Inference of human pigmentation from ancient DNA by genotype likelihood

Abstract

Light eyes, hair and skins probably evolved several times as Homo sapiens dispersed from Africa. In areas with lower UV radiation, light pigmentation alleles increased in frequency because of their adaptive advantage and of other contingent factors such as migration and drift. However, the tempo and mode of their spread is not known. Phenotypic inference from ancient DNA is complicated, both because these traits are polygenic, and because of low sequence depth. We evaluated the effects of the latter by randomly removing reads in two high-coverage ancient samples, the Paleolithic Ust-Ishim from Russia and the Mesolithic SF12 from Sweden. We could thus compare three approaches to pigmentation inference, concluding that, for suboptimal levels of coverage (<8x), a probabilistic method estimating genotype likelihoods leads to the most robust predictions. We then applied that protocol to 348 ancient genomes from Eurasia, describing how skin, eye and hair color evolved over the past 45,000 years. The shift towards lighter pigmentations turned out to be all but linear in time and place, and slower than expected, with half of the individuals showing dark or intermediate skin colors well into the Copper and Iron ages. We also observed a peak of light eye pigmentation in Mesolithic times, and an accelerated change during the spread of Neolithic farmers over Western Eurasia, although localized processes of gene flow and admixture, or lack thereof, also played a significant role.