title: Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity.
abstract: The development of morphological traits occurs through the collective action of networks of genes connected at the level of gene expression. As any node in a network may be a target of evolutionary change, the recurrent targeting of the same node would indicate that the path of evolution is biased for the relevant trait and network. Although examples of parallel evolution have implicated recurrent modification of the same gene and cis-regulatory element (CRE), little is known about the mutational and molecular paths of parallel CRE evolution. In Drosophila melanogaster fruit flies, the Bric-à-brac (Bab) transcription factors control the development of a suite of sexually dimorphic traits on the posterior abdomen. Female-specific Bab expression is regulated by the dimorphic element, a CRE that possesses direct inputs from body plan (ABD-B) and sex-determination (DSX) transcription factors. Here, we find that the recurrent evolutionary modification of this CRE underlies both intraspecific and interspecific variation in female pigmentation in the melanogaster species group. By reconstructing the sequence and regulatory activity of the ancestral Drosophila melanogaster dimorphic element, we demonstrate that a handful of mutations were sufficient to create independent CRE alleles with differing activities. Moreover, intraspecific and interspecific dimorphic element evolution proceeded with little to no alterations to the known body plan and sex-determination regulatory linkages. Collectively, our findings represent an example where the paths of evolution appear biased to a specific CRE, and drastic changes in function were accompanied by deep conservation of key regulatory linkages.
authors.affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.
authors.forename: William A
authors.initials: WA
authors.lastname: Rogers
authors.forename: Joseph R
authors.initials: JR
authors.lastname: Salomone
authors.forename: David J
authors.initials: DJ
authors.lastname: Tacy
authors.forename: Eric M
authors.initials: EM
authors.lastname: Camino
authors.forename: Kristen A
authors.initials: KA
authors.lastname: Davis
authors.forename: Mark
authors.initials: M
authors.lastname: Rebeiz
authors.forename: Thomas M
authors.initials: TM
authors.lastname: Williams
mesh_terms: D000818:Animals; D017124:Conserved Sequence / Q000235:genetics; D004268:DNA-Binding Proteins / Q000235:genetics* / Q000502:physiology; D029721:Drosophila Proteins / Q000235:genetics* / Q000502:physiology; D004331:Drosophila melanogaster / Q000235:genetics / Q000254:growth & development; D019143:Evolution, Molecular; D005260:Female; D018507:Gene Expression Regulation, Developmental; D014644:Genetic Variation; D018398:Homeodomain Proteins; D009154:Mutation; D010858:Pigmentation / Q000235:genetics*; D012045:Regulatory Sequences, Nucleic Acid / Q000235:genetics*; D012733:Sex Differentiation / Q000235:genetics*; D014157:Transcription Factors / Q000235:genetics* / Q000502:physiology
chemical_list: C093752:Bric-a-brac protein 1, Drosophila; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D014157:Transcription Factors; C097899:homeobox protein HOXA9