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BMC Genetics

Open AccesResearch article

Genetic affinities among the lower castes and tribal groups of India:inference from Y chromosome and mitochondrial DNA

Ismail Thanseem1

, Kumarasamy Thangaraj*1

, Gyaneshwer Chaubey1,2

,Vijay Kumar Singh1, Lakkakula VKS Bhaskar1, B Mohan Reddy3,Alla G Reddy1and Lalji Singh*1

Address: 1Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad- 500 007, India, 2Estonian Biocentre, Riia, 23, Tartu- 51010, Estoniaand 3Biological Anthropology Unit, Indian Statistical Research Institute, Habsiguda, Hyderabad, India

Email: Ismail Thanseem - [email protected]; Kumarasamy Thangaraj* - [email protected]; Gyaneshwer Chaubey - [email protected];Vijay Kumar Singh - [email protected]; Lakkakula VKS Bhaskar - [email protected]; B Mohan Reddy - [email protected];Alla G Reddy - [email protected]; Lalji Singh* - [email protected]

* Corresponding authors

Abstract

Background: India is a country with enormous social and cultural diversity due to its positioningon the crossroads of many historic and pre-historic human migrations. The hierarchical caste

system in the Hindu society dominates the social structure of the Indian populations. The origin ofthe caste system in India is a matter of debate with many linguists and anthropologists suggesting

that it began with the arrival of Indo-European speakers from Central Asia about 3500 years ago.

Previous genetic studies based on Indian populations failed to achieve a consensus in this regard.

We analysed the Y-chromosome and mitochondrial DNA of three tribal populations of southernIndia, compared the results with available data from the Indian subcontinent and tried to

reconstruct the evolutionary history of Indian caste and tribal populations.

Results: No significant difference was observed in the mitochondrial DNA between Indian tribal

and caste populations, except for the presence of a higher frequency of west Eurasian-specific

haplogroups in the higher castes, mostly in the north western part of India. On the other hand, the

study of the Indian Y lineages revealed distinct distribution patterns among caste and tribal

populations. The paternal lineages of Indian lower castes showed significantly closer affinity to the

tribal populations than to the upper castes. The frequencies of deep-rooted Y haplogroups such as

M89, M52, and M95 were higher in the lower castes and tribes, compared to the upper castes.

Conclusion: The present study suggests that the vast majority (>98%) of the Indian maternal gene

pool, consisting of Indio-European and Dravidian speakers, is genetically more or less uniform.

Invasions after the late Pleistocene settlement might have been mostly male-mediated. However,

Y-SNP data provides compelling genetic evidence for a tribal origin of the lower caste populations

in the subcontinent. Lower caste groups might have originated with the hierarchical divisions that

arose within the tribal groups with the spread of Neolithic agriculturalists, much earlier than the

arrival of Aryan speakers. The Indo-Europeans established themselves as upper castes among this

already developed caste-like class structure within the tribes.

Published: 07 August 2006

BMC Genetics2006, 7:42 doi:10.1186/1471-2156-7-42

Received: 30 January 2006Accepted: 07 August 2006

This article is available from: http://www.biomedcentral.com/1471-2156/7/42

2006 Thanseem et al; licensee BioMed Central Ltd.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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BMC Genetics2006, 7:42 http://www.biomedcentral.com/1471-2156/7/42


Background"Out-of-Africa" hypothesis suggests that the anatomicallymodern humans originated in Africa about 160,000 150,000 years ago, and then spread outward, completelyreplacing the local archaic hominid populations outside

Africa. India has served as a major corridor for the disper-sal of modern humans out of Africa, owing to the posi-tioning of the Indian Peninsula at the crossroads of Africa,the Pacific and the West and East Eurasia. The enormouscultural, linguistic and genetic diversity of the more thanone billion people living in the contemporary ethnicIndia can be attributed to this. The Indian society and cul-ture might have been affected by multiple waves of migra-tion and gene flow that occurred in the historic and pre-historic times [1]. The first among this is the ancient Pale-olithic migration by the modern humans during their ini-tial colonization of Eurasia. This is followed by the earlyNeolithic migration, probably of proto-Dravidian speak-

ers, from the eastern horn of the Fertile Crescent. TheIndo-European speakers, who might have arrived ~3,500

years ago, are the third potential source of Indian genepool. The Austro-Asiatic and Tibeto-Burman speakers

with ties to East/Southeast Asia form the fourth majorcontributors. The most recent conquerors from Central

Asia and the colonizers from Europe might also haveadded to this ethnic multiplicity.

The social structure of the Indian population is domi-nated by the hierarchical Hindu caste system. There are4,635 well-defined endogamous populations in India,

which are culturally stratified as tribes and non-tribes. The

532 tribal communities, who are supposed to be the abo-riginal inhabitants of the sub-continent, constitute 7.76%of the total population (Indian Census 2001). The ori-gin of caste system in India is a matter of debate. Previousgenetic studies on Indian castes and tribes failed toachieve a consensus on Indian origins and affinities. A fewstudies reported closer affinity of Indian castes with eitherthe Europeans or the Asians. Studies of Bamshad et al [2]and Basu et al [3]support the genetic differentiation ofcaste and tribal populations, and the North Indian inva-sion of Indo-European speaking nomads, pushing theDravidian tribes to southern peninsula. On the otherhand, Kivisild et al [4] suggest that Indian tribal and caste

populations derived largely from the same genetic herit-age of Pleistocene southern and western Asians, receivinglimited gene flow from external regions since Holocene.Further, Cordaux et al [5] reports that the paternal line-ages of Indian castes are more closely related to the Cen-tral Asians than to the Indian tribal groups, therebysupporting the view that Indian caste groups are primarilythe descendents of the Indo-European migrants. Morestudies are required for a better understanding of thegenetic structure of the diverse Indian populations, wheremany questions remain unanswered. In the present study,

mtDNA and Y chromosome of three different tribal pop-ulations of Andhra Pradesh (AP), South India, were ana-lyzed. On comparing the results with available data, we

were able to reconstruct the evolutionay history of Indiancaste and tribal populations, by providing a comprehen-

sive picture of their genetic structure.

Results and discussionMitochondrial DNA variation

The sequence data corresponding to nucleotide positions15927 16550 [revised Cambridge Reference Sequence(rCRS)] [6] that includes the HVR I region was obtainedfrom 347 individuals belonging to the three tribal popu-lations. Insertions were observed at two positions(16169_16170insC, 16262_16263insT). Nucleotide sub-stitutions were observed at 120 sites, defining 149 HVR Imotifs. Seventy haplotypes were observed among Pard-han, 53 among Naikpod and 48 among Andh tribes. A

total of 131 (76.5%) unique haplotypes were observed;56 (80%) in Pardhan, 37 (70%) in Naikpod and 38(79%) in Andh. Only two HVR I motifs were found to beshared among all the three populations; 10 haplotypes

were shared between Pardhan and Naikpod, four betweenPardhan and Andh and six between Naikpod and Andh.

At the individual level, 43% of haplotypes were shared bytwo or more individuals, 75% of this being within thesame population.

Demographic expansion of the populations

Based on AMOVA, the variation among studied popula-tions was only 2.1%, while the remaining 97.9% variation

was within populations. The number of haplotypes, hap-lotype diversity, nucleotide diversity, mean number ofmismatches, Fu's Fs statistic values, raggedness index (r),expansion ages and initial effective population sizes of thethree populations are summarized in Table 1. The demo-graphic history of each population was examined by com-puting the pairwise difference distributions. Unimodeldistribution curves were observed, which could be inter-preted as signs of demographic expansion. Likewise, theraggedness index was found to be less than 0.02 in all thepopulations studied; values of r lower than 0.05 also sug-gest demographic expansions [7]. Negative values of Fsthat differ significantly from zero, and the significant (P 98%) of theIndian maternal gene pool that consists of the Dravidianand Indo-European speakers is genetically more similar,and received only minor gene flow with the recent inva-sions from both the West and the East, since their initiallate Pleistocene settlement. On the other hand, the Indian

Y-chromosome lineages show obvious difference in theirdistribution pattern among the tribal and caste popula-

tions. However, the lower castes, (backward classes andscheduled castes, as per the Indian Constitution) showstriking similarity with the Indian tribal populations.

These groups, which constitute more than 85% of thehierarchical Hindu caste system, have the indigenousM52, M95 and M89, as their major Y lineages. This resultsuggests that the Indian lower castes are genetically moreassociated with the tribal populations, than to the highercastes, an evocative of their tribal origins. The presence ofthese native haplogroups in the Indo-European nomads,

who arrived ~3500 ybp and established themselves asupper castes, might be due to the recent admixture withthe local populations. The presence of the so called west/

central Asian lineages like J2, R1 and R2 in most of theendogamous tribal populations, and its higher STR diver-sity indicates its presence in the sub-continent muchbefore the arrival of the Indo-European pastoralists. Inshort, the impact of their arrival in the Indian sub-conti-nent is rather social and political, than genetic.

MethodsDNA isolation

About 10 ml of blood samples from healthy unrelatedindividuals belonging to three tribal populations namelyPardhan (n = 193), Naikpod (88) and Andh (66) werecollected from the northwestern region of Adilabad dis-

trict of AP, southern India with their informed writtenconsent with the help of the Tribal Welfare Department,Government of AP. DNA was isolated from the samplesusing the standard protocol [29].

Amplification of mitochondrial DNA

The hyper-variable regions (HVR I and HVR II) andselected coding regions of the mtDNA were amplifiedfrom 10 ng of template DNA using 10 pM of each primer,100 M dNTPs, 1.5 mM MgCl2 and 1 U of Taq DNApolymerase. Generally, 35 cycles of reaction was per-
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formed with 30 sec denaturation at 94C, 1 min anneal-ing at 58C and 2 min extension at 72C. Annealingtemperature and time were slightly modified for few setsof primers. The reactions were carried out in MJ Researchthermal cycler (PTC-200).

Y-chromosomal markers

Sixteen Y-chromosome biallelic polymorphic markers vizM89, M216, M9, M45, M82, M69, M170, M172, M11,M175, M95, M122, M207, M173, M17, and M124 weretyped to construct the Y-chromosome phylogeny of thestudied populations according to Y- Chromosome Con-sortium nomenclature [30]. The PCR cycles were set-up

with an initial denaturation of 5 min at 95C, followed by3035 cycles of 30 sec at 94C, 30 sec at the primer-spe-cific annealing temperature (52 60C), and 45 sec. at72C, and final extension of 7 min at 72C. Length varia-tions at 6 Y-STR loci, DYS19, DYS389-1, DYS389-2,

DYS390, DYS391 and DYS393, were typed using previ-ously published primer sequences [31]. The multiplexPCR amplifications were performed in reaction volumesof 10.0 l with 1U of AmpliTaq Gold DNA polymerase(Applied Biosystems, Foster City, CA), 10 mM Tris-HCl(pH 8.3), 50 mM KCl, 1.5 mM MgCl2, 250 m dNTPs, 3.0m of each primer (forward primers are fluorescentlylabeled), and 10 ng of DNA template. Thermal cyclingconditions were as follows: (1) 95C for 10 min, (2) 28cycles: 94C for 1 min, 55C for 1 min, 72C for 1 min,(3) 60C for 45 min, and (4) 25C hold. The PCR ampli-cons along with GS500 LIZ size standard were analyzedusing the ABI 3730 DNA Analyser (Applied Biosystems,

Foster City, CA). The raw data were analyzed using theGeneMapper v3.7 software program (Applied Biosystems,Foster City, CA).

Sequencing of the PCR products

PCR products were directly sequenced using BigDye Ter-minator cycle sequencing kit (Applied Biosystems) in ABIPrism 3730 DNA Analyzer following manufacture's pro-tocol. The individual mtDNA sequences were judgedagainst the rCRS [6] using AutoAssembler ver 2.1(Applied Biosystems, Foster City, USA). The sequences

were aligned using CLUSTAL X [32,33], and mutationdata were scored with MEGA ver 3.1 [34,35]. Mitochon-

drial haplogroups were assigned to all samples accordingto Sun et al [36] and Thangaraj et al [9].

Phylogenetic and statistical analyses

Data analyses for mtDNA sequences and Y-SNPs were per-formed using the ARLEQUIN software package [37,38].Haplotype- and nucleotide- diversity and their standarddeviations (SD); mismatch distributions, mean pairwisedifferences and their SD; Fu's Fs statistics [39] and associ-ated P-values based on 1000 stimulated samples, ragged-ness index 'r', Fst distances between pairs of populations

and associated P-values based on 1000 permutations andTajima's Dvalue [40] were calculated. Analyses of molec-ular variance (AMOVA) were performed to evaluate thegenetic structure of the populations; the significance of

variance components tested with 10,000 permutations.

Other statistical inferences, including initial theta (a) andvalues of tau () were used to calculate effective popula-tion size (Ne = a/2) and population expansion age (Y=Ax/2) [41]. An average mutation rate = 0.00124 persite per generation with an average generation timeA = 20

years, was used for calculation. Median joining networks[42] were constructed with the help of Network 4.112program [43] with default settings. Haplotype diversityand STR variance were calculated according to Kivisild etal [4].

Authors' contributionsLS, KT and IT conceived the study and drafted the final

manuscript. IT, GC, VKS and LVKSB performed the exper-iments and aligned the sequences. BMR participated inthe design of the study. AGR contributed to the overallstudy design; all authors read, revised and approved thefinal manuscript.

Additional material

AcknowledgementsWe are grateful to all the original donors for making this work happen. We

thank Mr. Aggarwal, Mr. Prasad and primary health officers, Tribal Research

Institute, Government of Andhra Pradesh for helping in the collection of

samples. The support offered by the Commissioner, Department of Tribal

Welfare is also thankfully acknowledged. IT is grateful to Department of

Biotechnology, Government of India for financial support.

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Additional File 1

Indian Y-SNP data. Y-chromosome biallelic polymorphism data of 1285

Indian samples are given. The Y-SNP and Y-STR haplotypes of the three

populations analyzed are also provided.

Click here for file

[http://www.biomedcentral.com/content/supplementary/1471-2156-7-42-S1.xls]

Additional File 2

Mitochondrial DNA mutation data. The data provided represent the

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[http://www.biomedcentral.com/content/supplementary/1471-

2156-7-42-S2.xls]
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