Pigmentation Genes Show Evidence of Repeated Divergence and Multiple Bouts of Introgression in Setophaga Warblers

Abstract

Species radiations have long served as model systems in evolutionary biology.1,2 However, it has only recently become possible to study the genetic bases of the traits responsible for diversification and only in a small number of model systems.3 Here, we use genomes of 36 species of North, Central, and South American warblers to highlight the role of pigmentation genes-involved in melanin and carotenoid processing-in the diversification of this group. We show that agouti signaling protein (ASIP) and beta-carotene oxygenase 2 (BCO2) are predictably divergent between species that differ in the distribution of melanin and carotenoid in their plumages, respectively. Among species, sequence variation at ASIP broadly mirrors the species' phylogenetic history, consistent with repeated, independent mutations generating melanin-based variation. In contrast, BCO2 variation is highly discordant from the species tree, with evidence of cross-lineage introgression among species like the yellow warbler (Setophaga petechia) and magnolia warbler (S.magnolia) with extensive carotenoid-based coloration. We also detect introgression of a small part of the BCO2 coding region (<3 kb) in S.discolor and S.vitellina, including an amino acid substitution that is unique to warblers but otherwise highly conserved across birds. Lateral transfer of carotenoid-processing genes has been documented in arthropods, but introgression of BCO2 as demonstrated here-presumably adaptive-represents the first example of carotenoid gene transfer among vertebrates. These contrasting genomic patterns show that both independent evolution in a common set of genes and past hybridization have fueled plumage diversification in this colorful avian radiation.