Y Chromosome Haplogroup Distribution in IndoEuropean Speaking Tribes of Gujarat, Western India
Priyanka Khurana1., Aastha Aggarwal2, Siuli Mitra3, Yazdi M. Italia4, Kallur N. Saraswathy3,
Adimoolam Chandrasekar5, Gautam K. Kshatriya3*.
1 Department of Anthropology, School of Applied Sciences, Dr. Harisingh Gour University, Sagar, Madhya Pradesh, India, 2 South Asia Network for Chronic Disease, Public
Health Foundation of India, Delhi, India, 3 Department of Anthropology, University of Delhi, Delhi, India, 4 Valsad Raktdan Kendra, R.N.C. Free Eye Hospital Complex,
Valsad, Gujarat, India, 5 Anthropological Survey of India, Southern Regional Center, Mysore, Karnataka, India
Abstract
The present study was carried out in the Indo-European speaking tribal population groups of Southern Gujarat, India to
investigate and reconstruct their paternal population structure and population histories. The role of language, ethnicity and
geography in determining the observed pattern of Y haplogroup clustering in the study populations was also examined.
A set of 48 bi-allelic markers on the non-recombining region of Y chromosome (NRY) were analysed in 284 males;
representing nine Indo-European speaking tribal populations. The genetic structure of the populations revealed that none
of these groups was overtly admixed or completely isolated. However, elevated haplogroup diversity and FST value point
towards greater diversity and differentiation which suggests the possibility of early demographic expansion of the study
groups. The phylogenetic analysis revealed 13 paternal lineages, of which six haplogroups: C5, H1a*, H2, J2, R1a1* and R2
accounted for a major portion of the Y chromosome diversity. The higher frequency of the six haplogroups and the pattern
of clustering in the populations indicated overlapping of haplogroups with West and Central Asian populations. Other
analyses undertaken on the population affiliations revealed that the Indo-European speaking populations along with the
Dravidian speaking groups of southern India have an influence on the tribal groups of Gujarat. The vital role of geography in
determining the distribution of Y lineages was also noticed. This implies that although language plays a vital role in
determining the distribution of Y lineages, the present day linguistic affiliation of any population in India for reconstructing
the demographic history of the country should be considered with caution.
Citation: Khurana P, Aggarwal A, Mitra S, Italia YM, Saraswathy KN, et al. (2014) Y Chromosome Haplogroup Distribution in Indo-European Speaking Tribes of
Gujarat, Western India. PLoS ONE 9(3): e90414. doi:10.1371/journal.pone.0090414
Editor: Michael D. Petraglia, University of Oxford, United Kingdom
Received November 15, 2013; Accepted February 1, 2014; Published March 10, 2014
Copyright: ß 2014 Khurana et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The work was funded by Department of Biotechnology (DBT) grant (vide letter BT/PR9840/MED/12/366/2007). The funders had no role in study design,
data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: g26_51@yahoo.co.in
. These authors contributed equally to this work.
with Africa in the west, Eurasia in the north and the Orient in the
east. The country’s unique location gives rise to a great variety of
environmental conditions and associated biodiversity [12] which
in turn has attracted people from all over the globe.
Archaeological and paleontological evidence dating back to the
middle and late Pleistocene era points towards early human
occupation of the Indian subcontinent [13–16]. Similar evidence
of antiquity of Indian populations has been established by genetic
marker studies. The high levels of gene diversity and coefficients of
gene differentiation obtained using autosomal markers for Indian
populations are a testimony of both, the antiquity and the complex
population structure, of this massive human conglomeration
existing in the southern part of Asia [17–19]. Recent genetic
studies based on mtDNA showing the high frequency of
mitochondrial lineages with greater age, high diversity and wide
distribution amply demonstrate the prehistoric existence of
mankind on the Indian subcontinent [20–21]. Similar analyses
of Y chromosome variation based on both bi-allelic and
microsatellite markers have documented the existence of substantially deep rooted lineages among Indian populations buttressing
Introduction
India is the second most populous country in the world with a
population of 1.21 billion [1]. About 4,635 different population
groups are spread across the country [2]. Exorbitant as it may
sound, existence of at least 50–60 thousand essentially endogamous groups has been reported in the country [3–4]. The present
day Indian population is divided into tribal and non-tribal groups.
Tribal populations constitute 8.2% of the total population [5] and
are considered to be the indigenous populations of India [6–8].
The tribal groups of India belong to four broad linguistic families:
Austro-Asiatic, Dravidian, Indo-European and Tibeto-Burman
[9]. The Indo-European and Dravidian speaking populations are
considered to be the major contributors to the development of
Indian culture and society [10]. Both Austro-Asiatic and
Dravidian speaking tribes belong to the primary pre-historic
populations of India [7,11]. Tibeto-Burman speakers also include
many tribal populations but their geographical distribution is
largely restricted to the North-Eastern region of India. India thus
exhibits an enormous genetic, cultural and linguistic diversity
which can partly be attributed to its position at the tri-junction:
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Y Haplogroups in Tribes of Western India
districts of Gujarat. A description of relevant population
characteristicsof study groups along with populations from other
studies is presented in Table 1. Figure 1 illustrates the sampling
location of study populations from Gujarat. The detailed
description of the study populations has been given previously
[42]. Blood samples collected in EDTA coated vacutainers were
subjected to DNA extraction following salting-out method [43]. A
total of 48 bi-allelic markers were analysed to identify the Y
chromosome haplogroups. The markers were typed using primer
pairs described in Karafet et al. [44]. The PCR cycling conditions
with an initial denaturation of 5 minutes at 95uC; followed by 35
cycles of 1 minute at 94uC; 45 seconds at the primer-specific
annealing temperature (52–60)uC and extension at 72uC for
2 minutes and 30 seconds; followed by final extension of
7 minutes at 72uC were followed. The amplicons generated were
subjected to sequence reactions using BigDyeTM (Applied Biosystems, Foster City, USA) Terminator Cycle sequencing kit in ABI
Prism 3730 DNA analyser following manufacturer’s protocol and
further analysed in SeqScape software, version 2.5.
the claim of early habitation of humans on the Indian
subcontinent [22–25].
The unique and complex structure of the Indian population is
attributed to the multiple waves of migration and the resultant
gene-flow which occurred in the past [12,26]. Some scholars have
provided evidence to explain the origin and migration of the major
linguistic families extant in India [25,27]. It is worth mentioning
that speakers of Austro-Asiatic language in India are exclusively
tribal, which may be indicative of their being one of the oldest
inhabitants of India [28,29]. The arrival of the Indo-European
speakers via the Northern corridor of India around 3,500–4,000
years ago is believed to be responsible for one of the major influxes
of people in the Indian subcontinent [30], followed later by the
infiltration of colonizers from different parts of the world. Thus,
several studies have affirmed the influence of Eurasian and Asian
populations on the Indian gene pool [23–24,31–34].
Within this complex scenario, many interaction models such as
gene-language, gene-geography and gene-ethnicity have been
contested. Previous studies have shown inverse correlation
between genetic affinities and geographical distance [11,35].
Significant genetic differentiation between caste and tribal
populations has been reported [31,33,36], as against a model
which suggests that there is considerable sharing of Pleistocene
heritage among them with a limited gene flow [34]. Similarly,
congruence between language and genes has been proposed by
various scholars [9,37–38] along with a competing view supporting that genetic affinities may not necessarily be dependent on
linguistic similarities [39–41]. Although each study has contributed
significantly to understanding the role of language, culture and
geography in relation to the genetic affiliation and demographic
history of Indian populations; a major limitation in them has been
the poor representation of Indo-European speaking tribal populations. This is a critically important limitation since the IndoEuropean speaking tribes provide ample opportunity for examining the influence of linguistic assimilation on the genomic diversity
of India.
Keeping the above in view, we present an analysis based on the
study of 48 bi-allelic markers in nine Indo-European speaking
tribal groups of Southern Gujarat which lies in the western part of
India. The main objectives of the study were (a) to study the
distribution of Y haplogroups; (b) to study the relative influence of
language, geography or ethnicity on the genetic structure of
populations using the pattern of Y haplogroup clustering and
finally (c) to relate the observed pattern of Y haplogroup clustering
with the Y chromosome lineages which arrived in India largely
from the Northern corridor at different points of time. To achieve
the study objectives the results were first compared with published
studies on the Indian populations and then with available data on
the Eurasian populations. The Indian populations were selected
keeping in view the availability of data, their linguistic and socioculture status and geographical position. Similarly, the Eurasian
populations for which published sources were available were
considered for analysis since the historical migrations from these
regions are known.
Statistical and phylogenetic analysis
The revised Y-Chromosome phylogenetic tree [44] was referred
to for the assignment of haplogroups based on informative binary
markers. Haplogroup frequencies were estimated by a simple gene
count method. In order to determine the genetic structure of study
populations, a model propounded by Harpending and Ward [45]
was applied. The model examines the relative role of genetic drift
and gene flow in causing population differentiation. In the model,
the expected frequency of gene diversity for each population is first
graphically represented with respect to the distance from the gene
frequency centroid, rii, which is given by the formula:
rii ~
Where, pi and P are the frequency of the haplogroups in a
population i and in the pooled populations respectively. In the
second stage of the model, Harpending and Ward propose an
island model of population structure in which there is a linear
relationship between gene diversity and the distance from the
centroid which is calculated by the formula:
hi ~H(1{rii )
Where, hi and H correspond to the gene diversity value in the
population i and in all the populations as a whole respectively. As
per the model, outlier populations that have undergone systematic
migrations will show greater gene diversity than predicted by the
regression line, while outlier groups that are isolated will exhibit
lower than predicted gene diversity.
In order to determine whether the Y chromosome haplogroup
distribution among Indian populations is structured on the basis of
ethnicity, geography or linguistic affiliation, an analysis of
molecular variance (AMOVA) based on haplogroup frequencies
was computed for the various tentative categories using ARLEQUIN software, version 3.1 [46]. Using the same software
Slatkin’s lineraised pairwise FST values were calculated on
haplogroup frequencies and analysed through non metric multidimensional scaling (MDS) in SPSS version 16.0 using ALSCAL
programme. The MDS plot was constructed in order to
graphically represent the nature of clustering between the study
populations and other world populations.
Materials and Methods
Collection and processing of blood samples
This study was approved by the Departmental Ethical
Committee of the Department of Anthropology, University of
Delhi. Informed written consent was obtained from all the
participants. A 5 ml blood sample was drawn by a trained
medical practitioner from randomly chosen 284 healthy, unrelated
males from nine tribal population groups of Valsad and Surat
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(pi {P)2
½P(1{P)
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Y Haplogroups in Tribes of Western India
Figure 1. Sampling areas; Map of India highlighting Gujarat (top); Regions of study pointed out in the map of Gujarat (bottom).
doi:10.1371/journal.pone.0090414.g001
For carrying out AMOVA on different populations secondary
source haplogroup frequency data (Table S1) was compiled from
different studies [23–25,47]. For the construction of the MDS plot
data (Table S2) was compiled from various studies [48–53].
the haplogroups. Its frequency varied from 3.45% among
Pavagadhi Chaudhari to 40.74% among Mota Chaudhari.
However, H2-Apt was found to be absent among Vasava and
Gamit populations. While lineage H* was observed in only three
individuals, one each from Konkana, Gamit and Mota Chaudhari.
Haplogroup R. R1a1*a sub-clade of R haplogroup was
found to be the next most frequently occurring lineage after H1a*.
Its frequency was found ranging from 5.56% in Gamit to 62.07%
in Pavagadhi Chaudhari. Its sister sub-clade R2-M124 was
observed 27 times with a frequency varying from 5.56% among
Gamit to 20.83% among the Konkana tribe. Barring Valvi
Chaudhari, R2 was absent from all other Chaudhari groups.
Haplogroup J. J2 with its two sub-clades J2b2* and J2a
constituted a major portion of Haplogroup J in the current study.
Except Konkana and Mota Chaudhari, either of the two J2 subclades was present in all other groups. J2b2* sub-clade was
observed in 21 Y chromosomes. Its frequency was found to be
11% in Gamit, 19% in Valvi Chaudhari and 21% in Pavagadhi
Chaudhari. The remaining four populations of Dhodia, Dubla,
Vasava and Nana Chaudhari exhibited similar frequency values
varying in a narrow range between 4% and 4.48%. Sub-clade J2a
was observed only 8 times in the nine groups. It was present in four
of the groups with a minimum frequency of 3.17% in Dhodia to a
maximum frequency of 7.14% in Dubla.
Haplogroup C. Out of the seven sub-clades of C haplogroup,
only one sub-clade C5 with its two main derivatives C5a and C5*
was observed 21 times in all the populations except Pavagadhi
Chaudhari. C5a lineage was observed to be 62 times more
frequent then its sister branch C5*. Its frequency varied from
3.17% in Dhodia to 12.5% in Valvi Chaudhari, while that of C5*
was found to vary from 3.7% in Mota Chaudhari to 9.38% in
Valvi Chaudhari.
Results
Haplogroups distribution
The frequency distribution of Y chromosome haplogroups
among the study populations along with the phylogenetic
relationship between them is presented in Figure 2. The side
branches on the tree represent Y SNP for which the ancestral state
was observed, while the direct branch represents Y markers for
which the mutant allelic state was observed; leading to haplogroup
designation in the particular sample. Analysis of 48 bi-allelic
markers of the Y chromosome showed 13 paternal lineages that
were distributed throughout haplogroups H, R, J, C, F, L, K and
Q. Haplogroup H represented the most frequently occurring
haplogroup (40.14%) followed by groups R (28.17%), J (10.21%)
and C (8.45%) respectively. Sparse distribution was observed for
the lineages F*, L1, Q3 and K* across all the populations.
Haplogroup H. M69 mutation, which is a characteristic of
haplogroup H was found on 114 of the total 284 Y chromosomes.
Haplogroup H was further segregated into three lineages, H1 by
the presence of M52-C allele, H2 by the presence of Apt-A allele
and H* by absence of the two alleles. These haplogroups were
further subdivided into a number of sub-clades. Lineage H1a* of
H1 group was observed 71 times and represented the most
frequently occurring lineage across all the populations. Its
frequency varied from a minimum of 3.45% among Pavagadhi
Chaudhari to a maximum of 62.5% in Vasava. Lineage H2
represented the second most frequently occurring lineage among
the H haplogroup and third most common haplogroup among all
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Table 1. Geographical, Social and Linguistic description of study groups and populations included in the study for Y haplogroup
comparison.
Population
Linguistic affiliationa
Socio-Culture affiliationb
Sample size
South Asia
India
West
Dhodia
IE
T
63
Dubla
IE
T
42
Konkana
IE
T
24
Vasava
IE
T
24
Gamit
IE
T
18
Valvi Chaudhari
IE
T
32
Nana Chaudhari
IE
T
25
Mota Chaudhari
IE
T
27
Pavagadhi Chaudhari
IE
T
29
Madia Gond
DR
T
14
Katkari
IE
T
19
MahadeoKoli
IE
T
11
Pawara
IE
T
16
Thakur
IE
T
48
Desasth Brahmin
IE
C
16
Maratha
IE
C
16
Dhangar
IE
C
16
Chitpavan Brahmin
IE
C
15
Gujrat Patel
IE
C
9
Chenchu
DR
T
20
Yerukula
DR
T
18
Kuruva
DR
T
10
Irular
DR
T
10
Naikpod Gonnd
DR
T
18
Andhra Brahmin
DR
C
15
Kamma Chaudhary
DR
C
15
Kappu naidu
DR
C
18
Komati
DR
C
20
Raju
DR
C
19
Reddy
DR
C
12
Bhovi
DR
C
13
Gowda
DR
C
4
Iyengar
DR
C
17
Lingayat
DR
C
10
Chakkliar
DR
C
9
Gounder
DR
C
14
Kallar
DR
C
9
Pallar
DR
C
15
Vanniyar
DR
C
10
Mahali
AA
T
25
Bhumij
AA
T
15
Birhor
AA
T
10
Ho
AA
T
7
Kharia
AA
T
10
South
East
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Table 1. Cont.
Population
Linguistic affiliationa
Socio-Culture affiliationb
Sample size
Munda
AA
T
7
Santhal
AA
T
7
Juang
AA
T
10
Saora
AA
T
13
Paroja
DR
T
13
Bhuiyan
IE
T
81
Bathudi
IE
T
36
Kora
IE
T
17
Bihar brahmin
IE
C
18
kayasth
IE
C
14
bhumihar
IE
C
20
Baniya
IE
C
11
Rajput
IE
C
12
Yadav
IE
C
8
Gope
IE
C
16
Karan
IE
C
18
Oriya Brahmin
IE
C
24
Bauri
IE
C
19
Mahishiya
IE
C
17
Namasudra
IE
C
13
Central
Halba
IE
T
21
jaunsri
IE
T
6
Bhoksha
IE
C
10
Kanyakubj Brahmin
IE
C
10
Khatri
IE
C
7
Kurmi
IE
C
13
UP Thakur
IE
C
5
UP Kurmi
IE
C
6
9
North-East
Hamar
TB
T
Kuki
TB
T
7
Lai
TB
T
10
Lusei
TB
T
6
Mara
TB
T
5
Himachal Pradesh RAJPUT
IE
C
15
North
Afganistan
204
Pakistan
718
Iran
150
West Asia
Iraq
139
Jordan
146
Turkey
523
Lebanon
104
Syria
111
Central Asia
Kazakhstan
30
Alltai
98
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Table 1. Cont.
Population
Linguistic affiliationa
Socio-Culture affiliationb
Sample size
Uzbekistan
54
Kyrgyzthan
13
Uyghursta
68
Europe
Greece
442
France
23
Netherlands
27
Germany
16
Czech and Slovakia
45
Alabina
51
Macedonia
20
Poland
55
Hungary
45
Ukraine
50
Georgia
63
a
Linguistic affiliation: Indo-European (IE), Dravidian (DR), Tibeto-Burman (TB) and Austro-Asiatic (AA);
Socio-cultural affiliation: Tribe (T), Caste (C).
doi:10.1371/journal.pone.0090414.t001
b
Haplogroup F*, K*, L1 and Q3. Parahaplogroup F* along
with the other parahaplogroup K* and two haplogroups L and Q
accounted for 13.03% of the total haplogroups. After initial
screening of M89-T allele, 11 samples failed to resolve further and
were therefore grouped under F*. Similarly, 8 individuals did not
exhibit any mutation except G allele for M9 and were therefore
grouped under K*. Other two sub-clades L1-M27 and Q3-M346
were present, but in low frequencies only.
(p,0.001) is due to differences between the populations. In the
hierarchical approach taken, at the next level populations were
subdivided according to their affiliation into: Indo-European,
Dravidian, Tibeto-Burman and Austro-Asiatic language families.
A substantially high percentage of difference between populations
(13.21%) was observed indicating strong distinctiveness of
populations belonging to the different linguistic families. This
was followed by the subdivision of populations by the geographical
regions they inhabit. The geographical clustering of populations
displayed comparatively lower (6.25%) amount of differentiation
between the populations. Similarly, in a comparison between
Indian castes and tribes a comparatively lower fraction of variance
(5.13%) points towards relatively lesser differences between them.
Following this, further categories of Indo-European speaking tribal
populations of Gujarat were made for comparing with other
Indian populations, keeping in mind the effect of language,
geography and ethnicity; in that order of importance. The results
showed that the lowest group variance among all categories was
between Indo-European speaking groups of Gujarat and other
Indo-European populations; it was almost 5 times lesser than the
variance observed between the studied populations and the
Dravidian speaking groups of India. Interestingly, further subdivision of Indo-European populations into tribes and castes
revealed a lesser fraction of variability among study populations
and Indo-European caste populations (3.45%) as compared to
Indo-European speaking tribes (6.57%). Moreover, as compared
to Dravidian speaking caste populations, the population in Gujarat
showed less differentiation with Dravidian speaking tribes as
reflected by low group variance values (5.3%). Subdivision of
Indo-European populations simultaneously by caste, tribe and
geographical zones (West, Central and East) indicated effective
role of geographic distance in determining genetic distance. All the
values compared were found to be highly significant.
Y chromosome diversity
Haplogroup diversity values for each of the nine populations
along with haplogroup distribution are given in Figure 2.
Haplogroup diversity (h) which is equivalent to gene diversity for
haploid genomes ranged from 0.586 in Pavagadhi Chaudhari to
0.899 in Valvi Chaudhari.
Population Structure and Gene Flow
Figure 3 represents a plot of haplogroup diversity regressed
against distance from gene frequency centroid (rii). The values of
gene diversity (hi) and genetic distances from centroid (rii) used in
the nine study population groups along with their standard errors
are given in Table 2. Majority of the populations exhibited higher
than predicted gene diversity combined with a low to moderate
deviation from the theoretical line of regression and the distance
from the gene frequency centroid. Three populations Gamit,
Vasava and Pavagadhi Chaudhari displayed lower than predicted
gene diversity. Pavagadhi Chaudhari showed the farthest distance
from the gene frequency centroid. The results indicated that the
tribal groups of Gujarat are neither explicitly isolated nor
absolutely admixed.
AMOVA
Table 3 presents the results of the AMOVA based on different
categories of populations subdivided by language, geography and
ethnicity. Analysis of molecular variance based on haplogroup
frequencies among the study groups showed that 91.6% of
variability is due to within population differences and 8.4%
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Genetic proximities
We compared the study populations with 24 additional world
populations already published in separate studies (Figure 4). A
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Y Haplogroups in Tribes of Western India
Figure 2. Distribution of Y-binary halpogroups and haplogroup diversity (h) among the study populations of Gujarat. The markers
used in the study are shown on each branch.
doi:10.1371/journal.pone.0090414.g002
belt of Gujarat and are composed of tribal populations which are
linguistically classified as Indo-European. To date several studies
have provided significant insights into the paternal genetic history
of India [23–24,34,36]; however none till now had taken into
consideration the Indo-European speaking tribal populations
inhabiting Gujarat in spite of their interesting geographical
location and cultural attributes. It is also worth mentioning that
the Indo-European speaking tribes of India not only exhibit the
complexity of historical interaction between the indigenous Indian
and migratory groups but also reflect lack of one-to-one
correlation between language, mode of subsistence and social
system [23]. Thus, the Indo-European speaking tribes represent an
appropriate model to study the possible genetic foot prints of the
multiple waves of migrations. In addition to tracing the origin and
impact of ancient migrations, evaluation of the impact of
geography and social structure in shaping the genetic structure
of the present day Indo-European speaking tribal populations of
Gujarat was considered equally important. Thus, in the subsequent text we examine the paternal genetic variation of the nine
Indo-European speaking tribes from Gujarat using high resolution
Y chromosomal unique event polymorphisms (UEPs).
stress value of 0.18 for the MDS plot indicated a good fit between
the two dimensional graph and the original distance matrix. The
comparison revealed four major clusters of South Asian, Central
Asian, West Asian and European populations. All the populations
under study with the exception of Pavagadhi Chaudhari were
found to be clustered together. The occurrence of South Asian
populations (the current study groups, Afghanistan, Pakistan and
Iran) with Central Asian populations (Kazakhstan, Altai Region,
Uzbekistan, Kyrgyzstan, Uyghurstan) on Axis I, conversely with
West Asian populations (Iraq, Jordan, Turkey, Lebanon, Syria)
with respect to Axis II probably indicate similarities of haplogroups between them.
Discussion
The North-Western corridor of India has witnessed many waves
of migrants from different parts of the world, with a majority being
male migrants [31]. Gujarat is located on the western most point
of the Indian sub-continent and has acted as a significant corridor
to draw outsiders -conquerors, refugees and travellers who have
contributed significantly to the present day gene pool of Indian
populations [34]. Valsad and Surat districts are part of the tribal
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Y Haplogroups in Tribes of Western India
Figure 3. Regression of gene diversity (hi) on distance from centroid (rii). The solid line represents the theoretical regression line.
doi:10.1371/journal.pone.0090414.g003
explanation for the observation of high gene diversity coupled
with high-level of genetic differentiation could lie in an
overwhelming genetic admixture from different sources or in an
early inflow of genes from a common source followed by rapid
population expansion and subsequent fission into isolated,
endogamous populations. Results from Harpending and Ward
analysis do not appear to favour the former explanation. Thus, the
most plausible explanation for the current diversity scenario in the
Indian population seems to be the suggestion made by Majumder
et al. [17], in which an early demographic expansion of modern
humans within India during Palaeolithic period and later fission of
the populations is conjectured.
Genetic structure of study populations
Our analysis based on Y chromosomal UEPs apportioned the
study samples into 13 haplogroups representing 10 major Y
lineages (C5, H1a*, H2, R1a1*, R2, J2, L1, F*, K* and Q3) in
India. Haplogroup diversity (0.772) was found to be comparable
with Dravidian speaking populations (0.723), but higher than
Indo-European speaking populations (0.684) in the country [54].
Given the number of views in support of Austro-Asiatic and
Dravidian speaking tribes belonging to the primary pre-historic
population of India [7,11]; the high gene diversity values observed
in the study populations, which are in turn comparable to
Dravidian speaking populations, are suggestive of greater antiquity, large effective size or role of gene flow in these groups. The
analysis of molecular variance revealed that the extent of genetic
differentiation was high among study populations which could be
attributed to either the lower effective population size of these
groups or the Y chromosome making them vulnerable to the effect
of genetic drift which further accelerates the process of differentiation between the populations. But, accentuated differentiation
due to genetic drift is expected to be accompanied with lower
diversity. However, in the present study, elevated levels of gene
diversity, rule out a major role of genetic drift in shaping the
observed pattern of genetic differentiation. Nevertheless, the
In-situ versus Ex-situ Origin of Y lineages
The indigenous versus exogenous origin of Indian paternal
lineages has been widely contested. Among the study populations,
six sub-haplogroups namely, C5, H1a*, H2, J2, R1a1* and R2
constituted the major paternal lineages that together accounted for
85.92% of the Y chromosomes. While the indigenous origin of
sub-clades C5, H1a*, H2 and R2 are accepted, the status of subclades J2 and R1a1* are contested as they are believed to have
been introduced in India with the demic diffusion of ProtoDravidian Neolithic agriculturists from West Asia and the influx of
Indo-European pastorals from Central Asia. It is worth mentioning here that the high frequency and associated diversity of a
haplogroup is correlated with the possible place of origin of a
particular haplogroup [55]. In the present investigation haplogroup H, especially H1a, represented the most frequently
observed Y chromosomal lineage followed by H2 sub-haplogroup.
Its higher frequency among the Indian tribes particularly among
the Dravidian speaking tribes of South India and its limited
presence elsewhere on the Indian subcontinent had led some
scholars to denote it as a tribe-specific haplogroup [36]. However,
several subsequent studies have confirmed the presence and equal
prevalence of haplogroup H and its associated H1a and H2
branches across linguistically and ethnically diverse populations
and in different regions of India, except the North-Eastern region
[23–24,54]; thus ruling it out as a tribal-specific marker and
supporting the uniform distribution of haplogroup H among
Indian populations. An Indian homeland for haplogroup H can
also not be refuted keeping in view its higher microsatellite
diversity among Indian populations [24]. Haplogroup H has also
Table 2. Gene diversity (hi) and genetic distances from the
centroid (rii) among the study populations of Gujarat.
Population
rii ± S.E
hi± S.E
Dhodia
0.02460.008
0.86960.002
Dubla
0.02460.006
0.86660.004
Konkana
0.05560.011
0.85560.009
Vasava
0.08660.057
0.60560.022
Gamit
0.09260.038
0.69960.028
Valvi Chaudhari
0.06260.019
0.89960.004
Nana Chaudhari
0.06760.029
0.82360.010
Mota Chaudhari
0.08960.043
0.79260.012
Pavagadhi Chaudhari
0.15760.093
0.58660.017
doi:10.1371/journal.pone.0090414.t002
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Y Haplogroups in Tribes of Western India
Table 3. AMOVA based on Y Chromosome haplogroup frequencies.
Categories
Among groups
variance (%)
Among populations
within groups variance (%)
Within populations
variance (%)
IE speaking tribes of Gujarat
8.40
4 language groupsa
13.21
18.52
91.60
Geographyb
6.25
23.22
70.53
Castes and tribes of India
5.13
24.70
70.17
68.27
IE speaking tribes of Gujarat with IE populations of India
1.81
19.57
78.62
IE speaking tribes of Gujarat with DR populations of India
9.61
11.55
78.84
IE speaking tribes of Gujarat with AA Populations of India
28.16
7.94
63.90
IE speaking tribes of Gujarat with IE castes of India
3.45
12.97
83.58
IE speaking tribes of Gujarat with IE tribes of India
6.57
15.17
78.26
IE speaking tribes of Gujarat with DR tribes of India
5.30
11.47
83.23
IE speaking tribes of Gujarat with DR caste of India
8.54
12.51
78.95
IE speaking tribes of Gujarat with IE tribes from three
geographical regions C,W & E of India
9.24
15.12
75.63
IE speaking tribes of Gujarat with IE castes from three
geographical regions C,W & E of India
7.59
9.78
82.63
a
Language groups = Indo-European (IE), Dravidian (DR), Tibeto-Burman (TB) and Austro-Asiatic (AA),
Geography = Central (C), West (W), East (E), South(S) and North East (NE). All the values are significant, p,0.05.
doi:10.1371/journal.pone.0090414.t003
b
recent back migration [32,52]. On the other hand, the established
Indian ancestry of gypsy populations is surely the reason for
elevated levels of H haplogroup among them [56]. All the
been reported from Central Asian, West Asian and Gypsy
populations in Europe. However, its low frequency and prevalent
diversity pattern in Central Asia and West Asia could be due to
Figure 4. MDS Plot showing genetic relationships particularly between the South Asian populations with the world populations.
The South Asian populations including the study populations of India are shown in as solid circles ( ), the European populations as open circles (o),
Central Asian populations as triangle (D) and West Asian population as cross (x). The abbreviation used are Afganistan (Afg), Pakistan (Pak), Iran (Ira),
Iraq (Irk), Jordan (Jor), Turkey (Tur), Lebanon (Leb), Syria (Syr), Kazakhstan (Kaz), Altai (Alt), Uzbekistan (Uzb), Kyrgyztan (Kyr), Uyghurstan (Uyg), Greece
(Gre), France (Fra), Netherlands (Net), Germany (Ger), Czech and Slovakia (CzandSlo), Alabina (Ala), Macedonia (Mac), Poland (Pol), Hungary (Hun),
Ukraine (Ukr), Georgia (Geo), Dhodia (Dh), Dubla (Du), Konkana (Kon), Vasava (Vas), Gamit (Gam), Valvi Chaudhari (VC), Nana Chaudhari (NC), Mota
Chaudhari (MC), Pavagadhi Chaudhari (PC).
doi:10.1371/journal.pone.0090414.g004
N
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Y Haplogroups in Tribes of Western India
three Y lineages based on their possible origin. These lineages
include Central Asian, West Asian and indigenous Indian Y
lineages.
observations, therefore clearly point towards in-situ origin of
haplogroup H among Indian populations.
Haplogroup C is widely distributed in Eastern and Central Asia,
Oceania and Australia [44]. As expected, all the Y chromosomes
under C haplogroup belonged to the C5 sub-clade. It was
observed in a frequency of 8.45% which is the highest ever
reported frequency for C5 in India and whose spread is
circumscribed along the coastal belt of India [24,54]. High STR
diversity in India and South-East Asia in the backdrop of
haplogroup C has also been observed [34,57]. Interestingly none
of the C haplogroup derivatives frequent in South-East Asia have
been reported from India. Therefore, the possibility of introduction of C5 haplogroup from South-East Asia as a result of back
migration to India appears doubtful and its indigenous origin
appears to be more probable [13].
Haplogroup J is predominantly found among the populations of
West Asia, North Africa, Europe, Central Asia, Pakistan, and
India [44] and widely linked with the spread of agriculture from
the Fertile Crescent that extends from Israel to Western Iraq. In
the Indian subcontinent two sub-clades of J - J2a and J2b have
been reported. Consistent with the previous studies, a higher
proportion of J2 in West India as compared to North and South
regions of India has been recorded in the present study [24,54].
Two models pertaining to the homeland for Indian J2 sub-clades
have been contested, West Asia and Central Asia. Cordaux et al.
[35] had proposed the Central Asian homeland for Indian J2 subclade mainly because of higher frequency of J2 in Central Asia. It
is worth mentioning here that J1 sub-clade which appears in
appreciable frequency in Central Asia is largely absent from the
Indian as well as most of the West Asian populations [44].
Haplogroup R is represented by two sub-clades R1a1* and R2
among the study populations. After haplogroup H1a, haplogroup
R1a1* represented the most frequently occurring haplogroup.
Haplogroup R is widely distributed in Central Asia, Eastern
Europe, West Asia and the Indian subcontinent [58–59]. The
higher frequency of haplogroup R1a, up to 63% in Central Asia
and its relatively lower occurrence in other regions has been linked
with Central Asian origin of R1a clade [36]. However, later
studies [24,54] showing higher prevalence of R1a sub-clade along
with high microsatellite diversity among the tribal populations of
India lend support to probable South Asian origin of R1a subclade as suggested by Kivisild et al. [34]. This is further
substantiated by almost the complete absence of other derivatives
of haplogroup R1 among the Indian populations, which is
expected in case of the inflow from Central Asia [23–24,41].
In the present investigation sub-clade R2 occurred with a
frequency of 9.51%, which is similar to its frequency reported from
other Indian populations [24,34,36,54]. The frequency of R2
decreases as one goes further west from India and its frequency is
almost negligible in Europe. Moreover, its frequent occurrence
among Dravidian speaking groups as compared to Indo-European
or Austro-Asiatic speaking groups of India can be attributed to its
indigenous Indian origin.
The MDS plot (Figure 4) also reflects the closeness of South
Asian populations with West Asian and Central Asian populations
possibly due to overlapping of haplogroups. In comparison to the
world populations the overall mean haplogroup diversity among
the study populations was relatively higher than in the European
or East Asian populations [32,48] whereas it was found to be lower
than that of Central Asian and West Asian populations [49,51]. As
mentioned earlier the high frequency and diversity of a
haplogroup is indicator of the possible place of origin of a
particular haplogroup [55]. Consequently, the observed haplogroups in the present investigation could be apportioned into
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Determinants of population Clustering
Lack of any major exogenous contribution of Y lineages and
existence of high haplogroup diversity indicate the possible male
assimilation from other neighbouring populations of India among
the study groups. Analysis of molecular variance (Table 3)
performed on the basis of haplogroup frequencies revealed some
interesting patterns. The quantification of variance into different
categories of population showed the highest variance between the
four linguistic groups of India followed by the variance between
geographical regions and finally the caste versus tribe categories.
The least percentage of variance was observed between the study
populations and other Indo-European speaking caste populations.
However, the geographical partitioning of the Indo-European
speaking tribal and caste populations into three major zones: West,
Central and East showed the important effect of geography in
shaping the Y diversity pattern since on this basis the zonal
percentage of variance was observed to elevate between the study
populations and other Indo-European groups of India. Thus,
pattern of Y chromosome clustering of Indian populations reflects
the major role of geography over language and ethnicity as far as
Y chromosomal lineages are concerned. After Indo-European
speaking caste populations, the lowest variance of Gujarat
populations was observed with Dravidian speaking tribal populations. These similarities suggest either shared paternal ancestries of
linguistically dissimilar groups or the influence over the indigenous
tribal groups of India of the Indo-European speakers, who arrived
later.
The present investigation indicates that tribes of Gujarat show
both high genetic diversity and genetic differentiation. It is
therefore conceivable that these groups, with a fairly large
population size, have passed through a long evolutionary history
experiencing an early demographic expansion and later fission of
the populations. Further affinities of study groups with IndoEuropean speaking non tribes followed by Dravidian speaking
tribal groups suggest the possibility that these native tribal
population groups of Western India might have adopted the
Indo-European language during the process of cultural assimilation and absorption while still retaining their genetic links with the
Dravidian speaking tribal populations. Thus, it is recommended
that the present day linguistic affiliation of any Indian population
should be considered with caution while reconstructing the
demographic history of the country. In conclusion, a study based
on the recently discovered bi-allelic loci and microsatellite loci in
the populations can shed light on the possible explanation of the
overlapping of haplogroup distribution between tribes of Gujarat
with other Asian populations and further deepen the understanding of the population history of India.
Supporting Information
Table S1 Y chromosome haplogroup frequencies data
among study populations and other populations of India
considered for AMOVA.
(XLS)
Table S2 Y chromosome haplogroup frequencies data
among study populations and other populations of
World considered for MDS analyses.
(XLS)
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Y Haplogroups in Tribes of Western India
the Department of Anthropology, University of Delhi, Delhi for granting us
the ethical clearance to carry out our work.
Acknowledgments
We would like to thank all the individuals who volunteered for this study on
genetic variation and provided their blood samples. We would like to
extend our gratitude towards the Valsad Raktdan Kendra (Centre for Blood
Donation, Valsad), Valsad, Gujarat for helping us collect the blood
samples. We would also like to thank the Anthropological Survey of India
for their collaboration and for giving the permission to undertake our
laboratory work in their Southern Regional Centre. We also wish to thank
Author Contributions
Conceived and designed the experiments: GKK KNS YMI PK. Performed
the experiments: PK SM AA. Analyzed the data: PK AA AC GKK.
Contributed reagents/materials/analysis tools: AC GKK YMI KNS.
Wrote the paper: PK AC AA GKK.
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