Letter | Published:

Burgess Shale fossils illustrate the origin of the mandibulate body plan

Nature volume 545, pages 8992 (04 May 2017) | Download Citation

Abstract

Retracing the evolutionary history of arthropods has been one of the greatest challenges in biology1. During the past decade, phylogenetic analyses of morphological and molecular data2,3,4 have coalesced towards the conclusion that Mandibulata, the most diverse and abundant group of animals, is a distinct clade from Chelicerata, in that its members possess post-oral head appendages specialized for food processing, notably the mandible2,5. The origin of the mandibulate body plan, however, which encompasses myriapods, crustaceans and hexapods, has remained poorly documented1,6. Here we show that Tokummia katalepsis gen. et sp. nov., a large bivalved arthropod from the 508 million-year-old Marble Canyon fossil deposit (Burgess Shale, British Columbia), has unequivocal mandibulate synapomorphies, including mandibles and maxillipeds, as well as characters typically found in crustaceans, such as enditic, subdivided basipods and ring-shaped trunk segments. Tokummia and its closest relative, Branchiocaris (in Protocarididae, emended), also have an anteriormost structure housing a probable bilobed organ, which could support the appendicular origin of the labrum7. Protocaridids are retrieved with Canadaspis and Odaraia (in Hymenocarina, emended) as part of an expanded mandibulate clade, refuting the idea that these problematic bivalved taxa, as well as other related forms, are representatives of the basalmost euarthropods8,9. Hymenocarines now illustrate that the subdivision of the basipod and the presence of proximal endites are likely to have been ancestral conditions critical for the evolution of coxal and pre-coxal features in mandibulates10,11. The presence of crustaceomorph traits in the Cambrian larvae of various clades basal to Mandibulata is reinterpreted as evidence for the existence of distinct ontogenetic niches among stem arthropods. Larvae would therefore have constituted an important source of morphological novelty during the Cambrian period, and, through heterochronic processes, may have contributed to the rapid acquisition of crown-group characters and thus to greater evolutionary rates during the early radiation of euarthropods12.

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.

    & Origins and early evolution of arthropods. Palaeontology 57, 457–468 (2014)

  2. 2.

    , , , & Arthropod cladistics: combined analysis of histone H3 and U2 snRNA sequences and morphology. Cladistics 16, 155–203 (2000)

  3. 3.

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

  4. 4.

    . et al. A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata. Proc. R. Soc. B 278, 298–306 (2011)

  5. 5.

    , & The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int. J. Dev. Biol. 42, 801–810 (1998)

  6. 6.

    , & Cambrian origins and affinities of an enigmatic fossil group of arthropods. Nature 430, 554–557 (2004)

  7. 7.

    , & Homeotic evidence for the appendicular origin of the labrum in Tribolium castaneum. Dev. Genes Evol. 211, 96–102 (2001)

  8. 8.

    A palaeontological solution to the arthropod head problem. Nature 417, 271–275 (2002)

  9. 9.

    ., ., . & Cambrian bivalved arthropod reveals origin of arthrodization. Proc. R. Soc. B 279, 4699–4704 (2012)

  10. 10.

    & in Arthropod Relationships (eds & ) 139–153 (Chapman & Hall, 1998)

  11. 11.

    The evolution of arthropod limbs. Biol. Rev. Camb. Philos. Soc. 79, 253–300 (2004)

  12. 12.

    , & Rates of phenotypic and genomic evolution during the Cambrian explosion. Curr. Biol. 23, 1889–1895 (2013)

  13. 13.

    Middle Cambrian Branchiopoda, Malacostraca, Trilobita and Merostomata. Smithson. Misc. Collect. 57, 145–228 (1912)

  14. 14.

    New Lower and Middle Cambrian Crustacea. Proc. US Natl Mus. 76, 1–18 (1929)

  15. 15.

    The Arthropod Branchiocaris n. gen., Middle Cambrian, Burgess Shale, British Columbia. Geol. Surv. Can. Bull. 264, 1–29 (1976)

  16. 16.

    The morphology, mode of life, and affinities of Canadaspis perfecta (Crustacea: Phyllocarida), Middle Cambrian, Burgess Shale, British Columbia. Phil. Trans. R. Soc. Lond. B 281, 439–487 (1978)

  17. 17.

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

  18. 18.

    Homology of head sclerites in Burgess Shale euarthropods. Curr. Biol. 25, 1625–1631 (2015)

  19. 19.

    Making sense of ‘lower’ and ‘upper’ stem-group Euarthropoda, with comments on the strict use of the name Arthropoda von Siebold, 1848. Biol. Rev. Camb. Philos. Soc. 91, 255–273 (2016)

  20. 20.

    An acercostracan marrellomorph (Euarthropoda) from the Lower Ordovician of Morocco. Sci. Nat. 103, 21 (2016)

  21. 21.

    , , , & A new phyllopod bed-like assemblage from the Burgess Shale of the Canadian Rockies. Nat. Commun. 5, 3210 (2014)

  22. 22.

    The epistomo-labral plate and lateral lips in solifuges, pseudoscorpions and mites. Ekologia (Bratisl.) 19, 67–78 (2000)

  23. 23.

    & External morphology of limb development in the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124, 89–99 (2005)

  24. 24.

    , & Early development of the anterior body region of the grey widow spider Latrodectus geometricus Koch, 1841 (Theridiidae, Araneae). Arthropod Struct. Dev. 38, 401–416 (2009)

  25. 25.

    & Hox genes and the evolution of the arthropod body plan. Evol. Dev. 4, 459–499 (2002)

  26. 26.

    , & A large new leanchoiliid from the Burgess Shale and the influence of inapplicable states on stem arthropod phylogeny. Palaeontology 58, 629–660 (2015)

  27. 27.

    , , & Specialized appendages in fuxianhuiids and the head organization of early euarthropods. Nature 494, 468–471 (2013)

  28. 28.

    et al. Arthropod eyes: the early Cambrian fossil record and divergent evolution of visual systems. Arthropod Struct. Dev. 45, 152–172 (2016)

  29. 29.

    & Cephalic and limb anatomy of a new isoxyid from the Burgess Shale and the role of “stem bivalved arthropods” in the disparity of the frontalmost appendage. PLoS One 10, e0124979 (2015)

  30. 30.

    Ontogenetic niche shifts matter in community ecology: a review and future perspectives. Popul. Ecol. 57, 347–354 (2015)

  31. 31.

    PAUP*. Phylogenetic Analysis using Parsimony (*and Other Methods) Version 4.0a147 (Sinauer Associates, 2002)

Download references

Acknowledgements

We thank D. Erwin and B. Lieberman for access to collections at the Smithsonian Institution and at the University of Kansas Natural History Museum, respectively, M. S. Lee for help with the phylogenetic reconstruction, S. Scharf for editorial comments, D. Dufault for the technical drawings of Tokummia and L. Fields for the animations. We thank T. Keith from Parks Canada for providing field and logistical assistance. C.A.’s research was supported by fellowships from the University of Toronto (Department of Ecology and Evolutionary Biology) and J.-B.C.’s Natural Sciences and Engineering Research Council Discovery Grant (341944). This is Royal Ontario Museum Burgess Shale project number 69.

Author information

Author notes

    • Cédric Aria

    Present address: Nanjing Institute of Geology and Palaeontology, 39 East Beijing Road, Nanjing 210008, China.

Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario M5S3B2, Canada

    • Cédric Aria
    •  & Jean-Bernard Caron
  2. Department of Natural History (Palaeobiology Section), Royal Ontario Museum, Toronto, Ontario M5S2C6, Canada

    • Cédric Aria
    •  & Jean-Bernard Caron
  3. Department of Earth Sciences, University of Toronto, Toronto, Ontario M5S3B1, Canada

    • Jean-Bernard Caron

Authors

  1. Search for Cédric Aria in:

  2. Search for Jean-Bernard Caron in:

Contributions

C.A. wrote the initial drafts of the manuscript, Supplementary Information (including the taxonomic description) and character list, compiled morphological data and ran the phylogenetic analyses. J.-B.C. organized the expeditions at Marble Canyon, and prepared and photographed the specimens. Both authors contributed to the collection, observation and interpretation of fossils, as well as the conception and realisation of figures and reconstructions, and the writing of the final version of this manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Cédric Aria or Jean-Bernard Caron.

Reviewer Information Nature thanks J. Vannier and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains a Supplementary Discussion, Character list and Supplementary references.

Excel files

  1. 1.

    Supplementary Data

    This file contains the morphological matrix in Excel format.

Text files

  1. 1.

    Supplementary Data

    This file contains PAUP* data and command lines (Nexus file).

Videos

  1. 1.

    Three-dimensional reconstruction of Tokummia katalepsis.

    Rotating animation by Lars Fields.

  2. 2.

    Three-dimensional reconstruction of Tokummia katalepsis.

    Walk cycle animation by Lars Fields.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature22080

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.