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Hum Genet (2006) 120:543–551DOI 10.1007/s00439-006-0234-x
 123
ORIGINAL INVESTIGATION
A shared Y-chromosomal heritage between Muslims and Hindusin India
Ramana Gutala · Denise R. Carvalho-Silva · Li Jin · Bryndis Yngvadottir ·Vasanthi Avadhanula · Khaja Nanne · Lalji Singh · Ranajit Chakraborty ·Chris Tyler-Smith
Received: 6 May 2006 / Accepted: 12 July 2006
 
/ Published online: 2 September 2006
©
Springer-Verlag 2006
Abstract
Arab forces conquered the Indus Deltaregion in 711 AD and, although a Muslim state wasestablished there, their in
X
uence was barely felt in therest of South Asia at that time. By the end of the tenthcentury, Central Asian Muslims moved into India fromthe northwest and expanded throughout the subconti-nent. Muslim communities are now the largest minorityreligion in India, comprising more than 138million peo-ple in a predominantly Hindu population of over onebillion. It is unclear whether the Muslim expansion inIndia was a purely cultural phenomenon or had agenetic impact on the local population. To address thisquestion from a male perspective, we typed eight micro-satellite loci and 16 binary markers from the Y chromo-some in 246 Muslims from Andhra Pradesh, andcompared them to published data on 4,204 males fromEast Asia, Central Asia, other parts of India, Sri Lanka,Pakistan, Iran, the Middle East, Turkey, Egypt andMorocco. We
W
nd that the Muslim populations in gen-eral are genetically closer to their non-Muslim geo-graphical neighbors than to other Muslims in India, andthat there is a highly signi
W
cant correlation betweengenetics and geography (but not religion). Our
W
ndingsindicate that, despite the documented practice of mar-riage between Muslim men and Hindu women, Islami-zation in India did not involve large-scale replacementof Hindu Y chromosomes. The Muslim expansion inIndia was predominantly a cultural change and was notaccompanied by signi
W
cant gene
X
ow, as seen in otherplaces, such as China and Central Asia.
Introduction
Islam is India’s largest minority religion, with Muslimso
Y
cially comprising
»
13 % of the population, or138million people (Census 2001). The history of Islamin India began in the year 711 AD, when it was intro-duced into Sind by the Arabs (Titus2005). Soon after,however, Sind was abandoned and for the next two anda half centuries there was little Muslim presence inIndia. Then, in 1001, the Turks entered India fromAfghanistan and started spreading Islam from west toeast (Titus2005). By the beginning of the fourteenthcentury the Deccan in south India had been invaded,and soon after that the Muslim empire and in
X
uenceattained its greatest extent and importance in the
Electronic supplementary material
Supplementary material isavailable in the online version of this article athttp://www.dx.doi.org/10.1007/s00439-006-0234-xand is accessible for authorizedusers.Ramana Gutala and Denise R. Carvalho-Silva contributedequally to the article.R. GutalaDepartment of Medicine, University of Texas Health ScienceCenter, San Antonio, TX, USAD. R. Carvalho-Silva · B. Yngvadottir · C. Tyler-Smith (
&
)The Wellcome Trust Sanger Institute,Wellcome Trust Genome Campus, Hinxton, CB10 1SA, UKe-mail: cts@sanger.ac.ukL. Jin · R. ChakrabortyCenter for Genome information, University of Cincinnati,Cincinnati, OH, USAV. Avadhanula · K. NanneDeccan College of Medical Sciences, Hyderabad, IndiaL. SinghCenter for Cellular and Molecular Biology, Hyderabad, India
 
544Hum Genet (2006) 120:543551
 123
history of India, remaining dominant up to 1707 AD(Titus2005).The Muslim conquest of India was undertaken withthe purpose of establishing a Muslim government overthe people and implementing the Muslim faith. Thiswas accomplished by foreign conquerors, traders, reli-gious devotees and preachers using a wide range of methods, including war, enslavement and conversion(voluntary or compulsory), and through marriagebetween Muslims and Hindus (Lal1993; Titus2005). Such mixed marriages appear to have been part of thepolicy of absorption and domination by which it washoped Hinduism would be overthrown (Titus2005).For that reason, the practice became well establishedand the resulting progeny contributed extensively tothe increase in the Muslim populations in India (Lal1993; Titus2005). The biological contribution to India accompanyingthese historical events has not been thoroughly investi-gated and the extensive studies of Indian genetic pre-history (reviewed by McElreavey and Quintana-Murci2005) have focused on the origin of caste and tribalpopulations, the birthplace of the Dravidian languages,and the contribution of genes from the Indo-Europeanspeakers during their movement out of Central Asia(e.g., Sahoo etal.2006; Sengupta etal.2006). The few studies examining the origins of Muslims in India haveprovided con
X
icting results. Classical marker studies,for example, have shown that Muslims and Hindus innorth and northwestern India are di
erent from eachother (Aarzoo and Afzal2005; Balgir2003; Balgir and Sharma1988), whereas a study of the Y chromosomerevealed close a
Y
nity between Muslims and Indo-European upper-caste groups (Basu etal.2003). Sincethe expansion of Islam in other places, such as Chinaand Central Asian countries, involved the movementof people and Y chromosomes (Wang etal.2003; Zerjaletal.2002) and left a detectable genetic signature inthe current populations, a similar genetic impact fromthe Middle East on the Hindu gene pool seems plausi-ble, but needs further investigation.We therefore set out to clarify this aspect of the his-tory of India by studying 24 Y-chromosomal markersin 246 Muslims from south India, and comparing ourresults to published data on 4,204 Muslim and non-Muslim males from several other countries. By investi-gating a large set of Indian Muslims and performing acomprehensive analysis of the data, we show that inIndia the spread of Islam did not have a detectablegenetic impact on the local populations and thusdi
ered from its expansion in neighboring countries. InIndia, the spread of Islam was predominantly a culturalevent.
Subjects and methods
DNA samples and Y-chromosomal polymorphismsThe sample consisted of 246 unrelated males from
W
vedi
erent populations from Andhra Pradesh, SouthIndia: Yamani, Pathans and Bohra Muslim groups, andtwo other Sunni and Shia groups here referred to as“Sunni” and “Shia”, respectively. Blood samples werecollected with informed consent and DNA wasextracted following standard procedures. Eight micro-satellite loci (
DYS19
,
DYS388
,
DYS389I 
,
DYS389II,DYS390
,
DYS391
,
DYS392
and
DYS393
) and 16 biall-elic markers (YAP, M9, M89, M52, M45, M173, M172,M17, M11, M15, M40, M70, M147, M95, M103 andM88) were typed as previously described (Ramanaetal.2001) and used to assign haplotypes and Y haplo-groups, respectively. In addition, relevant Y-chromo-somal data from literature sources were collated andanalyzed. In compiling these data, we were unable toreconcile all
DYS389
repeat counts from di
erentsources satisfactorily, and so excluded this locus fromour analyses. Data from 4,204 males (non-Muslims andMuslims) from other parts of India, East Asia, CentralAsia, Sri Lanka, Pakistan, Iran, the Middle East,Turkey, Egypt, and Morocco were included (Fig.1,Table1).Data analysesBoth haplotype and haplogroup frequencies weredetermined, and combined with their molecular infor-mation to compute genetic distances between all thepopulations depicted in Fig.1. Pairwise distances basedon microsatellite markers (
R
st
) and on biallelic marker(
 
) were obtained with Arlequin 2.0 (Schneider etal.2000). Distance matrices separating each pair of popu-lations were then used to perform multidimensionalscaling (MDS) analysis with the SPSS 13.0 softwarepackage. Negative genetic distances were assigned avalue of zero; when we alternatively increased all dis-tances to eliminate the negative values, or used addi-tional software tools (Statistica 6), the results werevery similar (not shown). For the Indian samples only,we combined the populations into classes and com-puted average
R
st
values (1) among Muslims, (2)among non-Muslims, and (3) between Muslims andnon-Muslims using a jackknife approach within eachgroup. Mantel tests to assess the signi
W
cance of correla-tions between genetics and religion, or geography werecarried out in populations from India by use of Arle-quin. Analysis of molecular variance (AMOVA) wasalso performed with Arlequin using microsatellite and
 
Hum Genet (2006) 120:543551545
 123
biallelic data in Indian populations, which were eithergrouped according to religion (Muslims and non-Mus-lims) or geographical regions, or not grouped at all.The possibility of gene
X
ow among the di
erent Mus-lim isolates, and among Muslims and Hindus in southIndia, was investigated by estimating the proportion of lineage sharing and the rho genetic distance (Helgasonetal.2000).
Results and discussion
We typed eight Y-chromosomal microsatellites and16binary markers in 246 Muslim men from AndhraPradesh (south India), and de
W
ned 124 di
erent haplo-types, or
W
ve haplogroups and four paragroups, respec-tively (Supplementary Table1). We then comparedour data (excluding
DYS389
) to published data from4,204 males (Muslims and non-Muslims) from otherparts of India, East Asia, Central Asia, Sri Lanka,Pakistan, Iran, the Middle East, Turkey, Egypt, andMorocco (Table1, Fig.1). For this worldwide comparison,
R
st
and
 
 
st
geneticdistances were calculated between all the populationsand their pairwise values were used to perform anMDS analysis. The resulting plots (Fig.2) showed con-siderable structure. Although a continuum of variationis seen, rather than discrete groups, populations from aparticular region or country tend to cluster together;this is in agreement with the expectation that humangenetic structure is predominantly geographical andclinal. Thus, for example, most Chinese populationsare seen in the left-hand part of each plot rather thandispersed throughout the plot. Interestingly, however,the three Chinese Muslim populations do not lie in thiscluster, but are located more towards the center of each plot, close to populations with geographical ori-gins lying further west. It has previously been reportedthat the conversion to Islam in China involved themovement of people, and, in particular, the in
X
ux of genes from the Middle East into China (Wang etal.2003) and Fig.2thus con
W
rms that our analysis readilydetects such events. The Indian populations show con-siderable diversity, and northern and southern popula-tions barely overlap (with the exception of Dravidiansand Chenchu) and tend to lie in two distinct clusters(Fig.2). Most importantly, the Muslim and non-Mus-lim populations are intermingled in these clusters: theY-chromosomal heritage in India is in
X
uenced more bygeographical location than by the religious practices. Itappears that the Muslim genetic contribution in Indiawas less important than in other places such as China.In order to assess the signi
W
cance of this observa-tion, we next combined the populations from India intotwo classes, Muslims and non-Muslims, and calculatedpairwise genetic distances (1) among Muslims, (2)among non-Muslims, and (3) between Muslims andnon-Muslims, and compared their average values afterfollowing a jackknife approach within each group. Thecomparison between Muslims and non-Muslims inIndia showed the lowest distance (Fig.3). We thenrestricted the comparisons to Muslim and non-Muslimpopulations who live in neighboring regions of southIndia (again under a jackknife approach). We foundthat this comparison resulted in the lowest averagevalue of genetic distances (Fig.3), which suggests thatthe close geographic proximity of Muslims and non-Muslims in south India might have facilitated gene
X
ow
Fig.1
Geographical locations of the populations analyzed. Sym-bol shapes indicate religion (
 squares
for Muslims and
circles
fornon-Muslims). The colors represent locations: Morocco (
light blue
), Egypt (
orange
), Israel (
black
), Iran, Iraq and Oman (
 yel-low
), Turkey, Azerbaijan, Georgia and Armenia (
red
), Kyrgyz-stan, Kazakhstan, Uzbekistan and Turkmenistan (
white
), China,Korea, Mongolia and Japan (
brown
), Pakistan (
dark green
),North India (
light green
), South India (
dark blue
), Sri Lanka(
 pink
)

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