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The specification of a highly derived arthropod appendage, the Drosophila labial palps, requires the joint action of selectors and signaling pathways

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Abstract

The remarkable diversity of form in arthropods reflects flexible genetic programs deploying many conserved genes. In the insect model Drosophila melanogaster, diversity of form can be observed between serially homologous appendages or when a single appendage is transformed by homeotic mutations, such as the adult labial mouthparts that can present alternative antennal, prothoracic, or maxillary identities. We have examined the roles of the Hox selector genes proboscipedia (pb) and Sex combs reduced (Scr), and the antennal selectors homothorax (hth) and spineless (ss) in labial specification, by tissue-directed mitotic recombination. Whereas loss of pb function transforms labium to prothoracic leg, loss of Scr, hth, or ss functions results in little or no change in labial specification. Results of analysis of single and multiple mutant combinations support a genetic hierarchy in which the homeotic pb gene possesses a primary role. It is surprising to note that while loss of ss activity alone had no detected effect, all mutant combinations lacking both pb and ss yielded the most severe phenotype observed: stunted, apparently tripartite legs that may correspond to a default state. The roles of the four selector genes are functionally linked to a cell nonautonomous mechanism involving the coupled activities of the decapentaplegic (dpp)/TGF-β and wingless (wg)/Wnt signaling pathways. Accordingly, several mutant combinations impaired in dpp signaling were seen to reorient labial-to-leg transformations toward antennal aristae. A crucial aspect of selector function in development and evolution may be in regulating diffusible signals, including those emitted by dpp and wg.

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Acknowledgements

We thank our colleagues in Toulouse for many helpful discussions and Fernando Roch and Corinne Benassayag for their critical readings of versions of the manuscript. The monoclonal antibodies directed against Wg (4D4, developed by S. Cohen) and Dac proteins (developed by G. M. Rubin) used in this work were obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the National Institute of Child Health and Human Development and maintained by The University of Iowa, Department of Biological Sciences, Iowa City, IA 52242, USA. Mouse anti-Dll, the plasmid sscA6 harboring a ss cDNA, and the ss D115-7 allele were provided by Dr. I. Duncan; rabbit anti-Hth and the hth 5E chromosome by A. Salzberg; rat anti-Dan by S. Cohen, FRT Scr 1 and FRT pb 27 Scr 2 by A. Percival-Smith. We thank Agnès Lepage for her expert technical assistance and Bruno Savelli and Brice Ronsin for their help with the confocal microscope. This work benefited from the ongoing support of the Centre National de Recherche Scientifique (CNRS) and grants from the Association pour la Recherche sur le Cancer (ARC). L. J. was supported by graduate fellowships from the French Ministère de l’Education Nationale et de la Recherche and the Ligue Nationale Contre le Cancer.

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  1. Centre de Biologie du Développement, CNRS, 118 route de Narbonne, 31062, Toulouse, Cedex 04, France

    Laurent Joulia, Henri-Marc Bourbon & David L. Cribbs

  2. Equipe Développement et Evolution, UMR 7622, Biologie du Développement, CNRS and Université Pierre et Marie Curie, 9 quai St-Bernard, case 24, 75252, Paris, Cedex 05, France

    Jean Deutsch

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  1. Laurent Joulia
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Correspondence to David L. Cribbs.

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Communicated by guest editors Jean Deutsch and Gerhard Scholtz

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Joulia, L., Deutsch, J., Bourbon, HM. et al. The specification of a highly derived arthropod appendage, the Drosophila labial palps, requires the joint action of selectors and signaling pathways. Dev Genes Evol 216, 431–442 (2006). https://doi.org/10.1007/s00427-006-0086-3

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