The evolutionary events during the Ediacaran–Cambrian transition (~541 Myr ago) are unparalleled in Earth history. The fossil record suggests that most extant animal phyla appeared in a geologically brief interval, with the oldest unequivocal bilaterian body fossils found in the Early Cambrian. Molecular clocks and biomarkers provide independent estimates for the timing of animal origins, and both suggest a cryptic Neoproterozoic history for Metazoa that extends considerably beyond the Cambrian fossil record. We report an assemblage of ichnofossils from Ediacaran–Cambrian siltstones in Brazil, alongside U–Pb radioisotopic dates that constrain the age of the oldest specimens to 555–542 Myr. X-ray microtomography reveals three-dimensionally preserved traces ranging from 50 to 600 μm in diameter, indicative of small-bodied, meiofaunal tracemakers. Burrow morphologies suggest they were created by a nematoid-like organism that used undulating locomotion to move through the sediment. This assemblage demonstrates animal–sediment interactions in the latest Ediacaran period, and provides the oldest known fossil evidence for meiofaunal bilaterians. Our discovery highlights meiofaunal ichnofossils as a hitherto unexplored window for tracking animal evolution in deep time, and reveals that both meiofaunal and macrofaunal bilaterians began to explore infaunal niches during the late Ediacaran.
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McIlroy, D. & Logan, G. A. The impact of bioturbation on infaunal ecology and evolution during the Proterozoic–Cambrian transition. Palaios 14, 58–72 (1999).
Mángano M. G. & Buatois, L. A. Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks. Proc. R. Soc. B 281, 20140038 (2014).
Cunningham, J. A., Liu, A. G., Bengtson, S. & Donoghue, P. C. The origin of animals: can molecular clocks and the fossil record be reconciled? Bioessays 39, 1–12 (2017).
Van Iten, H. et al. in The Cnidaria, Past, Present and Future (eds Goffredo, S. & Dubinsky, Z.) 31–40 (Springer, Berlin, 2016).
Penny, A. M. et al. Early animals. Ediacaran metazoan reefs from the Nama Group, Namibia. Science 344, 1504–1506 (2014).
Bengtson, S. & Zhao, Y. Predatorial borings in Late Precambrian mineralized exoskeletons. Science 257, 367–369 (1992).
Vinther, J., Parry, L., Briggs, D. E. G. & Van Roy, P. Ancestral morphology of molluscs revealed by a new Ordovician stem aculiferan. Nature 542, 471–474 (2017).
Tarhan, L. G., Droser, M. L., Planavsky, N. J. & Johnston, D. T. Protracted development of bioturbation through the early Palaeozoic era. Nat. Geosci. 8, 865–869 (2015).
Vannier, J., Calandra, I., Gaillard, C. & Żylińska, A. Priapulid worms: pioneer horizontal burrowers at the Precambrian–Cambrian boundary. Geology 38, 711–714 (2010).
Buatois, L. A. & Mángano, M. G. Ichnology: Organism–Substrate Interactions in Space and Time (Cambridge Univ. Press, Cambridge, 2011).
Jensen, S. The Proterozoic and earliest Cambrian trace fossil record; patterns, problems and perspectives. Integr. Comp. Biol. 43, 219–228 (2003).
Gehling, J. G., Runnegar, B. N. & Droser, M. L. Scratch traces of large Ediacara bilaterian animals. J. Paleontol. 88, 284–298 (2014).
Menon, L. R., McIlroy, D. & Brasier, M. D. Evidence for Cnidaria-like behavior in ca. 560 Ma Ediacaran Aspidella. Geology 41, 895–898 (2013).
Jensen, S., Saylor, B. Z., Gehling, J. G. & Germs, G. J. Complex trace fossils from the terminal Proterozoic of Namibia. Geology 28, 143–146 (2000).
Chen, Z. et al. Trace fossil evidence for Ediacaran bilaterian animals with complex behaviours. Precambrian Res. 224, 690–701 (2013).
Liu, A. G., McIlroy, 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).
Rogov, V. et al. The oldest evidence of bioturbation on Earth. Geology 40, 395–398 (2012).
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).
Yin, Z. et al. Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc. Natl Acad. Sci. USA 112, E1453–E1460 (2015).
Love, G. D. & Summons, R. E. The molecular record of Cryogenian sponges–a response to Antcliffe (2013). Palaeontology 58, 1131–1136 (2015).
Fortey, R. A., Briggs, D. E. G. & Wills, M. A. The Cambrian evolutionary ‘explosion’ recalibrated. BioEssays 19, 429–434 (1997).
Budd, G. E. & Jensen, S. A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. 75, 253–295 (2000).
Cannon, J. T. et al. Xenacoelomorpha is the sister group to Nephrozoa. Nature 530, 89–93 (2016).
Laumer, C. E. et al. Spiralian phylogeny informs the evolution of microscopic lineages. Curr. Biol. 25, 2000–2006 (2015).
Giere, O. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments (Springer Science & Business Media, Berlin, 2008).
Löhr, S. & Kennedy, M. Micro-trace fossils reveal pervasive reworking of Pliocene sapropels by low-oxygen-adapted benthic meiofauna. Nat. Commun. 6, 6589 (2015).
Cullen, D. J. Bioturbation of superficial marine sediments by interstitial meiobenthos. Nature 242, 323–324 (1973).
Harvey, T. H. P. & Butterfield, N. J. Exceptionally preserved Cambrian loriciferans and the early animal invasion of the meiobenthos. Nat. Ecol. Evol. 1, 0022 (2017).
Han, J., Morris, S. C., Ou, Q., Shu, D. & Huang, H. Meiofaunal deuterostomes from the basal Cambrian of Shaanxi (China). Nature 542, 228–231 (2017).
de Alvarenga, C. J. S et al. in Neoproterozoic–Cambrian Tectonics, Global Change and Evolution: A Focus on Southwestern Gondwana (eds Gaucher, C., Sial, A. N., Halverson, G. P. & Frimmel, H. E.) 15–28 (Elsevier, Amsterdam, 2009).
Gaucher, C., Boggiani, P. C., Sprechmann, P., Sial, A. N. & Fairchild, T. R. Integrated correlation of the Vendian to Cambrian Arroyo del Soldado and Corumba groups (Uruguay and Brazil): palaeogeographic, palaeoclimatic and palaeobiologic implications. Precambrian Res. 120, 241–278 (2003).
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).
Fillion, D. & Pickerill, R. K. Ichnology of the Cambrian? to Lower Ordovician Bell Island and Wabana Groups of Eastern Newfoundland, Canada (Palaeontographica Canadiana No. 7, Canadian Society of Petroleum Geologists, St. John’s, 1990).
Cai, Y., Hua, H., Xiao, S., Schiffbauer, J. D. & & Li, P. Biostratinomy of the late Ediacaran pyritized Gaojiashan Lagerstätte from southern Shaanxi, South China: importance of event deposits. Palaios 25, 487–506 (2010).
LoDuca, S., Bykova, N., Wu, M., Xiao, S. & Zhao, Y. Seaweed morphology and ecology during the great animal diversification events of the early Paleozoic: a tale of two floras. Geobiology 15, 588–616 (2017).
Virtasalo, J. J., Löwemark, L., Papunen, H., Kotilainen, A. T. & Whitehouse, M. J. Pyritic and baritic burrows and microbial filaments in postglacial lacustrine clays in the northern Baltic Sea. J. Geol. Soc. 167, 1185–1198 (2010).
Schratzberger, M. & Ingels, J. Meiofauna matters: the roles of meiofauna in benthic ecosystems. J. Exp. Mar. Biol. Ecol. http://dx.doi.org/10.1016/j.jembe.2017.01.007 (2017).
Schieber, J. The role of an organic slime matrix in the formation of pyritized burrow trails and pyrite concretions. Palaios 17, 104–109 (2002).
Uchman, A. Eocene flysch trace fossils from the Hecho Group of the Pyrenees, northern Spain. Beringeria 28, 3–41 (2001).
Garwood, R. & Dunlop, J. The walking dead: Blender as a tool for paleontologists with a case study on extinct arachnids. J. Paleontol. 88, 735–746 (2014).
Powilleit, M., Kitlar, J. & Graf, G. Particle and fluid bioturbation caused by the priapulid worm Halicryptus spinulosus (v. Seibold). Sarsia 79, 109–117 (1994).
Bromley, R. G. Trace Fossils: Biology, Taxonomy and Applications (Routledge, London, 2012).
Anderson, D. T. Embryology and Phylogeny in Annelids and Arthropods (International Series of Monographs in Pure and Applied Biology Zoology, Elsevier, Oxford, 2013).
Collins, A. G., Lipps, J. H. & Valentine, J. W. Modern mucociliary creeping trails and the bodyplans of Neoproterozoic trace-makers. Paleobiology 26, 47–55 (2000).
Seilacher A. Trace Fossil Analysis (Springer, Heidelberg, 2007).
Beron, C. et al. The burrowing behavior of the nematode Caenorhabditis elegans: a new assay for the study of neuromuscular disorders. Genes Brain Behav. 14, 357–368 (2015).
Baliński, A., Sun, Y. & Dzik, J. Traces of marine nematodes from 470 million years old Early Ordovician rocks in China. Nematology 15, 567–574 (2013).
McIlroy, D. & Brasier, M. D. Ichnological evidence for the Cambrian Explosion in the Ediacaran to Cambrian succession of Tanafjord, Finnmark, northern Norway. Geol. Soc. Spec. Publ. 448, 351–369 (2016).
Borner, J., Rehm, P., Schill, R. O., Ebersberger, I. & Burmester, T. A transcriptome approach to ecdysozoan phylogeny. Mol. Phylogenet. Evol. 80, 79–87 (2014).
Hua, H., Pratt, B. R. & Zhang, L.-Y. Borings in Cloudina shells: complex predator–prey dynamics in the terminal Neoproterozoic. Palaios 18, 454–459 (2003).
Darroch, S. A. F. et al. Biotic replacement and mass extinction of the Ediacara biota. Proc. R. Soc. B 282, 20151003 (2015).
Boggiani, P. C. et al. Chemostratigraphy of the Tamengo Formation (Corumba Group, Brazil): a contribution to the calibration of the Ediacaran carbon-isotope curve. Precambrian Res. 182, 382–401 (2010).
Gerstenberger, H. & Haase, G. A highly effective emitter substance for mass spectrometric Pb isotope ratio determinations. Chem. Geol. 136, 309–312 (1997).
Condon, D. J., Schoene, B., McLean, N. M., Bowring, S. A. & Parrish, R. R. Metrology and traceability of U–Pb isotope dilution geochronology (EARTHTIME tracer calibration part I). Geochim. Cosmochim. Acta 164, 464–480 (2015).
McLean, N., Condon, D. J., Schoene, B. & Bowring, S. A. Evaluating uncertainties in the calibration of isotopic reference materials and multi-element isotopic tracers (EARTHTIME tracer calibration part II). Geochim. Cosmochim. Acta 164, 481–501 (2015).
Jaffey, A. H., Flynn, K. F., Glendenin, L. E., Bentley, W. C. & Essling, A. M. Precision measurement of half-lives and specific activities of 235U and 238U. Phys. Rev. C4, 1889–1906 (1971).
Hiess, J., Condon, D. J., McLean, N. & Noble, S. R. 238U/235U systematics in terrestrial uranium-bearing minerals. Science 335, 1610–1614 (2012).
Hickman-Lewis, K., Garwood, R. J., Withers, P. J. & Wacey, D. X-ray microtomography as a tool for investigating the petrological context of Precambrian cellular remains. Geol. Soc. Spec. Publ. 448, 33–56 (2016).
Sutton, M. D., Garwood, R. J., Siveter, D. J. & Siveter, D. J. SPIERS and VAXML; a software toolkit for tomographic visualisation and a format for virtual specimen interchange. Palaeontol. Electron. 15, 1–14 (2012).
Garwood, R. et al. Tomographic reconstruction of neopterous Carboniferous insect nymphs. PLoS ONE 7, e45779 (2012).
Schindelin, J., Rueden, C. T., Hiner, M. C. & Eliceiri, K. W. The ImageJ ecosystem: an open platform for biomedical image analysis. Mol. Reprod. Dev. 82, 518–529 (2015).
Fraley, C. & Raftery, A. E. MCLUST: software for model-based cluster analysis. J. Classif. 16, 297–306 (1999).
Darroch, S. A., Laflamme, M. & Clapham, M. E. Population structure of the oldest known macroscopic communities from Mistaken Point, Newfoundland. Paleobiology 39, 591–608 (2013).
Grotzinger, J. P., Bowring, S. A., Saylor, B. Z. & Kaufman, A. J. Biostratigraphic and geochronologic constraints on early animal evolution. Science 270, 598–604 (1995).
Grazhdankin, D. Patterns of distribution in the Ediacaran biotas: facies versus biogeography and evolution. Paleobiology 30, 203–221 (2004).
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).
Condon, D. J. et al. U–Pb ages from the Neoproterozoic Doushantuo Formation, China. Science 308, 95–98 (2005).
Yang, C., Li, X. H., Zhu, M. & Condon, D. SIMS U–Pb zircon geochronological constraints on upper Ediacaran stratigraphic correlations, South China. Geol. Mag. 1–15 (2016).
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).
Noble, S. et al. Age and global context of the Ediacaran fossils of Charnwood Forest, Leicestershire, UK. Geol. Soc. Am. Bull. 127, 250–265 (2015).
We acknowledge the support and guidance of our co-author M. Brasier in the early stages of this work, and particularly his invitation for L.A.P. to undertake fieldwork in Brazil in 2012. Field costs for L.A.P. were supported by an undergraduate travel grant from St. Anne’s College, University of Oxford. Fieldwork costs for M.D.B. were supported by CNPq-Conselho Nacional Desenvolvimento Científico e Tecnológico- Brazil (Proc. 451245/2012-1). This project was supported by an NERC Isotope Geoscience Facilities Steering Committee grant (project IP-1560-0515). J.M.L., P.C.B., R.T., G.A.C.C., C.Q.C.D. and M.L.A.F.P. were supported by grant numbers 2009/02312-4, 2010/02677-0, 2013/17835-8 and 2016-06114-6, São Paulo Research Foundation (FAPESP), Brazil. A.G.L. and L.A.P. are supported by the Natural Environment Research Council (grant numbers NE/L011409/2 and NE/L501554/1, respectively). R.J.G. is a Scientific Associate at the Natural History Museum, London, and a member of the Interdisciplinary Centre for Ancient Life (UMRI). D.M. recognizes the support of an NSERC discovery grant. We are grateful to L. A. dos Santos Reis (Votorantim Cimentos) for facilitating access to the Laginha Mine. We thank L. Tarhan and S. Darroch for constructive reviews.
The authors declare no competing financial interests.
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Parry, L.A., Boggiani, P.C., Condon, D.J. et al. Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil. Nat Ecol Evol 1, 1455–1464 (2017). https://doi.org/10.1038/s41559-017-0301-9
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