Nature 375, 58 - 61 (04 May 1995); doi:10.1038/375058a0

Homeotic genes and the regulation and evolution of insect wing number

Sean B. Carroll, Scott D. Weatherbee & James A. Langeland

Howard Hughes Medical Institute and University of Wisconsin-Madison, 1525 Linden Drive, Madison, Wisconsin 53706, USA

THE evolution of wings catalysed the radiation of insects which make up some 75 per cent of known animals. Fossil evidence suggests that wings evolved from a segment of the leg¹ and that early pterygotes bore wings on all thoracic and abdominal segments². The pterygote body plan subsequently diverged producing orders bearing three, two or just one pair of thoracic wings. We have investigated the role of homeotic genes in pterygote evolution by examining their function in Drosophila wing development and their expression in a primitive apterygote. Wing formation is not promoted by any homeotic gene, but is repressed in different segments by different homeotic genes. We suggest here that wings first arose without any homeotic gene involvement in an ancestor with a homeotic 'groundplan' similar to modern winged insects and that wing formation subsequently fell under the negative control of individual homeotic genes at different stages of pterygote evolution.

References

1.	Kukalova-Peck, J. Can. J. Zool. 61, 1618−1669 (1983).
2.	Kukalova-Peck, J. J. Morph. 156, 53−126 (1978).
3.	Alberga, A., Boulay, J.-L., Kempe, E., Dennefeld, C. & Haenlin, M. Development 111, 983−992 (1991). | PubMed | ISI | ChemPort |
4.	Williams, J. A., Bell, J. & Carroll, S. B. Genes Dev. 5, 2481−2495 (1991). | PubMed | ISI | ChemPort |
5.	Simpson, P. Genetics 105, 615−632 (1983). | ISI |
6.	Levine, M., Hafen, E., Garber, R. L. & Gehring, W. J. EMBO J. 2, 2037−2046 (1983). | PubMed | ISI | ChemPort |
7.	Carroll, S. B., Laymon, R. A., McCutcheon, M. A., Riley, P. D. & Scott, M. P. Cell 47, 113−122 (1986). | Article | PubMed | ISI | ChemPort |
8.	Riley, P. D., Carroll, S. B. & Scott, M. P. Genes Dev. 1, 716−730 (1987). | PubMed | ChemPort |
9.	Mahaffey, J. W. & Kaufman, T. C. Genetics 117, 51−60 (1987). | PubMed | ChemPort |
10.	White, R. A. H. & Wilcox, M. EMBO J. 4, 2035−2043 (1985). | ISI | ChemPort |
11.	Bate, M. & Martinez-Arias, A. Development 112, 755−761 (1991). | PubMed | ChemPort |
12.	Castelli-Gair, J., Greig, S., Micklem, G. & Akam, M. Development 120, 1983−1995 (1994). | PubMed | ChemPort |
13.	Struhl, G. Proc. natn. Acad. Sci. U.S.A. 78, 7380−7384 (1982).
14.	Brand, A. H. & Perrimon, N. Development 118, 401−415 (1993). | PubMed | ISI | ChemPort |
15.	Wootton, R. J. Paleontology 15, 662−675 (1972).
16.	Kukalova Peck, J. in The Insects of Australia 2nd edn Vol. 1 141−179 (Cornell Univ. Press, Ithaca, N.Y., 1991).
17.	Averof, M. & Akam, M. Curr. Biol. 3, 73−78 (1993). | Article | PubMed | ISI | ChemPort |
18.	Kelsh, R., Weinzierl, R. O., White, R. A. & Akam, M. Devl Genet. 15, 19−31 (1994). | ChemPort |
19.	Cohen, B., Wimmer, E. & Cohen, S. M. Mech. Dev. 33, 229−240 (1991). | Article | PubMed | ChemPort |
20.	Vachon, G. et al. Cell 71, 437−450 (1992). | Article | PubMed | ISI | ChemPort |
21.	Mann, R. S. Development 121, 3205−3212 (1994).
22.	Snodgrass, R. Principles of Insect Morphology (McGraw-Hill, New York, 1935).
23.	Lewis, E. B. Nature 276, 565−570 (1978). | PubMed | ISI | ChemPort |
24.	Raff, R. & Kaufman, T. Embryos, Genes and Evolution (Indiana Univ. Press, Bloomington, 1983).
25.	Akam, M., Dawson, I. & Tear, G. Development 104, 123−133 (1988).
26.	Mauhin, V., Lutz, Y., Dennefeld, C. & Alberga, A. Nucleic Acids Res. 21, 3951−3957 (1993). | PubMed | ISI | ChemPort |
27.	Condie, J. M., Mustard, J. A. & Brower, D. L. Drosophila Information Service 70, 52−54 (1991).
28.	Williams, J. A., Paddock, S. W., Vorwerk, K. & Carroll, S. B. Nature 368, 298−305 (1994). | Article | ISI |
29.	Andrew, D. J., Horner, M. A., Petitt, M. G., Smolik, S. M. & Scott, M. P. EMBO J. 13, 1132−1144 (1994). | PubMed | ISI | ChemPort |
30.	Hinz, U., Biebel, B. & Campos-Ortega, J. A. Cell 76, 77−87 (1994). | Article | PubMed | ISI | ChemPort |