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The Evolutionary Origination and Diversification of a Dimorphic Gene Regulatory Network through Parallel Innovations in cis and trans

Camino, EM and Butts, JC and Ordway, A and Vellky, JE and Rebeiz, M and Williams, TM (2015) The Evolutionary Origination and Diversification of a Dimorphic Gene Regulatory Network through Parallel Innovations in cis and trans. PLoS Genetics, 11 (4). ISSN 1553-7390

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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.

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Details

Item Type: Article
Status: Published
Creators/Authors:
CreatorsEmailPitt UsernameORCID
Camino, EM
Butts, JC
Ordway, A
Vellky, JE
Rebeiz, Mrebeiz@pitt.eduREBEIZ0000-0001-5731-5570
Williams, TM
Contributors:
ContributionContributors NameEmailPitt UsernameORCID
EditorEisen, Michael B.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Date: 1 April 2015
Date Type: Publication
Access Restriction: No restriction; Release the ETD for access worldwide immediately.
Journal or Publication Title: PLoS Genetics
Volume: 11
Number: 4
DOI or Unique Handle: 10.1371/journal.pgen.1005136
Institution: University of Pittsburgh
Schools and Programs: Dietrich School of Arts and Sciences > Biological Sciences
Refereed: Yes
ISSN: 1553-7390
Date Deposited: 05 Jul 2016 17:28
Last Modified: 23 Nov 2021 16:55
URI: http://d-scholarship.pitt.edu/id/eprint/28526

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