Cis-regulatory evolution integrated the Bric-à-brac transcription factors into a novel fruit fly gene regulatory network

Cite as: eLife 2018;7:e32273 doi: 10.7554/eLife.32273


Gene expression evolution through gene regulatory network (GRN) changes has gained appreciation as a driver of morphological evolution. However, understanding how GRNs evolve is hampered by finding relevant cis-regulatory element (CRE) mutations, and interpreting the protein-DNA interactions they alter. We investigated evolutionary changes in the duplicated Bric-à-brac (Bab) transcription factors and a key Bab target gene in a GRN underlying the novel dimorphic pigmentation of D. melanogaster and its relatives. It has remained uncertain how Bab was integrated within the pigmentation GRN. Here, we show that the ancestral transcription factor activity of Bab gained a role in sculpting sex-specific pigmentation through the evolution of binding sites in a CRE of the pigment-promoting yellow gene. This work demonstrates how a new trait can evolve by incorporating existing transcription factors into a GRN through CRE evolution, an evolutionary path likely to predominate newly evolved functions of transcription factors.

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Using Drosophila pigmentation traits to study the mechanisms of cis-regulatory evolution

One primary agenda of the developmental evolution field is to elucidate molecular mechanisms governing differences in animal form. While mounting evidence has established an important role for mutations in transcription controlling cis-regulatory elements (CREs), the underlying mechanisms that translate these alterations into differences in gene expression are poorly understood. Emerging studies focused on pigmentation differences among closely related Drosophila species have provided many examples of phenotypically relevant CRE changes, and have begun to illuminate how this process works at the level of regulatory sequence function and transcription factor binding. We review recent work in this field and highlight the conceptual and technical challenges that currently await experimental attention.

Mark Rebeiz and Thomas M. Williams

Volume 19, February 2017, Pages 1–7


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Drosophilaphilia #2: Silencing silencers to evolve new patterns

Drosophilaphilia #2: Silencing silencers to evolve new patterns.


Nice thoughtful overview on my collaborator’s new publication!

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Collaborators publish a study showing how evolutionary changes in a transcriptional silencer shaped the repeated evolution of a fruit fly trait. Might be a first description of a pervasive mechanism of evolutionary change!

Genetic Changes to a Transcriptional Silencer Element Confers Phenotypic Diversity within and between Drosophila Species

Winslow C. Johnson , Alison J. Ordway , Masayoshi Watada, Jonathan N. Pruitt, Thomas M. Williams, Mark Rebeiz

Author Summary

One of the greatest challenges in understanding the relationship between genotype and phenotype is to discern how changes in DNA affect the normal functioning of genes. Mutations may generate a new function for a gene, yet it is frequently observed that they inactivate some aspect of a gene’s normal capacity. Investigations focused on understanding the developmental basis for the evolution of anatomical structures has found a prevalent role for mutations that alter developmental gene regulation. In animals, genes are transcriptionally activated in specific tissues during development by regulatory sequences distributed across their expansive non-protein coding regions. Regulatory elements known as silencers act to prevent genes from being expressed in certain tissues, providing a mechanism for precise control. Here, we show how a silencer that prevents expression of a pigment-producing enzyme in certain Drosophila species has repeatedly been subject to inactivating mutations that increased this gene’s expression. This example illustrates how such negative-acting regulatory sequences can represent a convenient target for increasing gene expression through the loss of a genetic element.

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Eric Camino, John Butts and team get published in PLoS Genetics!!

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

Author Summary

The genomic content of regulatory genes such as transcription factors is surprisingly conserved between diverse animal species, raising the paradox of how new traits emerge, and are subsequently modified and lost. In this study we make a connection between the developmental basis for the formation of a fruit fly trait and the evolutionary basis for that trait’s origin, diversification, and loss. We show how the origin of a novel pigmentation trait is associated with the evolution of two regulatory sequences that control the co-expression of two key pigmentation genes. These sequences interact in unique ways with evolutionarily conserved Hox transcription factors to drive gene co-expression. Once these unique connections evolved, the alteration of this trait appears to have proceeded through changes to regulatory genes rather than regulatory sequences of the pigmentation genes. Thus, our findings support a scenario where regulatory sequence evolution provided new functions to old transcription factors, how co-expression can emerge from different utilizations of the same transcription factors, and that trait diversity was surprisingly shaped by changes in some manner to the deeply conserved regulatory genes.”

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Tom Williams to speak at Pub Science 9/09/14

Tom Williams will tell the the Pub Science community about “Beyond the Birds and the Bees: Molecular Insights About the Making and Evolution of Fruit Fly Sexually Dimorphic Traits” on Tuesday September 9th. The presentation will begin at 7 PM and will take place at Blind Bob’s, which is located in Dayton’s Oregon District.

Pub Science

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2014 Midwest Ecology and Evolution Conference at UD (March 1st and 2nd, 2014)

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