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.

Complex brain and optic lobes in an early Cambrian arthropod

Abstract

The nervous system provides a fundamental source of data for understanding the evolutionary relationships between major arthropod groups1,2. Fossil arthropods rarely preserve neural tissue. As a result, inferring sensory and motor attributes of Cambrian taxa has been limited to interpreting external features, such as compound eyes3 or sensilla decorating appendages4, and early-diverging arthropods have scarcely been analysed in the context of nervous system evolution. Here we report exceptional preservation of the brain and optic lobes of a stem-group arthropod from 520 million years ago (Myr ago), Fuxianhuia protensa5, exhibiting the most compelling neuroanatomy known from the Cambrian. The protocerebrum of Fuxianhuia is supplied by optic lobes evidencing traces of three nested optic centres serving forward-viewing eyes. Nerves from uniramous antennae define the deutocerebrum, and a stout pair of more caudal nerves indicates a contiguous tritocerebral component. Fuxianhuia shares a tripartite pre-stomodeal brain and nested optic neuropils with extant Malacostraca and Insecta2,6, demonstrating that these characters were present in some of the earliest derived arthropods. The brain of Fuxianhuia impacts molecular analyses that advocate either a branchiopod-like ancestor of Hexapoda7,8 or remipedes and possibly cephalocarids as sister groups of Hexapoda9,10. Resolving arguments about whether the simple brain of a branchiopod approximates an ancestral insect brain or whether it is the result of secondary simplification has until now been hindered by lack of fossil evidence. The complex brain of Fuxianhuia accords with cladistic analyses on the basis of neural characters, suggesting that Branchiopoda derive from a malacostracan-like ancestor but underwent evolutionary reduction and character reversal of brain centres that are common to hexapods and malacostracans2. The early origin of sophisticated brains provides a probable driver for versatile visual behaviours, a view that accords with compound eyes from the early Cambrian that were, in size and resolution, equal to those of modern insects and malacostracans3.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Fuxianhuia protensa from the Chengjiang Lagerstätte.
Figure 2: Brain of Fuxianhuia protensa and comparison with Malacostraca.
Figure 3: Eyes of fuxianhuiids and comparison to Malacostraca.

Similar content being viewed by others

References

  1. Harzsch, S. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Integr. Comp. Biol. 46, 162–194 (2006)

    Article  Google Scholar 

  2. Strausfeld, N. J. & Andrew, D. R. A new view of insect–crustacean relationships I. Inferences from neural cladistics and comparative neuroanatomy. Arthropod Struct. Dev. 40, 276–288 (2011)

    Article  Google Scholar 

  3. Paterson, J. R. et al. Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480, 237–240 (2011)

    Article  ADS  CAS  Google Scholar 

  4. Strausfeld, N. J. Some observations on the sensory organization of the crustaceamorph Waptia fieldensis Walcott. Palaeontogr. Canadiana 31, 157–169 (2011)

    Google Scholar 

  5. Chen, J.-Y., Edgecombe, G. D., Ramsköld, L. & Zhou, G.-Q. Head segmentation in early Cambrian Fuxianhuia: implications for arthropod evolution. Science 268, 1339–1342 (1995)

    Article  ADS  CAS  Google Scholar 

  6. Strausfeld, N. J. Arthropod Brains: Evolution, Functional Elegance, and Historical Significance (Belknap Press, 2012)

    Google Scholar 

  7. Glenner, H., Thomsen, P. F., Hebsgaard, M. B., Sørensen, M. V. & Willerslev, E. The origin of insects. Science 314, 1883–1884 (2006)

    Article  CAS  Google Scholar 

  8. Campbell, L. I. et al. MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc. Natl Acad. Sci. USA 108, 15920–15924 (2011)

    Article  ADS  CAS  Google Scholar 

  9. von Reumont, B. M. et al. Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Mol. Biol. Evol. 29, 1031–1045 (2012)

    Article  CAS  Google Scholar 

  10. Regier, J. C. et al. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079–1083 (2010)

    Article  ADS  CAS  Google Scholar 

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

    Google Scholar 

  12. Bergström, J., Hou, X.-G., Zhang, X.-G. & Clausen, S. A new view of the Cambrian arthropod Fuxianhuia. GFF 130, 189–201 (2008)

    Article  Google Scholar 

  13. Budd, G. E. Head structure in upper stem-group euarthropods. Palaeontology 51, 561–573 (2008)

    Article  Google Scholar 

  14. Waloszek, D., Chen, J.-Y., Haas, A. & Wang, X.-Q. Early Cambrian arthropods – new insights into arthropod head and structural evolution. Arthropod Struct. Dev. 31, 189–205 (2005)

    Article  Google Scholar 

  15. Gaines, R. R. et al. Mechanism for Burgess Shale-type preservation. Proc. Natl Acad. Sci. USA 109, 5180–5184 (2012)

    Article  ADS  CAS  Google Scholar 

  16. Hou, X.-G., Ma, X.-Y., Zhao, J. & Bergstrom, J. The lobopodian Paucipodia inermis from the lower Cambrian Chengjiang fauna, Yunnan, China. Lethaia 37, 234–244 (2004)

    Article  Google Scholar 

  17. Land, M. F. in Facets of Vision 90–111 (Springer, 1989)

    Google Scholar 

  18. Sandeman, D. C. & Scholtz, G. in The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach 329–347 (Birkhäuser, 1995)

    Google Scholar 

  19. Sombke, A. et al. Comparative analysis of deutocerebral neuropils in Chilopoda (Myriapoda): implications for the evolution of the arthropod olfactory system and support for the Mandibulata concept. BMC Neurosci. 13, 1–17 (2012)

    Article  Google Scholar 

  20. Boyan, G. S., Williams, J. L. D. & Hirth, F. in Evolution of Nervous Systems I 249–360 (Academic Press, 2006)

    Google Scholar 

  21. Kirsch, R. & Richter, S. The nervous system of Leptodora kindtii (Branchiopoda, Cladocera) surveyed with confocal scanning microscopy (CLSM), including general remarks on the branchiopod neuromorphological ground pattern. Arthropod Struct. Dev. 36, 143–156 (2007)

    Article  Google Scholar 

  22. Elofsson, R. & Dahl, E. The optic neuropils and chiasmata of Crustacea. Z. Zellforsch. Mikrosk. Anat. 107, 343–360 (1970)

    Article  CAS  Google Scholar 

  23. Strausfeld, N. J. The evolution of crustacean and insect optic lobes and the origin of chiasmata. Arthropod Struct. Dev. 34, 235–256 (2005)

    Article  Google Scholar 

  24. Sinakevitch, I., Douglass, J. K., Scholtz, G., Loesel, R. & Strausfeld, N. J. Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J. Comp. Neurol. 467, 150–172 (2003)

    Article  CAS  Google Scholar 

  25. Wolff, G., Harzsch, S., Hansson, B. S., Brown, S. & Strausfeld, N. Neuronal organization of the hemiellipsoid body of the land hermit crab Coenobita clypeatus: correspondence with the mushroom body ground pattern. J. Comp. Neurol. 520, 2824–2846 (2012)

    Article  Google Scholar 

  26. Fanenbruck, M. & Harzsch, S. A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Struct. Dev. 34, 343–378 (2005)

    Article  Google Scholar 

  27. Andrew, D. R., Brown, S. M. & Strausfeld, N. J. The minute brain of the copepod Tigriopus californicus supports a complex ancestral ground pattern of the tetraconate cerebral nervous systems. J. Comp. Neurol. 520, 3446–3470 (2012)

    Article  Google Scholar 

  28. Stegner, M. E. & Richter, S. Morphology of the brain in Hutchinsoniella macracantha (Cephalocarida, Crustacea). Arthropod Struct. Dev. 40, 221–243 (2011)

    Article  Google Scholar 

  29. Hanström, B. Eine genetische Studie über die Augen und Sehzentren von Turbellarien, Anneliden und Arthropoden (Trilobiten, Xiphosuren, Eurypteriden, Arachnoiden, Myriapoden, Crustaceen und Insekten). Kungl. Svensk. Vetenskapsakad. Handl. 4, 1–176 (1926)

    Google Scholar 

  30. Dohle, W. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name ‘Tetraconata’ for the monophyletic unit Crustacea + Hexapoda. Ann. Soc. Entomol. Fr. 37, 85–103 (2001)

    Google Scholar 

Download references

Acknowledgements

This account is dedicated to J. Bergström, who was first in suggesting a brain in YKLP 15006. The present work was supported by the National Natural Science Foundation of China (40730211), a Leverhulme Trust Research Project Grant (F/00 696/T), and the Center for Insect Science, University of Arizona. We thank A. Ball and J. Spratt for their assistance with scanning electron microscopy imagery and energy-dispersive X-ray spectroscopy, respectively.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed equally to this work.

Corresponding author

Correspondence to Xiaoya Ma.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-4. (PDF 672 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ma, X., Hou, X., Edgecombe, G. et al. Complex brain and optic lobes in an early Cambrian arthropod. Nature 490, 258–261 (2012). https://doi.org/10.1038/nature11495

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11495

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