Abstract
Fossil records indicate that insect wings are pleural appendages, primitively present on three thoracic and the nine abdominal segments as wings and winglets, respectively1. Homeotic proteins are generally considered to be the ontogenic switches governing the choice of developmental pathway of such appendages2. Here we provide examples of regulatory changes in developmental genes leading to a homeotic transformation in the ectopic wing tissue of prothoracic or metathoracic segments in Drosophila melanogaster, which lead to the development of wings rather than halteres.
Main
Of the two homeotic clusters in Drosophila ( Antennapedia and Bithorax ) , only the Antennapedia ( Antp) gene is expressed in segments from which the wings and halteres arise. However, Antp is not required to form thoracic wing primordia or the adult wings3, indicating that ancestrally, wings probably arose in all segments without homeotic gene involvement (the homeotic ground state)3,4. Furthermore, regulatory interactions between homeotic proteins and the developmental genes involved in appendage formation seem to have been important evolutionary innovations in the diversification of arthropod body plans and appendages3. If this is true for the evolution of insect wings, then changes in homeotic or developmental genes should result in homeotic transformations.
The engrailed ( en ) gene encodes a homeodomain-containing transcription factor which establishes the posterior identity of embryonic and adult segments5. The wingless ( wg ) gene encodes a member of the Wnt family of signalling molecules which regulates several developmental pathways in embryos and imaginal discs6. We ectopically expressed en from a constitutive promoter in cell clones generated by the flp -out cassette7.
We identified clones expressing en on the wing and haltere by the presence of forked ( f ) bristles. As expected, those in the anterior compartment of wings showed characteristics of the posterior compartment and organized new anterior compartments in front of them (see also ref. 7). But all of the 65 clones that we observed induced transformations of halteres to wing in anterior haltere compartments, whereas the posterior haltere compartments maintained their normal structure and remained associated with transformed wing (Fig. 1a). Because Ultrabithorax ( Ubx ) mutations transform haltere primordia to wing primordia8, it is likely that this transformation of halteres into wings, or of wings into halteres by the absence of en function9, may be due to negative regulation of Ubx by en10.
To examine the role of wg, we used different hypomorphic alleles, such as wgP, wg1, wgCX3, wgCX4 and wglacZ (1112), some of which are regulatory mutations and, except for wg1, are homozygous lethal at different developmental stages. Several heteroallelic combinations are viable and we analysed these for defects or transformations at emergence or at pharate adult stages. Heteroallelic combination of wgP with wg1, wgCX3, wglacZ or wgCX4 induced the development of wings in the prothoracic (T1) segment. About 30% of the 200 wgP/ wglacZ flies examined had new T1 wing-like structures, ranging from rudimentary to well-formed (Fig. 1b).
In the wgP/ wg1 heteroallelic combination, T1 wings were seen in 25% of individuals whereas the mesothoracic (T2) wings and metathoracic (T3) halteres developed variably. In other heteroallelic combinations such as wgP/ wgCX3 or wgP/ wgCX4, 25% showed T1 wings but the T2 wings and T3 halteres were always absent. Presence of T1 wings even when normal T2 wings and T3 halteres were absent confirms a segment-specific differential expression and regulation between the homeotic and developmental genes.
The heteroallelic combination wgP/ wgCX3 also showed a varying degree of transformation of T3 legs into halteres in 10% of individuals (Fig. 1c), ranging from graded removal of the distal segments (tibia and tarsus), through distortion of the femur and graded removal of leg bristles, to transformation of the coxa and trochanter into the first and second segments of the haltere.
These homeotic transformations in Drosophila thoracic discs caused by the misexpression of developmental genes like wg or en indicate that altered regulation of developmental genes was important in the evolution of body plans and the elaboration of new structures.
References
Kukalova-Peck, J. Can. J. Zool. 61, 1618–1619 (1983).
Lewis, E. B. Nature 276, 565–570 (1978).
Carroll, S., Weatherbee, S. & Langeland, J. Nature 375, 58–61 (1995).
Warren, R. & Caroll, S. Curr. Opin. Genet. Dev. 5, 459–465 (1995).
Morata, G. & Lawrence, P. A. Nature 255, 614–617 (1975).
Siegfried, E. & Perrimon, N. BioEssays 16, 395–404 (1994).
Zecca, M., Basler, K. & Struhl, G. Development 121, 2265–2278 (1995).
Cohen, S. M. in The Development of Drosophila melanogaster (ed. Bate, M. & Martinez Arias, A.) 747-841 (Cold Spring Harbor Lab. Press, New York, 1993).
Eberlein, S. & Russell, M. A. Dev. Biol. 100, 227–237 (1983).
Qian, S., Capovilla, M. & Pirotta, V. EMBO J. 12, 3865–3877 (1993).
Baker, N. E. Development 102, 489–497 (1988).
Kassis, J. A., Noll, E., VanSickle, E. P., Odenwald, W. F. & Perrimon, N. Proc. Natl Acad. Sci. USA 89, 1919–1923 (1992).
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Emerald, B., Roy, J. Homeotic transformation in Drosophila. Nature 389, 684 (1997). https://doi.org/10.1038/39500
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DOI: https://doi.org/10.1038/39500
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