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. 2016 Feb;26(2):151-62.
doi: 10.1101/gr.191478.115. Epub 2016 Jan 4.

Indigenous Arabs Are Descendants of the Earliest Split From Ancient Eurasian Populations

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Free PMC article

Indigenous Arabs Are Descendants of the Earliest Split From Ancient Eurasian Populations

Juan L Rodriguez-Flores et al. Genome Res. .
Free PMC article

Abstract

An open question in the history of human migration is the identity of the earliest Eurasian populations that have left contemporary descendants. The Arabian Peninsula was the initial site of the out-of-Africa migrations that occurred between 125,000 and 60,000 yr ago, leading to the hypothesis that the first Eurasian populations were established on the Peninsula and that contemporary indigenous Arabs are direct descendants of these ancient peoples. To assess this hypothesis, we sequenced the entire genomes of 104 unrelated natives of the Arabian Peninsula at high coverage, including 56 of indigenous Arab ancestry. The indigenous Arab genomes defined a cluster distinct from other ancestral groups, and these genomes showed clear hallmarks of an ancient out-of-Africa bottleneck. Similar to other Middle Eastern populations, the indigenous Arabs had higher levels of Neanderthal admixture compared to Africans but had lower levels than Europeans and Asians. These levels of Neanderthal admixture are consistent with an early divergence of Arab ancestors after the out-of-Africa bottleneck but before the major Neanderthal admixture events in Europe and other regions of Eurasia. When compared to worldwide populations sampled in the 1000 Genomes Project, although the indigenous Arabs had a signal of admixture with Europeans, they clustered in a basal, outgroup position to all 1000 Genomes non-Africans when considering pairwise similarity across the entire genome. These results place indigenous Arabs as the most distant relatives of all other contemporary non-Africans and identify these people as direct descendants of the first Eurasian populations established by the out-of-Africa migrations.

Figures

Figure 1.
Figure 1.
Principal component analysis (PCA) (Price et al. 2006) of the 104 Qatari genomes (circle), 1000 Genomes (triangle), and Human Origins (square) study samples. Shown are individuals plotted on principal components PC1 and PC2, with genomes color-coded by study and population, with the Q0 (Subpopulation Unassigned) in gray, Q1 (Bedouin) in red, Q2 (Persian-South Asian) in azure, and Q3 (African) in black. (A) Plot of all populations, defined by study and by population, in which all populations from the same region and study are grouped and color-coded together (1000 Genomes: Africa, America, East Asia, and Europe; Human Origins: Africa, America, Central Asia/Siberia, East Asia, Middle East, Oceania, South Asia, and West Eurasia). (B) Plot of Middle Eastern subpopulations from Human Origins that cluster near Q1 (Bedouin) and Q2 (Persian-South Asian).
Figure 2.
Figure 2.
Y Chromosome (Chr Y) and mitochondrial DNA (mtDNA) haplogroup assignments. The Chr Y and mtDNA haplogroups were determined for Q1 (Bedouin), Q2 (Persian-South Asian), and Q3 (African). (A) Pie charts of the haplogroup frequencies for Chr Y. (B) Pie charts of the haplogroup frequencies for mtDNA.
Figure 3.
Figure 3.
Ancient bottlenecks in the 96 Q1 (Bedouin), Q2 (Persian-South Asian), or Q3 (African) Qatari genomes (56 Q1, 20 Q2, 20 Q3) determined by pairwise sequential Markov coalescent analysis (Li and Durbin 2011). Shown is the plot of the median effective population size (y-axis) across individuals in a subpopulation versus years in the past (log scale x-axis) for the samples in the three major Qatari subpopulations: Q1 (Bedouin) in red, Q2 (Persian-South Asian) in azure, Q3 (African) in black. A single individual of European ancestry (NA12879, violet) and a single individual of African ancestry (NA19239, orange) from the 1000 Genomes Project deep-coverage pilot (The 1000 Genomes Project Consortium 2010) are shown for comparison.
Figure 4.
Figure 4.
Neanderthal ancestry in world populations. F4 ratio estimation as implemented in ADMIXTOOLS 3.0 (Patterson et al. 2012) was used to calculate the Neanderthal ancestry proportion for each population in the combined data set of Qatari genomes, the 1000 Genomes Project, and Human Origins. The F4 ratio estimates α, the proportion of Neanderthal ancestry in a population. Shown are the results for populations of interest, including highest and lowest scoring populations from each region (the 1000 Genomes Project, Africa; the 1000 Genomes Project, America; the 1000 Genomes Project, East Asia, the 1000 Genomes Project, Europe, Human Origins, Africa; Human Origins, America; Human Origins, Central Asia/Siberia; Human Origins, East Asia; Human Origins, Oceania; Human Origins, South Asia; Human Origins, West Eurasia), Middle Eastern populations (Human Origins), Q1 (Bedouin), Q2 (Persian-South Asian) and Q3 (African). Populations are color-coded by region, and a distinct color is used for each Qatari population. A full set of results is presented in Supplemental Figure 10 and Supplemental Table XI. The population codes are as in the 1000 Genomes Project (The 1000 Genomes Project Consortium 2012).
Figure 5.
Figure 5.
TreeMix (Pickrell and Pritchard 2012) hierarchical clustering analysis of the Q1 (Bedouin), Q2 (Persian-South Asian), and Q3 (African) and the 1000 Genomes Project samples. Shown is a maximum-likelihood tree of population splits inferred without subsequent migration events, in which branch lengths estimate divergence between populations (Europeans in shades of purple: CEU, FIN, GBR, IBS, TSI; East Asians in shades of brown: CHB, CHS, JPT; Africans in shades of orange: LWK, YRI, with the Q1 [Bedouin] in red, Q2 [Persian-South Asian] in azure, and Q3 [African] in black). When allowing from one to five migration events in separate TreeMix analyses, none of the admixture loops connected the Q1 (Bedouin) with any African populations (Supplemental Fig. 10), consistent with the Q1 (Bedouin) having no recent African admixture.
Figure 6.
Figure 6.
Neighbor-joining tree hierarchical clustering analysis of the combined Qatari genomes and the 1000 Genomes Project Phase 1 samples based on pairwise proportion of shared alleles calculated across the entire autosome. (A) The entire neighbor-joining tree with each of the branches leading to individuals in the 1000 Genomes samples color-coded by continent (Europeans in shades of purple: CEU, FIN, GBR, IBS, TSI; Asians in shades of brown: CHB, CHS, JPT; Africans in shades of orange: LWK, YRI, ASW; Americans in shades of green: CLM, MXL, PUR) and with the Q1 (Bedouin) in red, Q2 (Persian-South Asian) in azure, Q3 (African) in black, and Q0 (Subpopulation Unassigned) in gray. (B) Detail of the three (15%) Q2 (Persian-South Asian) that cluster with Europeans. (C) Detail of the 11 (55%) Q2 (Persian-South Asian) individuals, with three (5%) Q1 (Bedouin), one (5%) Q3 (African), and one (13%) Q0 (Subpopulation Unassigned) that cluster as an outgroup to Asians. (D) Detail of the 50 (89%) Q1 individuals, with three (15%) Q2 (Persian-South Asian), one (5%) Q3 (African), and two (25%) Q0 (Subpopulation Unassigned), that cluster outside the Africans and African Ancestry in Southwest US and that also cluster as an outgroup to all other non-African populations, indicating that they are the most distant ancestors of all non-Africans. (E) Detail showing the three (15%) Q1 (Bedouin), three (15%) Q2 (Persian-South Asian), 12 (60%) Q3 (African), and four (50%) Q0 (Subpopulation Unassigned) that do not form large clusters but are all located within the admixed cluster. (F) Detail of the one (5%) Q3 (African) that clusters between Yoruba (YRI) and Luhya (LWK).

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