In search of the genetic footprints of Sumerians: A survey of Y-chromosome and mtDNA variation in the Marsh Arabs of Iraq

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Abstract
For millennia, the southern part of the Mesopotamia has been a wetland region generated by the Tigris and Euphrates rivers before flowing into the Gulf. This area has been occupied by human communities since ancient times and the present-day inhabitants, the Marsh Arabs, are considered the population with the strongest link to ancient Sumerians. Popular tradition, however, considers the Marsh Arabs as a foreign group, of unknown origin, which arrived in the marshlands when the rearing of water buffalo was introduced to the region. To shed some light on the paternal and maternal origin of this population, Y chromosome and mitochondrial DNA (mtDNA) variation was surveyed in 143 Marsh Arabs and in a large sample of Iraqi controls. Analyses of the haplogroups and sub-haplogroups observed in the Marsh Arabs revealed a prevalent autochthonous Middle Eastern component for both male and female gene pools, with weak South-West Asian and African contributions, more evident in mtDNA. A higher male than female homogeneity is characteristic of the Marsh Arab gene pool, likely due to a strong male genetic drift determined by socio-cultural factors (patrilocality, polygamy, unequal male and female migration rates). Evidence of genetic stratification ascribable to the Sumerian development was provided by the Y-chromosome data where the J1-Page08 branch reveals a local expansion, almost contemporary with the Sumerian City State period that characterized Southern Mesopotamia. On the other hand, a more ancient background shared with Northern Mesopotamia is revealed by the less represented Y-chromosome lineage J1-M267*. Overall our results indicate that the introduction of water buffalo breeding and rice farming, most likely from the Indian sub-continent, only marginally affected the gene pool of autochthonous people of the region. Furthermore, a prevalent Middle Eastern ancestry of the modern population of the marshes of southern Iraq implies that if the Marsh Arabs are descendants of the ancient Sumerians, also the Sumerians were most likely autochthonous and not of Indian or South Asian ancestry.
In search of the genetic footprints of Sumerians:
a survey of Y-chromosome and mtDNA variation
in the Marsh Arabs of Iraq
Al-Zahery et al.
Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
http://www.biomedcentral.com/1471-2148/11/288 (4 October 2011)
RESEARCH ARTIC LE Open Access
In search of the genetic footprints of Sumerians:
a survey of Y-chromosome and mtDNA variation
in the Marsh Arabs of Iraq
Nadia Al-Zahery
1
, Maria Pala
1
, Vincenza Battaglia
1
, Viola Grugni
1
, Mohammed A Hamod
2,3
,
Baharak Hooshiar Kashani
1
, Anna Olivieri
1
, Antonio Torroni
1
, Augusta S Santachiara-Benerecetti
1
and
Ornella Semino
1,4*
Abstract
Background: For millennia, the southern part of the Mesopotamia has been a wetland region generated by the
Tigris and Euphrates rivers before flowing into the Gulf. This area has been occupied by human communities since
ancient times and the present-day inhabitants, the Marsh Arabs, are considered the population with the strongest
link to ancient Sumerians. Popular tradition, however, considers the Marsh Arabs as a foreign group, of unknown
origin, which arrived in the marshlands when the rearin g of water buffalo was introduced to the region.
Results: To shed some light on the paternal and maternal origin of this population, Y chromosome and
mitochondrial DNA (mtDNA) variation was surveyed in 143 Marsh Arab s and in a large sample of Iraqi controls.
Analyses of the haplogroups and sub-haplogroups observed in the Marsh Arabs revealed a prevalent
autochthonous Middle Eastern component for both male and female gene pools, with weak South-West Asian and
African contributions, more evident in mtDNA. A higher male than female homogeneity is characteristic of the
Marsh Arab gene pool, likely due to a strong male gene tic drift determined by socio-cultural factors (patrilocality,
polygamy, unequal male and female migration rates).
Conclusions: Evidence of genetic stratification ascribable to the Sumerian development was provided by the Y-
chromosome data where the J1-Page08 branch reveals a local expansion, almost contemporary with the Sumerian
City State period that characterized Southern Mesopotamia. On the other hand, a more ancient background shared
with Northern Mesopotamia is revealed by the less represented Y-chromosome lineage J1-M267*. Overall our
results indicate that the introduction of water buffalo breeding and rice farming, most likely from the Indian sub-
continent, only marginally affected the gene pool of autochthonous people of the region. Furthermore, a prevalent
Middle Eastern ancestry of the modern population of the marshes of southern Iraq implies that if the Marsh Arabs
are descendants of the ancient Sumerians, also the Sumerians were most likely auto chthonous and not of Indian
or South Asian ancestry.
Background
The Near East is well known for its importan t role in
human history, particularly as a theatre for great histori-
cal events that changed the face of the world during the
Neolithic period. The temperate climate and fertile soil
brought by t he continuous flooding of t he Tigris and
Euphrates rivers, made the Mesopotamian region ideal
for early revolutions in agriculture and farming. In parti-
cular, the southern part of Mesopotamia (the delta
between the two rivers in the present day southern Iraq)
has been historically known as the Garden of Eden (bib-
lical name) or Sumer Land, the land of Abraham.
The Mesopotamian civilization originated around the
4
th
millennium BC in the low course of the Tigris and
Euphrates rivers. This alluvial territory, which emerged
progressively by soil sedimentation, attracted different
populations from the northern and easte rn mountains
but, whereas traces of their culture are present in the
* Correspondence: ornella.semino@unipv.it
1
Dipartimento di Genetica e Microbiologia, Università di Pavia, Via Ferrata 1,
27100 Pavia, Italy
Full list of author information is available at the end of the article
Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
http://www.biomedcentral.com/1471-2148/11/288
© 2011 Al-Zahery et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
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reproduction in any medium, provided the original work is pro perly cited.
territory, as d ocumented by the Ubaid-Eridu pott ery,
nothing is available for their identification. Only two
groups of populations arrived later and in larger number
leaved historical records: Sumerian and Semitic groups.
The Sumerians, who spoke an isolated language not cor-
related to any linguistic family, are the most ancient
group living in t he region for which we have his torical
evidence. They occupied the delta between the two riv-
ers i n the southern part of the present Iraq, one of the
oldest inhabite d wetland environ ments. The Semitic
groups were semi-nomadic people who spoke a Semitic
language and lived in the northern area of the Syro-Ara-
bian dese rt breeding small animals. From here, they
reached Mesopotamia where they settled among t he
pre-existing populations. The Semitic people, more
numerous in the nort h, and the Sumerians, more repre-
sented in the south, after having adsorbed the pre-exist-
ing populations, melted their cultures laying the basis of
the western civilization [1].
Mesopotamia Marshes
The Mesopotamian marshes are among the oldest and,
until twenty years ago, the largest wetland environments
in Southwest Asia, including three main areas (Figure
1): the northern Al-Hawizah, the southern Al-Hammar
and the so-called Central Marshes a ll rich in both nat-
ural resources and biodiversity [2,3]. However, during
the last decades of the past cent ury, a systematic plan of
water diversion and draining drastically reduced the
extension of the Iraqi marshes, and by the year 2000
only the northern portion of Al-Hawizah (about 10% of
its original extension ) remained as fun ctioning marsh-
land whereas the Central and Al-Hammar marshes were
completely d estroyed. This ecological catastrophe con-
strained Marsh Arabs of the drained zones to leave their
niche: some of them moved to the dry land next to the
marshes and others went in dia spora. However, due to
the attachment to their lifestyle, Marsh Arabs have been
returned to their land as soon as the restoration of
marshes began (2003) [4].
The ancient inhabitants of the marsh areas were
Sumerians, who were the first to develop an urban civili-
zation some 5,000 years ago. Although footprints of
their great civilization are still evident in prominent
archaeological sites lying on the edges of the marshes,
such as the ancient Sumerian cities of Lagash, Ur, Uruk,
Eridu and Larsa, the origin of Sumerians is still a matter
of debate [5]. With r espect to this question, two main
scenarios have been proposed: accordi ng to the first, the
original Sumerians were a group of populations who
had migrated from the Southeast (I ndia region) and
took the seashore route through Arabian Gulf before
settling down in the southern mar shes of Iraq [6]. The
second hypothesis posits that the advancement of the
Sumerian civilization was the result of human migra-
tions from the mountainous area of Northeastern Meso-
potamia to the southern marshes of Iraq [7], with
ensuing assimilation of the previous populations.
Over time, the many historical and archaeological
expeditions tha t have b een conducted in the mar shes
have consistently reported numerous parallelisms
between the modern and ancient life styles of the marsh
people [8,9]. Details such as home arch itecture (particu-
lar arched reed buildings), food gathering (grazing water
buffalos, trapping birds and spearing fish, rice cultiva-
tion), and means of transportation (slender bitumen-
covered wooden boats, called Tarada) are documented
as still being practiced by the indigenous population
locally named Madan or Marsh Arabs [10,11]. This
village life-style, which has remained unchanged for
seven millennia, suggests a p ossible link between the
present-day marsh inhabitants and ancient Sumerians.
However, popular tradition considers the Marsh Arabs
as a foreign group, of unknown origin, which arrived in
the marshlands when the rearing of w ater buffalo was
introduced to the region.
In order to shed some light on the origin of the
ancient and mode rn Mesopotamian marsh populations,
which remains ambiguous in spite of all the above men-
tioned theories, the genetic variation of a s ample of
Marsh Arabs has been investigated both for the mater-
nally transmitted mitochondrial DNA (mtDNA) and the
Male Specific region of the Y chromosome (MSY).
Permanent marsh
Flooded area
Area of substantial drying
I R A Q
Iran
Kuwait
Kumayt
Amarah
QaltSalih
Ash Shatrah
Samawah
Nasiriyah
Al Hammar
Marshes
Central
Marshes
Al Hawizah
Marshes
Kut
Euphrates
Tigris
Basrah
Qurnah
0 20 40
Km
Permanent marsh
Flooded area
Area of substantial drying
Permanent marsh
Flooded area
Area of substantial drying
I R A Q
Iran
Kuwait
Kumayt
Amarah
QaltSalih
Ash Shatrah
Samawah
Nasiriyah
Al Hammar
Marshes
Central
Marshes
Al Hawizah
Marshes
Kut
Euphrates
Tigris
Basrah
Qurnah
0 20 40
Km
0 20 40
Km
Figure 1 Map of Iraq illustrating present and former Marsh
areas. The majority of the subjects analysed in this study are from
the Al-Hawizah Marshes, the only natural remaining marsh area in
southern Iraq [4].
Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
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Page 2 of 15
Methods
The sample
The sample consists of 143 healthy unrelated males,
mainly from the Al-Hawizah Marshes (the only not
drained South Iraqi marsh a rea[4] (Figure 1). For each
subject the Marsh Arab ancestry (at least for last four
generations) was ascertained by interview after having
obtain ed the informed cons ent. The collection (5-10 ml
of blood each, in EDTA) was carried out in different vil-
lages during a field expedition. DNA was extracted from
whole blood by using a standard phenol/chloroform
protocol. For comparison, a sample of 154 Iraqi subjects
representative of the general Iraqi population and there-
fore referred throughou t the text as Iraqi was investi-
gated for both mtDNA and Y-chromosome mar kers.
This sample, previously analysed at low resolution [12]
is mainly composed of Arabs, living along the Tigris and
Euphrates Rivers. In addition, the distribution of the Y-
chromosome haplogroup (Hg) J1 sub-clades was a lso
investigated in four samples from Kuwait (N = 53),
Palestine ( N = 15), Israeli Druze (N = 37) and Khuze-
stan (South West Iran, N = 47) as well as in more than
3,700 subjects from 39 populations, mainly from Europe
and the Mediterran ean area but also from A frica and
Asia [13,14].
This research was approved by the Ethics Committee
for Clinical Experimentation at the University of Pavia
(Board minutes of October 5, 2010).
Y-chromosome genotyping
Y-chromosome haplogroup affiliation was determined
according to the most recently updated phylogeny
[15,16] by genotyping, in hierarchical order, 46 single
nucleotide pol ymorphisms (SNPs) (see the phylogeny in
Figure2oftheResultsection).Thenomenclaturewas
according to the Y chromosome Consortium rules
[17-19].
Mutations were detec ted either as RFLPs or by
DHPLC of pertinent fragments amplified by PCR [Addi-
tional file 1]. When n ecessary, results were verified by
sequencing.
J1-M267 Y chromosomes were analysed for a pa nel of
eight Y-chromosome microsatellite loci (DYS19,
YCAIIa/b, DYS389I/II, DYS390, DYS391 and DYS392)
by using multiplex reactions according to the STR DNA
Internet Data Base [20] and fragment analysis by capil-
lary electrophoresis on ABI PRISM
®
3100 Genetic
Analyzer.
MtDNA genotyping
Affiliation within mtDNA haplogroups was first
inferred through the sequencing of a fragment of 746-
846 base pairs (bps) from the control region that,
according to the rCRS [ 21], encom passes the entire
hypervariable segment I (HVS-I) and part of HVS-II
and then confirmed through a hierarchical survey by
PCR-RFLP/sequencing of coding region haplogroup
diagnostic markers. [Additional file 2]. The nomencla-
ture was according to van Oven and Kayser, built 12
(20 July 2011) [22].
M357
M168
M201
M170
M258
M89
M429
M304
*
*
*
V13
M78
M34
*
M2
M123
M267
*
PAGE08
M365
*
M172
M410
*
M47
M67
M92
M241
M68
M102
M12
M20
M76
M242
M25
M17
M269
SRY
10831.2
M207
M70
*
M9
M45
M74
M378
M412
*
YAP
M35
*
M173
M124
E
G
J
L
Q
R1
T
R2
J1
J2
P36
L23
H
(a)
I
R
PK3
Marsh Arabs Iraqis
N=143
N=154
1.3
2.1
0.7
5.2
2.6
1.4
4.5
2.1
nt
1.4
1.9
0.6
7.0
4.5
72.7
26.6
1.4
3.5
1.3
9.7
2.6
5.2
1.3
1.3
1.3
1.3
0.7
0.6
0.7
2.1
1.9
8.4
2.8
9.1
1.9
1.4
6.5
0.4613 0.8869
Figure 2 Phylogeny of Y-chromosome haplogroups and their
frequencies (%) in Marsh Arab and Iraqi populations.
Haplogroups are labelled according to the Y Chromosome
Consortium [17,18] and the International Society of Genetic
Genealogy [16]. Differently from previously reported [19], the M365
mutation was observed in two J1-Page08 Y-chromosomes (Marsh
Arabs). In these two subjects, M365 was observed in association
with the new mutation L267.2 discovered while typing the M365
marker. It consists of an A to G transition at nucleotide position 159.
The markers P37, M253, M223 of haplogroup I, M81 and M293 of
haplogroups E, and M367, M368 and M369 of haplogroup J1 were
typed but not observed. A star (*) indicates a paragroup: a group of
Y chromosomes not defined by any reported phylogenetic
downstream mutation. nt: not tested. (a) Heterogeneity.
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Sequence analys is of the control region was performed
by using primers F15973 (5 - AACTCCACCAT TAG-
CACCCA-3 )andR263(5-TGGCTGTGCAGACATT-
CAAT-3) on amplicons obtained by using the p rimers
F15877 (5 -CAAATGGGCCT GTCCTTGTA-3 )and
R468 (5-GGAGTGGGAGGGGAAAATAA-3)[23].All
the samples were sequenced starting from primer
F15973. Samples showing potential heteroplasmies or
ambiguities were also sequenced with primer R263.
Statistical analysis
Haplogroup diversity (H) was computed by using the
standard method of Nei [24]. Principal component (PC)
analysis was performed on haplogroup fre quencies using
Excel software implemented by XLstat. The relative
amount of accumulated diversity, as a function of geo-
graphy, was evaluated through the mean microsatellite
variance estimated on at least five individuals. Hap-
logroup frequenc y and variance maps were generated by
using Surfer software [25], following the Kriging proce-
dure. Median-Joining (MJ) networks [26] were con-
structed by the Network 4.5.0.0 program [27]. MtDNA
and Y -chromosome netwo rks were obtained by the MJ
method, with ε = 0 and weighting markers accordi ng to
their relative stability (Y-chromosome: microsatellite loci
were weighted proportionally to the inverse of the
repeat variance of each haplogroup. MtDNA: coding
region was weighted as four; control region as one - see
Additional file 2) and after having processed the data
with the reduced-median method. The age of microsa-
tellite variation within haplogroups was evaluated
according to Zhivotovsky et al. [28] and Sengupta et al.
[29] and through the BATWING procedure (Bayesian
Analysis of Trees With Internal Node Generation) [30].
Batwing runs used a model assuming an initial constant
population size followed by expansion at time b with a
growth ra te of a. Alfa and beta parameter s were as in
Tofanelli et al. [31]. F or both methods the effective
mutation rate and a generation time of 25 years [ 28]
were used.
Results
Y-chromosome variation
The screening of 45 SNPs, plus one identified in this
survey, in Marsh Arabs and Iraqis identified 28 hap-
logroups, 14 in the marsh sample and 22 in the control
Iraqis. Only eight haplogroups were shared by both
groups. Their phylogenetic relationships and frequencies
are shown in Figure 2. More than 90% of both Y-chro-
mosome gene pools can be traced back to Western Eur-
asian components: the Middle Eastern Hg J-M304, the
Near Eastern Hgs G-M201, E-M78 and E-M123, while
the Eurasian Hgs I-M170 and R-M207 are scarce and
less common in the Marsh Arabs than in t he control
sample. Contributions from eastern Asia, India and
Pakistan, represented by Hgs L-M76, Q-M378 and R2-
M124, are detected in the Marsh Arabs, but at a very
low frequency.
Haplogroup J accounts for 55.1% of the Iraqi sample
reaching 84.6% in the Marsh Arabs, one of the highest
frequencies r eported so far. U nlike the Iraqi s ample,
which displays a roughly equal proportion of J1-M267
(56.4%) and J2-M172 (43.6%), almost all Marsh Arab J
chromosomes (96%) belongs to the J1-M267 clade and,
in particular, to sub- Hg J1-Page08. Haplogroup E,
which characterizes 6.3% of Marsh Arabs and 13.6% of
Iraqis, is represented by E-M123 in both groups, and E-
M78 mainly in the Iraqis. Haplogroup R1 is present at
a sign ificantl y lower frequency in the Marsh Arabs than
in the Iraqi sample (2.8% vs 19.4%; P < 0.001), and is
present only as R1-L23. Conversely the Iraqis are dis-
tributed in all the three R1 sub-groups (R1-L23, R1-
M17 and R1 -M412) foun d in this survey at frequencies
of 9.1%, 8.4% and 1.9%, respectively. Other haplogroups
encountered at low fr equencies among the Mar sh Arabs
are Q (2.8%), G (1.4%), L (0.7%) and R2 (1.4%).
MtDNA variation
A total of 233 haplotypes [Additional file 2] and 77 sub-
haplogroups (Table 1) have been identified in this sur-
vey. Only 26 of the observed sub-haplogroups are
shared between the two populations, and most of the
remaining are represented by singletons. According to
their known or supposed geographic/ethnic origin
[32-34], in addition to a strong West Eurasian compo-
nent (77.8% and 84.1% in the Marsh Arabs and Iraqis,
respectively), it is possible to recognize contributions
from North/East and Sub-Sahar an Africa and from East
and South Asia.
West Eurasian mtDNA s obs erved in this study are
approximately equally distributed into macro-Hgs R0,
KU,andJT, although with haplogroup and sub-hap-
logroup differences between the two Iraqi samples. I n
the Marsh Arabs Hg J prevails (15.2%) followed by Hgs
H (12.4%), U (9.7%) and T (7.6%). Conversely, in the
control group, the most frequen t is Hg H (17.0%) fol-
lowed by Hgs U (14.8%), T (12.6%) and J (11.9%). Both
the less represented N1 and W haplogroups show
higher frequencies (marginally significant) in Marsh
Arabs. The most frequent macro-Hg R0 includes mole-
cules R0a ((preHV)I), more represented a mong the
Marsh Arabs (6.9% vs 4.0%) , HV,observedmainlyas
HV*, but especially H mtDNAs. Although the majority
of the H mtDNAs (7.6% in Marsh Arabs vs 10.8% in Ira-
qis) d id not fall into any of the tested sub-haplogroups,
a limited number of H s ubsets (H1, H5, H6, and H14)
have been observed. In particular, while H5 (3.4% vs
2.8%), H1 (0.7% vs 1.7%) and H14 (0.7% vs 1.1%) were
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Table 1 MtDNA haplogroup frequencies (%) observed in the Marsh Arabs in comparison to Iraqis.
Haplogroups
a
Marsh
Arabs
(N = 145)
Iraqis
b
(N = 176)
Haplogroups
a
Marsh
Arabs
(N = 145)
Iraqis
b
(N = 176)
West Eurasia 77.8% 84.1% West Eurasia (cont.)
R0 24.1% 33.5% N 15.1% 6.8%
R0 0.7 - I 0.7% 1.7%
R0a 6.9 4.0 I 0.7 0.6
I1 - 1.1
HV 4.1% 12.5%
HV* 3.4 9.1 N1 8.2% 2.3%
HV0a 0.7 - N1b1 4.8 2.3
HV1 - 3.4 N1c 3.4 -
H 12.4% 17.0% W 4.8% 1.1%
H* 7.6 10.8 W 2.7 1.1
H1 0.7 1.7 W4 0.7 -
H5 3.4 2.8 W6 1.4 -
H6b - 0.6 X 1.4% 1.7%
H14a 0.7 1.1 X2 1.4 1.7
KU 15.9% 19.4%
North/East Africa 2.8% 1.8%
K 6.2% 4.6%
K1 4.1 3.4 M1a 1.4 0.6
K1a8 2.1 0.6 M1a1 - 0.6
K2 - 0.6 M1b2 1.4 -
U 9.7% 14.8% U6a - 0.6
U - 1.1
U1ac - 2.3
Sub-Saharan Africa 4.9% 9.1%
U1b - 0.6
U2e - 0.6 L0a14 0.7 -
U3 5.5 2.8 L0a2 - 1.1
U3a - 0.6 L1b 1.4 -
U3b1a1 - 0.6 L1c2 - 0.6
U4 2.1 4.0 L1c3a - 0.6
U5a1 1.4 1.1 L2a12 0.7 -
U5b3 0.7 - L2a1 0.7 2.8
U9 - 1.1 L3* 0.7 -
L3b - 0.6
JT 22.7% 24.5% L3e5 - 1.1
J 15.2% 11.9% L3f 0.7 -
J1* 0.7 - L3f1b - 2.3
J1b 5.5 5.7
J1b1b - 0.6
East Asia 1.4% 1.1%
J1c 2.1 1.1
J1d 0.7 1.1 B4 - 1.1
J1d1 - 1.1 B4c2 1.4 -
J1d2 - 0.6
J2a 4.1 1.7
Southwest Asia 10.4%** 4.0%
J2b 2.1 -
M* 0.7 -
T 7.6% 12.6% M33a2a 0.7 -
T1a 3.4 2.3 M37e 1.4 -
T1a1 - 0.6 R2 2.8 -
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found in both groups, H6 was observed only in one sub-
ject of the control group.
Almost all the main U sub-haplogroups and the
nested K b ranch were found in the Iraqi sample, but
only a sub-set of them (K1, U3, U4, U5, in addition to
the South West Asian U7) were observed in the Marsh
Arabs. The nested Hg K, mainly K1, was observed at a
comparable frequency in both groups (6.2% in the
marshes vs 4.6%). The situation of macro-Hg JT is more
complex. Significant differences (P < 0.05) emerged in
the distribution of J1 and J2 sub-clades, with the latter
much more frequent in the marshes (6.2% vs 1.7%). By
contrast, Hg T displayed a lower frequency in the
marshes (7.6% vs 12.6%) due to a significant lower inci-
dence of its T2 sub-c lade (2.1% vs 6.9%, P < 0.05). On
the other hand, Hgs N1 (8.2%) and W (4.8%), were both
present in the marshes at a three-fold higher frequency
than in Iraqis. Haplogr oup X was detected as X2 with a
frequency lower than 2% in both population samples.
African haplogroups are of North/East and sub-
Saharan African origin and represent minor components
in both groups. The North/East African contribution is
mainly represented by Hg M1 which accounts for 2.8%
of Marsh Arabs and 1.2% of the Iraqi sample, the latter
displayi ng also 0.6% of Hg U6. The sub-Saharan African
component comprised Hgs L0, L1, L2 and L3 and
accounted for 4.9% in the marshes and 9.1% of the con-
trol sample. Out of t he twelve African sub-haplogroups
identified in this survey, six in the marshes and seven in
the control sample, only one (L2a1) was shared between
the two Iraqi groups.
The Asian contribution was significantly higher (P <
0.01) in the Marsh Arabs than in the control sample
(11.8% vs 5.2%). It includes mtDNAs belonging t o the
Southern As ian Hgs M (M*, M33, M37e) and R2 in
Marsh A rabs, and R5a and U2d in the contro l sample.
Haplogroup U7,frequentinSouthwestAsia,was
observed in both groups. The East Asian haplogroup B4
was detected at a very low frequency in both Iraqi
groups.
PC analyses
In order to visualize the relationship linking Marsh
Arabs with other Iraqis and surro unding ne ighbours
[Additional files 3 and 4], principal component analyses
of Y-chromosome and mtDNA ha plogroups were car-
ried out and the two PCs are illustrated in Figure 3.
For the Y-chromosome, the first two components,
although accounting for only a quarter of the total var-
iance, gather Marsh Arabs wi th almo st all Arab popula-
tions and separate them along the first PC from western
Eurasians, along the second PC from the African groups
and by both components from South Asian populations.
When the PCA was based on mtDNA ha plogroup fre-
quencies, Marsh Arabs occupied, toget her with Iraqi
and Saudi Arabian populations, a position in the middle
of the plot among three d istinct groupings: the first
included western Eurasian, the second embraced all the
South Asian groups while t he third represented the
North Africa and South Arabian Peninsula peoples.
For both systems, the longitudinal separation operated
by the first PC is mainly due to t he East-West decreas-
ing frequency of East Asian haplogroups (see for exam-
ple: Y-ch romosome Hgs R2-M124, C-RPS4Y and H-
M69; mtDNA Hgs A, F, D and G) and the increasing
frequencies of the African haplogroups (see for example:
Y-chromosome Hgs A-M13, B-M60, E-M35; mtDNA
Hgs L1, L2 and L3) while the latitudinal separation
operated by the second PC is m ainly ascribable to the
different dis tribution of haplogroups most frequent in
West Eurasian (Y-chromosome Hgs J-M172, M267 and
mtDNA Hgs H and U5), and the African-speci fic hap-
logroups (Y-chromosome Hgs A-M13, B-M60, E-M35
and mtDNA Hgs L0-3).
Network analyses
Y-STR diversity at eight informative loci [Additional
file 5] was used to evaluate t he internal v ariation and
phylogenetic relationships of J1-M267 Marsh Arab
samples in comparison with neighbouring populations.
Figure 4 illustrates the haplotype networks of
Table 1 MtDNA haplogroup frequencies (%) observed in the Marsh Arabs in comparison to Iraqis. (Continued)
T1b 2.1 2.8 R5a - 0.6
T2 - 2.3 U2d - 0.6
T2a1b - 1.1 U7 4.8 2.8
T2b 0.7 0.6
T2c - 2.3
Others 2.8% -
T2c1 0.7 - N* 0.7 -
T2e 0.7 0.6 R* 2.1 -
a
nomenclature according to van Oven and Kayser, bu ilt 12 (20 July 2011) [22].
b
included in the sample analysed by Al-Zahery et al. [12]; * indicates: groups of mtDNAs not belonging to any of the listed sub-haplogroups. For example,H*
contains all H mtDNAs not belonging to the sub-clades investigated in this survey (H1 , H5, H6, H14) ** value statically significant at p < 0.05.
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N-Eur
mtDNA
M13
M60
RPS4
Y
P2
M2
M35
M78
M81
M69
M47
M67
M12
M20
LLY22
g
M207
M173
M17
M70
Y Chromosome
Figure 3 Principal component analyses of Y-chromosome and mtDNA haplogroup frequencies. The PCA analyses were carried out on
haplogroups listed in Additional files 3 and 4. Haplogroups with frequencies lower than 5% in all the populations were not considered. On the
whole, 28% of the total variance is represented for the Y-chromosome (16% by the first PC and 12% by the second PC) and 39% for the mtDNA
(20% by the first PC and 19% by the second PC). Populations included are: IRM, Marsh Arabs; IRQ, Iraqi; Alb, Albania; Alg-A, Algeria-Arabs; Alg-B,
Algeria-Berbers; Aze, Azerbaijan; Ben, Benin; Bos, Bosnia; Bul, Bulgaria; Cau, Caucasus; Crt, Crete; Cro, Croatia; Cze, Czech Republic; Dru, Druze; Egy,
Egypt; Egy-A, Egypt-Arabs; S-Egy, South Egypt; N-Egy, North Egypt; Eth-A, Ethiopia-Amhara; Eto-O, Ethiopia-Oromo; Geo, Georgia; Gre, Greece;
Hun, Hungary; Ind, India; Ind-AA, India-Austro-Asiatics; Ind-D, India-Dravidians; Ind-IN, India-Indo-Europeans; Ind-TB, India-Tibeto-Burmans; N-Eur,
North Europe (Austria, Germany, Ireland, North Italy, Poland, Scotland); N-Irn, North Iran; S-Irn, South Iran; IRN, Iran; NeI, North East Italy; C-Ita,
Central Italy; S-Ita, South Italy; Sar, Sardinia; Jor, Jordan; Kur, Kurds; Leb-C, Lebanon-Christians; Leb-D, Lebanon-Druze; Leb-M, Lebanon-Muslims;
Mar, Morocco; Ber, Morocco-Berbers; Oma, Oman; Pak, Pakistan; Pak-D, Pakistan-Dravidians; Pak-B, Pakistan-Burushaski; Pak-IE, Pakistan-Indo-
Europeans; Pal, Palestinian; Pol, Poland; Qat, Qatar; Rwa-H, Rwanda-Hutu; Rwa-T, Rwanda-Tutsi; Sau, Saudi Arabia; Slv, Slovenia; Som, Somalia; Spa,
Spain; Sud-A, Sudan-Arabs; Sud-N, Sudan-Niloti; Taj, Tajikistan; Tun, Tunisia; Tur, Turkey; Tuk, Turkmenistan; Ukr, Ukraine; Uae, United Arab Emirates;
Yem, Yemen (Details in Additional files 3 and 4).
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paragroup J1-M267* and of the most frequent sub-
lineage J1-Page08. Wh ile the J1-M267* network shows
scarce structure, suggestive of a still heterogeneous
clade, the J1-Page08 network displays a star-like shape
centred around the most frequent haplotype of Marsh
Arabs, which is shared with the majority of the Middle
Eastern Arab groups. Signs of expansion were revealed
by both networks but, in particular by that of J1-
Page08 which, besides the central haplotype, includes
at least three one-step derivatives overrepresented by
Marsh Arab chromosom es. This expansio n event of
haplogroup J1-Page08 has a mino r impact on the Iraqi
control sample and the other Middle Eastern Arab
populations.
J1-Page08
J1-M267*
Negev Bedouins
Iraqis
Marsh Arabs
Syrians
Omanis
Kurds
Palestinians
Europeans
Algerians
Emiratis
Kuwaitis
Qataris
Jordanians
Iranians
Ethiopians
Jews
Assyrians
Turks
Lebanese
Tunisians
Georgians
Figure 4 Networks of the STR haplotypes associated w ith haplogroups J1-M267* and J1-P age08, respectively. The eight STR (YCAIIa,
YCAIIb, DYS19, DYS389I, DYS389II, DYS390, DYS391 and DYS392) haplotypes observed in 54 and 377 samples, respectively, are listed in
Additional file 5. Circles and coloured sectors are proportional to the number of subjects, with the smallest circle and sector equal to 1.
Connecting lines are proportional to the number of mutations.
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Figure 5 illustrates the network of the control-region
mtDNA haplotypes associated with each haplogroup
found in this survey [Additional file 2]. The majority of
haplogroups were present in both population samples
although with scarce sub-haplogroup and haplotype
overlapping. In addition, different ly from the control
sample, a number of Marsh Arab haplotypes were
shared between two or more subjects.
Discussion
Two hypotheses have been proposed for the origin of
Marsh Arabs: (i) they could be a boriginal inhabitants of
Mesopotamia, correlated to the old Sumerians; (ii) t hey
could be foreign people of unknown origin. Although
the origin of Sumerians has yet to be clarified [5], the
two main scenarios, autochthonous vs foreign ancestry,
mayhaveproduceddifferentgeneticoutcomeswith
Marsh A rabs being genetically closer to Middle Eastern
groups or other populations, for instance those of the
Indi an sub-continent. Thus, i n order to shed some light
on this quest ion Marsh A rab population was investi-
gated for mtDNA and Y c hromosome markers. Due to
their characteristics (uniparental transmission and
absence of recombina tion) and thei r wide datasets, they
are, at present, among the best genetic systems for
detecting signs of ancient migration events and to evalu-
ate socio-cultural behaviours [35,36].
Evidence of a Middle Eastern origin of the Marsh Iraqi
Arabs comes mainly from the Y chromosome
Although different Western European mtDNA hap-
logroups were present in the Middle East in Palaeolithic
times, they cannot always be interprete d as markers of
Middle Eastern origin. For example, even if the mtDNA
haplogroup H evolved in the Middle East ~18,000-
15,000 years ago [34], different H sub-groups observed
I
UK
Marsh Arabs
Iraqis
Figure 5 Network of 233 mtDNA control-region haplotypes observed among 319 Iraqi samples. These haplotypes [Additional file 2] refer
to the variation observed between np 16024 and np 200. Circles are proportional to the number of subjects, with the smallest circle equal to 1.
Connecting lines are proportional to the number of mutations including haplogroup diagnostic markers. Haplogroups and sub-haplogroups are
labelled according to Table 1.
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in this region, albeit at a rather low frequency, such as
H1, arose outside and are most likely the result of gene
flow from Europe [34,37].
Y-chromosome variation, like that of mtDNA, is
highly geographically structured [34,38,39]. However,
Middle Eastern haplogroup J, which accounts for the
great majority of paternal lineages of this region and
marks different migration events toward Europe, Africa
and Asia, does not d isplay, at present, e vidence of back
migrations.
A common ancestral origin of Marsh Arabs and Southern
Arabian peoples
Haplogroup J, with its two branches J1-M267 and J2-
M172, is a Y-chromosome lineage dating to about 30,000
years ago. Its place of origin is still under discussion, but
it is considered a landmark geographically linked to the
Near Eastern region where the agricultural revolution
and animal domestication appeared for the first time
[34]. Accordingly, the frequency distribution of Hg J
[13,40] shows radial decreasing clines toward the Levant
area, Central Asia, the Caucasus, North Africa, and Eur-
ope from focal points of high frequency in the Near East
[12,40,41]. Although both clades (J1-M267 and J2-M172)
evolved in situ and participated in the Neolithic revolu-
tion, their different geographic distributions suggest two
distinct histories. While J 2-M172 has been linked to the
development and e xpansion of agriculture i n the wetter
northern zone an d is also considered the Y-chromosome
marker for the spread of farming into South East Eur ope,
J1-M267 has been associated with pastorali sm in the
semi-arid area of the Arabian Peninsula [42,43]. Despite
this purported initial association, no evidence of pastoral-
ism has been reported in the marsh area where one of
the J1-M267 highest values (81.1%) has been observed
(Additional file 6, Figure 6).
J1-M267
J1-Page08
J1-M267*
Figure 6 Fr equency (left panels) and variance (right panels) distributions of Y-chromosome haplogroups J1-M267, J1-M267* and J1-
Page08. Maps are based on 102 digit points [Additional file 6]. Variance data are relative to the microsatellite loci DYS19, DYS389I, DYS389II,
DYS390, DYS391 and DYS392 typed in all the reported samples. Frequency and variance details are reported in Additional files 6, 7 and 8.
Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
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Recent expansions shape the present Marsh Arab Y-
chromosome landscape
When the two J1-M267 sub-clades, J1-M267* and J1-
Page08 are considered (Figure 6), d ifferential frequency
trends emerge. The less represented J1-M267* pr imarily
diffuses towards North East Mesopotamia and shows its
highest incidence in the Assyrians of northern Iraq, and
Turkey. By contrast, J1-Page08 accounts for the great
majority of the J1 distribution in South Western Meso-
potamia, reaching its highest value (74.1%) in the mars h
area. By considering the STR haplotypes associated with
the two bran ches, the highest values of variance are
localized in northe rn Mesopota mia (North I raq/South
East Turkey) (Figure 6, Additional files 7, 8 and 9). For
the J1-Page08 lineage, high variance values were also
observed in Ethiopia, O man and South Eastern Italy
(Table 2). Although present data are not adequate to
define the homeland of the J1-Page08 sub-clade, some
useful information can be obtained from the haplotype
network analysis (Figure 4). Thus, the pheripheric posi-
tion of the Ethiopian and South Eastern Italian (Eur-
opean) haplotypes suggests that the high values of
variance registered in these regions likely reflect the
stratification of different migratory events, some of
which occurred before the expansion and diffusion of
thelineageoutsidetheMiddleEasternarea.Aspre-
viously reported [31,41], also the value of variance in
the Omani is affected by the concomitant presence of
both pheripheric and centrally expanded haplotypes. In
this context, the low variance (0.118) observed in th e
Marsh Arabs underlines a recent expansion involving
few haplotypes, all of which occupying a central position
in the J1-Page08 network (Figure 4). In the less frequent
J1-M267*clade,onlymarginallyaffectedbyeventsof
Table 2 Y-chromosome haplogroup J1-Page08 variance, divergence and expansion times based on six
(a)
STR loci.
Population N Mean YSTR Variance Divergence time ± SD kya Expansion time (95% CI) Reference
Mean Median
Turkish/Area 4 5 0.367 12.1 ± 4.0 [43]
Turkish/Areas 6,5 7 0.294 9.5 ± 6.5 [43]
Turkish/Area 1 7 0.357 13.8 ± 3.7 [43]
Turkish/Area 9 5 0.150 6.0 ± 2.2 [43]
Assyrian 7 0.262 10.4 ± 5.2 [43]
Iraqi/Kurd 7 0.325 13.8 ± 6.5 [43]
Iraqi 41 0.154 5.9 ± 2.0 8.4 (1.9-20.1) 6.6 (1.7-17.9) [Present study]
Iraqi/Marsh Arab 104 0.118 4.5 ± 2.6 4.8 (0.7-16.1) 3.5 (0.6-14.2) [Present study]
Iraqi/Nassiriya 14 0.153 5.6 ± 2.9 [43]
Iranian/S-West 18 0.157 5.5 ± 2.0 8.1 (1.3-22.3) 5.9 (1.1-19.3) [Present study]
Syrian 68 0.221 8.6 ± 2.9 9.8 (1.8-25.6) 7.3 (1.6-22.3) [43]
Jordanian 35 0.234 9.3 ± 2.8 11.4 (2.2-30.2) 8.4 (2.0-26.4) [43]
Palestinian 16 0.206 7.5 ± 3.7 [43]
Jewish 15 0.149 5.2 ± 2.6 [Present study]
Negev Bedouin 18 0.099 4.0 ± 1.9 [43]
Kuwaitian 16 0.221 11.0 ± 9.6 [Present study]
Qatarian 41 0.149 6.5 ± 2.2 6.6 (0.7-17.5) 5.1 (0.6-15.5) [43]
Emirati 57 0.186 7.7 ± 2.1 8.9 (1.4-23.4) 6.6 (1.3-20.7) [43]
Omanian 45 0.310 13.3 ± 4.4 [43]
Yemeni 42 0.205 8.8 ± 3.7 [43]
Egyptian 29 0.226 8.5 ± 2.6 [43]
Tunisian 19 0.158 5.9 ± 1.2 [Present study]
Algerian 6 0.189 6.0 ± 4.9 [Present study]
Ethiopian/Amhara 10 0.270 9.5 ± 2.7 [Present study]
Sudanese 26 0.091 3.5 ± 1.9 [31]
Italian 13 0.252 9.5 ± 3.6 [Present study]
Balkan/Central 7 0.171 8.1 ± 2.7 [14, Present study]
(a)
DYS19, DYS389I, DYS389II, DYS390, DYS391 and DYS392.
(b)
Divergence time according to [28,29].
(c)
Expansion time was estimated only in the populations involved in the J1-Page08 expansion as revealed by the network illustrated in figure 6, through the
BATWING procedure [30], assuming an initial constant population size followed by expansion at time b with a growth rate of a. Alfa and beta parameters are as
in [31].
For both methods the effective mutati on rate and a generation time of 25 years [28] were used.
Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
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expansion, Marsh Arabs shar ed haplotypes with other
Iraqi and Assyrian samples, supporting a common local
background (Figure 4).
Minor genetic influences in Marsh Arabs
Only a small proportion of the Marsh Arab gene pool
derives from gene flow from neighbouring regions. O n
the paternal side, our phylogeographic data highlight
some southwest Asian specific contributions as testified
to by Hgs Q, L and R2, known as South Asian Y-chro-
mosome lineages, primarily observed in India and P aki-
stan [29,44-47]. Different from the Iraqi co ntrol sample,
the Marsh Arab gene pool displays a very scarce input
from the northern Middle East (Hgs J2-M172 and deri-
vatives, G-M201 and E-M123), virtually lacks western
Eurasian (Hgs R1-M17, R1-M412 and R1-L23) and sub -
Saharan African (Hg E-M2) co ntributions. On the other
hand, the absence in b oth Iraqi groups of the North
African E-M81 branch [ 13,48-50], speaks a gainst sub-
stantial patrilineal gene flow from this region.
On the maternal s ide, a significant (East/Southwest)
Asian component (11.8%) is present among Marsh Arabs
as testified to by Hgs B4, M, R2 and U7. The B4 mtDNAs
carry cont rol-region motifs observed in Iran, Kirghizstan,
Western Siberia, Vietnam, Korea [51-53] attesting to
contact with Central and East Asia. This observation is
likely due to recent gene flow, although it is worth noting
that the ancient Silk Road passed through t he Iraqi
region from Basra to Baghdad. On the other hand, the
majority o f M, R2 and U7 mtDNAs display control-
region motifs observed in South West Asian and in parti-
cular in India [47,54-57]. Additional evidence of the mul-
tiple relationships with South West Asia derives from the
presence of one M33 mtDNA , whic h was c ompletely
sequenced, (GenBank accession number: JN540042).
This mtDNA belongs to the M33a2a clade and clusters
with three sequences, from Uttar Pradesh, Saudi Arabia
[58] and Egypt [47], respectively. On the o ther hand, the
presence in Iraq of Hgs M1 (in both Iraqi groups) and
U6 (in the control sample) of North/East African origin
[59] is indicative of some limited gene flow from that
area. The sub-Saharan contributi on is inste ad repre-
sented by ha plogroups L0, L1, L2 and L3. It reaches
values (~8%) in line with th ose reported for othe r Middle
Eastern Arab populations [60,61].
Gender differences in the Marsh Arab gene pool
In comparison with the control sample, representative of
the general Iraqi population, Marsh Arabs are character-
ized by an important lower Y-chromosome heterogeneity
(H
Y
= 0.461 vs 0.887) whereas similar values of heteroge-
neitywereobservedformtDNA(H
mtDNA
=0.963vs
0.957). This is due to the presence of one prevalent Y-
chromosome haplogroup, the J1-M267, which alone
characterizes more than 80% of the Marsh Y-chromosome
gene pool. Although patterns of lower male than female
heterogeneity have been reported in many populations
and usually ascribed to patrilocal residence [62-64], such a
scenario can explain only part of the large difference
observed in the geographically isolated marsh population.
Among the different factors (e.g. polygamy, unequal male
and female migration rates and se lective processes) that
can differently affect the extent of mtDNA and Y-chromo-
some heterogeneity, nonrandom-mating practices, com-
mon in the area, in association with cultural beliefs that
support polygamy, may have contributed to cause the dif-
ference observed in the Marsh Arabs.
Conclusions
The analyses carried out on the mtDNA and Y chromo-
some of the Iraqi Marsh Arabs, a population living in
the Tigris-Euphrates marshlands, have shown: (i) a pre-
valent autochthonous Middle Eastern component both
in male and female gene pools; (ii) weak South-West
Asian and African heritages, more evident for mtDNA;
(iii) a higher male than female homogeneity, mainly
determined by the co-occurrence of socio-cultural and
genetic factors; (iv) a g enetic stratification not only
ascribable to recent events. The last point i s well illu-
strated by Y-chromosome data where the less repre-
sented J1-M267* lineage indicates Northern
Mesopotamia contributions, w hereas the most frequent
J1-Page08 branch reveals a local recent expansion about
4,000 years ago (Table 2). Although the Y-chromoso me
age estimates deserve caution, particularly when samples
are small and standard errors large, it is interesting to
note that these estimates overlap the City State period
which characterised Southern Mesopotamia, and is testi-
fied to by numerous ancient Sumerian cities (Lagash,
Ur, Uruk, Eridu and Larsa).
In conclusion, our data show that the modern Marsh
Arabs of Iraq harbour mtDNAs and Y chromosomes
that are predominant ly of Middle Eastern origin. There-
fore, certain cultural features of the area such as water
buffalo breeding and rice farming, whi ch were most
likely introduced from the Indian sub-continent, only
marginally affected the gene pool of the autochthonous
people of the region. Moreover, a Middle Eastern ances-
tral origin of the modern population of the marshes of
southern Iraq implies that, if the Marsh Arabs are des-
cendants of the ancient Sumeri ans, also Sumerians were
not of Indian or Southern Asian ancestry.
Additional material
Additional file 1: Y-chromosome markers examined in this study.
The file provides information on the Y-chromosome markers examined in
the present study.
Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
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Additional file 2: MtDNA control-region data of the samples
reported in Table 1. The file provides information about the mtDNA
control-region haplotypes observed in the subjects of the present study.
Additional file 3: Absolute frequencies of Y-chromosome
haplogroups and sub-haplogroups in the 48 populations included
in the PCA. The file provides the list of the populations and Y-
chromosome haplogroups, along with their frequencies, used in the PCA
analysis.
Additional file 4: Absolute frequencies of mtDNA haplogroups and
sub-haplogroups in the 35 populations included in the PCA. The file
provides the list of the populations and mtDNA haplogroups, along with
their frequencies, used in the PCA analysis.
Additional file 5: Y-STR haplotypes associated with J1-M267* and
J1-Page08. The file provides the Y-chromosome STR haplotypes used for
the construction of the networks illustrated in Figure 4.
Additional file 6: Frequencies of Y-chromosome haplogroup J1-
M267 and J1-Page08 from published sources and present study
used for Figure 6. The file provides the data used for constructing the
maps illustrated in Figure 6.
Additional file 7: Y-chromosome haplogroup J1-Page-08
microsatellite variance from published sources and present study
used for Figure 6. The file provides the data used for constructing the
map illustrated in Figure 6.
Additional file 8: Y-chromosome haplogroup J1-M267*
microsatellite variance from published sources and present study
used for Figure 6. The file provides the data used for constructing the
map illustrated in Figure 6.
Additional file 9: Y-chromosome J1 sub-haplogroups variance,
divergence and expansion times based on six STR loci. The file
provides the variance, divergence and expansion times of the two J1
sub-haplogroups.
Acknowledgements
We are grateful to all donors for providing DNA samples for this study and
to the Marsh Arab people for their hospitality during the field expedition. In
addition, we warmly thank K. Al-Saadi for his help in the samples collection
and C. Mora for comments on the historical background. We are also
grateful to the anonymous reviewers for their constructive criticisms. This
research received support from the American Academic Research Institute in
Iraq (to N. A-Z.), Italian Ministry of the University: Progetti Ricerca Interesse
Nazionale 2009 (to O.S. and A.T.) and FIRB-Futuro in Ricerca 2008 (to A.O.),
Ministero degli Affari Esteri (to N.A-Z. and O.S.), Fondazione Alma Mater
Ticinensins (to O.S. and A.T.). N.A-Z. was supported by a fellowship from the
Institute of International Education.
Author details
1
Dipartimento di Genetica e Microbiologia, Università di Pavia, Via Ferrata 1,
27100 Pavia, Italy.
2
Department of Biotechnology, Faculty of Sciences,
Baghdad University, 10001 Ba ghdad, Iraq.
3
Department of Microbiology,
UNESCO-MIRCEN for Marine Biotechnology, College of Fisheries, 575002
Mangalore, India.
4
Centro Interdipartimentale Studi di Genere, Università di
Pavia, 27100 Pavia, Italy.
Authors contributions
NAZ., OS and ASSB designed the research; NAZ and MAH performed the
sample collection; NAZ, VB, VG generated the Y-chromosomal data; NAZ,
MP, AO and BHK generated the mtDNA data; NAZ, VG and OS carried out
the data analyses; NAZ, OS, AT, and ASS-B wrote the paper. All authors
discussed the results, read and approved the final manuscript.
Received: 27 May 2011 Accepted: 4 October 2011
Published: 4 October 2011
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Al-Zahery et al. BMC Evolutionary Biology 2011, 11:288
http://www.biomedcentral.com/1471-2148/11/288
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doi:10.1186/1471-2148-11-288
Cite this article as: Al-Zahery et al.: In search of the genetic footprints of
Sumerians: a survey of Y-chromosome and mtDNA variation in the
Marsh Arabs of Iraq. BMC Evolutionary Biology 2011 11:288.
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    To construct maternal phylogeny and prehistoric dispersals of modern human being in the Indian sub continent, a diverse subset of 641 complete mitochondrial DNA (mtDNA) genomes belonging to macrohaplogroup M was chosen from a total collection of 2,783 control-region sequences, sampled from 26 selected tribal populations of India. On the basis of complete mtDNA sequencing, we identified 12 new haplogroups -M53 to M64; redefined/ascertained and characterized haplogroups M2 and M49, which were previously described by control and/or coding-region polymorphisms. Our results indicate that the mtDNA lineages reported in the present study (except East Asian lineages M89C9Z, M9, M10, M11, M12-G, D) are restricted to Indian region.The deep rooted lineages of macrohaplogroup 'M' suggest in-situ origin of these haplogroups in India. Most of these deep rooting lineages are represented by multiple ethnic/linguist groups of India. Hierarchical analysis of molecular variation (AMOVA) shows substantial subdivisions among the tribes of India (FST = 0.16164). The current Indian mtDNA gene pool was shaped by the initial settlers and was galvanized by minor events of gene flow from the east and west to the restricted zones. Northeast Indian mtDNA pool harbors region specific lineages, other Indian lineages and East Asian lineages. We also suggest the establishment of an East Asian gene in North East India through admixture rather than replacement.
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    BACKGROUND: Recent advances in the understanding of the maternal and paternal heritage of south and southwest Asian populations have highlighted their role in the colonization of Eurasia by anatomically modern humans. Further understanding requires a deeper insight into the topology of the branches of the Indian mtDNA phylogenetic tree, which should be contextualized within the phylogeography of the neighboring regional mtDNA variation. Accordingly, we have analyzed mtDNA control and coding region variation in 796 Indian (including both tribal and caste populations from different parts of India) and 436 Iranian mtDNAs. The results were integrated and analyzed together with published data from South, Southeast Asia and West Eurasia. RESULTS: Four new Indian-specific haplogroup M sub-clades were defined. These, in combination with two previously described haplogroups, encompass approximately one third of the haplogroup M mtDNAs in India. Their phylogeography and spread among different linguistic phyla and social strata was investigated in detail. Furthermore, the analysis of the Iranian mtDNA pool revealed patterns of limited reciprocal gene flow between Iran and the Indian sub-continent and allowed the identification of different assemblies of shared mtDNA sub-clades. CONCLUSIONS: Since the initial peopling of South and West Asia by anatomically modern humans, when this region may well have provided the initial settlers who colonized much of the rest of Eurasia, the gene flow in and out of India of the maternally transmitted mtDNA has been surprisingly limited. Specifically, our analysis of the mtDNA haplogroups, which are shared between Indian and Iranian populations and exhibit coalescence ages corresponding to around the early Upper Paleolithic, indicates that they are present in India largely as Indian-specific sub-lineages. In contrast, other ancient Indian-specific variants of M and R are very rare outside the sub-continent.
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    We develop a flexible class of Metropolis-Hastings algorithms for drawing inferences about population histories and mutation rates from deoxyribonucleic acid (DNA) sequence data. Match probabilities for use in forensic identification are also obtained, which is particularly useful for mitochondrial DNA profiles. Our data augmentation approach, in which the ancestral DNA data are inferred at each node of the genealogical tree, simplifies likelihood calculations and permits a wide class of mutation models to be employed, so that many different types of DNA sequence data can be analysed within our framework. Moreover, simpler likelihood calculations imply greater freedom for generating tree proposals, so that algorithms with good mixing properties can be implemented. We incorporate the effects of demography by means of simple mechanisms for changes in population size and structure, and we estimate the corresponding demographic parameters, but we do not here allow for the effects of either recombination or selection. We illustrate our methods by application to four human DNA data sets, consisting of DNA sequences, short tandem repeat loci, single-nucleotide polymorphism sites and insertion sites. Two of the data sets are drawn from the male-specific Y-chromosome, one from maternally inherited mitochondrial DNA and one from the "&bgr;"-globin locus on chromosome 11. Copyright 2003 Royal Statistical Society.
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    Spectacular progress has been made recently in the study of evolution at the molecular level, primarily due to new biochemical techniques such as gene cloning and DNA sequencing. In this book, the author summarizes new developments and seeks to unify studies of evolutionary histories of organisms and the mechanisms of evolution into a single science - molecular evolutionary genetics.