Disruptions of feather carotenoid pigmentation in a subset of hybrid northern flickers (Colaptes auratus) may be linked to genetic incompatibilities.

Abstract

Hybridization can bring in single individuals alleles that were never designed to work together, which can result in unexpected or transgressive phenotypes. The Yellow-shafted (auratus group) and Red-shafted (cafer group) subspecies groups of the Northern Flicker (Colaptes auratus) differ conspicuously in the coloration of their flight feathers, but hybridize freely where their ranges overlap in western North America. The difference in color is largely the result of the Red-shafted form harboring ketolated products at C4(4') of the carotenoids found in the Yellow-shafted form. Characterizing the carotenoid pigments in a series of birds of intermediate color (presumed hybrids) revealed that most accumulated a product of β-cryptoxanthin with a keto group on its hydroxylated ring (3-hydroxy-echinenone), while a few accumulated the product with a keto group on the unhydroxylated ring (3'-hydroxy-echinenone). Surprisingly, the latter group also had feather barbs that were noticeably yellower than the associated rachis, corresponding to a lower level of ketolation at C4(4'). We assessed possible biochemical explanations for the differences by probing the relative carotenoid concentration data in individuals of varying color. The difference between the hybrids could not be explained by the general level of ketolation of carotenoids or a particular selectivity of the 4-ketolase involved. We present a testable genetic explanation that invokes incompatibilities between divergent alleles of the two parental forms at interacting loci. Because the idiosyncrasies affect oxidation, they may be the product of mitonuclear incompatibilities.