Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Homeotic genes and the evolution of arthropods and chordates

Abstract

Clusters of homeotic genes sculpt the morphology of animal body plans and body parts. Different body patterns may evolve through changes in homeotic gene number, regulation or function. Recent evidence suggests that homeotic gene clusters were duplicated early in vertebrate evolution, but the generation of arthropod and tetrapod diversity has largely involved regulatory changes in the expression of conserved arrays of homeotic genes and the evolution of interactions between homeotic proteins and the genes they regulate.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Conway Morris, S. Nature 361, 219–225 (1993).

    ADS  Article  Google Scholar 

  2. 2

    Ohno, S. Evolution by Gene Duplication (Springer, New York, 1970).

    Google Scholar 

  3. 3

    Wilson, A. C. Scient. Am. 253, 164–173 (1985).

    CAS  Article  Google Scholar 

  4. 4

    Jacob, F. Science 196, 1161–1166 (1977).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Gould, S. Ontogeny and Phylogeny (Belknap, Cambridge, MA, 1977).

    Google Scholar 

  6. 6

    Raff, R. & Kaufman, T. Embryos, Genes and Evolution (Indiana Univ. Press, Bloomington, 1983).

    Google Scholar 

  7. 7

    Schummer, M., Scheurlen, I., Schaller, C. & Galliot, B. EMBO J. 11, 1815–1823 (1992).

    CAS  Article  Google Scholar 

  8. 8

    Wang, B. et al. Cell 74, 29–42 (1993).

    CAS  Article  Google Scholar 

  9. 9

    Akam, M. et al. Development (suppl.) 209–215 (1994).

  10. 10

    Kenyon, C. Cell 78, 175–180 (1994).

    CAS  Article  Google Scholar 

  11. 11

    Slack, J., Holland, P. & Graham, C. Nature 361, 490–492 (1993).

    ADS  CAS  Article  Google Scholar 

  12. 12

    Kaufman, T., Seeger, M. & Olsen, G. in Genetic Regulatory Hierarchies in Development (ed. Wright, T.) (Academic, San Diego, 1990).

    Google Scholar 

  13. 13

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

    ADS  CAS  Article  Google Scholar 

  14. 14

    Beeman, R., Stuart, J., Brown, S. & Denell, R. BioEssays 15, 439–444 (1993).

    CAS  Article  Google Scholar 

  15. 15

    Krumlauf, R. Cell 78, 191–201 (1994).

    CAS  Article  Google Scholar 

  16. 16

    Misof, B. & Wagner, G. CCE Tech. Report 24, Yale Univ. (1995).

  17. 17

    Stuart, J., Brown, S., Beeman, R. & Denell, R. Nature 350, 72–74 (1991).

    ADS  CAS  Article  Google Scholar 

  18. 18

    Ekker, S. C. et al. EMBO J. 13, 3551–3560 (1994).

    CAS  Article  Google Scholar 

  19. 19

    Gehring, W. et al. Cell 78, 211–233 (1994).

    CAS  Article  Google Scholar 

  20. 20

    Smith, D. L. & Johnson, A. D. EMBO J. 13, 2378–2387 (1994).

    CAS  Article  Google Scholar 

  21. 21

    Botas, J. Curr. Biol. 5, 1015–1022 (1993).

    CAS  Article  Google Scholar 

  22. 22

    Mastick, G., McKay, R., Oligino, T., Donovan, K. & Lopez, A. Genetics 139, 349–363 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23

    McGinnis, W., Levine, M., Hafen, E., Kuroiwa, A. & Gehring, W. Nature 308, 428–433 (1984).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Scott, M. P. & Weiner, A. J. Proc. natn. Acad. Sci. U.S.A. 81, 4115–4119 (1984).

    ADS  CAS  Article  Google Scholar 

  25. 25

    McGinnis, B. Genetics 137, 607–611 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

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

    ADS  CAS  Article  Google Scholar 

  27. 27

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

  28. 28

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

    CAS  Article  Google Scholar 

  29. 29

    Dick, M. & Buss, L. Molec. Phylog. Evol. 3, 146–158 (1994).

    CAS  Article  Google Scholar 

  30. 30

    Holland, P. W. H., Garcia-Fernandez, J., Williams, N. A. & Sidow, A. Development (suppl.) 125–133 (1994).

  31. 31

    Schubert, F., Nieselt-Struwe, K. & Gruss, P. Proc. natn. Acad. Sci. U.S.A. 90, 143–147 (1993).

    ADS  CAS  Article  Google Scholar 

  32. 32

    Brusca, R. & Brusca, G. Invertebrates (Sinauer, Sunderland, MA, 1990).

    Google Scholar 

  33. 33

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

    CAS  Article  Google Scholar 

  34. 34

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

    ADS  CAS  Article  Google Scholar 

  35. 35

    Mann, R. Development 120, 3205–3212 (1994).

    CAS  PubMed  Google Scholar 

  36. 36

    Averof, M. & Akam, M. Nature 376, 420–423 (1995).

    ADS  CAS  Article  Google Scholar 

  37. 37

    Warren, R., Nagy, L., Selegue, J., Gates, J. & Carroll, S. Nature 372, 458–461 (1994).

    ADS  CAS  Article  Google Scholar 

  38. 38

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

    Google Scholar 

  39. 39

    Carroll, S., Weatherbee, S. & Langeland, J. Nature 375, 58–61 (1995).

    ADS  CAS  Article  Google Scholar 

  40. 40

    Kukalova-Peck, J. J. Morph. 156, 53–126 (1978).

    Article  Google Scholar 

  41. 41

    Kukalova-Peck, J. Can. J. Zool. 61, 1618–1669 (1983).

    Article  Google Scholar 

  42. 42

    Condie, J., Mustard, J. & Brower, D. Drosoph. Inf. Serv. 70, 52–54 (1991).

    Google Scholar 

  43. 43

    Morata, G. & Garcia-Bellido, A. Wilhelm Roux Arch. Entw. Mech. Org. 179, 125–143 (1976).

    CAS  Article  Google Scholar 

  44. 44

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

    ADS  CAS  Article  Google Scholar 

  45. 45

    White, R. A. H. & Wilcox, M. Cell 39, 163–171 (1984).

    CAS  Article  Google Scholar 

  46. 46

    Nijhout, H. F. The Development and Evolution of Butterfly Wing Patterns (Smithsonian Institution, Washington DC, 1991).

    Google Scholar 

  47. 47

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

    CAS  Article  Google Scholar 

  48. 48

    Rancourt, D., Teruhisa, T. & Capecchi, M. Genes Dev. 9, 108–122 (1995).

    CAS  Article  Google Scholar 

  49. 49

    Graham, A. Curr. Biol. 4, 1135–1137 (1994).

    CAS  Article  Google Scholar 

  50. 50

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

    ADS  CAS  Article  Google Scholar 

  51. 51

    Pendleton, J., Nagai, B., Murtha, M. & Ruddle, F. Proc. natn. Acad. Sci. U.S.A. 90, 6300–6304 (1993).

    ADS  CAS  Article  Google Scholar 

  52. 52

    Kessel, M. & Gruss, P. Science 249, 374–379 (1990).

    ADS  CAS  Article  Google Scholar 

  53. 53

    Burke, A., Nelson, C., Morgan, B. & Tabin, C. Development 121, 333–346 (1995).

    CAS  PubMed  Google Scholar 

  54. 54

    Ahlberg, P. Nature 354, 298–301 (1991).

    ADS  Article  Google Scholar 

  55. 55

    Tabin, C. & Laufer, E. Nature 361, 692–693 (1993).

    ADS  Article  Google Scholar 

  56. 56

    Carroll, R. Vertebrate Paleontology and Evolution (Freeman, New York, 1988).

    Google Scholar 

  57. 57

    Ruddle, F., Bentley, K., Murtha, M. & Risch, N. Development (suppl.) 155–161 (1994).

  58. 58

    Gans, C. Am. Zool 15, 455–467 (1975).

    Article  Google Scholar 

  59. 59

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

    CAS  Article  Google Scholar 

  60. 60

    Jacobs, D. Proc. natn. Acad. Sci. U.S.A. 87, 4406–4410 (1990).

    ADS  CAS  Article  Google Scholar 

  61. 61

    Bonner, J. The Evolution of Complexity (Princeton Univ. Press, Princeton, NJ, 1988).

    Google Scholar 

  62. 62

    Duboule, D. BioEssays 14, 375–384 (1992).

    CAS  Article  Google Scholar 

  63. 63

    Sidow, A. Proc. natn. Acad. Sci. U.S.A. 89, 5098–5102 (1992).

    ADS  CAS  Article  Google Scholar 

  64. 64

    Simeone, A. et al. Proc. natn. Acad. Sci. U.S.A. 91, 2250–2254 (1994).

    ADS  CAS  Article  Google Scholar 

  65. 65

    Dickinson, W. J. in Evolutionary Biology (eds Dobzhansky, T., Hecht, M. & Steere, W. C.) 127–173 (Appleton-Century-Crofts, New York, 1991).

    Google Scholar 

  66. 66

    Galloni, M., Gyurkovics, P., Schedl, P. & Karch, F. EMBO J. 12, 1087–1097 (1993).

    CAS  Article  Google Scholar 

  67. 67

    Gindhart, J. Jr, King, A. & Kaufman, T. Genetics 139, 781–795 (1995).

    CAS  PubMed  Google Scholar 

  68. 68

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

    Google Scholar 

  69. 69

    Wallace, B. Q. Rev. Biol. 60, 31–42 (1985).

    Article  Google Scholar 

  70. 70

    Kostriken, R. & Weisblat, D. Devl Biol. 151, 225–241 (1992).

    CAS  Article  Google Scholar 

  71. 71

    Kingsley, D. Genes Dev. 8, 133–146 (1994).

    CAS  Article  Google Scholar 

  72. 72

    Hogan, B., Blessing, M., Winnier, G. & Suzuki, N. Development (suppl.) 53–60 (1994).

  73. 73

    Cohen, S., Bronner, F., Kuttner, G., Jurgens, G. & Jäckle, H. Nature 338, 432–434 (1989).

    ADS  CAS  Article  Google Scholar 

  74. 74

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

    CAS  Article  Google Scholar 

  75. 75

    McGinnis, W. & Kuziora, M. Scient. Am. 270, 58–66 (1994).

    CAS  Article  Google Scholar 

  76. 76

    Wheeler, W., Cartwright, P. & Hayashi, C. Cladistics 9, 1–39 (1993).

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Carroll, S. Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479–485 (1995). https://doi.org/10.1038/376479a0

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing