Title

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

Author(s)

Eric M. Camino, University of DaytonFollow
John C. Butts, University of Dayton
Alison J. Ordway, University of Pittsburgh
Jordan E. Vellky, University of Dayton
Mark Rebeiz, University of Pittsburgh
Thomas M. Williams, University of DaytonFollow

Document Type

Article

Publication Date

4-2015

Publication Source

PLOS Genetics

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-àbrac 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.

Inclusive pages

1-30

ISBN/ISSN

1553-7390

Document Version

Published Version

Comments

This document is provided for download in compliance with the publisher's open-access policies. Permission documentation is on file.

Copyright

Copyright © 2015, Camino et al.

Publisher

PLOS

Volume

11

Peer Reviewed

yes

Issue

4

eCommons Citation

Camino, Eric M.; Butts, John C.; Ordway, Alison J.; Vellky, Jordan E.; Rebeiz, Mark; and Williams, Thomas M., "The Evolutionary Origination and Diversification of a Dimorphic Gene Regulatory Network through Parallel Innovations in cis and trans" (2015). Biology Faculty Publications. 198.
https://ecommons.udayton.edu/bio_fac_pub/198