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Early back-to-Africa migration into the Horn of Africa - PubMed

  • ️Wed Jan 01 2014

Early back-to-Africa migration into the Horn of Africa

Jason A Hodgson et al. PLoS Genet. 2014.

Abstract

Genetic studies have identified substantial non-African admixture in the Horn of Africa (HOA). In the most recent genomic studies, this non-African ancestry has been attributed to admixture with Middle Eastern populations during the last few thousand years. However, mitochondrial and Y chromosome data are suggestive of earlier episodes of admixture. To investigate this further, we generated new genome-wide SNP data for a Yemeni population sample and merged these new data with published genome-wide genetic data from the HOA and a broad selection of surrounding populations. We used multidimensional scaling and ADMIXTURE methods in an exploratory data analysis to develop hypotheses on admixture and population structure in HOA populations. These analyses suggested that there might be distinct, differentiated African and non-African ancestries in the HOA. After partitioning the SNP data into African and non-African origin chromosome segments, we found support for a distinct African (Ethiopic) ancestry and a distinct non-African (Ethio-Somali) ancestry in HOA populations. The African Ethiopic ancestry is tightly restricted to HOA populations and likely represents an autochthonous HOA population. The non-African ancestry in the HOA, which is primarily attributed to a novel Ethio-Somali inferred ancestry component, is significantly differentiated from all neighboring non-African ancestries in North Africa, the Levant, and Arabia. The Ethio-Somali ancestry is found in all admixed HOA ethnic groups, shows little inter-individual variance within these ethnic groups, is estimated to have diverged from all other non-African ancestries by at least 23 ka, and does not carry the unique Arabian lactase persistence allele that arose about 4 ka. Taking into account published mitochondrial, Y chromosome, paleoclimate, and archaeological data, we find that the time of the Ethio-Somali back-to-Africa migration is most likely pre-agricultural.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Multidimensional scaling analysis shows the great genetic diversity within the Horn of Africa.

We plotted the first two dimensions of a multidimensional scaling analysis of pairwise identity by state across all study populations. (A) The HOA populations are broadly scattered between out-of-African populations and the bulk of sub-Saharan African populations along the first dimension. Some clusters of HOA individuals are much closer to the main sub-Saharan African cluster, while others are much closer to North African and Arabian clusters. (B) In this plot, we zoom in on the HOA samples and leave out all other populations. While the region as a whole covers a broad swath of the first MDS dimension, most individual populations are tightly clumped, with groups separated by language. The Nilo-Saharan speaking Gumuz are on the far left, the Omotic speaking Ari are in the center, and the Cushitic and Semitic speaking populations are on the right.

Figure 2
Figure 2. Population structure of Horn of Africa populations in a broad context.

ADMIXTURE analysis reveals both well-established and novel ancestry components in HOA populations. We used a cross-validation procedure to estimate the best value for the parameter for the number of assigned ancestral populations (K) and found that values from 9 to 14 had the lowest and similar cross-validation errors (Figure S2). (A) The differences in inferred ancestry from K = 9–14 are most pronounced in the HOA for K = 10–12, where two ancestry components that are largely restricted to the HOA appear (the dark purple and dark green components). (B) Surface interpolation of the geographic distribution of eight inferred ancestry components that are relatively unchanging and common to the ADMIXTURE results from K = 10–12. (C) Individual ancestry estimation for HOA populations (with language groups indicated) and surface plots of the changing distributions of the Nilo-Saharan (light blue) and Arabian (brown) ancestry components for K = 10–12. At K = 11, a new HOA-specific ancestry component that we call Ethiopic appears (dark purple) and at K = 12 a second new ancestry component that we call Ethio-Somali (dark green) appears with its highest frequencies in the HOA.

Figure 3
Figure 3. Tests of gene flow and population structure in the African ancestry of HOA populations.

Using the African origin partition of the HOA data identified in a chromosome painting analysis, we evaluated the evidence for gene flow with neighboring populations and for population structure within and between the HOA and neighboring populations. (A) Shared gene identity plotted against distance for the HOA populations and the neighboring Anuak, Gumuz, and South Sudanese. (B) Linguistically structured population tree model within the African ancestry partition of HOA populations with the FST estimate from this tree model, the goodness-of-fit statistic Λ, and the likelihood ratio test statistic K for the improvement in model fit from the unstructured tree. (C) The linguistically structured population tree model for neighboring Nilo-Saharan language family populations. (D) Structured population tree models for the combined HOA and neighboring populations.

Figure 4
Figure 4. Relationship between non-African ADMIXTURE ancestry components and shared gene identity between HOA and MENA populations.

ADMIXTURE results for K = 10,11 suggest that the non-African ancestry in HOA populations is indistinguishable from the “Maghrebi,” “Arabian,” and “Eurasian” ancestry components found in MENA populations. If this is a correct inference, then the shared gene identity of HOA populations should be higher with MENA populations with higher proportions of these ancestries. (A) There is significant positive relationship between shared gene identity and the proportion of Maghrebi ancestry in MENA populations. While there is variation across HOA populations in the overall shared gene identity (different intercepts for each population), the magnitude of the relationship is consistent (adding varying slopes did not significantly improve the model fit). This relationship holds whether or not the Mozabite (a high Maghrebi ancestry outlier) are included in the model. However, contrary to expectations, both the Arabian (B) and Eurasian (C) ancestry components showed a reduction in shared gene identity as the representation of these ancestry components in MENA populations increased.

Figure 5
Figure 5. Tests of gene flow and population structure in the non-African ancestry of HOA populations.

Using the non-African origin partition of the HOA data identified in a chromosome painting analysis, we evaluated the evidence for gene flow with MENA populations and for population structure within and between the HOA and MENA populations. (A) The only clear and statistically significant pattern of decreasing gene identity with geographic distance was between HOA populations and the Yemen and Saudi Arabia populations on the Arabian peninsula as evaluated by a Mantel test. This relationship only held for “as the crow flies” geographic distances; the relationship disappears using a waypoint through Egypt (Figure S3). (B) Shared gene identity between the non-African ancestry partition of HOA populations and MENA populations presented in increasing order. (C) Structured population tree model within the non-African ancestry partition of HOA populations with the FST estimate from this tree model, the goodness-of-fit statistic Λ, and the likelihood ratio test statistic K for the improvement in model fit from the unstructured tree. (D) Structured population tree model within the non-African ancestry partition of MENA populations. (E) Structured population tree models for the non-African ancestry partitions of both HOA and MENA populations. Both are significantly better fits to the data than the unstructured tree and the regional structure (HOA vs MENA) is a slightly better fit to the data as measured by the goodness-of-fit Λ statistic.

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Grants and funding

This work was supported by NSF BCS-0518530 to CJM and by research funds provided by the School of Natural and Social Sciences of Lehman College to RLR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.