Genetic Convergence in the Evolution of Male-Specific Color Patterns in Drosophila

Abstract

Convergent evolution provides a type of natural replication that can be exploited to understand the roles of contingency and constraint in the evolution of phenotypes and the gene networks that control their development. For sex-specific traits, convergence offers the additional opportunity for testing whether the same gene networks follow different evolutionary trends in males versus females. Here, we use an unbiased, systematic mapping approach to compare the genetic basis of evolutionary changes in male-limited pigmentation in several pairs of Drosophila species that represent independent evolutionary transitions. We find strong evidence for repeated recruitment of the same genes to specify similar pigmentation in different species. At one of these genes, ebony, we observe convergent evolution of sexually dimorphic and monomorphic expression through cis-regulatory changes. However, this functional convergence has a different molecular basis in different species, reflecting both parallel fixation of ancestral alleles and independent origin of distinct mutations with similar functional consequences. Our results show that a strong evolutionary constraint at the gene level is compatible with a dominant role of chance at the molecular level.

Perspectives on Gene Regulatory Network Evolution

“…In other systems, detailed CRM characterizations have yielded important insights and demonstrated the prevalence of convergent evolutionary events targeting key GRN nodes. For example, multiple independent changes in the pdm3 locus affect female-limited color dimorphism in members of the Drosophila montium subgroup [33], and multiple independent mutations in CRMs for ebony underlie the convergent evolution of male color pattern in the Drosophila ananassae subgroup [34]. …”

Novel approach to quantitative spatial gene expression uncovers genetic stochasticity in the developing Drosophila eye

“…This points to a potential abundance of hidden noise in spatial and quantitative gene expression. The evolutionary approach to development generally targets large changes that have occurred over broad phylogenetic distances (Ito et al, ; Jeong et al, ; Kopp, Duncan, Godt, & Carroll, ; Reed et al, ; Rosenblum, Römpler, Schöneberg, & Hoekstra, ; Signor et al, ; Yassin et al, ). Accordingly, the presence of abundant underlying variation is perhaps not a huge surprise.…”

“…In contrast, on evolutionary timescales organisms must produce adaptive heritable variation in response to selection pressures, tapping those same sources of variation to which they might otherwise be robust. Indeed, the genetic basis of adaptation is often inferred to be due to differences in gene expression (Chan et al, ; Gompel, Prud'homme, Wittkopp, Kassner, & Carroll, ; Hoekstra & Coyne, ; Jeong et al, ; Pai & Gilad, ; Signor, Liu, Rebeiz, & Kopp, ; Wray, ; Yassin et al, ). This balance between stability and lability is a question that has been addressed philosophically, but little experimental evidence exists to suggest the mechanisms underlying these phenomena (Casci, ; Gibson, ; Green et al, ; Heranz & Cohen, ; Hermisson & Wagner, ; Nijhout et al, ; Rutherford et al, ; Stern, ; True & Haag, ).…”

“…Indeed, the genetic basis of adaptation is often inferred to be due to differences in gene expression (Chan et al, 2010;Gompel, Prud'homme, Wittkopp, Kassner, & Carroll, 2005;Hoekstra & Coyne, 2007;Jeong et al, 2008; Sammi Ali and Sarah A. Signor are co-first author. Pai & Gilad, 2014;Signor, Liu, Rebeiz, & Kopp, 2016;Wray, 2007;Yassin et al, 2016). This balance between stability and lability is a question that has been addressed philosophically, but little experimental evidence exists to suggest the mechanisms underlying these phenomena (Casci, 2005;Gibson, 2009;Green et al, 2017;Heranz & Cohen, 2010;Hermisson & Wagner, 2004;Nijhout et al, 2017;Rutherford et al, 2007;Stern, 2000;True & Haag, 2001).…”

Quantifying the extent of morphological homoplasy: A phylogenetic analysis of 490 characters inDrosophila

“…Annotated genome sequences for multiple species are available and links between genetic mutations and morphological aberrations are curated in accessible online databases such as Flybase (www.flybase.org). Besides the availability of unique genetic toolkits, these resources have made the genus ideal for studies aiming to trace morphological homoplasy between species to their molecular underpinnings (e.g., Wittkopp et al 2003b;Prud'homme et al 2006;Kagesawa et al 2008;Tanaka et al 2009;Frankel et al 2012;Signor et al 2016;Yassin et al 2016a, b). From two major taxonomic references, we conceptualized 490 morphological characters among 56 drosophilid species.…”