Hunter-gatherer genomes reveal diverse demographic trajectories during the rise of farming in Eastern Africa

Abstract

The fate of hunting and gathering populations following the rise of agriculture and pastoralism remains a topic of debate in the study of human prehistory. Studies of ancient and modern genomes have found that autochthonous groups were largely replaced by expanding farmer populations with varying levels of gene flow, a characterization that is influenced by the almost universal focus on the European Neolithic.^1-5 We sought to understand the demographic impact of an ongoing cultural transition to farming in Southwest Ethiopia, one of the last regions in Africa to experience such shifts.⁶ Importantly, Southwest Ethiopia is home to several of the world's remaining hunter-gatherer groups, including the Chabu people, who are currently transitioning away from their traditional mode of subsistence.⁷ We generated genome-wide data from the Chabu and four neighboring populations, the Majang, Shekkacho, Bench, and Sheko, to characterize their genetic ancestry and estimate their effective population sizes over the last 60 generations. We show that the Chabu are a distinct population closely related to ancient people who occupied Southwest Ethiopia >4,500 years ago. Furthermore, the Chabu are undergoing a severe population bottleneck, which began approximately 1,400 years ago. By analyzing eleven Eastern African populations, we find evidence for divergent demographic trajectories among hunter-gatherer-descendant groups. Our results illustrate that although foragers respond to encroaching agriculture and pastoralism with multiple strategies, including cultural adoption of agropastoralism, gene flow, and economic specialization, they often face population decline.

Keywords: Eastern Africa; Neolithic transition; Southwest Ethiopia; agriculture; hunter-gatherers.

Figure 1.. Global Ancestry Proportions of Individuals Inferred from Unsupervised Clustering of Genotype Data.

A) Each color corresponds to one of the K=7 hypothesized genetic components, and each vertical bar represents one individual genome (Bayira bar is widened for visualization). Population labels include linguistic codes in brackets; Afro-Asiatic (AA), Niger-Congo (NC), Nilo-Saharan (NS), linguistic isolates (I). Within Afro-Asiatic speakers, we further differentiate between Chadic (Ch), Cushitic (Cu), Egyptian (E), Omotic (O), and Semitic (S) speakers. For panels B-F) The geographic distributions for 5 of these ancestry components are depicted, with the intensity of the color corresponding to the mean population proportion of the respective ancestry. Each component is labeled below the map. G) The effective migration surface, inferred from the rate of decay of genetic similarity across geographic space, is depicted. Cool colors correspond to effective migration corridors, while warm colors correspond to effective migration barriers. See also Figures S1 and S2 and Table S1.

Figure 2.. Population Structure and F3 Outgroup Estimates for Modern and Ancient Individuals.

A) A principal component analysis (PCA) of genotype data from modern populations from Eastern Africa and the Near East, with ancient DNA samples superimposed, for PC1 and PC2. Bayira falls close to the Chabu cluster, which anchors the second PC. B) As in panel A, but for PC1 and PC3. In the first and third PCs, the Chabu lie near other modern and ancient hunter-gatherers. F3 outgroup tests for X, listed in each row, for shared drift with C) ancient Bayira or D) the Chabu relative to the Yoruba. E) The Anuak, a Nilo-Saharan-speaking Ethiopian group have higher F3 outgroup statistics with the Majang and Gumuz than with the Dinka or Shilluk, despite having a high proportion of NS ancestry (Figure 1A). The F3 outgroup statistic indicates that, among extant populations, Bayira is most closely related to the Aari Blacksmiths, Aari Cultivators, Bench, and Sheko, followed by the Chabu; conversely, the Chabu carry the most shared drift with their Majang neighbors, followed by Bayira.

Figure 3.. Distributions of the Total Amount of the Genome in Runs of Homozygosity (RoH) in Southwest Ethiopian Populations.

RoH are represented by colored violins for A) all RoH segments and B) separate RoH size classes. The white point represents the median value of the distribution, and the black rectangle represents values between the lower and upper quartiles. The thin black ‘whiskers’ extend to data points that lie within 1.5 times the interquantile range below or above the lower and upper quantiles, respectively. The Chabu and Aari Blacksmiths showed significantly elevated total RoH in only the longest class suggesting that these populations’ genomic signatures of isolation and demographic decline are a result of relatively recent events. See also Figure S3.

Figure 4.. Divergent Demographic Trajectories for Eastern and Central African Populations over the Past 2,000 Years.

Historical effective population sizes (N_e), from 4 to 60 generations ago, were inferred from distributions of identical-by-descent segments >4 cM among pairs of individuals. Shown from the upper left are the Chabu, the Majang and Gumuz, the Aari populations, the Bench and Sheko, the Shekkacho and Wolyata, and the Hadza and Sandawe hunter-gatherers of Tanzania. Filled circles represent the estimated N_e at a given generation. Colored ribbons indicate bootstrapped confidence intervals around these estimates. Note that the y-axis scale changes across panels and is on a log scale for the Shekkacho/Wolyata panel.