Global distribution of genomic diversity underscores rich complex history of continental human populations

Abstract

Characterizing patterns of genetic variation within and among human populations is important for understanding human evolutionary history and for careful design of medical genetic studies. Here, we analyze patterns of variation across 443,434 single nucleotide polymorphisms (SNPs) genotyped in 3845 individuals from four continental regions. This unique resource allows us to illuminate patterns of diversity in previously under-studied populations at the genome-wide scale including Latin America, South Asia, and Southern Europe. Key insights afforded by our analysis include quantifying the degree of admixture in a large collection of individuals from Guadalajara, Mexico; identifying language and geography as key determinants of population structure within India; and elucidating a north-south gradient in haplotype diversity within Europe. We also present a novel method for identifying long-range tracts of homozygosity indicative of recent common ancestry. Application of our approach suggests great variation within and among populations in the extent of homozygosity, suggesting both demographic history (such as population bottlenecks) and recent ancestry events (such as consanguinity) play an important role in patterning variation in large modern human populations.

Figure 1.

Global and regional patterns of population structure. (A) structure analysis with K = 5 for the POPRES populations combined with the HapMap populations. (B–D) For each region, the first two principal components are shown, with the proportion of variance explained by each component shown in parentheses. Results from structure are shown below the PCA results, with K = 2 for East Asia, and K = 3 for South Asia and Mexico. HapMap samples have been included in the East Asia analysis for comparison. In South Asia, individuals have been colored by spoken language group, with each individual's spoken language shown in Supplemental Figure S5.

Figure 2.

Principal component analysis of Europe and Mexico (A) and Europe and South Asia (B). Each point represents an individual and is colored by the assigned population group.

Figure 3.

Haplotype diversity within Europe. Geographic regions are color coded. Individuals from Switzerland (striped region) were grouped into adjoining regions on the basis of spoken language. Two numbers are shown within each region, with the first representing H₁₀ and the second representing H₂₅.

Figure 4.

Patterns of homozygosity in the human genome. (A) Genome ideograms (ordered by chromosome number with chromosome 1 at the top) showing LROHs in two European individuals. The female individual shown on the left shows typical levels of homozygosity, whereas the male individual shown on the right shows the most LROHs in the study. (B) Distribution of the cumulative total LROH per individual by continental population (shown on a log scale). The location of the most extreme individual (shown in A) is indicated by a vertical dashed black line. Note that the total genetic length of the human genome is ∼3614 cM (Kong et al. 2002).