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

Species radiations have long served as model systems in evolutionary
biology. 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. 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 gene flow have fueled plumage
diversification in this colorful avian radiation.