Genetic architecture and evolution of color variation in American black bears

SUMMARY Color variation is a frequent evolutionary substrate for camouflage in small mammals but the underlying genetics and evolutionary forces that drive color variation in natural populations of large mammals are mostly unexplained. The American black bear, Ursus americanus , exhibits a range of colors including the cinnamon morph which has a similar color to the brown bear, U. arctos , and is found at high frequency in the American southwest. Reflectance and chemical melanin measurements showed little distinction between U. arctos and cinnamon U. americanus individuals. We used a genome-wide association for hair color as a quantitative trait in 151 U. americanus individuals and identified a single major locus ( P < 10 −13 ). Additional genomic and functional studies identified a missense alteration (R153C) in Tyrosinase-related protein 1 ( TYRP1 ) that impaired protein localization and decreased pigment production. Population genetic analyses and demographic modeling indicated that the R153C variant arose 9.36kya in a southwestern population where it likely provided a selective advantage, spreading both northwards and eastwards by gene flow. A different TYRP1 allele, R114C, contributes to the characteristic brown color of U. arctos , but is not fixed across the range. HIGHLIGHTS The cinnamon morph of American black bears and brown bears have different missense mutations in TYRP1 that account for their similar coloration TYRP1 variants in American black bears and brown bears are loss-of-function alleles associated with impaired protein localization to melanosomes In American black bears, the variant causing the cinnamon morph arose 9,360 years ago in the western lineage where it provides an adaptive advantage, and has spread northwards and eastwards by migration