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

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.