Identification of the Yellow Skin Gene Reveals a Hybrid Origin of the Domestic Chicken

Abstract

Yellow skin is an abundant phenotype among domestic chickens and is caused by a recessive allele (W*Y) that allows deposition of yellow carotenoids in the skin. Here we show that yellow skin is caused by one or more cis-acting and tissue-specific regulatory mutation(s) that inhibit expression of BCDO2 (beta-carotene dioxygenase 2) in skin. Our data imply that carotenoids are taken up from the circulation in both genotypes but are degraded by BCDO2 in skin from animals carrying the white skin allele (W*W). Surprisingly, our results demonstrate that yellow skin does not originate from the red junglefowl (Gallus gallus), the presumed sole wild ancestor of the domestic chicken, but most likely from the closely related grey junglefowl (Gallus sonneratii). This is the first conclusive evidence for a hybrid origin of the domestic chicken, and it has important implications for our views of the domestication process. Many bird species possess yellow skin and legs whereas other species have white or black skin color. Yellow or white skin is due to the presence or absence of carotenoids. The genetic basis underlying this diversity is unknown. Domestic chickens with yellow skin are homozygous for a recessive allele, and white skinned chickens carry the dominant allele. As a result, chickens represent an ideal model for analyzing genetic mechanism responsible for skin color variation. In this study we demonstrate that yellow skin is caused by regulatory mutation(s) that inhibit expression of the beta-carotene dioxygenase 2 (BCDO2) enzyme in skin, but not in other tissues. Because BCDO2 cleaves colorful carotenoids into colorless apocarotenoids, a reduction in expression of this gene produces yellow skin. This study also provides the first conclusive evidence of a hybrid origin of the domestic chicken. It has been generally assumed that the red junglefowl is the sole ancestor of the domestic chicken. A phylogenetic analysis, however, demonstrates that though the white skin allele originates from the red junglefowl, the yellow skin allele originates from a different species, most likely the grey junglefowl. This result significantly advances our understanding of chicken domestication.