Global patterns of natural selection inferred using ancient DNA

Abstract

Ancient DNA has revolutionized our understanding of human history, and is now yielding important insights into evolution and natural selection. However, studies of selection using ancient DNA have largely been limited to Europe, excluding populations in other parts of the world. While many selective pressures were local to specific populations others, for example those related to the development of agriculture, may have been universal. By studying a broader range of global populations, we can identify examples of local adaption but also more general principles of adaptation to climatic, social and technological changes. We therefore leverage ancient DNA to test for selection in 7244 individuals from 13 ancient and 19 present-day populations across five regions: Europe, East Asia, South Asia, Africa and the Americas. In each region, we tested for selection using multiple approaches that account for complex demographic histories. We identify 31 genome-wide significant signals of selection, including both known and novel loci. We find a high degree of shared signal across regions, suggesting extensive parallel or shared adaptation. Using a novel admixture-aware time series method, we find that the strength of selection on many variants changed over time, for example decreasing selection at LCT in Europe and increasing selection at ADH1B in East Asia over the past few thousand years. Finally, we developed a test for polygenic selection on complex traits by modeling the frequencies of trait-associated alleles identified in GWAS. We tested for selection jointly across regions, avoiding the confounding effect of population stratification by excluding the European or East Asian GWAS population from the selection test. We find evidence for directional selection on pigmentation and immune traits, and that strong stabilizing selection on female waist-hip ratio was universal across human populations suggesting a fundamental constraint on human morphology.