Adaptive introgression of putative carotenoid pigment genes explains geographic variation in a sexually-selected plumage trait

Abstract

Understanding the genetic architecture of sexually-selected traits is a fundamental goal in evolutionary biology because it can explain the constraints and processes that shape the production of these traits and emergent evolutionary processes, such as introgression. To address these topics, we leverage populations of hybridizing red-backed fairywrens (Malurus melanocephalus) that differ by plumage color (orange vs. red) across a well-classified hybrid zone with a priori evidence of strong female preference for males with redder plumage. We sequenced whole genomes of 36 individuals that vary in plumage hue and found that divergence between even the most phenotypically different individuals was very low, yet we identified several regions with high FST estimates relative to the background divergence. To determine whether loci in these elevated regions were linked to plumage variation across the species range, we sequenced top candidate genetic variants for color differentiation in 285 individuals from 16 populations and traced their frequencies across the range of the species. We found that 15% of these variants were concordant with the plumage cline, with some linked to putative carotenoid processing genes and exhibiting evidence of selection. Considered together, these findings suggest that geographic variation in the sexually-selected plumage color of male red-backed fairywrens is in part explained by adaptive introgression of genes involved in carotenoid coloration. This study highlights how genetic mechanisms underlying color variation can shape patterns of adaptive introgression via sexual selection and phenotypic differentiation in hybridizing taxa.