title: Sex-specific repression of dachshund is required for Drosophila sex comb development.
abstract: The origin of new morphological structures requires the establishment of new genetic regulatory circuits to control their development, from initial specification to terminal differentiation. The upstream regulatory genes are usually the first to be identified, while the mechanisms that translate novel regulatory information into phenotypic diversity often remain obscure. In particular, elaborate sex-specific structures that have evolved in many animal lineages are inevitably controlled by sex-determining genes, but the genetic basis of sexually dimorphic cell differentiation is rarely understood. In this report, we examine the role of dachshund (dac), a gene with a deeply conserved function in sensory organ and appendage development, in the sex comb, a recently evolved male-specific structure found in some Drosophila species. We show that dac acts during metamorphosis to restrict sex comb development to the appropriate leg region. Localized repression of dac by the sex determination pathway is necessary for male-specific morphogenesis of sex comb bristles. This pupal function of dac is separate from its earlier role in leg patterning, and Dac at this stage is not dependent on the pupal expression of Distalless (Dll), the main regulator of dac during the larval period. Dll acts in the epithelial cells surrounding the sex comb during pupal development to promote sex comb rotation, a complex cellular process driven by coordinated cell rearrangement. Our results show that genes with well-conserved developmental functions can be re-used at later stages in development to regulate more recently evolved traits. This mode of gene co-option may be an important driver of evolutionary innovations.
authors.affiliation: Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA. Electronic address: jatallah@ucdavis.edu.
authors.forename: Joel
authors.initials: J
authors.lastname: Atallah
authors.affiliation: Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA.
authors.forename: Gerard
authors.initials: G
authors.lastname: Vurens
authors.affiliation: Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA.
authors.forename: Setong
authors.initials: S
authors.lastname: Mavong
authors.affiliation: Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA.
authors.forename: Alexa
authors.initials: A
authors.lastname: Mutti
authors.affiliation: Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA.
authors.forename: Don
authors.initials: D
authors.lastname: Hoang
authors.affiliation: Department of Evolution & Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA.
authors.forename: Artyom
authors.initials: A
authors.lastname: Kopp
mesh_terms: D000818:Animals; D004330:Drosophila; D029721:Drosophila Proteins / Q000235:genetics* / Q000378:metabolism; D005121:Extremities / Q000033:anatomy & histology / Q000254:growth & development*; D018507:Gene Expression Regulation, Developmental / Q000235:genetics* / Q000502:physiology; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism; D018613:Microscopy, Confocal; D008855:Microscopy, Electron, Scanning; D009687:Nuclear Proteins / Q000235:genetics* / Q000378:metabolism; D034622:RNA Interference; D012727:Sex Characteristics; D019849:Sex Determination Processes / Q000235:genetics*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D009687:Nuclear Proteins; D014157:Transcription Factors; C103968:dac protein, Drosophila; C117261:distal-less protein, insect
keywords: Distalless; Drosophila; Novelty; Sex comb; Sex determination; dachshund