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

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

Plots representing the genetic relationships among the 31 tribal and non-tribal populations of Tamil Nadu.

<p>(A) PCA plot based on HG frequencies. The two dimensions display 36% of the total variance. The contribution of the first four HGs is superimposed as grey component loading vectors: the HTF populations clustered in the direction of the F-M89 vector, HTK in the H1-M52 vector, BRH in the R1a1-M17 vector, while the HG L1-M27 is less significant in discriminating populations. (B) MDS plot based on 17 microsatellite loci <i>R_st</i> distances. The two tribal groups (HTF and HTK) are clustered at the left side of the plot while BRH form a distant cluster at the opposite side. The colors and symbols are the same 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>, while 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

Haplogroup variances and age estimates based on 17 microsatellite loci.

<p>Var (Variance), SE (Standard Error), SD (Standard Deviation).</p><p>Haplogroup age estimates are given in years; groups with less than 5 STRs (samples) were excluded from calculations. Non-tribal groups (castes) displayed the oldest age estimates for most of the Y chromosome haplogroups.</p