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Apoptotic wing degeneration and formation of an altruism-regulating glandular appendage (gemma) in the ponerine ant Diacamma sp. from Japan (Hymenoptera, Formicidae, Ponerinae)

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Abstract

We here show an example of morphological novelties, which have evolved from insect wings into the specific structures controlling social behaviour in an ant species. Most ant colonies consist of winged queen(s) and wingless workers. In the queenless ponerine ant Diacamma sp. from Japan, however, all female workers have a pair of small thoracic appendages, called “gemmae”, which are homologous to the forewings and acts as an organ regulating altruism expression. Most workers, whose gemmae are clipped off by other colony members, become nonreproductive helpers, while only a single individual with complete gemmae becomes functionally reproductive. We examined histologically the development of gemmae, and compared it with that of functional wings in males. Female larvae had well-developed wing discs for both fore- and hindwings. At pupation, however, the wing discs started to evaginate and later degenerate. The hindwing discs completely degenerated, while the degeneration of forewing discs was incomplete, leading to the formation of gemmae. The degeneration process involved apoptotic cell death as confirmed by TUNEL assay. In addition, glandular cells differentiated from the epithelial cells of the forewing buds after completion of pupation. The mechanism of developmental transition from wing to gemma can be regarded as an evolutionary gain of new function, which can be seen in insect appendages and vertebrate limbs.

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Acknowledgements

We thank S. Kawabata for introducing us to the sampling site of the focal ant species and for help in field sampling. Thanks are also due to R. Cornette, M. Machida, H. Katoh and S. Koshikawa for their assistance in field investigations, to C. Peeters for constructive comments on the manuscript, and to F. G. Issa for English editing. This work was supported by a Grant-in-Aid for Scientific Research (nos. 15687001, 13740435 and 13440228) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and by a Grant-in-Aid from the Research for the Future Program of the Japan Society for the Promotion of Sciences (JSPS).

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Correspondence to T. Miura.

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Edited by P. Simpson

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Gotoh, A., Sameshima, S., Tsuji, K. et al. Apoptotic wing degeneration and formation of an altruism-regulating glandular appendage (gemma) in the ponerine ant Diacamma sp. from Japan (Hymenoptera, Formicidae, Ponerinae). Dev Genes Evol 215, 69–77 (2005). https://doi.org/10.1007/s00427-004-0456-7

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