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Chelicerate neural ground pattern in a Cambrian great appendage arthropod

Nature volume 502, pages 364–367 (2013)Cite this article

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Abstract

Preservation of neural tissue in early Cambrian arthropods has recently been demonstrated1, to a degree that segmental structures of the head can be associated with individual brain neuromeres. This association provides novel data for addressing long-standing controversies about the segmental identities of specialized head appendages in fossil taxa2,3. Here we document neuroanatomy in the head and trunk of a ‘great appendage’ arthropod, Alalcomenaeus sp., from the Chengjiang biota, southwest China, providing the most complete neuroanatomical profile known from a Cambrian animal. Micro-computed tomography reveals a configuration of one optic neuropil separate from a protocerebrum contiguous with four head ganglia, succeeded by eight contiguous ganglia in an eleven-segment trunk. Arrangements of optic neuropils, the brain and ganglia correspond most closely to the nervous system of Chelicerata of all extant arthropods, supporting the assignment of ‘great appendage’ arthropods to the chelicerate total group4,5. The position of the deutocerebral neuromere aligns with the insertion of the great appendage, indicating its deutocerebral innervation and corroborating a homology between the ‘great appendage’ and chelicera indicated by morphological similarities4,6,7. Alalcomenaeus and Fuxianhuia protensa1 demonstrate that the two main configurations of the brain observed in modern arthropods, those of Chelicerata and Mandibulata, respectively8, had evolved by the early Cambrian.

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Figure 1: Alalcomenaeus sp. from the Chengjiang Lagerstätte.
Figure 2: Details of eye pairs and visual neuropils in Alalcomenaeus sp. YKLP 11075.
Figure 3: Leanchoiliid megacheiran arthropods from the Chengjiang Lagerstätte.
Figure 4: Nervous systems of Chelicerata.

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Acknowledgements

We thank N. Shimobayashi, H. Maeda, and T. Kogiso for arranging and performing EDXRF analyses, and D. Andrew for advice on cladistics. This work was supported by grants from the Natural Science Foundation of China (no. 40730211), Research in Education and Science from the Government of Japan (no. 21740370), a Leverhulme Trust Research Project Grant (F/00 696/T), by the Center for Insect Science, University of Arizona, and a grant from the Air Force Research Laboratories (FA8651-10-1-0001) to N.J.S.

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Authors and Affiliations

  1. Japan Agency for Marine-Earth Science and Technology, Yokosuka 2370061, Japan,

    Gengo Tanaka

  2. Yunnan Key Laboratory for Palaeobiology, Yunnan University, Kunming 650091, China,

    Xianguang Hou & Xiaoya Ma

  3. Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK,

    Xiaoya Ma & Gregory D. Edgecombe

  4. Department of Neuroscience and Center for Insect Science, University of Arizona, Tucson, 85721, Arizona, USA

    Nicholas J. Strausfeld

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  1. Gengo Tanaka
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  2. Xianguang Hou
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  4. Gregory D. Edgecombe
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  5. Nicholas J. Strausfeld
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Contributions

The project was conceived by G.T. Fossil data were analysed by all authors. G.D.E., N.J.S. and X.M. composed the text.

Corresponding authors

Correspondence to Xianguang Hou or Nicholas J. Strausfeld.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Cephalic region of Alalcomenaeus sp. YKLP 11075

All in dorsal view, composites of part and counterpart (upper left). Second left to right: CT scan (green); EDXRF Fe (red); superimposition of CT and EDXRF Fe. Lower row, left to right: EDXRF Cu (blue); superimposition of CT and EDXRF Cu; superimposition of EDXRF Fe and EDXRF Cu; superimposition of all scans. C1, first post-GA neuropil = tritocerebrum (tri); C2, second post-GA neuropil; GA, great appendage neuropil = deutocerebrum (deu); on1, first optic neuropil; pr, protocerebrum.

Extended Data Figure 2 Arthropod relationships based on neuroanatomical characters.

Strict consensus of 34 shortest cladograms based on 145 characters in Supplementary Information Table 2.

Supplementary information

Supplementary Information

This file contains Supplementary Tables 1-2, Phylogenetic Methods and Supplementary References. (PDF 249 kb)

Supplementary Data

This zipped file contains characters coded in phylogenetic analysis (in nexus format, it can be opened in freeware such as Mesquite and Nexus Data Editor). (ZIP 3 kb)

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Tanaka, G., Hou, X., Ma, X. et al. Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 502, 364–367 (2013). https://doi.org/10.1038/nature12520

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