Exceptional preservation of soft-bodied Cambrian chordates provides our only direct information on the origin of vertebrates1,2. Fossil chordates from this interval offer crucial insights into how the distinctive body plan of vertebrates evolved, but reading this pre-biomineralization fossil record is fraught with difficulties, leading to controversial and contradictory interpretations3,4. The cause of these difficulties is taphonomic: we lack data on when and how important characters change as they decompose, resulting in a lack of constraint on anatomical interpretation and a failure to distinguish phylogenetic absence of characters from loss through decay3. Here we show, from experimental decay of amphioxus and ammocoetes, that loss of chordate characters during decay is non-random: the more phylogenetically informative are the most labile, whereas plesiomorphic characters are decay resistant. The taphonomic loss of synapomorphies and relatively higher preservation potential of chordate plesiomorphies will thus result in bias towards wrongly placing fossils on the chordate stem. Application of these data to Cathaymyrus (Cambrian period of China) and Metaspriggina (Cambrian period of Canada) highlights the difficulties: these fossils cannot be placed reliably in the chordate or vertebrate stem because they could represent the decayed remains of any non-biomineralized, total-group chordate. Preliminary data suggest that this decay filter also affects other groups of organisms and that ‘stem-ward slippage’ may be a widespread but currently unrecognized bias in our understanding of the early evolution of a number of phyla.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Holland, N. D. & Chen, J.-y. Origin and early evolution of the vertebrates: new insights from advances in molecular biology, anatomy, and palaeontology. Bioessays 23, 142–151 (2001)
Donoghue, P. C. J. & Purnell, M. A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312–319 (2005)
Donoghue, P. C. J. & Purnell, M. A. Distinguishing heat from light in debate over controversial fossils. Bioessays 31, 178–189 (2009)
Janvier, P. Les vertébrés avant le Silurien. Geobios 30, 931–950 (1997)
Janvier, P. The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Palaeontology 39, 259–287 (1996)
Smith, M. P., Sansom, I. J. & Cochrane, K. D. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 67–84 (System. Assoc. Spec. Vol. Ser. 61, Taylor & Francis, 2001)
Conway Morris, S. A redescription of a rare chordate, Metaspriggina walcotti Simonetta and Insom, from the Burgess Shale (Middle Cambrian), British Columbia, Canada. J. Paleontol. 82, 424–430 (2008)
Swalla, B. J. & Smith, A. B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Phil. Trans. R. Soc. Lond. B 363, 1557–1568 (2008)
Yasui, K. & Kaji, T. The lancelet and ammocoete mouths. Zool. Sci. 25, 1012–1019 (2008)
Gee, H. The amphioxus unleashed. Nature 453, 999–1000 (2008)
Janvier, P. Vertebrate characters and Cambrian vertebrates. C. R. Palevol 2, 523–531 (2003)
Mallatt, J. & Chen, J.-y. Fossil sister group of craniates: predicted and found. J. Morphol. 258, 1–31 (2003)
Briggs, D. E. G. Experimental taphonomy. Palaios 10, 539–550 (1995)
Briggs, D. E. G. The role of decay and mineralization in the preservation of soft-bodied fossils. Annu. Rev. Earth Planet. Sci. 31, 275–301 (2003)
Briggs, D. E. G. & Kear, A. J. Decay and preservation of polychaetes; taphonomic thresholds in soft-bodied organisms. Paleobiology 19, 107–135 (1993)
Briggs, D. E. G. & Kear, A. J. Decay of Branchiostoma: implications for soft-tissue preservation in conodonts and other primitive chordates. Lethaia 26, 275–287 (1993)
Richardson, M. K. & Wright, G. M. Developmental transformations in a normal series of embryos of the sea lamprey Petromyzon marinus (Linnaeus). J. Morphol. 257, 348–363 (2003)
Butterfield, N. J. Organic preservation of non-mineralizing organisms and the taphonomy of the Burgess Shale. Paleobiology 16, 272–286 (1990)
Butterfield, N. J. Exceptional fossil preservation and the Cambrian explosion. Integr. Comp. Biol. 43, 166–177 (2003)
Gaines, R. R., Briggs, D. E. G. & Zhao, Y. Cambrian Burgess Shale-type deposits share a common mode of fossilization. Geology 36, 755–758 (2008)
Shu, D.-g., Morris, S. C. & Zhang, X. L. A Pikaia-like chordate from the Lower Cambrian of China. Nature 384, 157–158 (1996)
Eriksson, M. Taxonomic discussion of the scolecodont genera Nereidavus Grinnel, 1877, and Protarabellites Stauffer, 1933 (Annelida, Polychaeta). J. Paleontol. 73, 403–406 (1999)
Merz, R. A. & Woodin, S. A. Polychaete chaete: function, fossils, and phylogeny. Integr. Comp. Biol. 46, 481–496 (2006)
Bartolomaeus, T., Purschke, G. & Hausen, H. Polychaete phylogeny based on morphological data – a comparison of current attempts. Hydrobiologia 535–536, 341–356 (2005)
Rouse, G. W. & Fauchald, K. Cladistics and polychaetes. Zool. Scr. 26, 139–204 (1997)
Fuentes, M. et al. Preliminary observations on the spawning conditions of the European Amphioxus (Branchiostoma lanceolatum) in captivity. J. Exp. Zool. B 302, 384–391 (2004)
Fedewa, L. A. & Lindell, A. Inhibition of growth for select gram-negative bacteria by tricaine methane sulfonate (MS-222). J. Herpetol. Med. Surg. 15, 13–17 (2005)
Sagemann, J., Bale, S. J., Briggs, D. E. G. & Parkes, R. J. Controls on the formation of authigenic minerals in association with decaying organic matter: an experimental approach. Geochim. Cosmochim. Acta 63, 1083–1095 (1999)
Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006)
Delarbre, C., Gallut, C., Barriel, V., Janvier, P. & Gachelin, G. Complete mitochondrial DNA of the hagfish, Eptatretus burgeri: the comparative analysis of mitochondrial DNA sequence strongly supports the cyclostome monophyly. Mol. Phylogenet. Evol. 22, 184–192 (2002)
This work was funded by UK Natural Environment Research Council grant NE/E015336/1. Specimens were provided by H. Escriva (Banyuls-sur-Mer, France) and B. Morland and S. Morland (Bellflask Ecological Survey), with practical assistance from C. Koch, C. Pratt and P. Griffiths. We thank D. Briggs for his feedback on the submitted manuscript.
Author Contributions S.E.G. and M.A.P. conceived and designed the research program; R.S.S., S.E.G. and M.A.P. designed the experimental setup; R.S.S. conducted the experimental work and analysed the data; and R.S.S., S.E.G. and M.A.P. wrote the paper.
The authors declare no competing financial interests.
About this article
Cite this article
Sansom, R., Gabbott, S. & Purnell, M. Non-random decay of chordate characters causes bias in fossil interpretation. Nature 463, 797–800 (2010). https://doi.org/10.1038/nature08745
Flume experiments reveal flows in the Burgess Shale can sample and transport organisms across substantial distances
Communications Earth & Environment (2021)
BMC Evolutionary Biology (2020)
Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence
Scientific Reports (2020)
First arboreal 'pelycosaurs' (Synapsida: Varanopidae) from the early Permian Chemnitz Fossil Lagerstätte, SE Germany, with a review of varanopid phylogeny