Population differentiation of Southern Indian male lineages correlates with agricultural expansions predating the caste system

Christina J. Adler, Alan Cooper, Clio S.I. Der Sarkissian and Wolfgang Haak are contributors to the Genographic ConsortiumPrevious studies that pooled Indian populations from a wide variety of geographical locations, have obtained contradictory conclusions about the processes of the establishment of the Varna caste system and its genetic impact on the origins and demographic histories of Indian populations. To further investigate these questions we took advantage that both Y chromosome and caste designation are paternally inherited, and genotyped 1,680 Y chromosomes representing 12 tribal and 19 non-tribal (caste) endogamous populations from the predominantly Dravidian-speaking Tamil Nadu state in the southernmost part of India. Tribes and castes were both characterized by an overwhelming proportion of putatively Indian autochthonous Y-chromosomal haplogroups (H-M69, F-M89, R1a1-M17, L1-M27, R2-M124, and C5-M356; 81% combined) with a shared genetic heritage dating back to the late Pleistocene (10–30 Kya), suggesting that more recent Holocene migrations from western Eurasia contributed, <20% of the male lineages. We found strong evidence for genetic structure, associated primarily with the current mode of subsistence. Coalescence analysis suggested that the social stratification was established 4–6 Kya and there was little admixture during the last 3 Kya, implying a minimal genetic impact of the Varna(caste) system from the historically-documented Brahmin migrations into the area. In contrast, the overall Y-chromosomal patterns, the time depth of population diversifications and the period of differentiation were best explained by the emergence of agricultural technology in South Asia. These results highlight the utility of detailed local genetic studies within India, without prior assumptions about the importance of Varna rank status for population grouping, to obtain new insights into the relative influences of past demographic events for the population structure of the whole of modern India.GaneshPrasad ArunKumar, David F. Soria-Hernanz, Valampuri John Kavitha, Varatharajan Santhakumari Arun, Adhikarla Syama, Kumaran Samy Ashokan, Kavandanpatti Thangaraj Gandhirajan, Koothapuli Vijayakumar, Muthuswamy Narayanan, Mariakuttikan Jayalakshmi, Janet S. Ziegle, Ajay K. Royyuru, Laxmi Parida, R. Spencer Wells, Colin Renfrew, Theodore G. Schurr, Chris Tyler Smith, Daniel E. Platt, Ramasamy Pitchappan, The Genographic Consortiu

Genome-wide signatures of male-mediated migration shaping the Indian gene pool

Multiple questions relating to contributions of cultural and demographical factors in the process of human geographical dispersal remain largely unanswered. India, a land of early human settlement and the resulting diversity is a good place to look for some of the answers. In this study, we explored the genetic structure of India using a diverse panel of 78 males genotyped using the GenoChip. Their genome-wide single-nucleotide polymorphism (SNP) diversity was examined in the context of various covariates that influence Indian gene pool. Admixture analysis of genome-wide SNP data showed high proportion of the Southwest Asian component in all of the Indian samples. Hierarchical clustering based on admixture proportions revealed seven distinct clusters correlating to geographical and linguistic affiliations. Convex hull overlay of Y-chromosomal haplogroups on the genome-wide SNP principal component analysis brought out distinct non-overlapping polygons of F*-M89, H*-M69, L1-M27, O2a-M95 and O3a3c1-M117, suggesting a male-mediated migration and expansion of the Indian gene pool. Lack of similar correlation with mitochondrial DNA clades indicated a shared genetic ancestry of females. We suggest that ancient male-mediated migratory events and settlement in various regional niches led to the present day scenario and peopling of India

Distinct diversity of KIR genes in three Southern Indian populations: comparison with world populations revealed a link between KIR gene content and pre-historic human migrations

By interacting with polymorphic HLA class I molecules, the killer cell immunoglobulin-like receptors (KIR) influence the innate and adaptive immune response to infection. The KIR family varies in gene content and sequence polymorphism, thereby, distinguishing individuals and populations. To investigate KIR diversity in the earliest settlers of India, we have characterized the KIR gene content in three Dravidian-speaking populations (Mollukurumba, Kanikar, and Paravar) from the state of Tamil Nadu, southern India. The activating KIR genes and putative group-B KIR haplotypes were frequent in Paravar and Kanikar, a scenario analogous to those seen previously in other populations of Indian origin, indicating that predominance of group-B KIR haplotypes is the characteristic feature of Indian populations. In contrast, the KIR gene profile of Mollukurumba was more related to Caucasian type. It is not clear whether a local-specific selection or a recent admixture from Iran is responsible for such discrete profile in Mollukurumba. Each southern Indian population had distinct KIR genotype profile. Comparative analyses with world populations revealed that group-B KIR haplotypes were frequent in the natives of India, Australia, and America, the populations associated with those involved in extensive prehistoric human migrations. Whether or not natural selection has acted to enrich group-B KIR haplotypes in these migratory descendants is an issue that requires objective testing

A late neolithic expansion of Y chromosomal haplogroup O2a1-M95 from east to west

The origin and dispersal of Y-Chromosomal haplogroup O2a1-M95, distributed across the Austro Asiatic speaking belt of East and South Asia, are yet to be fully understood. Various studies have suggested either an East Indian or Southeast Asian origin of O2a1-M95. We addressed the issue of antiquity and dispersal of O2a1-M95 by sampling 8748 men from India, Laos, and China and compared them to 3307 samples from other intervening regions taken from the literature. Analyses of haplogroup frequency and Y-STR data on a total 2413 O2a1-M95 chromosomes revealed that the Laos samples possessed the highest frequencies of O2a1-M95 (74% with &gt;0.5) and its ancestral haplogroups (O2*-P31, O*-M175) as well as a higher proportion of samples with 14STR-median haplotype (17 samples in 14 populations), deep coalescence time (5.7 ± 0.3 Kya) and consorted O2a1-M95 expansion evidenced from STR evolution. All these suggested Laos to carry a deep antiquity of O2a1-M95 among the study regions. A serial decrease in expansion time from east to west: 5.7 ± 0.3 Kya in Laos, 5.2 ± 0.6 in Northeast India, and 4.3 ± 0.2 in East India, suggested a late Neolithic east to west spread of the lineage O2a1-M95 from Laos

Description of the 31 tribal and non-tribal endogamous populations studied.

a<p>- 2001 Census, Government of India, <a href="http://censusindia.gov.in/" target="_blank">http://censusindia.gov.in/</a>.</p>b<p>-1981 Indian Census.</p>c<p>-1931 Indian Census.</p>d<p>- Estimated census size.</p>e<p>-1901 Indian Census.</p>f<p>- All Brahmin-related castes in Tamil Nadu,</p>g<p>-No information available.</p>h<p>-Population code used in PCA & MDS plots,</p>i<p>-Sanskrit is the language of scriptures and ceremonies, but populations quickly adopted local cultures and languages.</p>j<p>-Lower, Middle & Higher social ranks are self-perceived/assigned classifications.</p>k<p>-Approximate coordinates.</p><p>NTN (North Tamil Nadu),TNV (Tirunelveli).</p><p>DR (Dravidian), IE (Indo-European).</p

Tamil Nadu map showing the sampling location of the 12 tribal (squares) and 19 non-tribal (circles) populations.

<p>The majority of tribal populations are located in the mountains of the Western Ghats. The color codes are: Red – Hill Tribe Foragers (HTF); Turquoise – Hill Tribe Cremating (HTC); Green – Hill Tribe Kannada (HTK); Grey – Schedule Castes (SC); Pink – Dry-Land Farmers (DLF); Deep Blue – Artisan and Warriors (AW) and Yellow – Brahmin related (BRH). Population abbreviations are as shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0050269#pone-0050269-t001" target="_blank">Table 1</a>.</p

Reduced median network of 17 microsatellite haplotypes within haplogroup F-M89.

<p>The network depicts clear isolated evolution among HTF populations with a few shared haplotypes between Kurumba (HTK) and Irula (HTF) populations. Circles are colored based on the 7 Major Population Groups as shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0050269#pone-0050269-g001" target="_blank">Figure 1</a>, and the area is proportional to the frequency of the sampled haplotypes. Branch lengths between circles are proportional to the number of mutations separating haplotypes.</p

Y chromosome haplogroup frequencies (%) in the 31 populations from Tamil Nadu.

<p>SD (Standard Deviation).</p

Analysis of molecular variance (AMOVA).

a<p> <i>P</i><0.00001.</p>b<p> <i>P</i><0.001.</p>c<p> <i>P</i><0.01.</p>d<p> No Significant, <i>P</i><0.2.</p><p>TR (Tribes), HTF (Hill Tribe Foragers), BRH (Brahmins), HTK (Hill Tribe Kannada speakers), SC (Schedule Castes), DLF (Dry Land Farmers), AW (Artisan & Warriors).</p><p>HG, MID, LOW – High, Middle and Low caste-rank hierarchy as described in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0050269#pone-0050269-t001" target="_blank">Table 1</a>.</p><p>Endogamous populations were grouped based on geography, tribe-caste dichotomy, caste-rank hierarchy, and socio-cultural features mainly reflecting subsistence (7 Major Population Groups, MPG). The maximal genetic variation among groups (<i>F_CT</i>) and the minimal variation among populations within groups (<i>F_SC</i>) was observed when populations were grouped based on the 7 MPG classification.</p