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.
Highlights
The complexity of developmental processes often hinders our ability to trace their evolutionary history
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
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
Summary
The complexity of developmental processes often hinders our ability to trace their evolutionary history. Genetic programs of development are structured into convoluted networks of genes, interconnected at the level of transcriptional regulation [1]. Regulatory linkage, is formed through interactions between a transcription factor protein and binding site sequences within a cis-regulatory element (CRE). The collection of regulatory linkages possessed by a CRE encodes the pattern of gene expression driven by the CRE. Networks culminate in the regulation of differentiation genes whose encoded products generate cell typespecific phenotypes. To understand how a developmental program originated or was diversified, one must trace how individual connections were formed between transcription factors and the CREs of the network
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