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Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum

Nature volume 433, pages 643–647 (2005)Cite this article

Abstract

The two pairs of wings that are characteristic of ancestral pterygotes (winged insects) have often undergone evolutionary modification. In the fruitfly, Drosophila melanogaster, differences between the membranous forewings and the modified hindwings (halteres) depend on the Hox gene Ultrabithorax (Ubx). The Drosophila forewings develop without Hox input, while Ubx represses genes that are important for wing development, promoting haltere identity1,2. However, the idea that Hox input is important to the morphologically specialized wing derivatives such as halteres, and not the more ancestral wings, requires examination in other insect orders. In beetles, such as Tribolium castaneum, it is the forewings that are modified (to form elytra), while the hindwings retain a morphologically more ancestral identity. Here we show that in this beetle Ubx ‘de-specializes’ the hindwings, which are transformed to elytra when the gene is knocked down. We also show evidence that elytra result from a Hox-free state, despite their diverged morphology. Ubx function in the hindwing seems necessary for a change in the expression of spalt, iroquois and achaete-scute homologues from elytron-like to more typical wing-like patterns. This counteracting effect of Ubx in beetle hindwings represents a previously unknown mode of wing diversification in insects.

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Figure 1: Function of Hox genes in fore- and hindwing differentiation in insects.
Figure 2: RNAi phenotypes of Hox genes in Tribolium.
Figure 3: Wing genes' expression in hindwing and elytron disc.

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Acknowledgements

We thank G. Bucher, M. Weber and M. Klingler for the pu11 enhancer-trap line, R. White for the FP6.86 antibody, DSHB for the 4D9 antibody and G. Pflugfelder for sharing information about omb degenerate primers. We thank K. Leonard for maintaining beetle stocks, T. Shippy for discussion and reading and S. Brown, R. Beeman, S. Haas and all the Manhattan beetle/insect laboratory members for discussion and comments. Y.T. thanks A. Sato and T. Yamaguchi for discussion. This work was supported by the international Human Frontier Science Program Organization (Long-term Fellow) and the National Science Foundation.

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  1. Scott R. Wheeler

    Present address: Program in Molecular Biology and Biotechnology, The University of North Carolina at Chapel Hill, Campus Box 3280 - Fordham Hall, Chapel Hill, North Carolina, 27599-3280, USA

Authors and Affiliations

  1. Division of Biology, Chalmers Hall, Kansas State University, Manhattan, Kansas, 66506, USA

    Yoshinori Tomoyasu & Robin E. Denell

  2. Department of Genetics, Washington University School of Medicine, 4566 Scott Avenue, St Louis, Missouri, 63110, USA

    Scott R. Wheeler

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  1. Yoshinori Tomoyasu
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Correspondence to Yoshinori Tomoyasu.

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Supplementary information

Supplementary Figure 1

Detailed structures of elytra from wild-type, Cx RNAi (T1), and Utx RNAi (T3) adults. (PDF 107 kb)

Supplementary Figure 2

Transformed dorsal structures of Utx and ptl RNAi beetles. (PDF 85 kb)

Supplementary Figure 3

Relationship of Tc-iro stripes to the A/P boundary in the wing disc. (PDF 76 kb)

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Tomoyasu, Y., Wheeler, S. & Denell, R. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433, 643–647 (2005). https://doi.org/10.1038/nature03272

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