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First published online February 9, 2006
doi: 10.1242/10.1242/dev.02260

Development 133, 785-790 (2006)
Published by The Company of Biologists 2006
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Association of tracheal placodes with leg primordia in Drosophila and implications for the origin of insect tracheal systems

Xavier Franch-Marro1,*, Nicolás Martín1, Michalis Averof2,{dagger} and Jordi Casanova1,{dagger}

1 Institut de Biologia Molecular de Barcelona (CSIC), Parc Científic de Barcelona, C/Josep Samitier 1-5, 08028 Barcelona, Spain.
2 Institute of Molecular Biology and Biotechnology (IMBB), 71110 Iraklio Crete, Greece.

{dagger} Authors for correspondence (e-mail: jcrbmc{at}cid.csic.es; averof{at}imbb.forth.gr)

Accepted 21 December 2005

Adaptation to diverse habitats has prompted the development of distinct organs in different animals to better exploit their living conditions. This is the case for the respiratory organs of arthropods, ranging from tracheae in terrestrial insects to gills in aquatic crustaceans. Although Drosophila tracheal development has been studied extensively, the origin of the tracheal system has been a long-standing mystery. Here, we show that tracheal placodes and leg primordia arise from a common pool of cells in Drosophila, with differences in their fate controlled by the activation state of the wingless signalling pathway. We have also been able to elucidate early events that trigger leg specification and to show that cryptic appendage primordia are associated with the tracheal placodes even in abdominal segments. The association between tracheal and appendage primordia in Drosophila is reminiscent of the association between gills and appendages in crustaceans. This similarity is strengthened by the finding that homologues of tracheal inducer genes are specifically expressed in the gills of crustaceans. We conclude that crustacean gills and insect tracheae share a number of features that raise the possibility of an evolutionary relationship between these structures. We propose an evolutionary scenario that accommodates the available data.

Key words: Tracheae, Appendage primordia, Gills, wingless signalling, Distal-less (Dll), buttonhead (btd), trachealess (trh), ventral veinless (vvl)


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