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Abstract

Carotenoid pigmentation produces most of the yellow and red coloration of birds and other vertebrates, but our understanding of the genetic architecture of carotenoid ornamentation is largely limited to studies of novel color variants observed in captively bred populations. The complexity of carotenoid-based color evolution in nature remains poorly characterized. Here, we examine the long-tailed finch Poephila acuticauda, an Australian songbird with two hybridizing subspecies that differ in bill coloration: yellow in western subspecies acuticauda and red in eastern subspecies hecki. We characterize the carotenoid composition of each subspecies and find that yellow bills can be explained by the loss of C(4)-oxidation, thus blocking yellow dietary pigments from being metabolized to red. Combining linked-read genomic sequencing and reflectance spectrophotometry measurements of bill color collected from wild-sampled finches and laboratory crosses, we identify four loci that together explain 53% of variance in this trait. The two loci of largest effect contain the genes CYP2J19, an essential enzyme for the ketolation via C(4)-oxidation of dietary carotenoids, and TTC39B, an enhancer of ketocarotenoid production. Evolutionary genealogy reconstruction indicates that the red-billed phenotype is ancestral and that yellow alleles at both CYP2J19 and TTC39B arose and fixed in acuticauda approximately 100 kya. Yellow alleles then introgressed into hecki less than 5 kya. Across all four loci, acuticauda derived variants show evidence of selective sweeps, implying that yellow bill coloration has been favored by natural selection. Our study suggests that the frequent adaptive evolutionary transitions between red and yellow ornamentation in nature can have a simple genetic basis.