Skip to main content

Thank you for visiting 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.

Changing role of even-skipped during the evolution of insect pattern formation


THE development of Drosophila is typical of the so-called long germband mode of insect development, in which the pattern of segments is established by the end of the blastoderm stage1,2. Short germband insects, such as the grasshopper Schistocerca americana, by contrast, generate all or most of their metameric pattern after the blastoderm stage by the sequential addition of segments during caudal elongation3. This difference is discernible at the molecular level in the pattern of initiation of the segment polarity gene engrailed4, and the homeotic gene abdominal-A (ref. 5). For example, in both types of insects, engrailed is expressed by the highly conserved germband stage4,6 in a pattern of regularly spaced stripes, one stripe per segment7–9. In Drosophila, the complete pattern is visible by the end of the blastoderm stage, although engrailed appears initially in alternate segments in a pair-rule pattern9–10 that reflects its known control by pair-rule genes such as even-skipped11*15. In contrast, in the grasshopper, the engrailed stripes appear one at a time after the blastoderm stage as the embryo elongates4. To address the molecular basis for this difference, we have cloned the grasshopper homologue of the Drosophila pair-rule gene even-skipped and show that it does not serve a pair-rule function in early development, although it does have a similar function in both insects during neurogenesis later in development.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


Prices may be subject to local taxes which are calculated during checkout


  1. Ingham, P. Nature 335, 25–34 (1988).

    Article  ADS  CAS  Google Scholar 

  2. Akam, M. Development 101, 1–22 (1987).

    CAS  Google Scholar 

  3. Sander, K. Adv. Insect Physiol. 12, 125–238 (1976).

    Article  Google Scholar 

  4. Patel, N. H., Kornberg, T. B. & Goodman, C. S. Development 107, 201–212 (1989).

    CAS  PubMed  Google Scholar 

  5. Tear, G., Akam, M. & Martinez-Arias, A. Development 110, 915–925 (1990).

    CAS  PubMed  Google Scholar 

  6. Sander, K. Development 104, (suppl.) 112–121 (1988).

    Google Scholar 

  7. Kornberg, T., Siden, I., O'Farrell, P. H. & Simon, M. Cell 40, 45–53 (1985).

    Article  CAS  Google Scholar 

  8. Fjose, A., McGinnis, W. & Gehring, W. J. Nature 313, 284–289 (1985).

    Article  ADS  CAS  Google Scholar 

  9. DiNardo, S., Kuner, J., Theis, J. & O'Farrell, P. H. Cell 43, 59–69 (1985).

    Article  CAS  Google Scholar 

  10. Weir, M. P. & Kornberg, T. Nature 318, 433–439 (1985).

    Article  ADS  CAS  Google Scholar 

  11. DiNardo, S. & O'Farrell, P. H. Genes Dev. 1, 1212–1225 (1987).

    Article  CAS  Google Scholar 

  12. Lawrence, P. A., Johnston, P., Macdonald, P. & Struhl, G. Nature 328, 440–442 (1987).

    Article  ADS  CAS  Google Scholar 

  13. Macdonald, P., Ingham, P. & Struhl, G. Cell 47, 721–734 (1986).

    Article  CAS  Google Scholar 

  14. Frasch, M., Hoey, T., Rushlow, C., Doyle, H. & Levine, M. EMB0 J. 6, 749–759 (1987).

    Article  CAS  Google Scholar 

  15. Frasch, M., Warrior, R., Tugwood, J. & Levine, M. Genes Dev. 2, 1824–1838 (1988).

    Article  CAS  Google Scholar 

  16. Doe, C. Q., Smouse, D. & Goodman, C. S. Nature 333, 376–378 (1988).

    Article  ADS  CAS  Google Scholar 

  17. Thomas, J. B., Bastiani, M. J., Bate, C. M. & Goodman, C. S. Nature 310, 203–207 (1984).

    Article  ADS  CAS  Google Scholar 

  18. Ruiz i Altaba, A. & Melton, D. A. Development 106, 173–183 (1989).

    CAS  PubMed  Google Scholar 

  19. Bastian, H. & Gruss, P. EMBO J. 9, 1839–1852 (1990).

    Article  CAS  Google Scholar 

  20. Dush, M. K. & Martin, G. M. Devl Biol. (in the press).

  21. Ruiz i Altaba, A. & Melton, D. A. Cell 57, 317–326 (1989).

    Article  CAS  Google Scholar 

  22. Ruiz i Altaba, A. & Melton, D. A. Trends Genet. 6, 57–64 (1990).

    Article  Google Scholar 

  23. D'Esposito, M. et al. Genomics 10, 43–50 (1991).

    Article  CAS  Google Scholar 

  24. Boncinelli, E., Simeone, A., Acampora, D. & Mavilio, F. Trends Genet. 7, 329–334 (1991).

    Article  CAS  Google Scholar 

  25. Cavener, D. R. Nucleic Acids Res. 15, 1353–1361 (1989).

    Article  Google Scholar 

  26. Grenningloh, G., Rehm, E. J. & Goodman, C. S. Cell 67, 45–57 (1991).

    Article  CAS  Google Scholar 

  27. Snow, P. M. et al. Proc. natn. Acad. Sci. U.S.A. 85, 5291–5295 (1988).

    Article  ADS  CAS  Google Scholar 

  28. Nilsson, B. & Abrahmsen, L. Meth. Enzym. 185, 144–161 (1990).

    Article  CAS  Google Scholar 

  29. Koerner, T. J., Hill, J. E., Meyers, A. M. & Tzagoloff, A. Meth. Enzym. 194, 477–490 (1991).

    Article  CAS  Google Scholar 

  30. Patel, N. H. et al. Cell 58, 955–968 (1989).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations


Rights and permissions

Reprints and Permissions

About this article

Cite this article

Patel, N., Ball, E. & Goodman, C. Changing role of even-skipped during the evolution of insect pattern formation. Nature 357, 339–342 (1992).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


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.


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