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Evolution of homeotic gene regulation and function in flies and butterflies

Nature volume 372, pages 458–461 (1994)Cite this article

An Erratum to this article was published on 02 February 1995

Abstract

IT has been proposed that the evolution of homeotic genes parallels, and to some degree directs, the evolution of segment diversity in the myriapod–insect lineage1–3. But the discovery of discrete Antennapedia complex (ANT-C) and bithorax complex (BX-C) gene members in Crustacea4, chelicerates5, annelids6–8 and various insects9–11, as well as in vertebrates12, indicates that the expansion and diversification of homeotic genes preceded the diversification of arthropods and insects. How, then, have these genes influenced the evolution of body plans? To address this question, we now examine homeotic gene expression and regulation in butterflies (Lepidoptera), which, unlike flies, possess larval abdominal limbs and two pairs of wings. We show that the difference in larval limb number between these insects results from striking changes in BX-C gene regulation in the butterfly abdomen, and we deduce that the wing-patterning genes regulated by Ultrabithorax have diverged in the course of butterfly and fly evolution. These findings have gen-eral implications for the role of homeotic genes in animal evolution.

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References

  1. Lewis, E. B. Am. Zoologist 3, 33–56 (1963).

    Article  Google Scholar 

  2. Lewis, E. B. Nature 276, 565–570 (1978).

    Article  ADS  CAS  Google Scholar 

  3. Akam, M., Dawson, I. & Tear, G. Development (suppl.) 104, 123–133 (1988).

    Google Scholar 

  4. Averof, M. & Akam, M. Curr. Biol. 3, 73–78 (1993).

    Article  CAS  Google Scholar 

  5. Cartwright, P., Dick, M. & Buss, L. W. Molec. Phylogent Evol. 2, 185–192 (1993).

    Article  CAS  Google Scholar 

  6. Wysocka-Diller, J. W., Aisemberg, G. O., Baumgarten, M., Levine, M. & Macagno, E. R. Nature 341, 760–763 (1989).

    Article  ADS  CAS  Google Scholar 

  7. Shankland, M., Martindale, M. Q., Nardelli-Haefliger, D., Baxter, E. & Price, D. Development (suppl.) 2, 29–38 (1991).

    Google Scholar 

  8. Dick, M. H. & Buss, L. W. Molec. Phylogenet. Evol. 3, 146–158 (1994).

    Article  CAS  Google Scholar 

  9. Stuart, J. J., Brown, S. J., Beeman, R. W. & Denell, R. E. Development 117, 233–243 (1993).

    CAS  Google Scholar 

  10. Kelsh, R., Dawson, I. A. & Akam, M. Development 117, 293–305 (1993).

    CAS  Google Scholar 

  11. Akam, M. et al. Development (in the press).

  12. McGinnis, W. & Krumlauf, R. Cell 68, 283–302 (1992).

    Article  CAS  Google Scholar 

  13. Karch, F. et al. Cell 43, 81–96 (1985).

    Article  CAS  Google Scholar 

  14. Karch, F., Bender, W. & Weiffenbach, B. Genes Dev. 4, 1573–1587 (1990).

    Article  CAS  Google Scholar 

  15. Macias, A., Casanova, J. & Morata, G. Development 110, 1197–1207 (1990).

    CAS  Google Scholar 

  16. Panganiban, G., Nagy, L. & Carroll, S. B. Curr. Biol. 4, 671–675 (1994).

    Article  CAS  Google Scholar 

  17. Vachon, G. et al. Cell 71, 437–450 (1992).

    Article  CAS  Google Scholar 

  18. Birket-Smith, S. J. R. Prolegs. Legs and Wings of Insects (Scandinavian Science, Copenhagen, 1984).

    Google Scholar 

  19. Beachy, P. A., Helfand, S. L. & Hogness, D. S. Nature 313, 545–551 (1985).

    Article  ADS  CAS  Google Scholar 

  20. White, R. A. H. & Wilcox, M. Cell 39, 163–167 (1984).

    Article  CAS  Google Scholar 

  21. Morata, G. & Garcia-Bellido, A. Wilhelm Roux Arch. dev. Biol. 179, 125–143 (1976).

    Article  CAS  Google Scholar 

  22. Struhl, G. Proc. natn. Acad. Sci. U.S.A. 79, 7380–7384 (1982).

    Article  ADS  CAS  Google Scholar 

  23. Beeman, R., Stuart, J. J., Haas, M. S. & Denell, R. E. Devl Biol. 133, 196–209 (1989).

    Article  CAS  Google Scholar 

  24. Bateson, W. Materials for the Study of Variation (Macmillan, London, 1894).

    Google Scholar 

  25. Goldschmidt, R. The Material Basis of Evolution (Yale University Press, New Haven, 1940).

    Google Scholar 

  26. Garcia-Bellido, A. Am. Zool. 17, 613–629 (1977).

    Article  Google Scholar 

  27. Raff, R. & Kaufman, T. Embryos, Genes and Evolution: The Development Genetic Basis of Evolutionary Change (Macmillan, New York, 1983).

    Google Scholar 

  28. Garcia-Fernandez, J. & Holland, P. W. H. Nature 370, 563–566 (1994).

    Article  ADS  CAS  Google Scholar 

  29. Sanger, F., Niden, S. & Coulson, A. R. Proc. natn. Acad. Sci. U.S.A. 74, 5463–5467 (1977).

    Article  ADS  CAS  Google Scholar 

  30. Tabor, S. & Richardson, C. C. Proc. natn. Acad. Sci. U.S.A. 84, 4767–4771 (1987).

    Article  ADS  CAS  Google Scholar 

  31. Kelsh, R., Weinzierl, R. O. J., White, R. A. H. & Akam, M. Devl Genet. 15, 19–31 (1994).

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Howard Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin-Madison, 1525 Linden Drive, Madison, Wisconsin, 53706, USA

    Robert W. Warren, Lisa Nagy, Jane Selegue, Julie Gates & Sean Carroll

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  1. Robert W. Warren
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  2. Lisa Nagy
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Warren, R., Nagy, L., Selegue, J. et al. Evolution of homeotic gene regulation and function in flies and butterflies. Nature 372, 458–461 (1994). https://doi.org/10.1038/372458a0

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