28.

    Guilbaud, R. et al. Oxygen minimum zones in the early Cambrian ocean.Geochem. Perspect. Lett. 6, 33–38 (2018).

    Google Scholar 

  29. 29.

    Hammarlund, E. U. et al. Early Cambrian oxygen minimum zone-like conditions at Chengjiang. Earth Planet. Sci. Lett. 475, 160–168 (2017).

    CAS  Google Scholar 

  30. 30.

    Bowyer, F., Wood, R. A. & Poulton, S. W. Controls on the evolution of Ediacaran metazoan ecosystems: a redox perspective. Geobiology 15, 516–551 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Mills, D. B. et al. Oxygen requirements of the earliest animals. Proc. Natl Acad. Sci. USA 111, 4168–4172 (2014).

    CAS  PubMed  Google Scholar 

  32. 32.

    Mills, D. B. et al. The last common ancestor of animals lacked the HIF pathway and respired in low-oxygen environments. eLife 7, e31176 (2018).

    PubMed  PubMed Central  Google Scholar 

  33. 33.

    Wood, R. A. et al. Dynamic redox conditions control late Ediacaran ecosystems in the Nama Group, Namibia. Precambr. Res. 261, 252–271 (2015).

    CAS  Google Scholar 

  34. 34.

    Tostevin, R. et al. Uranium isotope evidence for an expansion of anoxia in terminal Ediacaran oceans. Earth Planet. Sci. Lett. 506, 104–112 (2018).

    Google Scholar 

  35. 35.

    Wang, D. et al. Coupling of ocean redox and animal evolution during the Ediacaran–Cambrian transition. Nat. Commun. 9, 2575 (2018).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Chen, X. et al. Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nat. Commun. 6, 7142 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Sahoo, S. K. et al. Oceanic oxygenation events in the anoxic Ediacaran ocean. Geobiology 14, 457–468 (2016).

    CAS  PubMed  Google Scholar 

  38. 38.

    Li, C. et al. Coupled oceanic oxygenation and metazoan diversification during the early–middle Cambrian? Geology 45, 743–746 (2017).

    Google Scholar 

  39. 39.

    Zhang, J. et al. Heterogenous oceanic redox conditions through the Ediacaran–Cambrian boundary limited the metazoan zonation. Sci. Rep. 7, 8550 (2017).

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Zhang, F. et al. Extensive marine anoxia during the terminal Ediacaran Period. Sci. Adv. 4, eaan8983 (2018).

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Wei, G.-Y. et al. Marine redox fluctuation as a potential trigger for the Cambrian Explosion. Geology 46, 587–590 (2018).

    CAS  Google Scholar 

  42. 42.

    Zhuravlev, A. Y. & Wood, R. A. The two phases of the Cambrian Explosion. Sci. Rep. 8, 16656 (2018).

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Woods, M. A., Wilby, P. R., Leng, M. J., Rushton, A. W. & Williams, M. The Furongian (late Cambrian) Steptoean positive carbon isotope excursion (SPICE) in Avalonia. J. Geol. Soc. Lond. 164, 851–862 (2011).

    Google Scholar 

  44. 44.

    Muscente, A. D., Boag, T. H., Bykova, N. & Schiffbauer, J. D. Environmental disturbance, resource availability, and biologic turnover at the dawn of animal life. Earth Sci. Rev. 177, 248–264 (2017).

    Google Scholar 

  45. 45.

    Laflamme, M., Darroch, S. A. F., Tweedt, S. M., Peterson, K. J. & Erwin, D. H. The end of the Ediacara biota: extinction, biotic replacement, or Cheshire Cat? Gondwana Res. 23, 558–573 (2013).

    Google Scholar 

  46. 46.

    Darroch, S. A. F. et al. Biotic replacement and mass extinction of the Ediacara biota. Proc. Biol. Sci. 282, 20151003 (2015).

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Chen, Z. et al. Trace fossil evidence for Ediacaran bilaterian animals with complex behaviors. Precambr. Res. 224, 690–701 (2013).

    CAS  Google Scholar 

  48. 48.

    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).

    PubMed  PubMed Central  Google Scholar 

  49. 49.

    Gehling, J. G. & Droser, M. Ediacaran scavenging as a prelude to predation. Emerg. Top. Life Sci. 2, 213–222 (2018).

    CAS  Google Scholar 

  50. 50.

    Mitchell, E.G., . & Kenchington, C.G. The utility of height for the Ediacaran organisms of Mistaken Point. Nat. Ecol. Evol. 2, 1218–1222 (2018).

    PubMed  Google Scholar 

  51. 51.

    Wilby, P. R., Carney, J. N. & Howe, M. P. A rich Ediacaran assemblage from eastern Avalonia: evidence of early widespread diversity in the deep ocean. Geology 39, 655–658 (2011).

    Google Scholar 

  52. 52.

    Pu, J. P. et al. Dodging snowballs: geochronology of the Gaskiers glaciation and the first appearance of the Ediacaran biota. Geology 44, 955–958 (2016).

    CAS  Google Scholar 

  53. 53.

    Canfield, D. E. & Poulton, S. W. & Narbonne, G.M. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92–95 (2007).

    CAS  PubMed  Google Scholar 

  54. 54.

    Gehling, J. G. & Droser, M. How well do fossil assemblages of the Ediacara Biota tell time? Geology 41, 447–450 (2013).

    Google Scholar 

  55. 55.

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

  56. 56.

    Grazhdankin, D. Patterns of distribution in the Ediacaran biotas: facies versus biogeography and evolution. Paleobiology 30, 203–221 (2004).

    Google Scholar 

  57. 57.

    Evans, S. D., Diamond, C. W., Droser, M. L. & Lyons, T. W. Dynamic oxygen and coupled biological and ecological innovation during the second wave of the Ediacara biota. Emerg. Top. Life Sci. 2, 223–233 (2018).

    CAS  Google Scholar 

  58. 58.

    Chen, Z. et al. New Ediacara fossils preserved in marine limestone and their ecological implications. Sci. Rep. 4, 4180 (2014).

    PubMed  PubMed Central  Google Scholar 

  59. 59.

    Ling, H.-F. et al. Cerium anomaly variations in Ediacaran-earliest Cambrian carbonates from the Yangtze Gorges area, South China: implications for oxygenation of coeval shallow seawater. Precambr. Res. 225, 110–127 (2013).

    CAS  Google Scholar 

  60. 60.

    Duda, J.-P. et al. Geobiology of a palaeoecosystem with Ediacara-type fossils: the Shibantan Member (Dengying Formation, South China). Precambr. Res. 255, 48–62 (2014).

    CAS  Google Scholar 

  61. 61.

    Zhang, L. Y. A discovery and preliminary study of the late stage of late Gaojiashan biota from Sinian in Ningqiang County, Shaanxi. Northwest Geoscience 13, 67–88 (1986).

    Google Scholar 

  62. 62.

    Hua, H., Chen, Z. & Yuan, X. The advent of mineralized skeletons in Neoproterozoic Metazoa — new fossil evidence from the Gaojiashan Fauna. Geol. J. 42, 263–279 (2007).

    Google Scholar 

  63. 63.

    Xing, Y.-S., Ding, Q.-X., Luo, H.-L., He, T.-G. & Wang, Y.-G. The Sinian–Cambrian boundary of China. Bulletin of the Institute of Geology of the Chinese Academy Special Issue 10, 182–183 (1984).

    Google Scholar 

  64. 64.

    Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. Morphology and paleoecology of the late Ediacaran tubular fossil Conotubus hemiannulatus from the Gaojiashan Lagerstätte of southern Shaanxi Province. South China. Precambr. Res. 191, 46–57 (2011).

    CAS  Google Scholar 

  65. 65.

    Chen, L. Y., Chu, X. L., Zhang, X. L. & Zhai, M. G. Carbon isotopes, sulfur isotopes, and trace elements of the dolomites from the Dengying Formation in Zhenba area southern Shaanxi: implications for shallow water redox conditions during the terminal Ediacaran. Sci. China Earth Sci. 58, 1107–1122 (2015).

    CAS  Google Scholar 

  66. 66.

    Saylor, B. Z. Sequence stratigraphy and carbonate–siliciclastic mixing in a terminal Proterozoic foreland basin, Urusis Formation, Nama Group, Namibia. J. Sediment. Res. 73, 264–279 (2003).

    Google Scholar 

  67. 67.

    Jensen, S. M. & Runnegar, B. N. A complex trace fossil from the Spitskop Member (terminal Ediacaran–? Lower Cambrian) of southern Namibia. Geol. Mag. 142, 561–569 (2005).

    Google Scholar 

  68. 68.

    Wood, R. A. Paleoecology of the earliest skeletal metazoan communities: implications for early biomineralization. Earth Sci. Rev. 106, 184–190 (2011).

    CAS  Google Scholar 

  69. 69.

    Murdock, D. J. E. & Donoghue, P. C. J. Evolutionary origins of animal skeletal biomineralization. Cells Tissues Organs 194, 98–102 (2011).

    PubMed  Google Scholar 

  70. 70.

    Wood, R. & Penny, A. Substrate growth dynamics and biomineralization of an Ediacaran encrusting poriferan. Proc. Biol. Sci. 285, 20171938 (2018).

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Wood, R., Ivantsov, A. Y. & Zhuravlev, A. Y. First macrobiota biomineralization was environmentally triggered. Proc. Biol. Sci. 284, 20170059 (2017).

    PubMed  PubMed Central  Google Scholar 

  72. 72.

    Porter, S. M. Seawater chemistry and early carbonate biomineralization. Science 316, 1302 (2007).

    CAS  PubMed  Google Scholar 

  73. 73.

    Brennan, S. T., Lowenstein, T. K. & Horita, J. Seawater chemistry and the advent of biocalcification. Geology 32, 473–476 (2004).

    CAS  Google Scholar 

  74. 74.

    Wood, R., Zhuravlev, A. Yu, Sukhov, S. S., Zhu, M. & Zhao, F. Demise of Ediacaran dolomitic seas marks widespread biomineralization on the Siberian Platform. Geology 45, 27–30 (2017).

    Google Scholar 

  75. 75.

    Clapham, M. E., Narbonne, G. M. & Gehling, J. G. Paleoecology of the oldest known animal communities: Ediacaran assemblages at Mistaken Point, Newfoundland. Paleobiology 29, 527–544 (2003).

    Google Scholar 

  76. 76.

    Droser, M., Gehling, J. & Jensen, S. Assemblage palaeoecology of the Ediacara biota: the unabridged edition? Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 131–147 (2006).

    Google Scholar 

  77. 77.

    Boag, T. H., Darroch, S. A. F. & Laflamme, M. Ediacaran distributions in space and time: testing assemblage concepts of earliest macroscopic body fossils. Paleobiology 42, 574–594 (2016).

    Google Scholar 

  78. 78.

    Jensen, S., Gehling, J. G. & Droser, M. L. Ediacara-type fossils in Cambrian sediments. Nature 393, 567 (1998).

    CAS  Google Scholar 

  79. 79.

    Hagadorn, J. W., Fedo, C. M. & Waggoner, B. M. Early Cambrian Ediacaran-type fossils from California. J. Paleontol. 74, 731–740 (2000).

    Google Scholar 

  80. 80.

    Shu, D.-G. et al. Lower Cambrian vendobionts from China and early diploblast evolution. Science 312, 731–734 (2006).

    CAS  PubMed  Google Scholar 

  81. 81.

    Hoyal Cuthill, J. F. & Han, J. Cambrian petalonamid Stromatoveris phylogenetically links Ediacaran biota to later animals. Palaeontology 61, 813–823 (2018).

    Google Scholar 

  82. 82.

    Conway Morris, S. Ediacaran-like fossils in Cambrian Burgess Shale-type faunas of North America. Palaeontology 36, 593–635 (1993).

    Google Scholar 

  83. 83.

    Zhuravlev, A., Yu., Linan, E., Vintaned, J. A. G., Debrenne, F. & Fedorov, A. B. New finds of skeletal fossils in the terminal Neoproterozoic of the Siberian Platform and Spain. Acta Palaeontol. Pol. 57, 205–224 (2012).

    Google Scholar 

  84. 84.

    Yang, B. et al. Transitional Ediacaran–Cambrian small skeletal fossil assemblages from South China and Kazakhstan: implications for chronostratigraphy and metazoan evolution. Precambr. Res. 285, 202–215 (2016).

    CAS  Google Scholar 

  85. 85.

    McIlroy, D., Green, O. R. & Brasier, M. D. Palaeobiology and evolution of the earliest agglutinated Foraminifera: Platysolenites, Spirosolenites and related forms . Lethaia 34, 13–29 (2001).

    Google Scholar 

  86. 86.

    Kontorovich, A. E. et al. A section of Vendian in the east of West Siberian Plate (based on data from the Borehole Vostok 3). Russ. Geol. Geophys. 49, 932–939 (2008).

    Google Scholar 

  87. 87.

    Budd, G. E. Early animal evolution and the origins of nervous systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20150037 (2015).

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    Yang, C., Li, X. H., Zhu, M. & Condon, D. J. SIMS U–Pb zircon geochronological constraints on upper Ediacaran stratigraphic correlations. South China. Geol. Mag. 154, 1202–1216 (2017).

    CAS  Google Scholar 

  89. 89.

    Martin, M. W. et al. Age of Neoproterozoic bilatarian body and trace fossils, White Sea, Russia: implications for metazoan evolution. Science 288, 841–845 (2000).

    CAS  PubMed  Google Scholar 

  90. 90.

    Bowring, S. A. et al. Geochronologic constraints on the chronostratigraphic framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman. Am. J. Sci. 307, 1097–1145 (2007).

    CAS  Google Scholar 

  91. 91.

    Waggoner, B. Biogeographic analyses of the Ediacara biota: a conflict with paleotectonic reconstructions. Paleobiology 25, 440–458 (1999).

    Google Scholar 

  92. 92.

    Smith, E. F. et al. The end of the Ediacaran: two new exceptionally preserved body fossil assemblages from Mount Dunfee, Nevada, USA. Geology 44, 911–914 (2016).

    CAS  Google Scholar 

  93. 93.

    Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. 94.

    Brocks, J. J. et al. The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Yuan, X., Chen, Z., Xiao, S., Zhou, C. & Hua, H. An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes. Nature 470, 390–393 (2011).

    CAS  PubMed  Google Scholar 

  96. 96.

    Xiao, S., Zhang, Y. & Knoll, A. H. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391, 553–558 (1998).

    CAS  Google Scholar 

  97. 97.

    Liu, A. G., McIlroy, D., Matthews, J. J. & Brasier, M. D. A new assemblage of juvenile Ediacaran fronds from the Drook Formation, Newfoundland. J. Geol. Soc. Lond. 169, 395–340 (2012).

    Google Scholar 

  98. 98.

    Liu, A. G., Mcllroy, D. & Brasier, M. D. First evidence for locomotion in the Ediacara biota from the 565 Ma Mistaken Point Formation, Newfoundland. Geology 38, 123–126 (2010).

    Google Scholar 

  99. 99.

    Germs, G. J. B. New shelly fossils from the Nama Group, South West Africa. Am. J. Sci. 272, 752–761 (1972).

    Google Scholar 

  100. 100.

    Bengtson, S. & Zhao, Y. Predatorial borings in late Precambrian mineralized exoskeletons. Science 257, 367–369 (1992).

    CAS  PubMed  Google Scholar 

  101. 101.

    Landing, E. Precambrian–Cambrian boundary global stratotype ratified and a new perspective of Cambrian time. Geology 22, 179–182 (1994).

    Google Scholar 

  102. 102.

    Macdonald, F. A. et al. Calibrating the Cryogenian. Science 327, 1241–1243 (2010).

    CAS  PubMed  Google Scholar 

  103. 103.

    Macdonald, F. A. et al. The stratigraphic relationship between the Shuram carbon isotope excursion, the oxygenation of Neoproterozoic oceans, and the first appearance of the Ediacara biota and bilaterian trace fossils in northwestern Canada. Chem. Geol. 362, 250–272 (2013).

    CAS  Google Scholar 

  104. 104.

    Zhu, M., Babcock, L. E. & Peng, S.-C. Advances in Cambrian stratigraphy and paleontology: Integrating correlation techniques, paleobiology, taphonomy and paleoenvironmental reconstruction. Palaeoworld 15, 217–222 (2006).

    Google Scholar 

  105. 105.

    Canfield, D. E. et al. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321, 949–952 (2008).

    CAS  PubMed  Google Scholar 

  106. 106.

    Kendall, B. et al. Uranium and molybdenum isotope evidence for an episode of widespread ocean oxygenation during the late Ediacaran Period. Geochim. Cosmochim. Acta 156, 173–193 (2015).

    CAS  Google Scholar 

  107. 107.

    Dahl, T. W. et al. Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. Proc. Natl Acad. Sci. USA 107, 17911–17915 (2010).

    CAS  PubMed  Google Scholar 

  108. 108.

    Narbonne, G. M. & Gehling, J. G. Life after snowball: the oldest complex Ediacaran fossils. Geology 31, 27–30 (2003).

    Google Scholar 

  109. 109.

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

    PubMed  Google Scholar 

  110. 110.

    Liu, A. G., Matthews, J. J., Menon, L. R., McIlroy, D. & Brasier, M. D. Haootia quadriformis n. gen., n. sp., interpreted as a muscular cnidarian impression from the Late Ediacaran period (approx. 560 Ma). Proc. Biol. Sci. 281, 20141202 (2014).

    PubMed  PubMed Central  Google Scholar 

  111. 111.

    Amthor, J. E. et al. Extinction of Cloudina and Namacalathus at the Precambrian–Cambrian boundary in Oman. Geology 31, 431–434 (2003).

    Google Scholar 

  112. 112.

    Zhu, M., Zhang, J. & Yang, A. Integrated Ediacaran (Sinian) chronostratigraphy of South China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 7–61 (2007).

    Google Scholar 

  113. 113.

    Zhu, M. et al. Early Cambrian stratigraphy of east Yunnan, southwestern China: a synthesis. Acta Palaeontologica Sin. 40, 4–39 (2001).

    Google Scholar 

  114. 114.

    Zhu, M. & Li, X.-H. Introduction: from Snowball Earth to Cambrian explosion — evidence from China. Geol. Mag. 154, 1187–1192 (2017).

    Google Scholar 

  115. 115.

    Ahn, S. Y. & Zhu, M. Lowermost Cambrian acritarchs from the Yanjiahe Formation, South China: implication for defining the base of the Cambrian in the Yangtze Platform. Geol. Mag. 154, (1217–1231 (2017).

    Google Scholar 

  116. 116.

    Saltzman, M. R., Edwards, C. T., Adrain, J. M. & Westrop, S. R. Persistent oceanic anoxia and elevated extinction rates separate the Cambrian and Ordovician radiations. Geology 43, 807–810 (2015).

    CAS  Google Scholar 

  117. 117.

    Boyle, R. A., Dahl, T. W., Bjerrum, C. J. & Canfield, D. E. Bioturbation and directionality in Earth’s carbon isotope record across the Neoproterozoic–Cambrian transition. Geobiology 16, 252–278 (2018).

    CAS  PubMed  Google Scholar 

  118. 118.

    Shields, G. A. & Mills, B. J. W. Tectonic controls on the long-term carbon isotope mass balance. Proc. Natl Acad. Sci. USA 114, 4318–4323 (2017).

    CAS  PubMed  Google Scholar 

  119. 119.

    Pogge von Strandmann, P. A. E. et al. Selenium isotope evidence for progressive oxidation of the Neoproterozoic biosphere. Nat. Commun. 6, 10157 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120.

    Wen, H. et al. Molybdenum isotopic records across the Precambrian–Cambrian boundary. Geology 39, 775–778 (2011).

    CAS  Google Scholar 

  121. 121.

    Kimura, H. & Watanabe, Y. Oceanic anoxia at the Precambrian–Cambrian boundary. Geology 29, 995–998 (2001).

    CAS  Google Scholar 

  122. 122.

    Wille, M., Nägler, T. F., Lehmann, B., Schröder, S. & Kramers, J. D. Hydrogen sulphide release to surface waters at the Precambrian/Cambrian boundary. Nature 453, 767–769 (2008).

    CAS  PubMed  Google Scholar 

  123. 123.

    Tostevin, R. et al. Constraints on the late Ediacaran sulfur cycle from carbonate associated sulfate. Precambr. Res. 230, 113–125 (2017).

    Google Scholar 

  124. 124.

    Dececchi, T. A., Narbonne, G. M., Greentree, C. & Laflamme, M. Relating Ediacaran fronds. Paleobiology 43, 171–180 (2017).

    Google Scholar 

  125. 125.

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

    Google Scholar 

  126. 126.

    Bobrovskiy, I. et al. Ancient steroids establish the Ediacaran fossil Dickinsonia as one of the earliest animals. Science 361, 1246–1249 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. 127.

    Carbone, C. A. & Narbonne, G. M. When life got smart: the evolution of behavioral complexity through the Ediacaran and Early Cambrian of NW Canada. J. Paleontol. 88, 309–330 (2014).

    Google Scholar 

  128. 128.

    Buatois, L.A. & Mángano, M.G. In The Trace-Fossil Record of Major Evolutionary Events, Topics in Geobiology Vol. 39 (eds. Mángano, M.G. & Buatois, L.A.) 27–72 (Springer, 2016).

  129. 129.

    Penny, A. M. et al. Ediacaran metazoan reefs from the Nama Group, Namibia. Namibia. Science 344, 1504–1506 (2014).

    CAS  PubMed  Google Scholar 

  130. 130.

    Mehra, A. & Maloof, A. Multiscale approach reveals that Cloudina aggregates are detritus and not in situ reef constructions. Proc. Natl Acad. Sci. USA 115, E2519–E2527 (2018).

    CAS  PubMed  Google Scholar 

  131. 131.

    Bengtson, S. Origins and early evolution of predation. Paleontological Society Papers 8, 289–318 (2002).

    Google Scholar 

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Acknowledgements

This work was funded by the following Natural Environment Research Council (NERC) Grants: NE/P013643/1 (BETR Collaboration Grant to R.W. and A.L.), NE/L002558/1 (E3 DTP studentship to F.B.), NE/L002434/1 (GW4+ DTP studentship to F.D.), NE/L011409/2 (Independent Research Fellowship to A.L.), NE/P002412/1 (E.G.M.), NEE3849S (NERC-BGS project support to P.R.W.). Funding also came from a Leverhulme Early Career Fellowship and Isaac Newton Trust Early Career Fellowship to C.G.K.; a Henslow Research Fellowship from Cambridge Philosophical Society to E.G.M.; and a School of GeoSciences studentship to A.P.

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All authors were involved in conceiving the work. F.B., A.L., J.H.C., E.G.M., C.G.K., F.D. and A.P. collated data for figures. R.W. co-ordinated the work, and all authors wrote the paper.

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Correspondence to Rachel Wood.

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Supplementary Figure 1 and Supplementary Tables 1 and 2 (Fossil key and occurrence catalogue for Fig. 3 and 4).

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Wood, R., Liu, A.G., Bowyer, F. et al. Integrated records of environmental change and evolution challenge the Cambrian Explosion. Nat Ecol Evol 3, 528–538 (2019). https://doi.org/10.1038/s41559-019-0821-6

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