Letter | Published:

Primitive soft-bodied cephalopods from the Cambrian

Nature volume 465, pages 469472 (27 May 2010) | Download Citation

Abstract

The exquisite preservation of soft-bodied animals in Burgess Shale-type deposits provides important clues into the early evolution of body plans that emerged during the Cambrian explosion1. Until now, such deposits have remained silent regarding the early evolution of extant molluscan lineages—in particular the cephalopods. Nautiloids, traditionally considered basal within the cephalopods, are generally depicted as evolving from a creeping Cambrian ancestor whose dorsal shell afforded protection and buoyancy2. Although nautiloid-like shells occur from the Late Cambrian onwards, the fossil record provides little constraint on this model, or indeed on the early evolution of cephalopods. Here, we reinterpret the problematic Middle Cambrian animal Nectocaris pteryx3,4 as a primitive (that is, stem-group), non-mineralized cephalopod, based on new material from the Burgess Shale. Together with Nectocaris, the problematic Lower Cambrian taxa Petalilium5 and (probably) Vetustovermis6,7 form a distinctive clade, Nectocarididae, characterized by an open axial cavity with paired gills, wide lateral fins, a single pair of long, prehensile tentacles, a pair of non-faceted eyes on short stalks, and a large, flexible anterior funnel. This clade extends the cephalopods’ fossil record2 by over 30 million years, and indicates that primitive cephalopods lacked a mineralized shell, were hyperbenthic, and were presumably carnivorous. The presence of a funnel suggests that jet propulsion evolved in cephalopods before the acquisition of a shell. The explosive diversification of mineralized cephalopods in the Ordovician may have an understated Cambrian ‘fuse’.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    The Crucible of Creation: the Burgess Shale and the rise of animals (Oxford Univ. Press, 1997)

  2. 2.

    , & The bearing of new Late Cambrian monoplacophoran genus Knightoconus upon the origin of Cephalopoda. Lethaia 6, 275–309 (1973)

  3. 3.

    Nectocaris pteryx, a new organism from the Middle Cambrian Burgess Shale of British Columbia. Neues Jb. Geol. Paläont. MH 12, 703–713 (1976)

  4. 4.

    Is Nectocaris pteryx a chordate? Boll. Zool. 55, 63–68 (1988)

  5. 5.

    et al. Early Cambrian Chengjiang fauna from Kunming region, China (Yunnan Science and Technology Press, 1999)

  6. 6.

    , & An Early Cambrian problematic fossil: Vetustovermis and its possible affinities. Proc. R. Soc. B 272, 2003–2007 (2005)

  7. 7.

    Lower Cambrian Crustacea and annelid worms from Kangaroo Island, South Australia. Alcheringa 3, 21–31 (1979)

  8. 8.

    The Arthropod Odaraia alata Walcott, Middle Cambrian, Burgess Shale, British Columbia. Phil. Trans. R. Soc. Lond. B 291, 541–582 (1981)

  9. 9.

    , & Fossil diagenesis in the Burgess Shale. Palaeontology 50, 537–543 (2007)

  10. 10.

    , & Sedimentation of the Phyllopod Bed within the Cambrian Burgess Shale Formation of British Columbia. J. Geol. Soc. Lond. 165, 307–318 (2008)

  11. 11.

    A redescription of the Middle Cambrian worm Amiskwia sagittiformis Walcott from the Burgess Shale of British Columbia. Paläontologische Zeitschrift 51, 271–287 (1977)

  12. 12.

    & Pennsylvanian invertebrates of the Mazon Creek Area, Illinois: the morphology and affinities of Tullimonstrum. Fieldiana: Geology 12, 119–150 (1969)

  13. 13.

    Major divisions of the Cephalopoda. J. Paleontol. 35, 569–574 (1961)

  14. 14.

    Ontogeny of the fused tentacles in three species of ommastrephid squids (Cephalopoda, Ommastrephidae). Invertebr. Biol. 124, 25–38 (2005)

  15. 15.

    An Early Cambrian Radula. J. Paleontol. 82, 543–554 (2008)

  16. 16.

    in Palaeontology and neontology of cephalopods (eds Clarke, M. R. & Trueman, E. R.) 103–122 (Academic Press, 1985)

  17. 17.

    Brachiopod identity of the alleged monoplacophoran ancestors of cephalopods. Malacologia 52, 97–113 (2010)

  18. 18.

    , , , & Molluscan shell evolution with review of shell calcification hypothesis. Comp. Biochem. Physiol. B 154, 351–371 (2009)

  19. 19.

    , & New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. Geological Society, London, Special Publications 286, 157–179 (2007)

  20. 20.

    , , & A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale. Nature 442, 159–163 (2006)

  21. 21.

    & The cuticle of the Aplacophora and its evolutionary significance in the Mollusca. J. Zool. 154, 443–451 (1968)

  22. 22.

    , , , & Skeletal matrices, muci, and the origin of invertebrate calcification. Proc. Natl Acad. Sci. USA 93, 1554–1559 (1996)

  23. 23.

    , , , & Molluscan shell proteins: primary structure, origin, and evolution. Curr. Top. Dev. Biol. 80, 209–276 (2007)

  24. 24.

    et al. Parallel evolution of nacre building gene sets in molluscs. Mol. Biol. Evol. 27, 591–608 (2010)

  25. 25.

    , , & Arthropod visual predators in the early pelagic ecosystem: evidence from the Burgess Shale and Chengjiang biotas. Proc. R. Soc. B 276, 2567–2574 (2009)

Download references

Acknowledgements

We thank S. Conway Morris, D. Fuchs, A. Lindgren, A. Scheltema, C. Schander and M. Vecchione for critically reading earlier drafts; R. Gaines for comments on preservation; J.-Y. Chen, M.-Y. Zhu and J. Paterson for images of Petalilium and Vetustovermis; and Parks Canada for research and collection permits delivered to Royal Ontario Museum teams led by D. Collins. P. Fenton assisted with collections, and S. Lackie with scanning electron microscopy. This research was undertaken as part of a PhD thesis (M.R.S.) in the Department of Ecology and Evolutionary Biology, University of Toronto. Funding was provided by Natural Sciences and Engineering Research Council of Canada Discovery Grant through J.-B.C and University of Toronto fellowships to M.R.S. This is Royal Ontario Museum Burgess Shale Research Project 27.

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Toronto, 25 Harbord Street, Toronto, Ontario, M5S 3G5, Canada

    • Martin R. Smith
    •  & Jean-Bernard Caron
  2. Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario, M5S 2C6, Canada

    • Martin R. Smith
    •  & Jean-Bernard Caron

Authors

  1. Search for Martin R. Smith in:

  2. Search for Jean-Bernard Caron in:

Contributions

Both authors contributed to the research and writing of this article.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jean-Bernard Caron.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Information, References, Supplementary Figures 1-13 with legends and Supplementary Tables 1–2.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature09068

Further reading

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.