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Hox genes in brachiopods and priapulids and protostome evolution

Abstract

Understanding the early evolution of animal body plans requires knowledge both of metazoan phylogeny and of the genetic and developmental changes involved in the emergence of particular forms. Recent 18S ribosomal RNA phylogenies suggest a three-branched tree for the Bilateria comprising the deuterostomes and two great protostome clades, the lophotrochozoans1 and ecdysozoans2. Here, we show that the complement of Hox genes in critical protostome phyla reflects these phylogenetic relationships and reveals the early evolution of developmental regulatory potential in bilaterians. We have identified Hox genes that are shared by subsets of protostome phyla. These include a diverged pair of posterior (Abdominal-B -like) genes in both a brachiopod and a polychaete annelid, which supports the lophotrochozoan assemblage, and a distinct posterior Hox gene shared by a priapulid, a nematode and the arthropods, which supports the ecdysozoan clade. The ancestors of each of these two major protostome lineages had a minimum of eight to ten Hox genes. The major period of Hox gene expansion and diversification thus occurred before the radiation of each of the three great bilaterian clades.

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Figure 1: Alignment of Hox homeodomains and flanking sequences.
Figure 2: Phylogenetic analysis of bilaterian posterior Hox homeodomain sequences.
Figure 3: Distribution of Hox genes in bilaterians.

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References

  1. Halanych, K. M. et al. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267, 1641– 1643 (1995).

    Article  ADS  CAS  Google Scholar 

  2. Aguinaldo, A. M. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489– 493 (1997).

    Article  CAS  Google Scholar 

  3. Carroll, S. B. Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479–485 ( 1995).

    Article  ADS  CAS  Google Scholar 

  4. Balavoine, G. Are platyhelminthes coelomates without a coelom? An argument based on the evolution of Hox genes. Am. Zool. 38, 843–858 (1998).

    Article  CAS  Google Scholar 

  5. Grenier, J. K., Garber, T. L., Warre, R., Whitington, P. M. & Carroll, S. Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr. Biol. 7, 547–553 ( 1997).

    Article  CAS  Google Scholar 

  6. Adoutte, A., Balavoine, G., Lartillot, N. & de Rosa, R. Animal evolution: the end of the intermediate taxa? Trends Genet. 15, 104–108 ( 1999).

    Article  CAS  Google Scholar 

  7. Nielsen, C. Animal Evolution(Oxford Univ. Press, Oxford, 1995).

    Google Scholar 

  8. Lorenzen, S. in The Origins and Relationships of Lower Invertebrates(ed. Conway-Morris, S.) 210–223 (Clarendon, Oxford, 1985).

    Google Scholar 

  9. Boardmann, R. S., Cheetham, A. H. & Rowell, A. J. Fossil Invertebrates(Blackwell Scientific, Oxford, 1987).

    Google Scholar 

  10. Shankland, M., Martindale, M. Q., Nardelli-Haefliger, D., Baxter, E. & Price, D. J. Origin of segmental identity in the development of the leech nervous system. Development (Suppl. 2) 29–38 (1991).

  11. Wysocka-Diller, J. W., Aisemberg, G. O., Baumgarten, M., Levine, M. & Macagno, E. R. Characterization of a homologue of bithorax -complex genes in the leech Hirudo medicinalis. Nature 341, 760–763 (1989).

    Article  ADS  CAS  Google Scholar 

  12. Dick, M. H. & Buss, L. W. APCR-based survey of homeobox genes in Ctenodrilus serratus (Annelida: Polychaeta). Mol. Phylogenet. Evol. 3, 146–158 ( 1994).

    Article  CAS  Google Scholar 

  13. Wong, V. Y., Aisemberg, G. O., Gan, W. B. & Macagno, E. R. The leech homeobox gene Lox4 may determine segmental differentiation of identified neurons. J. Neurosci. 15, 5551–5559 (1995).

    Article  CAS  Google Scholar 

  14. Kmita-Cunisse, M., Loosli, F., Bièrne, J. & Gehring, W. J. Homeobox genes in the ribbonworm Lineus sanguineus : evolutionary implications. Proc. Natl Acad. Sci. USA 95, 3030– 3035 (1998).

    Article  ADS  CAS  Google Scholar 

  15. Snow, P. & Buss, L. W. HOM/Hox type homeoboxes from Stylaria lacustris (Annelida: Oligochaeta). Mol. Phylogenet. Evol. 3, 360–364 ( 1994).

    Article  CAS  Google Scholar 

  16. Degnan, B. M. & Morse, D. E. Identification of eight homeobox-containing transcripts expressed during larval development and at metamorphosis in the gastropod mollusc Haliotis rufescens. Mol. Mar. Biol. Biotechnol. 2, 1–9 (1993 ).

    CAS  PubMed  Google Scholar 

  17. Averof, M. & Akam, M. HOM/HOX genes in a crustacean: implications for the origin of insect and crustacean body plans. Curr. Biol. 3, 73–78 (1993 ).

    Article  CAS  Google Scholar 

  18. Akam, M. Hox and HOM: homologous gene clusters in insects and vertebrates. Cell 57, 347–349 ( 1989).

    Article  CAS  Google Scholar 

  19. Ruvkun, G. & Hobert, O. The taxonomy of developmental control in Caenorhabditis elegans. Science 282, 2033–2041 (1998).

    Article  ADS  CAS  Google Scholar 

  20. Brooke, N. M., Garcia-Fernàndez, J. & Holland, P. W. H. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392, 920–922 (1998).

    Article  ADS  CAS  Google Scholar 

  21. Schubert, F. R., Nieselt-Struwe, K. & Gruss, P. The Antennapedia -type homeobox genes have evolved from three precursors separated early in metazoan evolution. Proc. Natl Acad. Sci. USA 90, 143–147 (1993).

    Article  ADS  CAS  Google Scholar 

  22. Mackey, L. Y. et al. 18S rNA suggests that Entoprocta are protostomes, unrelated to Ectoprocta. J. Mol. Evol. 42, 552– 559 (1996).

    Article  ADS  CAS  Google Scholar 

  23. Balavoine, G. Identification of members of several homeobox gene classes in a planarian using a ligation-mediated polymerase chain reaction technique. Nucleic Acids Res. 24, 1547–1553 (1996).

    Article  MathSciNet  CAS  Google Scholar 

  24. Swofford, D. L. PAUP* Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4(Sinauer, Sunderland, MA, 1998).

    Google Scholar 

  25. Strimmer, K. & von Haeseler, A. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964–969 (1996).

    Article  CAS  Google Scholar 

  26. Garcia-Fernàndez, J. & Holland, P. W. H. Archetypal organization of the amphioxus Hox gene cluster. Nature 370, 563–566 (1994).

    Article  ADS  Google Scholar 

  27. Holland, P. W. H. & Garcia-Fernàndez, J. Hox genes and chordate evolution. Dev. Biol. 173 , 382–395 (1996).

    Article  CAS  Google Scholar 

  28. Duboule, D. et al. An update of mouse and human HOX gene nomenclature. Genomics 7, 458–459 (1990).

    Article  CAS  Google Scholar 

  29. Wang, B. B. et al. Ahomeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74, 29– 42 (1993).

    Article  CAS  Google Scholar 

  30. Martinez, P., Rast, J. P., Arenas-Mena, C. & Davidson, E. H. Organization of an echinoderm Hox gene cluster. Proc. Natl Acad. Sci. USA 96, 1469–1474 (1999).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank B. Winnepenninckx for L. anatina DNA; A. Knowlton, R. Highsmith, and P. Reynolds for P. caudatus tissue; E. Davidson for his interest and for sharing unpublished data; V. Kassner and N. Lartillot for their help; and A. Friday and G. Budd for comments on the manuscript. This work was supported by grants from the BBSRC and the Wellcome trust (M.E.A.); the Russian Basic Research Foundation and the Royal Society (T.A.); the CNRS, program ‘Genome’ and the Université Paris-Sud (A.A.); and the Howard Hughes Medical Institute (J.K.G. and S.B.C.).

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Correspondence to Guillaume Balavoine.

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de Rosa, R., Grenier, J., Andreeva, T. et al. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399, 772–776 (1999). https://doi.org/10.1038/21631

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