Abstract
Echinoderms possess one of the most highly derived body architectures of all metazoan phyla, with radial symmetry, a calcitic endoskeleton, and a water vascular system1,2. How these dramatic morphological changes evolved has been the subject of extensive speculation and debate3,4,5, but remains unresolved. Because echinoderms are closely related to chordates and postdate the protostome/deuterostome divergence2,3,6,7, they must have evolved from bilaterally symmetrical ancestors1,2,3,4,5,6. Here we report the expression domains in echinoderms of three important developmental regulatory genes ( distal-less, engrailed and orthodenticle ), all of which encode transcription factors that contain a homeodomain8. Our findings show that the reorganization of body architecture involved extensive changes in the deployment and roles of homeobox genes. These changes include modifications in the symmetry of expression domains and the evolution of several new developmental roles, as well as the loss of roles conserved between arthropods and chordates. Some of these modifications seem to have evolved very early in the history of echinoderms, whereas others probably evolved during the subsequent diversification of adult and larval morphology. These results demonstrate the evolutionary lability of regulatory genes that are widely viewed as conservative.
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References
Hyman, L. The Invertebrates Vol. 4, Echinodermata (McGraw-Hill, New York, 1955).
Brusca, R. C. & Brusca, G. J. Invertebrates (Sinauer, Sunderland, MA, 1990).
Jefferies, R. P. S., Brown, N. A. & Daley, P. E. J. The early phylogeny of chordates and echinoderms and the origin of chordate left-right asymmetry and bilateral symmetry. Acta Zool. 77, 101–122 (1996).
Holland, N. D. in Echinoderm Phylogeny and Evolutionary Biology (eds Paul, C. R. C. & Smith, A. B.) 13–25 (Clarendon, Oxford, 1988).
Raff, R. The Shape of Life (Chicago Univ. Press, 1996).
Nielsen, C. Animal Evolution: Interrelationships of the Animal Phyla (Oxford Univ. Press, 1995).
Turbeville, J. M., Schulz, J. R. & Raff, R. A. Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. Mol. Biol. Evol. 11, 648–655 (1994).
Duboule, D. (ed) Guidebook to the Homeobox Genes (Oxford Univ. Press, 1994).
Panganiban, G. et al. The origin and evolution of animal appendages. Proc. Natl Acad. Sci. USA 94, 5162–5166 (1997).
Patel, N. H. Developmental evolution: insights from studies of insect segmentation. Science 266, 581–590 (1994).
Finkelstein, R. & Boncinelli, E. From fly head to mammalian forebrain: the story of otx and Otd . Trends Genet. 10, 310–315 (1994).
Dickinson, J. Molecules and morphology: where's the homology? Trends Genet. 11, 119–121 (1995).
Bolker, J. & Raff, R. A. Developmental genetics and traditional homology. BioEssays 18, 489–494 (1996).
David, B. & Mooi, R. in Proceedings of the 9th International Echinoderm Conference (eds Mooi, R. & Telford, M.) (Balkema, Amsterdam, in the press).
Malinda, K. M. & Ettensohn, C. A. Primary mesenchyme cell migration in the sea urchin embryo: distribution of directional cues. Dev. Biol. 164, 562–578 (1994).
Kumé, M. & Dan, K. Invertebrate Embryology (NOLIT, Belgrade, 1968).
Holland, P. W. H. Homeobox genes and segmentation: co-option, co-evolution, and convergence. Semin. Sev. Biol. 1, 135–145 (1990).
Averof, M., Dawes, R. & Ferrier, D. Diversification of arthropod Hox genes as a paradigm for the evolution of gene functions. Semin. Cell Dev. Biol. 7, 539–551 (1996).
Gan, L. et al. An orthodentical-related protein from Strongylocentrotus purpuratus . Dev. Biol. 167, 517–528 (1995).
Dolecki, G. J. & Humphreys, T. An engrailed class homeo box gene in sea urchins. Gene 64, 21–31 (1988).
Sharman, A. C. & Holland, P. W. H. Conservation, duplication, and divergence of developmental genes during chordate evolution. Neth. J. Zool. 46, 47–67 (1996).
Smith, A. B. in Echinoderm Phylogeny and Evolutionary Biology (eds Paul, C. R. C. & Smith, A. B.) 85–97 (Clarendon, Oxford, 1988).
Wedeen, C. J. & Weisblat, D. A. Segmental expression of an engrailed -class gene during early development and neurogenesis in an annelid. Development 113, 805–814 (1991).
Lacalli, T. C. Mesodermal pattern and pattern repeats in the starfish bipinnaria larva, and related patterns in other deuterostome larvae and chordates. Phil. Trans. R. Soc. Lond. B 351, 1737–1758 (1996).
Slack, J. M. W., Holland, P. W. H. & Graham, C. F. The zootype and the phylotypic stage. Nature 361, 490–492 (1993).
DeRobertis, E. M. & Sasai, Y. Acommon plan for dorsoventral patterning in Bilateria. Nature 380, 37–40 (1996).
Strathmann, M. F. Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast (Univ. Washington Press, Seattle, WA, 1987).
Patel, N. H. et al. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955–968 (1989).
Patel, N. H. Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes. Methods. Cell Biol. 44, 446–487.
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Lowe, C., Wray, G. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389, 718–721 (1997). https://doi.org/10.1038/39580
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DOI: https://doi.org/10.1038/39580
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