A weakly structured stem for human origins in Africa

Abstract

Despite broad agreement that Homo sapiens originated in Africa, considerable uncertainty surrounds specific models of divergence and migration across the continent¹. Progress is hampered by a shortage of fossil and genomic data, as well as variability in previous estimates of divergence times¹. Here we seek to discriminate among such models by considering linkage disequilibrium and diversity-based statistics, optimized for rapid, complex demographic inference². We infer detailed demographic models for populations across Africa, including eastern and western representatives, and newly sequenced whole genomes from 44 Nama (Khoe-San) individuals from southern Africa. We infer a reticulated African population history in which present-day population structure dates back to Marine Isotope Stage 5. The earliest population divergence among contemporary populations occurred 120,000 to 135,000 years ago and was preceded by links between two or more weakly differentiated ancestral Homo populations connected by gene flow over hundreds of thousands of years. Such weakly structured stem models explain patterns of polymorphism that had previously been attributed to contributions from archaic hominins in Africa^2-7. In contrast to models with archaic introgression, we predict that fossil remains from coexisting ancestral populations should be genetically and morphologically similar, and that only an inferred 1-4% of genetic differentiation among contemporary human populations can be attributed to genetic drift between stem populations. We show that model misspecification explains the variation in previous estimates of divergence times, and argue that studying a range of models is key to making robust inferences about deep history.

Fig. 1. Proposed conceptual models of early human history in Africa.

a, Recent expansion. b, Recent expansion with regional persistence. c, Archaic admixture. d, African multiregional. The models have been designed to translate models from the palaeoanthropological literature into genetically testable demographic models (ref.  and Supplementary Information section 3). These parameters were then fitted to genetic data.

Fig. 2. Genetic diversity across Africa.

a, Selected populations from the 1000 Genomes Project and the African Diversity Reference Panel^, illustrate diversity from western, eastern and southern Africa. We chose representative ethnic groups from each region (bold labels) to build parameterized models, including the newly genetically sequenced Nama populations from South Africa, Mende from Sierra Leone, Gumuz, Oromo and Amhara from Ethiopia, British individuals and a Neanderthal from Vindija Cave, Croatia. b,c, Principal component analysis highlights the range of genetic divergence anchored by western African, Nama, Gumuz and British individuals between principal components (PC) 1 and 2 (b), and 1 and 3 (c). Percentages show variance explained by each principal component. Colours represent the groups shown in bold in a. d, ADMIXTURE analysis using K = 4 principal components reveals signatures of recent gene flow in Africa that reflect colonial-period migration into the Nama, back-to-Africa gene flow among some Ethiopians, and Khoe-San admixture in the Zulu population.

Fig. 3. A weakly structured stem best describes two-locus statistics.

a,b, In the two best-fitting parameterizations of early population structure, continuous migration (a) and multiple mergers (b), models that include ongoing migration between stem populations outperform those in which stem populations are isolated. Most of the recent populations are also connected by continuous, reciprocal migration that is indicated by double-headed arrows (labels matched to migration rates and divergence times in Table 1). These migrations last for the duration of the coexistence of contemporaneous populations with constant migration rates over those intervals. The merger-with-stem-migration model (b, with LL = −101,600) outperformed the continuous-migration model (a, with LL = −115,300). Colours are used to distinguish overlapping branches. The letters a–i represent continuous migration between pairs of populations, as described in Table 1.

Fig. 4. Structure among stems is weak and present-day structure is generally recent.

a–d, From the best-fit models of our two parameterizations (a,b, continuous migration; c,d, merger with stem migration), we predicted differentiation and shared drift between populations at past time points. a,c, We computed expected pairwise differences H_i,j between individuals sampled from populations i and j existing at time t. b,d, To understand how drift between stems explains contemporary structure, we computed the proportion α² of drift between pairs of sampled contemporary populations (here the Nama and Mende) that aligns with drift between past populations (see Supplementary Information section 5.2 for details and additional comparisons in Supplementary Figs. 16–19). Both models infer deep population structure with modest contributions to contemporary genetic differentiation. Most present-day differentiation dates back to the past 100 kyr.

Fig. 5. Model validation using independent statistics.

a–c, Using our best-fit models, we simulated expected cSFS and compared the simulated spectra to those observed from the data. Our inferred models provide a good fit to the data, even though this summary was not used in our inference. Across the three populations (a, Nama; b, Mende; c, Gumuz), ancestral-state misidentification was consistently inferred to be 1.5−1.7% for intergenic loci (Supplementary Information section 6.2.2). d,e, We used Relate to reconstruct genome-wide genealogies, which we used to estimate coalescence-rate trajectories and cross-coalescence rates between pairs of populations. Although coalescence-rate distributions are informative about past evolutionary processes, interpretation can be hindered by migration and population structure, and translating RCCR curves into population divergence times is especially prone to misinterpretation. d, Real data; e, our model. In our model, the Mende–Gumuz split occurs before the Gumuz–British split. However, the model also predicts a recent elevated Mende–Gumuz RCCR. This pattern, also observed in the data, does not indicate that the Mende and Gumuz split more recently than the Gumuz and British populations.