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

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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Figure 1: Hox gene expression in newly hatched Endeis spinosa protonymphon larvae.
Figure 2: Expression patterns of lab, pb and Dfd , and inferred correspondence among anterior body segments in mandibulates, arachnids and the protonymphon larva of pycnogonids.

References

  1. 1

    Maxmen, A., Browne, W. E., Martindale, M. Q. & Giribet, G. Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment. Nature 437, 1144–1148 (2005)

    ADS  CAS  Article  Google Scholar 

  2. 2

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

    ADS  CAS  Article  Google Scholar 

  3. 3

    Scholtz, G. & Edgecombe, G. Heads, Hox and the phylogenetic position of trilobites. Crustac. Issues 16, 139–165 (2005)

    Article  Google Scholar 

  4. 4

    Eriksson, B. J., Tait, N. N. & Budd, G. E. Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J. Morphol. 255, 1–23 (2003)

    Article  Google Scholar 

  5. 5

    Mayer, G. & Koch, M. Ultrastructure and fate of the nephridial anlagen in the antennal segment of Epiperipatus biolleyi (Onychophora, Peripatidae)—evidence for the onychophoran antennae being modified legs. Arthrop. Struct. Dev. 34, 471–480 (2005)

    Article  Google Scholar 

  6. 6

    Popadic, A., Panganiban, G., Rusch, D., Shear, W. A. & Kaufman, T. C. Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev. Genes Evol. 208, 142–150 (1998)

    CAS  Article  PubMed  Google Scholar 

  7. 7

    Damen, W. G. M., Hausdorf, M., Seyfarth, E.-A. & Tautz, D. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc. Natl Acad. Sci. USA 95, 10665–10670 (1998)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Telford, M. J. & Thomas, R. H. Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc. Natl Acad. Sci. USA 95, 10671–10675 (1998)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Mittmann, B. & Scholtz, G. Development of the nervous system in the “head” of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev. Genes Evol. 213, 9–17 (2003)

    Google Scholar 

  10. 10

    Mallatt, J. M., Garey, J. R. & Schultz, J. W. Ecdysozoan phylogeny and bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol. Phyl. Evol. 31, 178–191 (2004)

    CAS  Article  Google Scholar 

  11. 11

    Dunlop, J. A. & Arango, C. P. Pycnogonid affinities: a review. J. Zool. Syst. Evol. Res. 43, 8–21 (2005)

    Article  Google Scholar 

  12. 12

    Giribet, G., Edgecombe, G. D. & Wheeler, W. C. Arthropod phylogeny based on eight molecular loci and morphology. Nature 413, 157–161 (2001)

    ADS  CAS  Article  PubMed  Google Scholar 

  13. 13

    Brusca, R. C. & Brusca, G. J. Invertebrates 2nd edn (Sinauer, Sunderland, Massachusetts, 2003)

    Google Scholar 

  14. 14

    Budd, G. E. & Telford, M. J. Along came a sea spider. Nature 437, 1099–1102 (2005)

    ADS  CAS  Article  PubMed  Google Scholar 

  15. 15

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

    CAS  Article  PubMed  Google Scholar 

  16. 16

    Meisenheimer, J. Beiträge zur entwicklungsgeschichte der pantopoden. I. Die entwicklung von Ammothea echinata hodge bis zur ausbildung der larvenform. Z. Wiss. Zool. 72, 191–248 (1902)

    Google Scholar 

  17. 17

    Winter, G. Beiträge zur morphologie und embryologie des vorderen körperabschnitts (Cephalosoma) der Pantopoda gerstaecker, 1863. Z. Zool. Syst. Evol.-Forsch. 18, 27–61 (1980)

    Article  Google Scholar 

  18. 18

    Sanchez, S. Le Développement des Pycnogonides et leurs Affinités avec les Arachnides. Thesis, CNRS, Paris (1959)

    Google Scholar 

  19. 19

    Morgan, T. H. A contribution to the embryology and phylogeny of the pycnogonids. Stud. Biol. Lab. Johns Hopkins Univ. 5, 1–76 (1891)

    Google Scholar 

  20. 20

    Babu, K. S. Anatomy of the central nervous system of arachnids. Zool. Jb. Anat. 82, 1–154 (1965)

    Google Scholar 

  21. 21

    Weygoldt, P. in Neurobiology of Arachnids (ed. Barth, F. G.) 20–37 (Springer, Berlin/Heidelberg/New York, 1985)

    Book  Google Scholar 

  22. 22

    Sandeman, D. C., Scholtz, G. & Sandeman, R. Brain evolution in decapod Crustacea. J. Exp. Zool. 295, 112–133 (1993)

    Article  Google Scholar 

  23. 23

    Henry, L. M. The nervous system of the pycnogonids. Microentomology USA 18, 16–36 (1953)

    Google Scholar 

  24. 24

    Schmidt-Rhaesa, A., Bartolomaeus, T., Lemburg, C., Ehlers, U. & Garey, J. R. The position of the Arthropoda in the phylogenetic system. J. Morphol. 238, 263–285 (1998)

    Article  PubMed  Google Scholar 

  25. 25

    Wiren, E. Zur morphologie und phylogenie der pantopoden. Zool. Bidr. Uppsala 6, 41–181 (1918)

    Google Scholar 

  26. 26

    Bullock, T. H. & Horridge, G. A. Structure and Function in the Nervous Systems of Invertebrates Vol. 2 (Freeman, San Francisco/London, 1965)

    Google Scholar 

  27. 27

    Scholtz, G. in Arthropod Relationships (eds Fortey, R. A. & Thomas, R. H.) 317–332 (Chapman and Hall, London, 1997)

    Google Scholar 

  28. 28

    Simonnet, F., Deutsch, J. & Quéinnec, E. hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev. Genes Evol. 214, 537–545 (2004)

    CAS  Article  PubMed  Google Scholar 

  29. 29

    Gibert, J. M., Mouchel-Vielh, E., Quéinnec, E. & Deutsch, J. S. Barnacle duplicate engrailed genes: divergent expression patterns and evidence for a vestigial abdomen. Evol. Dev. 2, 194–202 (2000)

    CAS  Article  PubMed  Google Scholar 

Download references

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.

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Correspondence to Michaël 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 at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure 1

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

Supplementary Figure 2

Phylogenetic analysis of Endeis 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. Nature 441, 506–508 (2006). https://doi.org/10.1038/nature04591

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