Abstract
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.
Highlights
Recurring traits are widespread in nature, suggesting that evolution has predictable solutions to certain ecological challenges (Conway Morris, 2003; Losos, 2017; Blount et al, 2018)
We suggest that dimorphic pigmentation is a product of parallel evolution in Drosophila, and provide an example where constraint exists at the level of the differentiation genes in contrast to the regulatory tier of this gene regulatory networks (GRNs)
Previous phylogenetic analyses of the origin of D. melanogaster male-specific A5 and A6 tergite pigmentation suggested that monomorphism is the ancestral character state in the Sophophora subgenus, and dimorphism was derived
Summary
Recurring traits are widespread in nature, suggesting that evolution has predictable solutions to certain ecological challenges (Conway Morris, 2003; Losos, 2017; Blount et al, 2018) This discontinuous presence of similar phenotypes on phylogenies can result from different historical processes. Methods for ancestral character reconstruction can help discriminate losses from gains, these methods are often inconclusive and are sensitive to estimated differences in the relative rates of trait gain and loss (Cunningham et al, 1998; Joy et al, 2016) Distinguishing between these two scenarios comes down to whether the genetic processes that build the trait are homologous. Dissecting the individual genetic components underlying trait formation represents the most granular way to determine the elusive historical nature of recurring traits
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