abu-amero_09_saudi_798671.pdf.txt

<!DOCTYPE html PUBLIC "-//W3C//DTD XHTML 1.0 Transitional//EN" "http://www.w3.org/TR/xhtml1/DTD/xhtml1-transitional.dtd"><html xmlns="http://www.w3.org/1999/xhtml">
<head>
<title>1471-2156-10-59.fm</title>
<meta name="Author" content="sufi01"/>
<meta name="Creator" content="FrameMaker 8.0"/>
<meta name="Producer" content="Acrobat Distiller 8.1.0 (Windows)"/>
<meta name="CreationDate" content=""/>
</head>
<body>
<pre>
BMC Genetics

BioMed Central

Open Access

Research article

Saudi Arabian Y-Chromosome diversity and its relationship with
nearby regions
Khaled K Abu-Amero*1, Ali Hellani2, Ana M González3, Jose M Larruga3,
Vicente M Cabrera3 and Peter A Underhill4
Address: 1Molecular Genetics Laboratory, College of Medicine, King Saud University, Riyadh 11411, Saudi Arabia, 2Department of PGD, Saad
Specialist Hospital, Al-Khobar, Saudi Arabia, 3Departamento de Genética, Universidad de La Laguna, 38271 La Laguna, Tenerife, Spain and
4Department of Psychiatry and Behavioural Sciences, Stanford University, School of Medicine, Stanford, California 94304, USA
Email: Khaled K Abu-Amero* - abuamero@gmail.com; Ali Hellani - ahellani@gmail.com; Ana M González - amglez@ull.es;
Jose M Larruga - jlarruga@ull.es; Vicente M Cabrera - vcabrera@ull.es; Peter A Underhill - under@stanford.edu
* Corresponding author

Published: 22 September 2009
BMC Genetics 2009, 10:59

doi:10.1186/1471-2156-10-59

Received: 9 December 2008
Accepted: 22 September 2009

This article is available from: http://www.biomedcentral.com/1471-2156/10/59
© 2009 Abu-Amero et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract
Background: Human origins and migration models proposing the Horn of Africa as a prehistoric
exit route to Asia have stimulated molecular genetic studies in the region using uniparental loci.
However, from a Y-chromosome perspective, Saudi Arabia, the largest country of the region, has
not yet been surveyed. To address this gap, a sample of 157 Saudi males was analyzed at high
resolution using 67 Y-chromosome binary markers. In addition, haplotypic diversity for its most
prominent J1-M267 lineage was estimated using a set of 17 Y-specific STR loci.
Results: Saudi Arabia differentiates from other Arabian Peninsula countries by a higher presence
of J2-M172 lineages. It is significantly different from Yemen mainly due to a comparative reduction
of sub-Saharan Africa E1-M123 and Levantine J1-M267 male lineages. Around 14% of the Saudi
Arabia Y-chromosome pool is typical of African biogeographic ancestry, 17% arrived to the area
from the East across Iran, while the remainder 69% could be considered of direct or indirect
Levantine ascription. Interestingly, basal E-M96* (n = 2) and J-M304* (n = 3) lineages have been
detected, for the first time, in the Arabian Peninsula. Coalescence time for the most prominent J1M267 haplogroup in Saudi Arabia (11.6 ± 1.9 ky) is similar to that obtained previously for Yemen
(11.3 ± 2) but significantly older that those estimated for Qatar (7.3 ± 1.8) and UAE (6.8 ± 1.5).
Conclusion: The Y-chromosome genetic structure of the Arabian Peninsula seems to be mainly
modulated by geography. The data confirm that this area has mainly been a recipient of gene flow
from its African and Asian surrounding areas, probably mainly since the last Glacial maximum
onwards. Although rare deep rooting lineages for Y-chromosome haplogroups E and J have been
detected, the presence of more basal clades supportive of the southern exit route of modern
humans to Eurasian, were not found.

Background
The arid Arabian Peninsula can be viewed as a geographic
cul de sac and passive recipient of Near East cultural and

demic expansions since the Bronze Age. However, southern Arabian late Neolithic excavations revealing sorghum
and date palm cultivation attest to earlier influences from
Page 1 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

East Africa and South western Asia [1]. However, after the
southern dispersal route of modern humans across the
Bab el Mandeb Strait was proposed [2] and further developed [3], multidisciplinary interest on this region has dramatically increased in the search for traces of such putative
early southern dispersals across the Arabian threshold.
From an archaeological perspective, Lower Paleolithic
Oldowan industries found in the Arabian Peninsula indicated that, presumably, H. erectus or H. ergaster may have
been making forays into this region [4]. There is also evidence of Middle Paleolithic Mousterian and Aterian technologies in Arabia suggesting the possibility of an
expanded southern border for H. neanderthalensis and
potential links with populations from Northern Africa [5].
More recent field work has sampled new Palaeolithic sites
in Oman, under covering lithic assemblages with typological affinities to industries in the Levant, India and the
Horn of Africa, suggesting there were a series of huntergathers range expansions into southern Arabia from all
three refugia over the last quarter of a million years [6].
However, there are few reliable age estimates for these
industries. Furthermore, the passage of these hominids to
Arabia could be either through an overland route or across
a waterway.
From a population genetics perspective, the most recent
studies on the Arabian Peninsula have been carried out
using mainly uniparental, mitochondrial DNA (mtDNA)
and Y-chromosome, markers. Analysis based on maternal
lineages in the region has been interpreted to represent
traces of late Palaeolithic, Neolithic and more recent
inputs from nearby regions into Arabia as well as signatures of authochtonous expansions [7-12]. However, the
lack of deep rooting M and N sequences in the contemporary Arabian mtDNA pool leaves the proposed southern
coastal route without empirical support. Although Y-chromosome basal lineages remain undetected, phylogeographic patterns indicate that the Levant was an important
bidirectional corridor of human migrations [13,14].
Moreover, the Levant appeared as the main source of male
lineages to the Arabian Peninsula [15]. However, Saudi
Arabia, a country that occupies about 80% of the Arabian
Peninsula, was not directly included. In order to fill this
void, we performed a high resolution Y-chromosome SNP
analysis of 157 Saudi Arabian males and a STR-based
analysis of J1-M267, the most frequent Y-chromosome
haplogroup in Saudi Arabia. Comparisons to other published Arabian Peninsular populations and nearby
regions were made to further explore paternal traces of the
modern human transit across Arabia.

Methods
Sample and typing
All sample collecting and genotyping tasks were performed by the Saudi Arabian collaborators of this study.

http://www.biomedcentral.com/1471-2156/10/59

Buccal swabs or peripheral blood were obtained from 157
paternally unrelated Saudi Arab males whose all known
paternal lineages, at least for two generations, were of
Saudi Arabia origin. Due to its moderate size we have not
performed a regional subdivision of the sample. Informed
consent was obtained from all the participants. This
research followed the tenets of the Declaration of Helsinki. DNA was extracted using the Nucleon™ BACC
Genomic DNA Extraction Kit (GE healthcare, Piscataway,
NJ, USA). Sixty-seven Y-Chromosome binary genetic
markers were genotyped hierarchically. Primers, polymorphic positions and haplogroup nomenclature were as
recently actualized [16]. After amplification and purification, haplogroup typing was carried out in all cases by
direct sequencing on the ABI 3130 xI Genetic Analyzer
(Applied Biosystems, Foster city, CA, USA). The following
17 Y-STR loci: DYS19, DYS385 a/b, DYS389I/II, DYS390,
DYS391, DYS392, DYS393, DYS437, DYS438, DYS439,
DYS448, DYS456, DYS458, DYS635 and Y-GATA H4 were
amplified in a Gene Am PCR System 2700 (Applied Biosystems) using the AmpF/STR Yfiler Amplification Kit
(Applied Biosystems) following the manufacturers
instructions. DNA fragment separation was carried out in
an ABI Prism 3100 Genetic Analyzer (Applied Biosystems). STR alleles were identified by comparison to a
commercial allelic ladder using Genotyper 3.7 NT software.
Our Saudi Arabia sample was compared to other Arabian
Peninsula populations and to surrounding areas using
data from previous studies performed at a similar level of
haplogroup resolution. These samples comprise, 72
Qatari, 164 United Arab Emirate and 62 Yemeni [15]; 121
Omani and 147 Egyptian [14]; 201 Somalis [17]; 916 Lebanese [18]; 146 Jordanian [19]; 203 Iraqi (139 from AlZahery et al. [20] and 64 from Sanchez et al. [17]); 523
Turks [21];150 Irani [22] and 176 Pakistani [23].
Statistical analysis
To make comparisons reliable, haplogroup frequencies
were normalized to the same phylogenetic level as the
sample in the published studies with the most unrefined
haplogroup resolution. Analysis of molecular variance
(AMOVA) and haplogroup frequency pairwise FST genetic
distances [24] were performed using the ARLEQUIN 2000
package [25]. Principal component (PC) analysis and
two-dimensional graphics were carried out using the SPSS
statistical package 11.5 (SPSS, Inc). Times to most recent
common ancestor (TMRCA) for the J1-M267 clade were
calculated from STR variances and by coalescence methods (see Additional File 1). Mean STR variance was estimated as proposed by Kayser and others [26] and
transformed in divergence time using a mean STR mutation rate of 0.00069 per generation of 25 years [27]. For
coalescence age estimations STR loci were weighted by

Page 2 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

http://www.biomedcentral.com/1471-2156/10/59

their respective variances as described in Qamar and others [28]. Then, median-joining networks were constructed
after processing the data with the reduced median network method using Network version 4.5.1.0 [29]. The
rho-statistic was estimated with Network and converted
into time using the above mentioned Zhivotovsky and
others [27] mutation rate. For these estimations loci
DYS385 were excluded and the repeats of DYS389I were
subtracted to the DYS389II so that its diversity was not
considered twice.

Results
Y-SNP analysis
Only 27 of the 67 binary markers analyzed were informative in defining the haplogroup census of the Saudi Arabian sample (Table 1). The following 40 polymorphisms
(M60, M130, M217, M174, P147, M33, M75, P177, P2,
M215, M78, M81, M123, M329, M89, M282, M201, P20,
P16, M286, M52, M197, M370, M170, M172, M410,
M92, M241, M9, M20, M317, M231, M214, M119, M207,
M173, M343, P25, M18 and M124) were observed at
ancestral allele status in the sample set. The most abundant haplogroups in Saudi Arabia, J1-M267 (42%), J2M172 (14%), E1-M2 (8%), R1-M17 (5%) and K2-M184
(5%) are also well represented in other Arabian populations (Table 1). When the AMOVA analysis compared all
regions as unitary groups except the Arabian Peninsula, it
showed a partition of variance within populations (91%)
and among groups (6.8%) to be highly significant (p <
0.0001 in both cases) but an analysis among the samples
within the Arabian Peninsula (2.2%) did not reach statistical significance (p = 0.10 ± 0.01). The same trend is also
reflected in FST based pairwise distances (Table 2), as all
the distances not involving pairs of Arabian samples were
statistically highly significant (p < 0.0001) but those
within the Arabian Peninsula showed lower levels of significance, except when affecting Yemen (p < 0.0001) that
is the most divergent population of Arabia, although
showing its least distance to Qatar (p = 0.048). Precisely,
in addition to Yemen, Saudi Arabia has significant haplogroup frequency differences only with Qatar (p = 0.009).
Quantitatively, the main peculiarity of the Saudi male
pool with respect to the rest of the Arabian samples is a
significant higher presence of the J2-M172 related haplotypes (p = 0.001). On the other hand, the high divergence
of Yemen is mainly due to a significant excess of J1-M267
(p < 0.0001) types, a nearly significant excess of J2-M67
types (p = 0.062), and to a lack of R1-M17 representatives
(p = 0.04). In addition, southern Arabia, represented by
Yemen and Oman, show a greater E1-M123 account than
in northern areas (p = 0.006). As the Y-chromosome phylogeography is well structured [30,31], it is possible to
roughly quantify the different male inputs from surrounding regions into Arabia. When haplogroups A, B, E-M96,
E1-P2, E1-M2, and E1-M35 frequencies are assumed to be

Figure
tions 1
frequency data in the Arabian Peninsula and adjacent populaBidimensional plots based on Y-chromosome haplogroup
Bidimensional plots based on Y-chromosome haplogroup frequency data in the Arabian Peninsula and
adjacent populations. [A] MDS analysis (stress value =
0.265); [B] PC analysis. Abbreviations: ANA, Anatolia; EGY,
Egypt; IRN, Iran; IRQ, Iraq; JOR, Jordan; LEB, Lebanon;
OMA, Oman; PAK, Pakistan; QAT, Qatar; SAR, Saudi Arabia;
SOM, Somalia; UAE, United Arab Emirates; YEM, Yemen.

representative of the Africa contribution and frequencies
of C, F, G, H, L, O, Q and R1-M17 as arrivals, across Iran,
from Central, southern, and southeastern Asia, inputs of
13.4% and 16.6% from both areas are estimated for Saudi
Arabia. UAE is the region with the least African (5.5%)
and the greatest Iranian influence (36.8%). If the global
inputs for the Arabian Peninsula are estimated to approximate 10% from sub-Saharan Africa and 22% from Iran,

Page 3 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

http://www.biomedcentral.com/1471-2156/10/59

Table 1: Ychromosome haplogroup frequencies observed for Saudi Arabia and nearby regions
Haplogroup

SNP

A3a
A3b2*
B*
B2a*
B2a1a
B2b*
C*
C3*
C5*
E*
E1a*
E1b1*
E1b1a*
E1b1a7*
E1b1b*
E1b1b1*
E1b1b1a*
E1b1b1a2*
E1b1b1a3*
E1b1b1b*
E1b1b1c*
E1b1b1c1*
E1b1c
E2*
E2b*
F*
F1*
G*
G1*
G1a
G2a*
G2a1*
G2a2
G2b
G2c
H*
H1*
H1a*
H1a1
H1b
I*
I1*
I2a*
I2a1
I2b*
J*
J1*
J1b
J1e1
J1e2
J2*
J2a*
J2a
J2a1
J2a2*
J2a2a*
J2a5
J2a9
J2a10
J2b*
J2b2*
K*
K2
L*
L1
L2*
L2a*
L2b*
L3*

M32
M13
M139
M150
M109
M112
RPS4Y
M217
M356
M96
M33
P2
M2
M191
M215
M35
M78
V13
V22
M81
M123
M34
M329
M75
M98
M89
M282
M201
M285
P20
P15
P16
M286
M287
M377
M69
M52
M82
M197
M370
M170
M253
P37
M359
M223
M304
M267
M365
M368
M369
M172
M410
DYS413
M47
M67
M92
M158
M339
M340
M12
M241
M9
M184
M20
M76
M317
M274
M349
M357

Sar

Qatar

UAE

Oman

Yemen

Somalia

Egypt

Lebanon

Jordan

Iraq

Anatolia

Iran

Pakistan

0.50
1.00

3.00

0.68

0.38

1.00
0.64

1.39

1.27

1.39

2.00
2.00
1.27
1.27

0.11
0.96
0.38

1.23
1.00

3.82
3.82

5.52

1.50

1.00
1.00

2.00

1.50
77.60

3.00
18.00

0.22
10.48

1.50
0.50

8.00
7.00

1.2
4.26

1.61
3.23

4.46

1.39
1.39
1.39

1.39
1.39
1.39
2.78

0.61
0.61
6.75
0.61
3.07

8.06
2.00

2.78

1.27

2.45

0.57

9.36

4.97

3.33

1.14

2.74

0.19
1.48

0.68

1.84
0.61
1.84

1.33

5.54

0.50

9.00

6.55

1.61

0.49
2.46

3.42
0.68

1.39

0.19
0.19
0.76
8.41
0.96
0.19
0.19

1.33
1.33
4.67

0.57

7.33

4.55

1.14
0.57
5.11

2.00
0.50

0.64

0.67

0.50

2.00

2.55

10.27

0.38
0.19

13.01

3.68
0.61
0.64

0.99

0.66

2.55

0.64

3.23

6.82
0.57

0.55
0.22

12.00

2.78

5.00
2.00

0.67

0.38

1.84

2.00
0.57
1.00

1.91
40.13

58.33

34.97

11.46
2.55
0.64

2.78
1.39
1.39

1.23
4.29
1.84
0.61
1.23

1.27

1.39
1.39

38.00

5.00

5.10
1.27

1.23

4.91
2.78

3.42

0.49

2.50

19.00

20.09

30.82

31.03

0.50

72.58

4.8

8.00

6.16

26.6

0.19
1.15
1.15
2.29
0.19
0.57
0.19
8.41
0.19
0.19
0.19
14.34

4.84

1.00

3.00

4.00

8.00
1.00

10.40

15.28
7.75
0.11

4.79

1.00

4.84

2.73

2.05
0.68

8.00

0.87
4.69
5.24

1.15
3.63
2.68
0.38
0.19
0.19
0.76
0.96
0.99
5.91
0.99

2.49
4.02

2.45

0.19
0.64

0.61

0.57

11.33

3.41

4.00
9.33
3.33
2.00
1.33

8.52

2.00
1.33

1.14

2.27
0.57

2.67
2.67
0.67
0.67
0.67
0.67

Page 4 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

http://www.biomedcentral.com/1471-2156/10/59

Table 1: Ychromosome haplogroup frequencies observed for Saudi Arabia and nearby regions (Continued)
N*
N1c*
N1c1*
N2*
O*
O1a*
Q*
Q1a2*
Q1a3*
L1
L2*
L3*
O3*
O3a3c*
Q1a1
Q1a3*
Q1b
R*
R1*
R1a*
R1a1*
R1a1c
R1b*
R1b1*
R1b1a
R1b1b1
R1b1b2*
R1b1c
R2

M231
Tat
M178
P43
M175
M119
M242
M25
M346
M76
M317
M357
M122
M134
M120
M346
M378
M207
M173
SRY1532
M17
M204
M343
P25
M18
M73
M269
M335
M124
Sample

2.87
0.99
0.96
0.64
1.91

0.61
0.61
1.23

0.64

0.11

1.00

0.19

2.00
0.67

1.53
0.44

1.72
0.19

4.00

0.61

1.00

1.00

1.31
0.61
5.10

6.94

1.00

7.36

2.00

9.00

3.00

2.51

1.37

0.22

0.19

6.90

6.88

0.99

1.00

0.49

0.19
0.38

13.7

0.61

2.67
0.67
12.67
0.67

5.11
1.14
6.82
1.7
0.57
0.57
1.7
1.14
3.41
0.57
24.43

0.55
1.91

1.39

3.68

1.00

157

1.39
72

164

121

2.00

62

the remaining 68% could be considered of direct or indirect Levantine ascription. Relative relationships among
the Arabian samples to nearby regions are graphically represented in bidimensional plots, resulting from MDS
analysis obtained from a matrix of FST distances (Figure
1a) and as the two first components of a PC analysis (Figure 1b). In the first analysis, congruently with its pair-wise
distances, Somalia appears as an outlier, and the close
relationship found between Qatar and Yemen is also
reflected in the plot. For the rest of the Arabian samples a
clear partition exists, whereas Oman and UAE appear
closer to the Levant samples that include Egypt, the Saudi
component positions approximates towards the northeast
edge of the Near East. However, the population spatial
distribution along to the first and second principal components in the PC analysis is quite different. In this case,
the main haplogroups (C, H, L, O, Q and R1-M17),
responsible for the positive displacement along the first
component, are most abundant in Iran, Pakistan and
UAE. On the opposite side are E1-M35, E1-M123 and J1M267 that drives Yemen to the negative edge. For the second component, the main positive values correspond to
the Eurasian haplogroups G-M201. I-M170, J2-M67 and
R1-M269, that group all the Near East populations,
including Egypt, whereas the Arabian samples and Somalia fall on the negative side pulled by their comparatively
higher frequencies of the sub-Saharan Africa haplogroups
E1-M2 and E2-M75 and, again, the most prevalent haplogroup in Arabia J1-M267. As the first and second principal

201

7.31

4.11

9.85

1.00
147

0.22
916

1.37
146

203

0.76
14.53
0.19
0.96
523

8.00

4.55
2.84

1.33
150

7.39
176

components only capture the 26% and the 17% of the variance respectively and haplogroup E1-M78 has a minor
contribution in the first and second component matrix,
Somalia, that has the highest E1-M78 frequency of all the
samples, does not behave as an outlier in the bidimensional PC representation. Finally, it deserves mention
that, qualitatively, Saudi Arabia is also peculiar because of
the presence, in low frequencies, of two underived EM96* (1.3%) and J-M304* (1.9%) lineages that were not
detected in other surveys of the Arabian Peninsula
[14,15].
Y-STR analysis
Y-chromosome STR diversity was used to obtain age estimates in Saudi Arabia for the most frequent J1-M267 haplogroup. In order to compare these estimations with other
Arabian peninsula regions, we re-calculated the J1-M267
ages in UAE, Qatar and Yemen using the STR data already
published for these countries [15]. STR haplotypes found
in Saudi Arabia are listed in Additional file 1. Divergence
times obtained using mean variance and coalescence
methods are presented in Table 3. Values obtained using
coalescence resulted always larger than those based on
variance.

Discussion
Consistent with the rest of the Arabian Peninsula, haplogroup J is the most abundant component in Saudi Arabia
embracing 58% of its Y-chromosomes. Its two main sub-

Page 5 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

http://www.biomedcentral.com/1471-2156/10/59

Table 2: Fst distances between populations. Codes as in figure 1

SAR
SAR
QAT
UAE
OMA
YEM
SOM
EGY
LEB
JOR
IRQ
ANA
IRN
PAK

QAT

UAE

OMA

YEM

SOM

EGY

LEB

JOR

IRQ

ANA

IRN

PAK

0.023**
0.004ns
0.020**
0.082
0.664
0.065
0.057
0.04
0.066
0.089
0.056
0.126

0.031
0.039
0.021*
0.99
0.12
0.108
0.073
0.101
0.162
0.135
0.21

0.017**
0.102
0.602
0.05
0.045
0.033
0.055
0.068
0.041
0.095

0.107
0.671
0.045
0.053
0.048
0.047
0.085
0.067
0.116

1.367
0.215
0.188
0.137
0.185
0.262
0.255
0.352

0.33
0.326
0.502
0.523
0.381
0.484
0.539

0.028
0.039
0.041
0.048
0.048
0.093

0.046
0.066
0.047
0.037
0.086

0.051
0.054
0.059
0.113

0.046
0.077
0.128

0.025
0.055

0.029

-

* p < 0.05; ** p < 0.01; the rest of pairwise comparisons have p < 0.001 values

clades (J1-M267 and J2-M172), show opposite latitudinal
gradients in the Middle East. J1-M267 is more abundant
in the southern areas, reaching a frequency around 73% in
Yemen, whereas J2-M172 is more common in the Levant.
Most probably, the significant higher presence of J2-M172
in Saudi compared to other Arabian populations is due to
the larger northern boundary that Saudi Arabia shares
with the Levant. The Fertile Crescent region has been considered the most probable origin of the earliest dispersions of both subclades [21,32,33]. Further subdivisions
of J1-M172 have uncovered more recent Bronze age
expansions from Turkey and the Balkans traced by the J2M67/M92 and J2-M12 subgroups [21,34,35].
In a similar way, it is possible that J2-M47 signals a more
recent expansion from the Levant that also affected the
Arabian Peninsula. The peculiar distribution of J2-M67 in
Arabia could be explained assuming maritime contacts
from classical Mediterranean cultures. The presence in
Saudi Arabia of three males harbouring underived J1M304 chromosomes is intriguing. It could be that they
came together with the J1-M267 or J2-M172 expansive
waves, or they could represent the remnants of an old and
geographically widespread Palaeolithic substrate. This
type of underived chromosomes has been detected rarely
in Turkey [21], in Oman and in the eastern Mediterranean

area [34]. However, as the critical Levantine region has
not yet been adequately dissected for J1, it seems premature to favor any of these hypotheses. The geographic pattern and most probable origin of the Y-chromosome
haplogroup J in Arabia faithfully mirrors those found for
the most prevalent J and R0a mtDNA haplogroups in the
same region [7-9,12]. In addition, J1-M267 divergence age
calculated for Saudi Arabia (11.6 ± 2 kya) and Yemen
(11.3 ± 2 kya) are also very coincidental with those calculated for J1b (11.1 ± 8.4 kya) and R0a1 (9.6 ± 2.9 kya) in
Saudi Arabia [7,8]. It is worth mentioning that J1-M267
ages in Saudi Arabia and Yemen are significantly older
than those obtained for UAE and Qatar (Table 3)[15] and
for Oman [14] pointing to a terrestrial more than to a
maritime colonization. It has been suggested that Yemen
could be a center of expansion for mtDNA haplogroup
R0a [9].
Although the comparatively high divergence calculated
for J1-M267 Y-chromosomes in Yemen [15] could be in
support of primary or, at least, secondary human expansions from southern Arabia, it could also be explained as
result of successive arrivals of J1 chromosomes from different source regions. Furthermore, J 1-M267 diversities
found here for Saudi Arabia are of the same range than in
Yemen and both smaller than the one estimated for Tur-

Table 3: Y-haplogroup J1-M267 variance and divergence times deduced from Y-STR loci

Population

sample size

k17a

k14b

M-267 variance

T(ky)

Divergence time (ky) Mean ± SE

UAEc
Qatarc
Yemenc
Saudi Arabia
Arabian Peninsula

57
42
45
48
192

40
33
41
41
149

33
28
40
39
129

0.16
0.19
0.27
0.29
0.24

5.81
6.71
9.69
10.37
8.85

6.81 ± 1.53
7.27 ± 1.83
11.27 ± 2.03
11.59 ± 1.93
10.78 ± 1.65

a Haplotype number using 17 Y-STR loci
b Haplotype number using 14 Y-STR loci
c Estimated from the Cadenas et al. (2007) data

Page 6 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

key [21]. This southwards decreasing trend is more compatible with a Neolithic arrival to Arabia via the Levant as
proposed by others [15]. In fact, the coalescence ages calculated in Saudi Arabia for their most prominent mtDNA
and Y-chromosome lineages merged around 10 kya. This
period is coincidental with an improvement of the climatic conditions in the area that facilitated the spread of
Natufian and Neolithic cultures from the Fertile Crescent
north and southwards. The haplogroup E1-M123/M34
has an extended but sparse geographic distribution in
Eastern Africa, the Middle East and the Mediterranean
basin [14,32,35]. However, its frequency rises considerably in some populations, most probable because of isolation and genetic drift effects. This would explain
frequencies as high as 11% found in some Ethiopian samples [35] or the highest (31%) found, until now, in the
Dead Sea region of Jordan (Flores et al. 2005). In the Arabian Peninsula this clade is, in general, well represented
but reaches significant higher frequencies in the southern
countries of Yemen and Oman compared with northern
areas. An East African origin, and posterior spread to the
Near East through the Levantine corridor, of this lineage
was proposed based on the much larger variance of this
clade in Egypt (0.5) versus Oman (0.14) [14]. On the contrary, other authors have suggested that E1-M123 may
have originated in the Near East because of its generalized
implantation there [21] compared to its presence in Eastern Africa, mainly just localized in Ethiopia [32]. Recent
E-M123 haplogroup variances calculated for Yemen
(0.14) and UAE (0.25) were also lower than the Egyptian
one [15]. In addition, haplotypic differences found for
those two Arabian countries indicated that they do not
share a common ancestry [15]. So, from an Arabian
Peninsula perspective, E1-M123 could have come from
Ethiopia, across the Horn of Africa, or from the Levant, or
even from both sources, forming independent isolates.
Global male inputs from Sub-Saharan Africa and Asia
across Iran, not the Levant, into the Arabian Peninsula
have been estimated in this study, as 13.4% and 16.6%
from both source areas respectively. Recent mtDNA studies on the same Arabian Peninsula countries [7-9,12] have
confirmed a notable female-driven sub-Saharan African
input with a mean value around 15% for all the Peninsula, although frequencies as high as 60% have been
detected in Hadramawt populations of Yemen [9]. Curiously, the Iranian female flow (18%) was also rather similar to that calculated for Africa. Although a slight ratio
excess of Sub-Saharan African female versus male gene
flow is detected (1.12) we do not found the strong sexual
bias proposed by other authors for Arabian populations
and attributed to the peculiarities of the recent slave-trade
[12,36]. Without dismissing the role mediated by slavery,
the geographical distribution of these sub-Saharan African
lineages in the Arabian Peninsula seems to indicate a prehistoric entrance of a noticeable portion of these lineages

http://www.biomedcentral.com/1471-2156/10/59

that participated in the building of the primitive Arabian
population [8,9]. The presence of two underived E-M96
Saudi lineages raises interesting questions related to the
macrohaplogroup DE-YAP phylogeography. The recent
resolutions of the CDEF-M168 tripartite structure to the
bipartite DE-YAP and CF-P143 [16,31] extends the conversation regarding the early successful colonization of
Eurasia. While several scenarios remain potentially possible the most parsimonious model is the most prudent.
This model proposes the successful colonization of Eurasia by migration(s) of populations containing precursor
Y-chromosome founder macrohaplogroup CDET-M168
and basal mtDNA L3 representatives. Regions near but
external to northeast Africa, like the Levant or the southern Arabian Peninsula could have served as an incubator
for the early diversification of non-African uniparental
haplogroup varieties like Y chromosome DE-YAP*, CFP143* and mtDNA M and N molecular ancestors. These
would have spread globally and diversified over time and
space. This model would imply that both CF-P143 and
the DE-YAP evolved nearby but outside Africa. One DEYAP* ancestor would have spread to Asia and evolved to
haplogroup D while another DE-YAP* returned to northeast Africa and evolved into hg E. It is noteworthy that DEYAP* has been detected at low frequency in Africa [37].
Again, this hypothesis has its mtDNA counterpart as it is
well documented that, in the Palaeolithic, at least three
clades (X1, U6, M1) derived respectively from the three
main Eurasian macrohaplogroups (N, R, M) came back to
North Africa from Asia [38-42].
Within this frame, it should be expected that E-M96*
types appear in Africa although its presence in the Arabian
Peninsula instead Eastern Africa would not compromise
the last proposed model. It could be suggested that these
E-M96 Saudi lineages have a sub-Saharan Africa ancestry.
However, at least for one of them, all their known male
ancestors belong to a big Shammar Arab tribe that ruled
much of central and northern Arabia from Riyadh to the
frontiers of Syria and northern Iraq. In addition, it might
be present in Lebanon [18]. However, as the authors did
not type more markers derived within the E-M96 background such as P147, P177, P2, P75 or M329, more comprehensive phylogenetic resolution of YAP derived Ychromosomes in the Middle East and North and East
Africa are necessary to explore the topic further. In any
case, the presence of E-M96* in Saudi Arabia should not
be taken as support of the southern exit of modern
humans across the Srait of Bab el Mandab as no D nor CF
underived lineages have been yet found in this area.

Conclusion
The Y-chromosome genetic structure of the Arabian
Peninsula seems to be mainly modulated by geography.
The data confirm that this area has mainly been a recipi-

Page 7 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

ent of gene flow from its African and Asian surrounding
areas, probably mainly since the last Glacial maximum
onwards. Although rare deep rooting lineages for Y chromosome haplogroups E and J have been detected, the
presence of more basal clades supportive of the southern
exit route of modern humans to Eurasian, were not found.

Authors' contributions
KKA and AH was in charge of carrying out the sequences,
collection of samples, haplogrouping and writing part of
the manuscript. AMG, JML, VMC and PAU were in charge
of design of the experiments, analysis of the data and writing manuscript. All authors read and approved the final
version of the manuscript.

http://www.biomedcentral.com/1471-2156/10/59

11.

12.

13.

14.

15.

Additional material
16.

Additional file 1
Table S1. Y-chromosome STR haplotypes for haplogroup J1-M267 in
Saudi Arabia.
Click here for file
[http://www.biomedcentral.com/content/supplementary/14712156-10-59-S1.XLS]

17.

18.

19.

Acknowledgements
Dr. Abu-Amero is supported by grants from the Glaucoma Research Chair
at the Dept. Of Ophthalmology, College of Medicine, King Saud University,
Riyadh, Saudi Arabia. This research was also supported by grant BFU200604490 from Ministerio de Ciencia y Tenologia to J.M.L and Saad Specialist
Hospital, Al-Khobar (AH).

20.

21.

References
1.
2.
3.
4.
5.
6.

7.
8.
9.

10.

Tosi M: The emerging picture of Prehistoric Arabia. Ann Rev
Anthrop 1986, 15:461-490.
Sauer C: Seashore, primitive home of man? Proc Am Phil Soc
1962, 106:41-47.
Lahr M, Foley R: Multiple dispersals and modern human origins. Evol Anthropol 1994, 3:48-60.
Petraglia M: The lower Paleolithic of the Arabian Peninsula:
Occupations, adaptations, and dispersals. J World Prehist 2003,
17:141-179.
Petraglia M, Alsharekh A: The Middle Palaeolithic of Arabia:
Implications for modern human origins, behaviour and dispersals. Antiquity 2003, 77:671-684.
Rose J: The Arabian Corridor Migration Model: archaeological evidence for hominin dispersals into Oman during the
Middle and Upper Pleistocene. Proceedings of the Seminar for Arabian Studies 2007, 37:1-19.
Abu-Amero KK, Gonzalez AM, Larruga JM, Bosley TM, Cabrera VM:
Eurasian and African mitochondrial DNA influences in the
Saudi Arabian population. BMC Evol Biol 2007, 7:32.
Abu-Amero KK, Larruga JM, Cabrera VM, Gonzalez AM: Mitochondrial DNA structure in the Arabian Peninsula. BMC Evol Biol
2008, 8:45.
Cerny V, Mulligan CJ, Ridl J, Zaloudkova M, Edens CM, Hajek M,
Pereira L: Regional differences in the distribution of the subSaharan, West Eurasian, and South Asian mtDNA lineages
in Yemen.
American journal of physical anthropology 2008,
136(2):128-137.
Kivisild T, Reidla M, Metspalu E, Rosa A, Brehm A, Pennarun E, Parik
J, Geberhiwot T, Usanga E, Villems R: Ethiopian mitochondrial
DNA heritage: tracking gene flow across and around the
gate of tears. Am J Hum Genet 2004, 75(5):752-770.

22.
23.

24.
25.
26.

27.

28.
29.

Roostalu U, Kutuev I, Loogvali EL, Metspalu E, Tambets K, Reidla M,
Khusnutdinova EK, Usanga E, Kivisild T, Villems R: Origin and
expansion of haplogroup H, the dominant human mitochondrial DNA lineage in West Eurasia: the Near Eastern and
Caucasian perspective. Mol Biol Evol 2007, 24(2):436-448.
Rowold DJ, Luis JR, Terreros MC, Herrera RJ: Mitochondrial DNA
geneflow indicates preferred usage of the Levant Corridor
over the Horn of Africa passageway. J Hum Genet 2007,
52(5):436-447.
Cruciani F, La Fratta R, Trombetta B, Santolamazza P, Sellitto D,
Colomb EB, Dugoujon JM, Crivellaro F, Benincasa T, Pascone R, et al.:
Tracing past human male movements in northern/eastern
Africa and western Eurasia: new clues from Y-chromosomal
haplogroups E-M78 and J-M12.
Mol Biol Evol 2007,
24(6):1300-1311.
Luis JR, Rowold DJ, Regueiro M, Caeiro B, Cinnioglu C, Roseman C,
Underhill PA, Cavalli-Sforza LL, Herrera RJ: The Levant versus the
Horn of Africa: evidence for bidirectional corridors of
human migrations. Am J Hum Genet 2004, 74(3):532-544.
Cadenas AM, Zhivotovsky LA, Cavalli-Sforza LL, Underhill PA, Herrera RJ: Y-chromosome diversity characterizes the Gulf of
Oman. Eur J Hum Genet 2008, 16(3):374-386.
Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL,
Hammer MF: New binary polymorphisms reshape and
increase resolution of the human Y chromosomal haplogroup tree. Genome Res 2008, 18(5):830-838.
Sanchez JJ, Hallenberg C, Borsting C, Hernandez A, Morling N: High
frequencies of Y chromosome lineages characterized by
E3b1, DYS19-11, DYS392-12 in Somali males. Eur J Hum Genet
2005, 13(7):856-866.
Zalloua PA, Xue Y, Khalife J, Makhoul N, Debiane L, Platt DE, Royyuru
AK, Herrera RJ, Hernanz DF, Blue-Smith J, et al.: Y-chromosomal
diversity in Lebanon is structured by recent historical
events. Am J Hum Genet 2008, 82(4):873-882.
Flores C, Maca-Meyer N, Larruga JM, Cabrera VM, Karadsheh N,
Gonzalez AM: Isolates in a corridor of migrations: a high-resolution analysis of Y-chromosome variation in Jordan. J Hum
Genet 2005, 50(9):435-441.
Al-Zahery N, Semino O, Benuzzi G, Magri C, Passarino G, Torroni A,
Santachiara-Benerecetti AS: Y-chromosome and mtDNA polymorphisms in Iraq, a crossroad of the early human dispersal
and of post-Neolithic migrations. Mol Phylogenet Evol 2003,
28(3):458-472.
Cinnioglu C, King R, Kivisild T, Kalfoglu E, Atasoy S, Cavalleri GL, Lillie
AS, Roseman CC, Lin AA, Prince K, et al.: Excavating Y-chromosome haplotype strata in Anatolia.
Hum Genet 2004,
114(2):127-148.
Regueiro M, Cadenas AM, Gayden T, Underhill PA, Herrera RJ: Iran:
tricontinental nexus for Y-chromosome driven migration.
Hum Hered 2006, 61(3):132-143.
Sengupta S, Zhivotovsky LA, King R, Mehdi SQ, Edmonds CA, Chow
CE, Lin AA, Mitra M, Sil SK, Ramesh A, et al.: Polarity and temporality of high-resolution y-chromosome distributions in India
identify both indigenous and exogenous expansions and
reveal minor genetic influence of Central Asian pastoralists.
Am J Hum Genet 2006, 78(2):202-221.
Slatkin M: A measure of population subdivision based on microsatellite allele frequencies. Genetics 1995, 139(1):457-462.
Schneider S, Roessli D, Excoffier L: Arlequin: A software for population genetics data analysis. Second edition. Geneva, Switzerland: University of Geneva; 2000.
Kayser M, Krawczak M, Excoffier L, Dieltjes P, Corach D, Pascali V,
Gehrig C, Bernini LF, Jespersen J, Bakker E, et al.: An extensive
analysis of Y-chromosomal microsatellite haplotypes in globally dispersed human populations. Am J Hum Genet 2001,
68(4):990-1018.
Zhivotovsky LA, Underhill PA, Cinnioglu C, Kayser M, Morar B, Kivisild T, Scozzari R, Cruciani F, Destro-Bisol G, Spedini G, et al.: The
effective mutation rate at Y chromosome short tandem
repeats, with application to human population-divergence
time. Am J Hum Genet 2004, 74(1):50-61.
Qamar R, Ayub Q, Mohyuddin A, Helgason A, Mazhar K, Mansoor A,
Zerjal T, Tyler-Smith C, Mehdi SQ: Y-chromosomal DNA variation in Pakistan. Am J Hum Genet 2002, 70(5):1107-1124.
Bandelt HJ, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16(1):37-48.

Page 8 of 9
(page number not for citation purposes)

BMC Genetics 2009, 10:59

30.

31.
32.

33.

34.

35.

36.

37.

38.
39.

40.

41.

42.

http://www.biomedcentral.com/1471-2156/10/59

Underhill PA, Passarino G, Lin AA, Shen P, Mirazon Lahr M, Foley RA,
Oefner PJ, Cavalli-Sforza LL: The phylogeography of Y chromosome binary haplotypes and the origins of modern human
populations. Ann Hum Genet 2001, 65(Pt 1):43-62.
Underhill PA, Kivisild T: Use of y chromosome and mitochondrial DNA population structure in tracing human migrations. Annu Rev Genet 2007, 41:539-564.
Semino O, Magri C, Benuzzi G, Lin AA, Al-Zahery N, Battaglia V, Maccioni L, Triantaphyllidis C, Shen P, Oefner PJ, et al.: Origin, diffusion,
and differentiation of Y-chromosome haplogroups E and J:
inferences on the neolithization of Europe and later migratory events in the Mediterranean area. Am J Hum Genet 2004,
74(5):1023-1034.
Chiaroni J, King R, Underhill P: Correlation of annual precipitation with human Y-chromsome diversity and emergence of
Neolithic agricultural and pastoral economies in the Fertile
Crescent. Antiquity 2008, 82:281-289.
Di Giacomo F, Luca F, Popa LO, Akar N, Anagnou N, Banyko J,
Brdicka R, Barbujani G, Papola F, Ciavarella G, et al.: Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Europe. Hum Genet 2004, 115(5):357-371.
Cruciani F, La Fratta R, Santolamazza P, Sellitto D, Pascone R, Moral
P, Watson E, Guida V, Colomb EB, Zaharova B, et al.: Phylogeographic analysis of haplogroup E3b (E-M215) y chromosomes
reveals multiple migratory events within and out of Africa.
Am J Hum Genet 2004, 74(5):1014-1022.
Richards M, Rengo C, Cruciani F, Gratrix F, Wilson JF, Scozzari R,
Macaulay V, Torroni A: Extensive female-mediated gene flow
from sub-Saharan Africa into near eastern Arab populations.
Am J Hum Genet 2003, 72(4):1058-1064.
Weale ME, Shah T, Jones AL, Greenhalgh J, Wilson JF, Nymadawa P,
Zeitlin D, Connell BA, Bradman N, Thomas MG: Rare deep-rooting Y chromosome lineages in humans: lessons for phylogeography. Genetics 2003, 165(1):229-234.
Maca-Meyer N, Gonzalez AM, Larruga JM, Flores C, Cabrera VM:
Major genomic mitochondrial lineages delineate early
human expansions. BMC Genet 2001, 2:13.
Maca-Meyer N, Gonzalez AM, Pestano J, Flores C, Larruga JM,
Cabrera VM: Mitochondrial DNA transit between West Asia
and North Africa inferred from U6 phylogeography. BMC
Genet 2003, 4:15.
Reidla M, Kivisild T, Metspalu E, Kaldma K, Tambets K, Tolk HV, Parik
J, Loogvali EL, Derenko M, Malyarchuk B, et al.: Origin and diffusion
of mtDNA haplogroup X.
Am J Hum Genet 2003,
73(5):1178-1190.
Olivieri A, Achilli A, Pala M, Battaglia V, Fornarino S, Al-Zahery N,
Scozzari R, Cruciani F, Behar DM, Dugoujon JM, et al.: The mtDNA
legacy of the Levantine early Upper Palaeolithic in Africa.
Science 2006, 314(5806):1767-1770.
Gonzalez AM, Larruga JM, Abu-Amero KK, Shi Y, Pestano J, Cabrera
VM: Mitochondrial lineage M1 traces an early human backflow to Africa. BMC Genomics 2007, 8:223.

Publish with Bio Med Central and every
scientist can read your work free of charge
"BioMed Central will be the most significant development for
disseminating the results of biomedical researc h in our lifetime."
Sir Paul Nurse, Cancer Research UK

Your research papers will be:
available free of charge to the entire biomedical community
peer reviewed and published immediately upon acceptance
cited in PubMed and archived on PubMed Central
yours — you keep the copyright

BioMedcentral

Submit your manuscript here:
http://www.biomedcentral.com/info/publishing_adv.asp

Page 9 of 9
(page number not for citation purposes)

</pre>
</body>
</html>