Genomic reconstruction of the history of extant populations of India reveals five distinct ancestral components and a complex structure

Abstract

India, occupying the center stage of Paleolithic and Neolithic migrations, has been underrepresented in genome-wide studies of variation. Systematic analysis of genome-wide data, using multiple robust statistical methods, on (i) 367 unrelated individuals drawn from 18 mainland and 2 island (Andaman and Nicobar Islands) populations selected to represent geographic, linguistic, and ethnic diversities, and (ii) individuals from populations represented in the Human Genome Diversity Panel (HGDP), reveal four major ancestries in mainland India. This contrasts with an earlier inference of two ancestries based on limited population sampling. A distinct ancestry of the populations of Andaman archipelago was identified and found to be coancestral to Oceanic populations. Analysis of ancestral haplotype blocks revealed that extant mainland populations (i) admixed widely irrespective of ancestry, although admixtures between populations was not always symmetric, and (ii) this practice was rapidly replaced by endogamy about 70 generations ago, among upper castes and Indo-European speakers predominantly. This estimated time coincides with the historical period of formulation and adoption of sociocultural norms restricting intermarriage in large social strata. A similar replacement observed among tribal populations was temporally less uniform.

Keywords: admixture; ancestry; endogamy; haplotype blocks; social stratification.

Fig. 1.

(A) Scatterplot of the 367 individuals sampled from 20 Indian populations by the first two PCs extracted from genome-wide genotype data. The Andamanese populations (JRW and ONG) cluster together and are widely separated from mainland populations. (B) Ancestries of individuals estimated using ADMIXTURE with two ancestral components. The 367 individuals are clustered into two distinct groups: the mainlanders (red) and Andamanese islanders (green). (Ancestries of individuals estimated using ADMIXTURE for K = 2, 3, and 4 and related results are in SI Appendix.)

Fig. 2.

(A) Scatterplot of 331 individuals from 18 mainland Indian populations by the first two PCs extracted from genome-wide genotype data. Four distinct clines and clusters were noted; these are encircled using four colors. (B) Estimates of ancestral components of 331 individuals from 18 mainland Indian populations. A model with four ancestral components (K = 4) was the most parsimonious to explain the variation and similarities of the genome-wide genotype data on the 331 individuals. Each individual is represented by a vertical line partitioned into colored segments whose lengths are proportional to the contributions of the ancestral components to the genome of the individual. Population labels were added only after each individual’s ancestry had been estimated. We have used green and red to represent ANI and ASI ancestries; and cyan and blue with the inferred AAA and ATB ancestries. These colors correspond to the colors used to encircle clusters of individuals in A. (Also see SI Appendix, Figs. S2 and S3.)

Fig. 3.

Approximate “mirroring” of genes and geography. Genomic variation of individuals, represented by the first two PCs, sampled from 18 mainland Indians combined with the CS-Asians) and E-Asians from HGDP, compared with the map of the Indian subcontinent showing the approximate locations from which the individuals and populations were sampled.