CYP2J19 mediates carotenoid colour introgression across a natural avian hybrid zone

It has long been of interest to identify the phenotypic traits that mediate reproductive isolation between related species, and more recently, the genes that underpin them. Much work has focused on identifying genes associated with animal colour, with the candidate gene CYP2J19 identified in laboratory studies as the ketolase converting yellow dietary carotenoids to red ketocarotenoids in birds with red pigments. However, evidence that CYP2J19 explains variation between red and yellow feather coloration in wild populations of birds is lacking. Hybrid zones provide the opportunity to identify genes associated with specific traits. Here we investigate genomic regions associated with colour in red-fronted and yellow-fronted tinkerbirds across a hybrid zone in southern Africa. We sampled 85 individuals, measuring spectral reflectance of forecrown feathers and scoring colours from photographs, while testing for carotenoid presence with Raman spectroscopy. We performed a genome-wide association study to identify associations with carotenoid-based coloration, using double-digest RAD sequencing aligned to a short-read whole genome of a Pogoniulus tinkerbird. Admixture mapping using 104,933 single nucleotide polymorphisms (SNPs) identified a region of chromosome 8 that includes CYP2J19 as the only locus with more than two SNPs significantly associated with both crown hue and crown score, while Raman spectra provided evidence of ketocarotenoids in red feathers. Asymmetric backcrossing in the hybrid zone suggests that yellow-fronted females mate more often with red-fronted males than vice versa. Female red-fronted tinkerbirds mating assortatively with red-crowned males is consistent with the hypothesis that converted carotenoids are an honest signal of quality.