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, 99 (6), 1316-1324

Chad Genetic Diversity Reveals an African History Marked by Multiple Holocene Eurasian Migrations

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Chad Genetic Diversity Reveals an African History Marked by Multiple Holocene Eurasian Migrations

Marc Haber et al. Am J Hum Genet.

Abstract

Understanding human genetic diversity in Africa is important for interpreting the evolution of all humans, yet vast regions in Africa, such as Chad, remain genetically poorly investigated. Here, we use genotype data from 480 samples from Chad, the Near East, and southern Europe, as well as whole-genome sequencing from 19 of them, to show that many populations today derive their genomes from ancient African-Eurasian admixtures. We found evidence of early Eurasian backflow to Africa in people speaking the unclassified isolate Laal language in southern Chad and estimate from linkage-disequilibrium decay that this occurred 4,750-7,200 years ago. It brought to Africa a Y chromosome lineage (R1b-V88) whose closest relatives are widespread in present-day Eurasia; we estimate from sequence data that the Chad R1b-V88 Y chromosomes coalesced 5,700-7,300 years ago. This migration could thus have originated among Near Eastern farmers during the African Humid Period. We also found that the previously documented Eurasian backflow into Africa, which occurred ∼3,000 years ago and was thought to be mostly limited to East Africa, had a more westward impact affecting populations in northern Chad, such as the Toubou, who have 20%-30% Eurasian ancestry today. We observed a decline in heterozygosity in admixed Africans and found that the Eurasian admixture can bias inferences on their coalescent history and confound genetic signals from adaptation and archaic introgression.

Keywords: admixture; genetic isolate; genetic structure; genome-wide SNPs; human population history; whole-genome sequencing.

Figures

Figure 1
Figure 1
Population Locations and Genetic Structure (A) The map shows the location of newly genotyped or sequenced populations. (B) PCA of worldwide populations shows that Near Easterners and East Africans are intermediate to Eurasians and sub-Saharan Africans on PC1. Chad populations are close to sub-Saharan Africans and have some samples drawn toward Ethiopians. (C) Magnification of the African PCA shows different affinities of the Chad populations to other Africans: the Toubou cluster close to Ethiopians, whereas the Sara and Laal speakers are close to the Yoruba. The mixed samples from N’Djamena, the capital, are intermediate to the Toubou, Sara, and Laal speakers.
Figure 2
Figure 2
Population-Size Estimates from Whole-Genome Sequences Population size was inferred by MSMC analysis with four haplotypes from each population. Eurasian populations had a distinctive bottleneck at the time of their exodus from Africa ∼60,000 ya. Compared to other Africans, admixed Africans (from a Eurasian gene flow), such as Egyptians, Ethiopians, and the Toubou, also showed a decline in population size during the same period.
Figure 3
Figure 3
Timing of the Eurasian Admixture in Africa (A) Crosses represent significant admixture events in the history of the Toubou, Amhara, Sara, and Laal speakers. Time of admixture is estimated from LD by ALDER with all pairs of African-Eurasian populations in our dataset as references. MALDER extends ALDER inference by detecting multiple mixture events, such as in the case of the Toubou population (shown here in green lozenges). (B) A maximum-likelihood tree shows the males belonging to haplogroup R1b in the 1000 Genomes Project and the R1b males in our dataset. The number of samples is shown on each branch tip. We estimate that the Chadian R1b emerged 5,700–7,300 ya, whereas most European R1b haplogroups emerged 7,300–9,400 ya. The African and Eurasian lineages coalesced 17,900–23,000 ya. (C) Putative sources and times of admixture of the Eurasian ancestry in Chad and East Africa.
Figure 4
Figure 4
Sources of the Eurasian Ancestry in Chad and Ethiopia The plot shows significant Eurasian sources for the Toubou and Amhara according to a three-population test (Z score < −4). An increase in the absolute value of the f3 statistic implies an increase in the genetic affinity of the Eurasian population X to the Toubou and Amhara. (A) With the exception of North Africans, who showed increased affinity to the Toubou, present-day populations showed correlated affinity to both the Toubou and Amhara. Among modern populations, Sardinians showed the highest genetic affinity to both the Toubou and Amhara. (B) Ancient Eurasians also showed correlated affinity to both the Toubou and Amhara; the early Neolithic LBK (Linearbandkeramik, or Linear Pottery) population (∼5,000 BCE) had the highest affinity.
Figure 5
Figure 5
Neanderthal Ancestry Correlation with the African-Eurasian Admixture Neanderthal ancestry is not expected in Africa, yet today many Africans carry Neanderthal-derived alleles. The plot shows that the Neanderthal ancestry proportion in Africans is correlated with gene flow from Eurasians. For example, knowing that today Eurasians carry ∼2% of Neanderthal ancestry, we observed that East Africans (Ethiopians) had ∼1% Neanderthal ancestry and ∼50% Eurasian ancestry. Correspondingly, Near Easterners showed a decline in Neanderthal ancestry proportional to their levels of African ancestry.

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