title: The evolutionary origination and diversification of a dimorphic gene regulatory network through parallel innovations in cis and trans.
abstract: The origination and diversification of morphological characteristics represents a key problem in understanding the evolution of development. Morphological traits result from gene regulatory networks (GRNs) that form a web of transcription factors, which regulate multiple cis-regulatory element (CRE) sequences to control the coordinated expression of differentiation genes. The formation and modification of GRNs must ultimately be understood at the level of individual regulatory linkages (i.e., transcription factor binding sites within CREs) that constitute the network. Here, we investigate how elements within a network originated and diversified to generate a broad range of abdominal pigmentation phenotypes among Sophophora fruit flies. Our data indicates that the coordinated expression of two melanin synthesis enzymes, Yellow and Tan, recently evolved through novel CRE activities that respond to the spatial patterning inputs of Hox proteins and the sex-specific input of Bric-à-brac transcription factors. Once established, it seems that these newly evolved activities were repeatedly modified by evolutionary changes in the network's trans-regulators to generate large-scale changes in pigment pattern. By elucidating how yellow and tan are connected to the web of abdominal trans-regulators, we discovered that the yellow and tan abdominal CREs are composed of distinct regulatory inputs that exhibit contrasting responses to the same Hox proteins and Hox cofactors. These results provide an example in which CRE origination underlies a recently evolved novel trait, and highlights how coordinated expression patterns can evolve in parallel through the generation of unique regulatory linkages.
authors.affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.
authors.forename: Eric M
authors.initials: EM
authors.lastname: Camino
authors.affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.
authors.forename: John C
authors.initials: JC
authors.lastname: Butts
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: Alison
authors.initials: A
authors.lastname: Ordway
authors.affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.
authors.forename: Jordan E
authors.initials: JE
authors.lastname: Vellky
authors.affiliation: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
authors.forename: Mark
authors.initials: M
authors.lastname: Rebeiz
authors.affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America; Center for Tissue Regeneration and Engineering at Dayton, University of Dayton, Dayton, Ohio, United States of America.
authors.forename: Thomas M
authors.initials: TM
authors.lastname: Williams
mesh_terms: D000818:Animals; D001483:Base Sequence; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D004330:Drosophila / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D053263:Gene Regulatory Networks; D018398:Homeodomain Proteins / Q000235:genetics; D008969:Molecular Sequence Data; D050436:Regulatory Elements, Transcriptional; D015533:Transcriptional Activation
chemical_list: D002868:Chromosomal Proteins, Non-Histone; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D018398:Homeodomain Proteins; C431070:t protein, Drosophila; C050680:y protein, Drosophila
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