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

Naturevolume 441, pages506–508 (2006)Cite this article

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 spiderAnoplodactylus 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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Figure 1:Hox gene expression in newly hatchedEndeis spinosa protonymphon larvae.
Figure 2:Expression patterns oflab,pb andDfd, and inferred correspondence among anterior body segments in mandibulates, arachnids and the protonymphon larva of pycnogonids.

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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

  1. Jérôme Murienne

    Present address: Muséum National d'Histoire Naturelle, UMR 5202 CNRS, Département Systématique et Evolution, case 50, 45 rue Buffon, 75005, Paris, France

  2. Céline Clabaut

    Present address: Department of Biology, Evolutionary Biology, University of Konstanz, D-78457, Konstanz, Germany

Authors and 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

  3. Muséum National d'Histoire Naturelle, UMR 5202 CNRS, Département Systématique et Evolution, case 50, 45 rue Buffon, 75005, Paris, France

    Céline Clabaut

  4. Department of Biology, Evolutionary Biology, University of Konstanz, D-78457, Konstanz, Germany

    Jérôme Murienne

Authors
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Corresponding author

Correspondence toMichaël Manuel.

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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 atnpg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure 1

Amino-acid sequence alignment of pycnogonidHox genes from this work with representative genes from various arthropods. (PDF 15 kb)

Supplementary Figure 2

Phylogenetic analysis ofEndeis spinosa Hox genes from this work, establishing their orthology relationships. (PDF 15 kb)

Supplementary Figure Legends

Text to accompany Supplementary Figures 1 and 2. (DOC 24 kb)

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Jager, M., Murienne, J., Clabaut, C.et al. Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider.Nature441, 506–508 (2006). https://doi.org/10.1038/nature04591

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Editorial Summary

Talking heads

The arthropods are a good example of how evolution shapes different body forms from a single ancestral species. They consist of a series of head and body segments, each with different appendages — claws, antennae, wings, legs. A recentNature paper offered a new explanation of some apparent anomalies. The curious arthropods called sea spiders, it was suggested, have appendages on the first head segment, providing a link with the arthropod ancestor. That work was based on neuroanatomical observations, but now, using molecular techniques, Jageret al. show that sea spiders, like all other living arthropods,have lost the first head appendages seen in fossils.

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