Original Research ARTICLE
Front. Ecol. Evol., 26 March 2020 | https://doi.org/10.3389/fevo.2020.00080
Gene Regulatory Network Homoplasy Underlies Recurrent Sexually Dimorphic Fruit Fly Pigmentation
Jesse T. Hughes1, Melissa E. Williams1, Rachel Johnson1, Sumant Grover1, Mark Rebeiz2* and Thomas M. Williams1,3*
- 1Department of Biology, University of Dayton, Dayton, OH, United States
- 2Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, United States
- 3The Integrative Science and Engineering Center, University of Dayton, Dayton, OH, United States
Traits that appear discontinuously along phylogenies may be explained by independent origins (homoplasy) or repeated loss (homology). While discriminating between these models is difficult, the dissection of gene regulatory networks (GRNs) which drive the development of such repeatedly occurring traits can offer a mechanistic window on this fundamental problem. The GRN responsible for the male-specific pattern of Drosophila (D.) melanogaster melanic tergite pigmentation has received considerable attention. In this system, a metabolic pathway of pigmentation enzyme genes is expressed in spatial and sex-specific (i.e., dimorphic) patterns. The dimorphic expression of several genes is regulated by the Bab transcription factors, which suppress pigmentation enzyme expression in females, by virtue of their high expression in this sex. Here, we analyzed the phylogenetic distribution of species with male-specific pigmentation and show that this dimorphism is phylogenetically widespread among fruit flies. The analysis of pigmentation enzyme gene expression in distantly related dimorphic and monomorphic species shows that dimorphism is driven by the similar deployment of a conserved metabolic pathway. However, sexually dimorphic Bab expression was found only in D. melanogaster and its close relatives. These results suggest that dimorphism evolved by parallel deployment of differentiation genes, but was derived through distinct architectures at the level of regulatory genes. This work demonstrates the interplay of constraint and flexibility within evolving GRNs, findings that may foretell the mechanisms of homoplasy more broadly.
Dev Biol. 2018 Sep 1;441(1):159-175. doi: 10.1016/j.ydbio.2018.07.001. Epub 2018 Jul 4.
Augmentation of a wound response element accompanies the origin of a Hox-regulated Drosophila abdominal pigmentation trait.
A challenge for evolutionary research is to uncover how new morphological traits evolve the coordinated spatial and temporal expression patterns of genes that govern their formation during development. Detailed studies are often limited to characterizing how one or a few genes contributed to a trait’s emergence, and thus our knowledge of how entire GRNs evolve their coordinated expression of each gene remains unresolved. The melanic color patterns decorating the male abdominal tergites of Drosophila (D.) melanogaster evolved in part by novel expression patterns for genes acting at the terminus of a pigment metabolic pathway, driven by cis-regulatory elements (CREs) with distinct mechanisms of Hox regulation. Here, we examined the expression and evolutionary histories of two important enzymes in this pathway, encoded by the pale and Ddc genes. We found that while both genes exhibit dynamic patterns of expression, a robust pattern of Ddc expression specifically evolved in the lineage of fruit flies with pronounced melanic abdomens. Derived Ddc expression requires the activity of a CRE previously shown to activate expression in response to epidermal wounding. We show that a binding site for the Grainy head transcription factor that promotes the ancestral wound healing function of this CRE is also required for abdominal activity. Together with previous findings in this system, our work shows how the GRN for a novel trait emerged by assembling unique yet similarly functioning CREs from heterogeneous starting points.
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
Drosophilaphilia #2: Silencing silencers to evolve new patterns.
Nice thoughtful overview on my collaborator’s new publication!
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
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.
The Evolutionary Origination and Diversification of a Dimorphic Gene Regulatory Network through Parallel Innovations in cis andtrans
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.”
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.