Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Non-random decay of chordate characters causes bias in fossil interpretation

Abstract

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, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Phylogeny and anatomy of chordates.
Figure 2: Results of experimental decay.
Figure 3: Morphological decay stages of Branchiostoma (left) and larval Lampetra (right) and the phylogenetic position of each stage if interpreted as a fossil.

Similar content being viewed by others

References

  1. 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)

    Article  CAS  Google Scholar 

  2. Donoghue, P. C. J. & Purnell, M. A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312–319 (2005)

    Article  Google Scholar 

  3. Donoghue, P. C. J. & Purnell, M. A. Distinguishing heat from light in debate over controversial fossils. Bioessays 31, 178–189 (2009)

    Article  Google Scholar 

  4. Janvier, P. Les vertébrés avant le Silurien. Geobios 30, 931–950 (1997)

    Article  Google Scholar 

  5. Janvier, P. The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Palaeontology 39, 259–287 (1996)

    Google Scholar 

  6. 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)

    Google Scholar 

  7. 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)

    Article  Google Scholar 

  8. Swalla, B. J. & Smith, A. B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Phil. Trans. R. Soc. Lond. B 363, 1557–1568 (2008)

    Article  Google Scholar 

  9. Yasui, K. & Kaji, T. The lancelet and ammocoete mouths. Zool. Sci. 25, 1012–1019 (2008)

    Article  Google Scholar 

  10. Gee, H. The amphioxus unleashed. Nature 453, 999–1000 (2008)

    Article  ADS  CAS  Google Scholar 

  11. Janvier, P. Vertebrate characters and Cambrian vertebrates. C. R. Palevol 2, 523–531 (2003)

    Article  Google Scholar 

  12. Mallatt, J. & Chen, J.-y. Fossil sister group of craniates: predicted and found. J. Morphol. 258, 1–31 (2003)

    Article  Google Scholar 

  13. Briggs, D. E. G. Experimental taphonomy. Palaios 10, 539–550 (1995)

    Article  ADS  Google Scholar 

  14. 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)

    Article  ADS  CAS  Google Scholar 

  15. Briggs, D. E. G. & Kear, A. J. Decay and preservation of polychaetes; taphonomic thresholds in soft-bodied organisms. Paleobiology 19, 107–135 (1993)

    Article  Google Scholar 

  16. 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)

    Article  Google Scholar 

  17. 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)

    Article  Google Scholar 

  18. Butterfield, N. J. Organic preservation of non-mineralizing organisms and the taphonomy of the Burgess Shale. Paleobiology 16, 272–286 (1990)

    Article  Google Scholar 

  19. Butterfield, N. J. Exceptional fossil preservation and the Cambrian explosion. Integr. Comp. Biol. 43, 166–177 (2003)

    Article  Google Scholar 

  20. 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)

    Article  ADS  CAS  Google Scholar 

  21. Shu, D.-g., Morris, S. C. & Zhang, X. L. A Pikaia-like chordate from the Lower Cambrian of China. Nature 384, 157–158 (1996)

    Article  ADS  CAS  Google Scholar 

  22. Eriksson, M. Taxonomic discussion of the scolecodont genera Nereidavus Grinnel, 1877, and Protarabellites Stauffer, 1933 (Annelida, Polychaeta). J. Paleontol. 73, 403–406 (1999)

    Article  Google Scholar 

  23. Merz, R. A. & Woodin, S. A. Polychaete chaete: function, fossils, and phylogeny. Integr. Comp. Biol. 46, 481–496 (2006)

    Article  Google Scholar 

  24. Bartolomaeus, T., Purschke, G. & Hausen, H. Polychaete phylogeny based on morphological data – a comparison of current attempts. Hydrobiologia 535–536, 341–356 (2005)

    Google Scholar 

  25. Rouse, G. W. & Fauchald, K. Cladistics and polychaetes. Zool. Scr. 26, 139–204 (1997)

    Article  Google Scholar 

  26. 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)

    Article  Google Scholar 

  27. 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)

    Article  Google Scholar 

  28. 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)

    Article  ADS  CAS  Google Scholar 

  29. Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006)

    Article  ADS  CAS  Google Scholar 

  30. 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)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark A. Purnell.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-3 with Legends and Supplementary References. (PDF 2344 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08745

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing