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View Full Version : Y-chromosome diversity characterizes the Gulf of Oman



Kamal900
03-12-2015, 12:05 AM
Arabia has served as a strategic crossroads for human disseminations, providing a natural connection between the distant populations of China and India in the east to the western civilizations along the Mediterranean. To explore this region's critical role in the migratory episodes leaving Africa to Eurasia and back, high-resolution Y-chromosome analysis of males from the United Arab Emirates (164), Qatar (72) and Yemen (62) was performed. The role of the Levant in the Neolithic dispersal of the E3b1-M35 sublineages is supported by the data, and the distribution and STR-based analyses of J1-M267 representatives points to their spread from the north, most likely during the Neolithic. With the exception of Yemen, southern Arabia, South Iran and South Pakistan display high diversity in their Y-haplogroup substructure possibly a result of gene flow along the coastal crescent-shaped corridor of the Gulf of Oman facilitating human dispersals. Elevated rates of consanguinity may have had an impact in Yemen and Qatar, which experience significant heterozygote deficiencies at various hypervariable autosomal STR loci.

Arabia has played the role of a strategic crossroads between Africa and Eurasia, facilitating the first exodus of modern humans from the Horn of Africa to the present day Yemen through the Bab el Mandab Strait at mouth of the Red Sea.1, 2, 3 Subsequent migrations through the northern intercontinental passageway between Africa and the Levant (the Levantine corridor) have also been documented.4, 5 In addition, the Arabian Peninsula has linked the distant populations of China and India to communities of the Mediterranean and beyond. Although the Persian Gulf to the east and the Arabian Sea to the south offered easy passages to India and Asia, the Red Sea on the western coast of the Arabian Peninsula provided a natural connection to the Mediterranean Sea.

Just north of the peninsula, the Nile River Valley in Egypt and the Tigris–Euphrates area in Iraq comprised a region known as the Fertile Crescent. Recognized as the birthplace of agriculture during the Neolithic (~8000 yBP) based on linguistic and archaeological evidence,6, 7 the Fertile Crescent participated in ancient international trade. Although the fertile soils produced a surplus of food, the region lacked the natural resources necessary for building permanent structures (timber) or making metals (minerals). Therefore, early inhabitants relied on trade to acquire these raw materials and established close links with the commercial centers along the Persian Gulf as reflected in archaeological finds.8, 9, 10 At the extreme southern end of the Arabian Peninsula, referred to as Arabia Felix by the Romans (‘Happy Arabia’ in Latin) and including present day Yemen, the spice trade was an important source of wealth. Frankincense and myrrh were commonly exported to the Mediterranean via camels and to India by sea.

In agreement with archaeological and historical records that accentuate the region's active role as a point of contact between distant populations, the Middle East displays a high degree of genetic diversity.11, 12, 13, 14 Although genetic diversity is elevated, various analyses have identified structural barriers to gene flow into and out of the Near East. Specifically, mtDNA,15 Y-chromosome14, 16, 17, 18 and autosomal STR studies19 have identified the Dasht-e Kavir and Dash-e Lut deserts in Iran and the Hindu Kush mountains in eastern Afghanistan as potential barriers to gene flow to the surrounding regions. In contrast, geographic facilitators for gene flow have also been described, including a region along the southern coast of Iran, Afghanistan and Pakistan known as Balochistan mediating gene flow from South Pakistan to South Iran.14

Mitochondrial DNA analyses have been performed on collections from Qatar, United Arab Emirates (UAE) and Yemen,5, 20 yet the paternal component of this historically and geographically significant region is incomplete. Although Y-chromosome studies have focused on neighboring areas, including Egypt,4 Somalia,21 Iraq,22 Syria and Lebanon23 as well as on the southern Arabian populations of Oman4 and Yemen,24 high resolution Y-chromosome analyses of the Persian and Oman Gulfs are fragmentary.

Results

A total of 41 paternal haplogroups were identified from the analysis of 164 United Arab Emirate, 72 Qatari and 62 Yemeni males. Figure 1 displays their hierarchical phylogeny as well as the frequency (percentages) distributions for the populations under study. The geographic distribution of the major haplogroups is illustrated in Figure 2. Only three haplogroups (E, J and R) display frequencies above 5% in the three populations occupying the southern portion of the Arabian Peninsula and combined account for 74–98% of the chromosomes within these collections. Figure 3 displays the geographic distribution of E, J and R derivatives in a subset of the populations listed in Table 1.

Figure1:
http://www.nature.com/ejhg/journal/v16/n3/images/5201934f1.jpg

Figure2:
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An MDS test was performed to assess phylogenetic relationships among populations. The MDS analysis performed on a matrix of Fst values based on haplogroup frequencies for the populations in Table 1 is displayed in Figure 4. Geographic structuring is observed involving populations displaying affiliations with other populations within their biogeographic zone. Within the plot, the populations of Egypt, Iraq, Yemen, Qatar, Oman, UAE, Syria and Lebanon occupy an intermediate position with populations from Africa to one side and Anatolia, Caucasus, Iranian Plateau, Central Asia and South Asia on the other. Of note, for the observed partitioning is the affinity of Egypt to populations from the Arabian Peninsula. Furthermore, Yemen and Qatar segregate together but separate from their neighboring populations, Oman and UAE particularly along Dimension 2. As expected, the populations from Central Asia group together and away from the South Asian ones, however, there is a segregation of North Pakistan with populations from Central Asia, whereas South Pakistan shares a closer affinity to populations to the west.

http://www.nature.com/ejhg/journal/v16/n3/images/5201934f4.gif

Analyses of the South Arabian Y-haplogroup substructure as well as the region's phylogenetic relationships to neighboring populations have provided us information on the following points: (1) support of the role of the Levant in the Neolithic dispersal of the E3b1-M35 derivatives, (2) neolithic spread of the J1-M267 haplogroup from the north, (3) a high haplogroup diversity shared among populations along the eastern and western coasts of the Gulf of Oman and (4) a limited haplogroup diversity in Yemen also supported by significant heterozygote deficiencies at various hypervariable autosomal STR loci.

The presence of signature sub-Saharan African mtDNA lineages in the south Arabian populations has been attributed to various waves of gene flow to the region, including that associated with the East African slave trade. This is apparent from the exact mtDNA haplotype matches between lineages in Yemen and East Africa, including those associated with the Bantu expansion. The presence of the E3a-M2 lineage in Oman (7.4%),4 Yemen (3.2%), UAE (5.5%) and Qatar (2.8%) could lead to the oversimplified conclusion that these chromosomes are also a contribution from the East African slave trade. Mitochondrial DNA analysis of the Yemen Hadramawt indicates recent gene flow (~2500 yBP) from Africa to the Arab populations in part through the slave trade, yet an ancient arrival from East Africa is responsible for the Y-chromosome haplotypes.54 The contrast between female- versus male-mediated gene flow between these two areas can be attributed to the assimilation of females within the Arabian populations, whereas the males were often excluded from reproductive opportunities. The E3b1-M35 sub-haplogroups, M123 and M78, are believed to have spread from East Africa to North Africa and later expanded eastward through the Levantine corridor and westward to northwestern Africa. Although E3b1a-M78 data suggest that this dispersal occurred in both directions,4, 34, 47 E3b1c-M123 disseminated primarily to the east.4 The distribution of the E3b1-M35 derivatives in Yemen, Qatar and UAE agrees with their arrival by expansion via the Levantine corridor rather than through the Horn of Africa. This route is similar to general patterns of Levantine mtDNA gene flows during the Upper Paleolithic55 to the Neolithic.5, 55 This is immediately apparent by the M35 profile of several East African populations. Despite characterizing the East African populations and persisting even after introduction of E3a-M2 during the Bantu expansion, E3b1*-M35 is completely absent from the Omani,4 Qatari and UAE collections and relatively low in the Yemeni (3.2%). Kenya, Sudan and Tanzania4 also lack the E3b1c-M123 derivative that is common in the Near East.

The median expansion time for M123 in Egypt is 10.8 ky,4 comparable to the estimated age of M123 STR variation obtained through the method described by Zhivotovsky et al46 for UAE (11.1±3.9 ky) and Yemen (10.6±4.1 ky), although allelic differences between these two populations indicate that they do not share a common ancestry. Recent archaeological finds supports a trading relationship between Mesopotamia and the Arabian Gulf region dating back to the Al Ubaid Period (~7000 yBP) as evidenced by the excavation of Ubaid pottery from Mesopotamia in UAE.8, 9, 10 Ancient maritime trade routes linking Mesopotamia to the Indus Valley included Dilmun (the island of Bahrain) and Magan (in the southeastern tip of the Arabian Peninsula). It is possible that the close ties between Mesopotamia with both the Nile River Valley and the ancient Persian Gulf region during the Neolithic helped disseminate these haplogroups.

UAE is characterized by polymorphic levels of E3b1a-M78 (7.9%), similar to the Qatari (4.2%; χ2=1.12, d.f.=1, P=0.29), with lower values in Oman4 (1.7%; χ2=5.49, d.f.=1, P=0.02) and greater frequencies in Egypt4 (18%; χ2=6.73, d.f.=1, P=0.01) where it is the highest M35 derivative. The majority of the UAE M78 representatives belong to the E3b1a3-V22 clade (6.7%). STR networks of this newly defined marker indicate that it parallels the M78 haplotype cluster δ, although some discrepancies exist.36 Based on the distribution and high STR differentiation of cluster δ, its dispersal may have occurred early, the first to spread the E3b1a-M78 chromosomes to North Africa and then the Near East.

Previous studies on haplogroup J1-M267 have documented high frequencies of this haplogroup in the areas of Oman (38%),4 Iraq (33.1%),22 Egypt (20%),4 Lebanon (12.5%)23 and Turkey (8.99%).12 The combination of these data with the high frequency of J1-M267 in the Yemeni (72.6%), Qatari (58.3%) and UAE (34.8%) samples examined in the present study reveals a decreasing frequency moving from southern Arabia northwards (Spearman's correlation coefficient with ranks based on distance from Yemen: r=0.9286, n=8, P<0.01). It is also distributed throughout the northwestern African populations at considerable frequencies (35.0 and 30.1% in Algeria and Tunisia, respectively).

Based on binary and STR markers, the greatest degree of differentiation for J1-M267 is detected in the Levant with two distinct demographic dispersals generating its current distribution. A higher observed STR diversity of this clade among Europeans and Ethiopians in comparison to populations of North Africa points to its arrival to Ethiopia and Europe during Neolithic times with a more recent appearance in the latter.58 Semino et al58 describe a YCAIIa22-YCAIIb22 motif in the North African (>90%) and Middle Eastern (>70%) J1-M267 representatives that is less frequent in Ethiopia and Europe, postulating that the dispersal of the M267-YCAIIa22-YCAIIb22 clade occurred during the Arab expansion in the seventh century A.D.

Median BATWING expansion times based on Y-STR data for the Omani (2.3 ky; 95% CI: 0.6–29.2) J1-M267 chromosomes4 indicate a more recent arrival to the South Arabian populations as compared to the older expansion times obtained for the Egyptian (6.4 ky; 95% CI: 0.6–278.5)4 and Turkish (15.4 ky; 95% CI: 0.4–604.8)12 representatives of this haplogroup. Conversely, in the present study, Y-STR age estimates based on the method described by Zhivotovsky et al46 generated much older values for the J1-M267 haplogroup in Yemen, Qatar and UAE (9.7±2.4, 7.4±2.3 and 6.4±1.4 ky, respectively) than seen in the Omani,4 consistent with an earlier arrival to the region during the Neolithic.

To examine the degree and geographic extent of genetic homogeneity within the Gulf of Oman, the frequency of the predominant haplogroups were contrasted among the populations in the region. A χ2-test on the haplogroup frequencies of Oman, UAE, South Iran14 and South Pakistan30 indicates that the most frequent haplogroups, E (χ2=20.836, d.f.=3, P<0.0001), J (χ2=8.677, d.f.=3, P=0.0339) and R (χ2=40.142, d.f.=3, P<0.0001) are not evenly distributed among the four populations. As the MDS plot displayed a close affiliation between South Pakistan and North Iran and the former segregated away from the Gulf of Oman populations, the χ2-test was repeated excluding South Pakistan. Although statistically significant differences are still apparent for haplogroup E (χ2=10.170, d.f.=2, P=0.0062) and R (χ2=10.560, d.f.=2, P=0.0051), J (χ2=2.577, d.f.=2, P=0.2757) exhibits an even distribution among Oman, UAE and South Iran.

In addition, South Pakistan, South Iran, UAE, Oman and Qatar (although to a lesser extent) share a similar Y-haplogroup substructure with clinal decreases in diversity detected as one moves west to Africa, north to the Levant and Caucasus and east to south and central Asia (Figure 2). Although the Hindu Kush Mountains and Iranian deserts may have played a significant role in encapsulating the region and limiting gene flow,14, 25 the coastal area may have served as a unique corridor facilitating dispersals into and out of the region at various times in recent human evolution.

Conclusion

A comparison of Y-haplogroup substructure of the populations surrounding the Gulf of Oman reveals similarities among them with detectable clines in haplogroup frequencies. This can be attributed to the existence at different times of a coastal corridor along the Gulf of Oman that may have facilitated dispersals into and out of the area. Chromosomes like E3b1c-M123 support archaeological data linking the Fertile Crescent with trading cities along the Persian Gulf, whereas derivatives of E3b1-M35 point to a Neolithic arrival to southern Arabia via the Levant. The limited variability seen in Yemen (and to some extent Qatar) does not mirror the diversity observed in the coastal populations of UAE, Oman, South Iran and South Pakistan. An analysis of heterozygosity using hypervariable autosomal STR loci indicates that both Yemen and Qatar display a deficiency in observed heterozygosity that may be affected to some extent by high rates of consanguineous marriages in the region. In addition, a string of relatively recent events may have maintained Oman and UAE in close contact with other cultures, including attempts to gain control of the Persian Gulf and Oman's involvement in the East African slave trade.

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