Common genetic heritage and admixture among Indian population groups as revealed by mtDNA markers

Abstract

The present study determines the interand intra-population affinities or variations among the diverse population groups of India. The major goal of the present study was to understand the peopling of India and its role in the peopling of Southeast Asia using 11 restriction fragment length polymorphism (RFLP) mitochondrial DNA (mtDNA) markers. A total of 950 unrelated individuals belonging to 19 population groups having varied ethnic, linguistic, and geographic backgrounds were chosen for the present study. All the studied sites, except HpaI 3592, are found to be polymorphic in the data set. High frequencies of M haplogroup are found among the South Indian populations, whereas N haplogroup is found to be high among the North Indian populations. Sub-haplogroups C and D of M are found only in the Tibeto-Burman-speaking Northeast population groups, suggesting their probable migration from Central Asia. Sub-haplogroups A and B of N are shared by both Northeast and North Indian population groups. The sub-haplogroups of M and N are absent among the South Indian and East Indian populations except the Thoti of the South India Dravidian tribe. The Northeast Indian populations exhibit the highest haplotypic diversity, whereas the South and East Indian populations have the lowest haplotypic diversity. The study provides evidence for a common maternal genetic substratum of Indian populations with probable differential admixture from Eurasia, i.e Europe and Asia, with a decreasing trend from North to South India. Sub-haplogroups of M and N and 9 bp deletion frequency patterns suggest gene flow from East Asia to India was restricted only to Northeast India and not suggest significant movement of people from India to East Asia through Northeast India.

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1© 2012 The Anthropological Society of Nippon
A
NTHROPOLOGICAL SCIENCE
Vol. advpub(0), 000–000, 2012
Common genetic heritage and admixture among Indian population
groups as revealed by mtDNA markers
Sanjenbam Yaiphaba MEITEI
1
, Khangembam Somibabu MEITEI
2
, Benrithung MURRY
2
,
Prakash Ranjan M
ONDAL
2
, Kallur Nava SARASWATHY
2
*,
Pradeep Kumar G
HOSH
2
, Mohinder Pal SACHDEVA
2
1
Department of Anthropology, Vidyasagar University, Midnapore, West Bengal 721102, India
2
Biochemical and Molecular Anthropological Laboratory, Department of Anthropology, University of Delhi, Delhi 110007, India
Received 18 July 2011; accepted 30 July 2012
Abstract The present study determines the inter- and intra-population affinities or variations among
the diverse population groups of India. The major goal of the present study was to understand the
peopling of India and its role in the peopling of Southeast Asia using 11 restriction fragment length
polymorphism (RFLP) mitochondrial DNA (mtDNA) markers. A total of 950 unrelated individuals be-
longing to 19 population groups having varied ethnic, linguistic, and geographic backgrounds were
chosen for the present study. All the studied sites, except HpaI 3592, are found to be polymorphic in
the data set. High frequencies of M haplogroup are found among the South Indian populations, where-
as N haplogroup is found to be high among the North Indian populations. Sub-haplogroups C and D
of M are found only in the Tibeto-Burman-speaking Northeast population groups, suggesting their
probable migration from Central Asia. Sub-haplogroups A and B of N are shared by both Northeast
and North Indian population groups. The sub-haplogroups of M and N are absent among the South
Indian and East Indian populations except the Thoti of the South India Dravidian tribe. The Northeast
Indian populations exhibit the highest haplotypic diversity, whereas the South and East Indian popu-
lations have the lowest haplotypic diversity. The study provides evidence for a common maternal ge-
netic substratum of Indian populations with probable differential admixture from Eurasia, i.e Europe
and Asia, with a decreasing trend from North to South India. Sub-haplogroups of M and N and 9 bp
deletion frequency patterns suggest gene flow from East Asia to India was restricted only to Northeast
India and not suggest significant movement of people from India to East Asia through Northeast India.
Key words: haplogroup, haplotype, heterogeneity
Introduction
India, the major land bridge between Africa and Southeast
Asia, plays a key role in studies of human evolution and mi-
gration. Of the various theories proposed regarding human
migration, the southern coastal route has gained increasing
acceptance. The major findings of the HUGO Pan Asia SNP
Consortium (2009) where that peopling of Southeast Asia
occurred via the Northeastern part of India. However,
Cordaux et al. (2004) and Saraswathy et al. (2009) opined
that Northeast India was a barrier rather than a corridor. This
issue is still debated, and the role of India in the peopling of
East Asia remains controversial. Further, settlements in
various parts of the world had never been continuous and
systematic. This is evidenced through geography-specific
distribution of pre-human forms, e.g. Australopithecus in
Africa (Dart, 1925; White et al., 1994). Moreover, geograph-
ic and climatic catastrophies, such as the glaciations in
Eurasia, led to major migrations towards the southern part of
the globe. Prehistoric or historic human movements along
with the present globalization have lead to homogenization
of population groups, thus making human migratory history
obscure and difficult to study. Anthropologists have no other
option except to look at genetic signatures among the extant
population groups, by means of sophisticated technologies.
However, such huge investments simply to understand mi-
gratory histories may not be feasible for developing coun-
tries such as India. Thus an attempt is made in the present
study to understand the peopling of India and also its role in
the peopling of Southeast Asia using restriction fragment
length polymorphism (RFLP) mitochondrial DNA
(mtDNA) markers. The 19 populations selected for the
present study are from various geographical regions of India
with unique cultural, ethnic, and linguistic affiliations.
Materials and Methods
The details of the studied population groups are given in
Table 1. Genomic DNA was extracted from 5 ml of intrave-
nous blood samples collected from 950 unrelated individuals,
Advance Publication
* Correspondence to: Kallur Nava Saraswathy, Department of An-
thropology, University of Delhi, Delhi 110007, India.
E-mail: knsaraswathy@yahoo.com
Published online 20 October 2012
in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.120730

2 S.Y. MEITEI ET AL. ANTHROPOLOGICAL SCIENCE
with prior informed written consent, using the salting-out
technique (Miller et al., 1988). Ten mtDNA restriction site
polymorphisms (HaeIII np 663, HpaI np 3592, AluI np
5176, AluI np 7025, DdeI np 10394, AluI np 10397, MnlI np
10871, HincII np 13259, AluI np 13262, HaeIII np 16517)
and one insertion/deletion polymorphism (IDP; COII/
tRNA
Lys
intergenic 9 bp deletion) were screened through
polymerase chain reaction using standard primers and proto-
cols (Torroni et al., 1993, 1996; Santos et al., 2004). Of the
total collected samples, mitochondrial haplogroups could be
assigned to 780 samples. The geographical location of the
populations studied is shown in Figure 1.
Statistical analysis
Allele and haplotype frequencies were calculated. Haplo-
type diversities were estimated as described by Nei (1987) us-
ing the formula: haplotype diversity (h) = (n/n − 1) (1 −Σp
i
2
)
where p
i
is the sample frequency of ith haplotype and n is the
sample size. Haplogroups were identified on the basis of an-
alyzed sites (MITOMAP: www.mitomap.org). AMOVA
and pairwise Fst genetic distances were calculated using
ARLEQUIN 3.0 software (Excoffier et al., 2005).
Results
All the studied sites, except HpaI 3592, are polymorphic
in the data set. Only three sites (DdeI 10394, AluI 10397, and
MnlI 10871) are found to be polymorphic in all the popula-
tions (Table 2). These three sites are important for the iden-
tification of the major mitochondrial haplogroups M and N.
The 9 bp deletion is found in Northeast Indian populations,
except for three tribal groups—Paite, Thadou, and Koms;
and also in three North Indian populations (especially from
Himachal Pradesh)—Brahmins, Rajputs, and Jats. The fre-
quency of the 9 bp deletion exhibits a wide range of varia-
tion in the populations studied here, ranging from 0.023
among the Meiteis of Northeast India, and Brahmins and
Jats of North India to 0.06 among the Aimols.
The populations studied here also show variation in the
distribution of major haplogroups—M and N, and their sub-
haplogroups (Table 3). Haplogroup M seems to decrease as
one moves up from South India to North India and the re-
verse is the case for the N haplogroup. The Dravidian speak-
ers of East and South India possess high frequencies of M
haplogroup, ranging from 76.32% among the Nayakpod
tribe
(South
India)
to
81.58%
among
the
Oraon
tribe
of
East India. The Munda tribe, which speaks the Mundari
group of Austro-Asiatic linguistic family, also exhibits a
high percentage of M haplogroup, i.e 82.85%. Five North
Indian caste populations have M frequencies ranging from
31.25%
in
Sindhi
to
68.18%
in
Jats.
The
Northeastern
tribal and non-tribal populations are intermediate in the
distribution M of haplogroup, ranging from 24.33% in Koms
to 74.42% in Meiteis. Sub-haplogroups C and D of M
haplogroup are found only in the Tibeto-Burman-speaking
Table 1. Details of the 19 population groups studied with sample size, geographical distribution, population and linguistic affiliation
Population (code)
Sample
size
Population affinity
Geographical
distribution
Linguistic
affiliation
Social status
Andhra Brahmins (APB) 44 Proto-Australian South India Dravidian Caste
Nayakpods (NYP) 38 Proto-Australian South India Dravidian Tribe
Thotis (THO) 48 Proto-Australian South India Dravidian Tribe
Kolams (KLM) 36 Proto-Australian South India Dravidian Tribe
Munda (MUN) 35 Proto-Australian East India Austro-Asiatic Tribe
Oraons (ORN) 38 Proto-Australian East India Dravidian Tribe
Meitei (MEI) 43 East Asian North East India Tibeto-Burman Non-tribe
Paite (PAI) 41 East Asian North East India Tibeto-Burman Tribe
Thadou (THAD) 42 East Asian North East India Tibeto-Burman Tribe
Koms (KMS) 37 East Asian North East India Tibeto-Burman Tribe
Rongmei (RONG) 40 East Asian North East India Tibeto-Burman Tribe
Aimol (AML) 50 East Asian North East India Tibeto-Burman Tribe
Muslim (MSLM) 49 European with East Asian tinge North East India Tibeto-Burman Religious groups
Bamon (MBA) 38 European with East Asian tinge North East India Tibeto-Burman Non-tribe
Brahmins (HPB) 43 European North India Indo-European Caste
Jats (JTS) 44 European North India Indo-Europran Caste
Rajputs (RJP) 41 European North India Indo-European Caste
Sindhi (SIN) 32 European North India Indo-European Caste
Aggarwal (AGR) 41 European North India Indo-European Caste
Figure 1. Map showing the geographical distribution of the popu-
lations studied in this work.

mtDNA STUDY OF INDIAN POPULATION GROUPS 3Vol. 120, 2012
Northeast population groups. Sub-haplogroups A and B of N
are shared by both Northeast and North Indian population
groups, whereas these are absent among the Austro-Asiatic-
and Dravidian-speaking populations of India.
While analyzing the haplotypic structure in each haplo-
group, it is found that the M haplogroup has five haplotypes
(Table 4); of these, the 00111101010 haplotype is shared by
all the studied populations with frequencies ranging from
24.32% among Koms to 79.55% among Thotis. As com-
pared to the M haplogroup, which has five haplotypes, the N
haplogroup has nine haplotypes, whereas the 00110011010
haplotype is shared by all these studied populations with fre-
quencies ranging from 4.65% among Brahmins of Andhra
Pradesh to 38.78% among the Aimol tribe. Population-
specific haplotypic diversity reveals that the South Indian
and East Indian caste and tribal populations have the least
haplotypic diversity, i.e. below 50%. The Northeast Indian
tribal and non-tribal populations exhibit the highest haplo-
typic diversity, reaching as high as 85% among the Rongmei
tribe. The North Indian populations have similar diversity
values to those of Northeastern populations, except Jats,
who have 50% haplotypic diversity.
Table 2. Distribution of allele frequencies at 10 RFLP loci and 1 indel of mtDNA among the 19 population groups of India*
Table 3. Haplogroup frequency distribution among the populations studied
Population
Code (N)
HaeIII
663 (+)
HpaI
3592 (+)
AluI
5176 (−)
AluI
7025 (−)
DdeI
10394 (+)
AluI
10397 (+)
MnlI
10871 (+)
HincII
13259 (−)
AluI
13262 (−)
HaeIII
16517 (+)
9 bp (+)
APB (44) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.795 (35) 0.795 (35) 0.205 (9) 0.000 (0) 1.000 (44) 0.841 (37) 0.000 (0)
NYP (38) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.789 (30) 0.763 (29) 0.237 (9) 0.000 (0) 1.000 (38) 0.868 (33) 0.000 (0)
THO (48) 0.000 (0) 0.000 (0) 0.021 (1) 0.000 (0) 0.854 (41) 0.833 (40) 0.167 (0) 0.000 (0) 1.000 (48) 1.000 (48) 0.000 (0)
KLM (36) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.806 (29) 0.806 (29) 0.194 (7) 0.000 (0) 1.000 (36) 0.917 (33) 0.000 (0)
MUN (35) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.829 (29) 0.829 (29) 0.171 (6) 0.000 (0) 1.000 (35) 0.914 (32) 0.000 (0)
ORN (38) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.868 (33) 0.816 (34) 0.184 (4) 0.000 (0) 1.000 (38) 0.921 (35) 0.000 (0)
MEI (43) 0.023 (1) 0.000 (0) 0.093 (4) 0.046 (2) 0.744 (32) 0.744 (32) 0.256 (11) 0.046 (2) 0.907 (39) 0.605 (26) 0.023 (1)
PAI (41) 0.293 (12) 0.000 (0) 0.000 (0) 0.000 (0) 0.610 (25) 0.512 (21) 0.488 (20) 0.000 (0) 0.976 (40) 0.829 (34) 0.000 (0)
THAD (42) 0.238 (0) 0.000 (0) 0.093 (4) 0.000 (0) 0.667 (28) 0.643 (27) 0.357 (15) 0.024 (1) 1.000 (42) 0.762 (32) 0.000 (0)
KMS (37) 0.513 (19) 0.000 (0) 0.000 (0) 0.000 (0) 0.378 (14) 0.243 (9) 0.757 (28) 0.000 (0) 1.000 (37) 0.784 (29) 0.000 (0)
RONG (40) 0.025 (1) 0.000 (0) 0.200 (8) 0.000 (0) 0.625 (25) 0.625 (25) 0.375 (15) 0.050 (2) 0.950 (38) 0.775 (31) 0.050 (2)
AML (50) 0.020 (1) 0.000 (0) 0.120 (6) 0.000 (0) 0.480 (24) 0.460 (23) 0.540 (27) 0.000 (0) 0.980 (49) 0.820 (41) 0.060 (3)
MSLM (49) 0.000 (0) 0.000 (0) 0.163 (8) 0.000 (0) 0.775 (38) 0.735 (36) 0.265 (13) 0.020 (1) 0.979 (48) 0.653 (32) 0.041 (2)
MBA (38) 0.026 (1) 0.000 (0) 0.079 (3) 0.000 (0) 0.631 (24) 0.553 (21) 0.447 (17) 0.026 (1) 0.946 (36) 0.789 (30) 0.053 (2)
HPB (43) 0.000 (0) 0.000 (0) 0.070 (3) 0.000 (0) 0.535 (23) 0.488 (21) 0.512 (22) 0.023 (1) 0.977 (42) 0.651 (28) 0.023 (1)
JTS (44) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.682 (30) 0.682 (30) 0.318 (14) 0.023 (1) 1.000 (44) 0.909 (40) 0.023 (1)
RJP (41) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.537 (22) 0.512 (21) 0.488 (20) 0.024 (1) 0.976 (40) 0.927 (38) 0.049 (2)
SIN (32) 0.031 (1) 0.000 (0) 0.000 (0) 0.000 (0) 0.375 (12) 0.313 (10) 0.687 (22) 0.032 (1) 0.969 (31) 0.687 (22) 0.000 (0)
AGR (41) 0.000 (0) 0.000 (0) 0.000 (0) 0.000 (0) 0.341 (14) 0.341 (14) 0.659 (27) 0.000 (0) 1.000 (41) 0.660 (27) 0.000 (0)
* Number in parenthesis next to each site represents the number of mutant sites.
Population code
(N*)
Haplogroup frequency (%)
MCDNAB
APB (44) 79.55 (35) 20.45 (9)
NYP (38) 76.32 (29) 23.68 (9)
THO (48) 81.25 (39) 2.08 (1) 16.67 (8)
KLM (36) 80.56 (29) 19.44 (7)
MUN (35) 82.85 (29) 17.15 (6)
ORN (38) 81.58 (31) 18.42 (7)
MEI (43) 62.79 (27) 2.33 (1) 9.30 (4) 20.92 (9) 2.33 (1) 2.33 (1)
PAI (41) 51.22 (21) 19.51 (8) 29.27 (12)
THAD (42) 52.38 (22) 2.38 (1) 9.52 (4) 11.90 (5) 23.25 (10)
KMS (37) 24.33 (9) 24.32 (9) 51.35 (19)
RONG (40) 37.50 (15) 5.00 (2) 20.00 (8) 30.00 (12) 2.50 (1) 5.00 (2)
AML (50) 34.00 (17) 12.00 (6) 46.00 (23) 2.00 (1) 6.00 (3)
MSLM (49) 55.10 (27) 2.04 (1) 16.33 (8) 24.49 (12) 2.04 (1)
MBA (38) 44.75 (17) 2.63 (1) 7.89 (3) 36.84 (14) 2.63 (1) 5.26 (2)
HPB (43) 39.53 (17) 2.33 (1) 6.98 (3) 48.84 (21) 2.33 (1)
JTS (44) 68.18 (30) 29.55 (13) 2.27 (1)
RJP (41) 51.22 (21) 43.90 (18) 4.88 (2)
SIN (32) 31.25 (10) 65.63 (21) 3.13 (1)
AGR (41) 34.15 (14) 65.85 (27)
* N denotes sample size and the numbre in parenthesis next to each haplogroup represents the number of individuals bearing the haplogroup.

4 S.Y. MEITEI ET AL. ANTHROPOLOGICAL SCIENCE
Table 4. Haplotypic frequency distribution of the populations studied
Haplo-
group
Haplotype APB NYP THO KLM MUN ORN MEI PAI THAD KMS RONG AML MSLM MBA HPB JTS RAJ SIN AGR
M
00101101000 4.65
00111101000 2.78 9.09 7.89 7.89 16.28 10.00 2.38 10.26 2.04 10.42 8.82 2.33 2.56 2.78
00111101010 79.07 72.22 79.55 72.73 68.42 73.68 39.53 40.00 50.00 24.32 25.64 30.61 43.75 38.24 37.21 67.44 48.72 32.26 33.33
00111101100 2.33 2.56
00111101110 2.50 2.04
C
00111100010 2.38 5.13
00111100110 2.33 2.08 2.33
D
00011101000 4.65 4.76 7.69 10.20 6.25 4.65
00011101010 2.27 4.65 4.76 12.82 2.04 10.42 5.88 2.33
N
00110010010 2.33
00110010110 2.56 3.23
00110011000 16.28 5.56 9.30 2.50 13.51 6.12 16.67 8.82 23.26 9.30 5.13 32.26 30.56
00110011001 2.08
00110011010 4.65 16.67 15.91 18.18 15.79 13.16 6.98 15.00 11.90 8.11 25.64 38.78 4.17 29.41 20.93 20.93 33.33 29.03 33.33
00110011100 2.33
00110011110 2.56
00111011000 2.94 4.65
00111011010 2.78 2.27 5.26 2.50 2.70 2.04 2.08 2.56 3.23
A
10110011000 2.50 14.29 8.11 2.56
10110011010 2.33 20.00 4.76 32.43
10111011000 2.50
10111011010 2.50 2.38 10.81
B
00110010011 2.33
00110011011 5.13 6.12 2.33 5.13
00110011111 2.33
00111011011 2.08 5.88
Haplotypes are made in order to the position of restriction sites, i.e. mt663, mt3592, mt5176, mt7025, mt10394, mt10397, mt10871, mt13259, mt13262, mt16517 and 9 bp indel. ‘1’ and ‘0’ in
the haplotypes signify the presence and absence of restriction sites and deletion in the case of RFLP and indel markers, respectively.

mtDNA STUDY OF INDIAN POPULATION GROUPS 5Vol. 120, 2012
Discussion
The absence of the HpaI 3592 restriction site in the popu-
lations studied here reveals that all the mitochondrial ge-
nomes investigated belong to the L3 lineage of mtDNA,
which is further branched out into M, N and R haplogroups.
Sub-grouping of M, N and R occurred due to mutation and
drift, and spread along the Asian and European countries,
and at the same time L3 was lost (Macaulay et al., 2005).
The highly polymorphic nature of the DdeI 10394, AluI
10397 and MnlI 10871 in the present study indicates that all
the studied populations belong either to M or N haplogroups
as these sites are used as diagnostic restriction sites for these
haplogroups (MITOMAP: www.mitomap.org). Haplogroup
M was supposed to have originated in Eastern Africa
~60000 years ago and migrated towards Asia (Quintana-
Murci et al., 1999), and hence is regarded as an Asia-specific
haplogroup.
The presence of fewer M haplotypes is indicative of lower
heterogeneity among the studied populations. Furthermore,
sharing of these M haplogroups by all the populations stud-
ied here is suggestive of a common maternal genetic contri-
bution in the Indian population. The higher frequencies of
the M haplogroup among the South Indian (Dravidian
speakers) and East Indian (Proto-Australian: Dravidian and
Austro-Asiatic speakers) tribes support the hypothesis that
these populations could be the earliest settlers of India
(Guha, 1935; Keith, 1936; Thapar, 1966; Pattanayak, 1998;
Basu et al., 2003).
Regarding the sub-haplogroups of M, almost all (Meitei,
Thadou, Rongmei, Aimol, Manipur Muslim, and Manipur
Bamon) populations of Northeast India with East Asian eth-
nic background exhibit C, ranging from 2.33% among
Meitei to 5% among Rongmei, and D, ranging from 7.89%
among Manipur Bamon to 20% among Rongmei. If the
southern coastal route of human migration is to stand, this is
not expected as the sub-haplogroups are absent among the
Dravidian- and Austro-Asiatic-speaking tribals and also
among the North Indian caste populations except for the
presence of C and D sub-haplogroups among Himachal
Brahmin and D sub-haplogroup among Thoti of South Indi-
an Dravidian tribe with relatively lower frequencies. Thus,
one cannot presume that these sub-haplogroups of M are of
Indian origin. In other words, one can say that the presence
of these sub-haplogroups in Northeast India could mainly be
due to gene flow from Southeast Asian countries where their
frequencies are reported to be higher (Ballinger et al., 1992;
Kolman et al., 1996; Maca-Meyer et al., 2001; Wen et al.,
2004). Further, gene flow into Northeast India seems to be
mainly from Central Asia and Siberia as most of the popula-
tions of these regions have high frequencies of C and D
(Kolman et al., 1996). This further points to the fact that
gene flow was confined to the Northeastern Indian popula-
tions only and there was no further advance towards south-
ern or northern India. This is also supported by the studies
done by Cordaux et al. (2003, 2004) and Saraswathy et al.
(2009), who suggested Northeast India to be a major barrier
rather than a corridor as was proposed by Reddy et al.
(2007).
Like the M sub-haplogroups, only the Northeast Indian
populations document N sub-haplogroups, suggesting gene
flow into Northeast India from Eastern Eurasia leading to
heterogeneity of Northeast Indian populations as was also
reported by Saraswathy et al. (2009). This contradicts the
mythological history, in which it is believed that peopling of
Manipur was done from Southeast Asia (Shakespear, 1912).
However, the present findings are in agreement with the pro-
posal of the peopling of Manipur through China (Pemberton,
1835). The North to South decrease of N haplogroup fre-
quencies in the populations studied herein, with the lowest
frequency being documented among Dravidian and Austro-
Asiatic populations, reflects the extent of admixture, which
is decreasing from North India to South India as was also re-
ported by previous studies (Reich et al., 2009; Saraswathy et
al., 2010). B haplogroup is found to be absent among the
Siberian populations (Kolman et al., 1996). Therefore, Cen-
tral Asia seems to be the most probable region which could
have contributed to the maternal gene pool of Northeast
Indian populations and the presence of D among Thotis
(South Indian Dravidian population) seems inexplicable.
The genetic contribution of Southeast Asia to Northeast
Indian populations does not seem to be feasible because of
either the zero or low frequency of A and B haplogroups
amongst the Southeast Asian populations (Kolman et al.,
1996).
There are different opinions regarding the origin of the
9 bp deletion (Wrischnik et al., 1987; Passarino et al., 1993;
Merriwether et al., 1994; Graven et al., 1995; Soodyall et al.,
1996; Alves-Silva et al., 1999) and it is assumed that it might
have multiple origins (Thangaraj et al., 2008). Despite the
possible multiple origins of the 9 bp deletion, the deletion
motif remains a useful marker for tracing population affini-
ties and migration patterns as this deletion motif varies from
one geographical region to another (Yao et al., 2000). The
East Asian, Southeast Asian, and Polynesian 9 bp deletion
have been claimed to arise in China at about ~60000 BP
(Redd et al., 1995; Yao et al., 2000). The presence of the
9 bp deletion among three North Indian and five Northeast
Indian populations could be of Chinese origin as these pop-
ulations have high frequencies of East Asian specific haplo-
group. The absence of this deletion among South and East
Indian populations in the present study supports the genetic
discontinuity of these Proto-Australian populations with
Northeast Indian populations.
Further, the Tibeto-Burman-speaking tribes and non-
tribes of Northeast India are generally believed to have mi-
grated from Tibet and Yunan province of China (Ansari,
1991). It is possible that these East Asian population groups,
who entered the Indian mainland through Tibet and Hima-
layan tracts, might have carried this deletion from central
China and left their genetic imprints on the North Indian
Himalayan foothills and further moved into the Northeast
India. This is also supported by the present study where the
9 bp deletion, though in low frequency, was found only
among two populations of North India and five populations
of Northeast India. This is in accordance with the previous
reports on mtDNA studies where high degree of genetic ho-
mogeneity among Himalayan and Northeast Indian Tibeto-
Burman groups was observed (Su et al., 1999, 2000;
Cordaux et al., 2004).

6 S.Y. MEITEI ET AL. ANTHROPOLOGICAL SCIENCE
The highly diverse population of Northeast India is also
depicted in the population-specific haploytype diversity
graph (Figure 2) where these Northeast populations have the
highest haplotype diversity, followed by North Indian popu-
lations. Later gene flow from the Eurasian populations at
different periods among the North Indian populations might
have enhanced the diversity of these populations. On the
other hand the lower haplotypic diversity among the South
and East Indian populations (<50%) indicates more com-
monality and homogeneity of these population groups
though they belong to different linguistic groups—Dravidian
and Austro-Asiatic.
Further, AMOVA was performed to understand the mo-
lecular variance among various categories of the studied
populations (Table 5). Intra-population variation is highly
significant in all the studied populations as expected. Inter-
population variation among South Indian versus East Indian
and Dravidian versus Austro-Asiatic categories are found to
be non-significant, as both include population groups of
similar type. This indicates that the Austro-Asiatic speakers
of East Indian and Dravidian speakers of South India are
genetically similar with respect to the studied mtDNA mark-
ers, suggesting that they have an autochthonous common
genetic background that may be Proto-Australian. This find-
ing is consistent with the views of Thom (2007) and Kumar
et al. (2008), who they traced these two linguistically diverse
populations to a common archaic hunter-gatherer stock of
the Pleistocene era. Furthermore, the rest of the categorized
populations show significant differences, indicating diver-
sified gene pools due to differential genomic contributions
followed by cultural and geographical isolation. Among-
group variation based on geographical distribution show
significant differences among three categories, i.e. South
Indian versus Northeast Indian, South Indian versus North
Indian, and East Indian versus North Indian. Further, South
Indian versus East Indian and Northeast Indian versus North
Indian populations are found to be genetically close to each
other. Variation based on linguistic category, i.e. Dravidian
versus Austro-Asiatic groups, is found to be non-significant.
Further, variation based on linguistic and geographical
groups also show significant differences. The result of
AMOVA suggests that language and geography are the two
important factors influencing the Indian population struc-
ture. Further, castes versus tribes category of the presently
studied populations show non-significant differences, sug-
gesting common maternal genetic unity among the popula-
tions studied in this work.
Figure 2. Graph depicting the haplotypic diversity among the populations studied.
Table 5. Analysis of molecular variance (AMOVA) among the 19 population groups of India
Groups
Percentage of variation
FST values
Among groups Inter-population Intra-population
South Indian and North East Indian populations 6.89* 5.93** 87.17** 0.1283
South Indian and East Indian populations −0.10 −1.63 101.73 −0.0173
South Indian and North Indian populations 14.60* 2.89* 82.50** 0.1750
North East Indian and North Indian populations 0.76 6.81** 92.43** 0.0757
East Indian and North Indian populations 15.61* 3.94* 80.45** 0.1955
Linguistic groups 6.45* 5.53** 88.03** 0.1197
Dravidian and Austro-Asiatic linguistic groups −0.66 −1.48 102.14 −0.0214
Geographically 6.32* 5.53** 88.15** 0.1185
Castes and tribes 0.43 10.04** 89.53** 0.1047
* Significance level at 0.05.
** Significance level at 0.01.

mtDNA STUDY OF INDIAN POPULATION GROUPS 7Vol. 120, 2012
Conclusion
Although the present study has the limitation of not
having a huge number of markers and does not involve
advanced technologies, easy-to-type RFLP markers quite
convincingly reflect the migratory histories of the pop-
ulations of India. M and N haplogroup and their sub-
haplogroups distribution patterns, along with the allelic
distribution of the selected mtDNA markers among the pop-
ulations studied here, indicate the common maternal genetic
lineages of Indian populations. The study also reveals ad-
mixture among Indian populations with a decreasing trend
from North to South India and higher heterogeneity among
Northeast Indian populations. Moreover, the study also rais-
es doubts about the peopling of Southeast Asia through
India, because the present data indicates that gene flow
occurred from East Asia to Northeast India and not from
mainland India because of the genetic discontinuity ob-
served in this study in populations of Northeast India
compared to both the South and the East Indian populations.
The present study was restricted only to the major haplo-
groups which could be typed using less expensive RFLP
technology. Further studies on sub-haplogroups, which can
be typed only by sequencing, are likely to reveal better
insights into the peopling of India.
Acknowledgments
We are thankful to the University Grant Commission SAP
(Special Assistance Program), Department of Biotechnolo-
gy, and University Grant Commission for providing the fi-
nancial support for conducting the present study. We
acknowledge all the subjects for their help in providing their
blood samples. We are also grateful to the Department of
Anthropology, University of Delhi for providing the infra-
structure to carry out the study.
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