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Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider

Nature volume 441, pages 506508 (25 May 2006) | Download Citation

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Abstract

Arthropod head segments offer a paradigm for understanding the diversification of form during evolution, as a variety of morphologically diverse appendages have arisen from them. There has been long-running controversy, however, concerning which head appendages are homologous among arthropods, and from which ancestral arrangement they have been derived. This controversy has recently been rekindled by the proposition that the probable ancestral arrangement, with appendages on the first head segment, has not been lost in all extant arthropods as previously thought, but has been retained in the pycnogonids, or sea spiders1. This proposal was based on the neuroanatomical analysis of larvae from the sea spider Anoplodactylus sp., and suggested that the most anterior pair of appendages, the chelifores, are innervated from the first part of the brain, the protocerebrum. Our examination of Hox gene expression in another sea spider, Endeis spinosa, refutes this hypothesis. The anterior boundaries of Hox gene expression domains place the chelifore appendages as clearly belonging to the second head segment, innervated from the second part of the brain, the deutocerebrum. The deutocerebrum must have been secondarily displaced towards the protocerebrum in pycnogonid ancestors. As anterior-most appendages are also deutocerebral in the other two arthropod groups, the Euchelicerata and the Mandibulata, we conclude that the protocerebral appendages have been lost in all extant arthropods.

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Acknowledgements

We thank the Station Biologique de Roscoff for providing laboratory facilities for specimen collection and preparation. We are grateful to E. Quéinnec, N. Rabet and P. Bunje for advice and discussion, to P. Lamarre for technical help and to T. Jaffredo for laboratory facilities. E. Houliston and G. Scholtz provided much help and insight. This work was funded by the CNRS and the French Ministry of Research.

Author information

Author notes

    • Jérôme Murienne
    •  & Céline Clabaut

    †Present addresses: Muséum National d'Histoire Naturelle, UMR 5202 CNRS, Département Systématique et Evolution, case 50, 45 rue Buffon, 75005 Paris, France (J.M.); Department of Biology, Evolutionary Biology, University of Konstanz, D-78457 Konstanz, Germany (C.C.)

Affiliations

  1. Université Pierre et Marie Curie-Paris 6, UMR 7138 CNRS UPMC MNHN ENS IRD, Case 05, 9 quai St Bernard, 75005 Paris, France

    • Muriel Jager
    • , Jérôme Murienne
    • , Céline Clabaut
    • , Hervé Le Guyader
    •  & Michaël Manuel
  2. Université Pierre et Marie Curie-Paris 6, UMR 7622 CNRS UPMC, 9 quai St Bernard, 75005 Paris, France

    • Jean Deutsch

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Competing interests

Sequences from this work have been deposited in the GenBank database with the following accession numbers: DQ315728 (E. spinosa lab); DQ315730 (E. spinosa pb); DQ315733 (E. spinosa Dfd); and DQ315734 (E. spinosa Scr). Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding author

Correspondence to Michaël Manuel.

Supplementary information

PDF files

  1. 1.

    Supplementary Figure 1

    Amino-acid sequence alignment of pycnogonid Hox genes from this work with representative genes from various arthropods.

  2. 2.

    Supplementary Figure 2

    Phylogenetic analysis of Endeis spinosa Hox genes from this work, establishing their orthology relationships.

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    Supplementary Figure Legends

    Text to accompany Supplementary Figures 1 and 2.

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https://doi.org/10.1038/nature04591

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