Sequential introgression of a carotenoid processing gene underlies sexual ornament diversity in a genus of manakins

In a hybrid zone between two tropical lekking birds, the yellow male plumage of one species has introgressed asymmetrically replacing the white plumage of another via sexual selection. Here, we present a detailed analysis of the plumage trait to uncover its physical and genetic bases and trace its evolutionary history. We determine that the carotenoid lutein underlies the yellow phenotype, and describe microstructural feather features likely to enhance color appearance. These same features reduce the predicted water-shedding capacity of feathers, a potential liability in the tropics. Through genome-scale DNA sequencing of hybrids and each species in the genus, we identify BCO2 as the major gene responsible for the color polymorphism. The BCO2 gene tree and genome-wide allele frequency patterns suggest that carotenoid-pigmented collars initially arose in a third species and reached the hybrid zone through historical gene flow. The complex interplay between sexual selection and hybridization has thus shaped the phenotypes of these species, where conspicuous sexual traits are key to male reproductive success.