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.

Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia

Subjects

Abstract

Despite the status of the eye as an “organ of extreme perfection”1, theory suggests that complex eyes can evolve very rapidly2. The fossil record has, until now, been inadequate in providing insight into the early evolution of eyes during the initial radiation of many animal groups known as the Cambrian explosion. This is surprising because Cambrian Burgess-Shale-type deposits are replete with exquisitely preserved animals, especially arthropods, that possess eyes3,4,5. However, with the exception of biomineralized trilobite eyes, virtually nothing is known about the details of their optical design. Here we report exceptionally preserved fossil eyes from the Early Cambrian (515 million years ago) Emu Bay Shale of South Australia, revealing that some of the earliest arthropods possessed highly advanced compound eyes, each with over 3,000 large ommatidial lenses and a specialized ‘bright zone’. These are the oldest non-biomineralized eyes known in such detail, with preservation quality exceeding that found in the Burgess Shale and Chengjiang deposits. Non-biomineralized eyes of similar complexity are otherwise unknown until about 85 million years later6,7. The arrangement and size of the lenses indicate that these eyes belonged to an active predator that was capable of seeing in low light. The eyes are more complex than those known from contemporaneous trilobites and are as advanced as those of many living forms. They provide further evidence that the Cambrian explosion involved rapid innovation in fine-scale anatomy as well as gross morphology, and are consistent with the concept that the development of advanced vision helped to drive this great evolutionary event8.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Complex arthropod eyes from the Early Cambrian.
Figure 2: Cambrian arthropod eye SAM P43629, imaged using a Leica MZ16FA relief-map stereomicroscope.
Figure 3: Complexity of the Early Cambrian Emu Bay Shale eyes compared to eyes in other early Palaeozoic taxa.

References

  1. Darwin, C. On the Origin of Species by Means of Natural Selection (John Murray, 1859)

    Google Scholar 

  2. Nilsson, D. E. & Pelger, S. A pessimistic estimate of the time required for an eye to evolve. Proc. R. Soc. Lond. B 256, 53–58 (1994)

    ADS  CAS  Article  Google Scholar 

  3. Briggs, D. E. G., Erwin, D. H. & Collier, F. J. The Fossils of the Burgess Shale (Smithsonian Institution Press, 1994)

    Google Scholar 

  4. Hou, X.-G. et al. The Cambrian Fossils of Chengjiang, China: The Flowering of Early Animal Life (Blackwell, 2004)

    Google Scholar 

  5. Conway-Morris, S. The Crucible of Creation: The Burgess Shale and the Rise of Animals (Oxford Univ. Press, 1998)

    Google Scholar 

  6. Ritchie, A. Ainiktozoon loganense Scourfield, a protochordate? from the Silurian of Scotland. Alcheringa 9, 117–142 (1985)

    Article  Google Scholar 

  7. van der Brugghen, W., Schram, F. R. & Martill, D. M. The fossil Ainiktozoon is an arthropod. Nature 385, 589–590 (1997)

    ADS  CAS  Article  Google Scholar 

  8. Parker, A. On the origin of optics. Opt. Laser Technol. 43, 323–329 (2011)

    ADS  CAS  Article  Google Scholar 

  9. Haug, J. T., Maas, A. & Waloszek, D. Ontogeny of two Cambrian stem crustaceans, Goticaris longispinosa and Cambropachycope clarksoni . Palaeontographica Abt. A 289, 1–43 (2009)

    Article  Google Scholar 

  10. Plotnick, R. E., Dornbos, S. Q. & Chen, J.-Y. Information landscapes and sensory ecology of the Cambrian radiation. Paleobiology 36, 303–317 (2010)

    Article  Google Scholar 

  11. García-Bellido, D. C. et al. The bivalved arthropods Tuzoia and Isoxys with soft-part preservation from the lower Cambrian Emu Bay Shale Lagerstätte (Kangaroo Island, Australia). Palaeontology 52, 1221–1241 (2009)

    Article  Google Scholar 

  12. Gehling, J. G., Jago, J. B., Paterson, J. R., García-Bellido, D. C. & Edgecombe, G. D. The geological context of the lower Cambrian (Series 2) Emu Bay Shale Lagerstätte and adjacent stratigraphic units, Kangaroo Island, South Australia. Aust. J. Earth Sci. 58, 243–257 (2011)

    ADS  CAS  Article  Google Scholar 

  13. Paterson, J. R., Edgecombe, G. D., García-Bellido, D. C., Jago, J. B. & Gehling, J. G. Nektaspid arthropods from the lower Cambrian Emu Bay Shale Lagerstätte, South Australia, with a reassessment of lamellipedian relationships. Palaeontology 53, 377–402 (2010)

    Article  Google Scholar 

  14. Briggs, D. E. G. & Nedin, C. The taphonomy and affinities of the problematic fossil Myoscolex from the Lower Cambrian Emu Bay Shale of South Australia. J. Paleontol. 71, 22–32 (1997)

    Article  Google Scholar 

  15. McCormick, T. & Fortey, R. A. Independent testing of a paleobiological hypothesis: the optical design of two Ordovician pelagic trilobites reveals their relative paleobathymetry. Paleobiology 24, 235–253 (1998)

    Google Scholar 

  16. Zhang, X.-G. & Clarkson, E. N. K. The eyes of Lower Cambrian eodiscid trilobites. Palaeontology 33, 911–932 (1990)

    Google Scholar 

  17. Harzsch, S. & Hafner, G. Evolution of eye development in arthropods: Phylogenetic aspects. Arthropod Struct. Dev. 35, 319–340 (2006)

    Article  PubMed  Google Scholar 

  18. Wehner, R. in Comparative Physiology and Evolution of Vision in Invertebrates: C 287–616 (Springer, 1981)

    Book  Google Scholar 

  19. Oldham, S. et al. The Drosophila insulin/IGF receptor controls growth and size by modulating PtdInsP 3 levels. Development 129, 4103–4109 (2002)

    CAS  PubMed  Google Scholar 

  20. Freeman, M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651–660 (1996)

    CAS  Article  PubMed  Google Scholar 

  21. Land, M. F. & Nilsson, D.-E. Animal Eyes (Oxford Univ. Press, 2002)

    Google Scholar 

  22. Snyder, A. W. in Comparative Physiology and Evolution of Vision in Invertebrates A (ed. Autrum, H. ) 225–313 (Springer, 1979)

    Book  Google Scholar 

  23. Warrant, E. & Nilsson, D.-E. Invertebrate Vision (Cambridge Univ. Press, 2006)

    Google Scholar 

  24. Harzsch, S., Melzer, R. R. & Müller, C. H. G. Mechanisms of eye development and evolution of the arthropod visual system: The lateral eyes of myriapoda are not modified insect ommatidia. Org. Divers. Evol. 7, 20–32 (2007)

    Article  Google Scholar 

  25. Daley, A. C., Budd, G. E., Caron, J.-B., Edgecombe, G. D. & Collins, D. The Burgess Shale anomalocaridid Hurdia and its significance for early euarthropod evolution. Science 323, 1597–1600 (2009)

    ADS  CAS  Article  PubMed  Google Scholar 

  26. Vannier, J. et al. Tuzoia: morphology and lifestyle of a large bivalved arthropod of the Cambrian seas. J. Paleontol. 81, 445–471 (2007)

    Article  Google Scholar 

  27. Clarkson, E., Levi-Setti, R. & Horváth, G. The eyes of trilobites: The oldest preserved visual system. Arthropod Struct. Dev. 35, 247–259 (2006)

    Article  PubMed  Google Scholar 

  28. Schoenemann, B. & Clarkson, E. N. K. Eyes and vision in the Chengjiang arthropod Isoxys indicating adaptation to habitat. Lethaia 10.1111/j.1502–3931.2010.00239.x (30 September 2010)

  29. Schoenemann, B. & Clarkson, E. N. K. Analysis of fossilised eye systems and its relevance to palaeobiology. Entomol. Gen. 31, 287–299 (2008)

    Article  Google Scholar 

  30. Parker, A. In the Blink of an Eye: The Cause of the Most Dramatic Event in the History of Life (The Free Press, 2003)

    Google Scholar 

Download references

Acknowledgements

We thank P. and C. Buck for access to and assistance at the fossil site; N. Schroeder, M. Gemmell, R. Atkinson, M. A. Binnie and numerous others (Supplementary Table 3) for help with excavations and curatorial assistance; A. Netting, P. Hudson and Adelaide Microscopy for imaging; D. Birch and G. Brock for SEM-EDS analysis; A. Baonza and J. F. de Celis for discussions on arthropod eye development; R. Fortey and A. Parker for comments and the Australian Research Council (grant LP0774959), South Australian Museum, Spanish Ministry of Science (RYC2007-00090 and grant CGL2009-07073), Beach Energy and Sealink Pty Ltd for funding.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed directly to excavation and interpretation of fossil specimens, analysis and writing the paper. J.B.J., J.R.P. and M.S.Y.L. compiled comparative eye data, M.S.Y.L. conducted the stereomicroscopy and J.R.P. conducted the SEM-EDS analyses and digital photography.

Corresponding authors

Correspondence to Michael S. Y. Lee or John R. Paterson.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Tables 1-3, Supplementary References and Supplementary Figures 1-4 with legends. (PDF 1044 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lee, M., Jago, J., García-Bellido, D. et al. Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia. Nature 474, 631–634 (2011). https://doi.org/10.1038/nature10097

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature10097

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.

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