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

Abstract

two principal components (PCs). A decreasing proportion of “Middle Easterners, Central Asians, and Europeans-like” ancestry from north to south was noted (9). However, TB- and AAspeaking individuals, who were “off-cline” in the PC plot and excluded from further analysis (9, 10), represent additional ancestral components in the Indian population. By analyzing more representative population samples using robust statistical methods, here we provide a fine-grained reconstruction of India’s population history. Contemporary populations of India are linguistically, geographically, and socially stratified (6, 16), and are largely endogamous with variable degrees of porosity. We analyzed highquality genotype data, generated using a DNA microarray (Methods) at 803,570 autosomal SNPs on 367 individuals drawn from 20 ethnic populations of India (Table 1 and SI Appendix, Fig. S1), to provide evidence that the ancestry of the huntergatherers of A&N is distinct from mainland Indian populations, but is coancestral to contemporary Pacific Islanders (PI). Our analysis reveals that the genomic structure of mainland Indian populations is best explained by contributions from four ancestral components. In addition to the ANI and ASI, we identified two ancestral components in mainland India that are major for the AA-speaking tribals and the TB speakers, which we respectively denote as AAA (for “Ancestral Austro-Asiatic”) and ATB (for “Ancestral Tibeto-Burman”). Extant populations have experienced extensive multicomponent admixtures. Our results indicate that the census sizes of AA and TB speakers in contemporary India are gross underestimates of the extent of the AAA and the ATB components in extant populations. We have Significance India, harboring more than one-sixth of the world population, has been underrepresented in genome-wide studies of variation. Our analysis reveals that there are four dominant ancestries in mainland populations of India, contrary to two ancestries inferred earlier. We also show that (i) there is a distinctive ancestry of the Andaman and Nicobar Islands populations that is likely ancestral also to Oceanic populations, and (ii) the extant mainland populations admixed widely irrespective of ancestry, which was rapidly replaced by endogamy, particularly among Indo-European–speaking upper castes, about 70 generations ago. This coincides with the historical period of formulation and adoption of some relevant sociocultural norms. Author contributions: A.B. and P.P.M. designed research; A.B. and N.S.-R. performed research; A.B. analyzed data; and A.B. and P.P.M. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Freely available online through the PNAS open access option.