African evolutionary history inferred from whole genome sequence data of 44 indigenous African populations

Abstract

Background: Africa is the origin of modern humans within the past 300 thousand years. To infer the complex demographic history of African populations and adaptation to diverse environments, we sequenced the genomes of 92 individuals from 44 indigenous African populations.

Results: Genetic structure analyses indicate that among Africans, genetic ancestry is largely partitioned by geography and language, though we observe mixed ancestry in many individuals, consistent with both short- and long-range migration events followed by admixture. Phylogenetic analysis indicates that the San genetic lineage is basal to all modern human lineages. The San and Niger-Congo, Afroasiatic, and Nilo-Saharan lineages were substantially diverged by 160 kya (thousand years ago). In contrast, the San and Central African rainforest hunter-gatherer (CRHG), Hadza hunter-gatherer, and Sandawe hunter-gatherer lineages were diverged by ~ 120-100 kya. Niger-Congo, Nilo-Saharan, and Afroasiatic lineages diverged more recently by ~ 54-16 kya. Eastern and western CRHG lineages diverged by ~ 50-31 kya, and the western CRHG lineages diverged by ~ 18-12 kya. The San and CRHG populations maintained the largest effective population size compared to other populations prior to 60 kya. Further, we observed signatures of positive selection at genes involved in muscle development, bone synthesis, reproduction, immune function, energy metabolism, and cell signaling, which may contribute to local adaptation of African populations.

Conclusions: We observe high levels of genomic variation between ethnically diverse Africans which is largely correlated with geography and language. Our study indicates ancient population substructure and local adaptation of Africans.

Keywords: African populations; Demographic history; Effective population size; Genomic variation; Human evolution; Local adaptation; Whole genome sequencing.

Fig. 1

Locations of samples included in this study. Each dot is an individual and the color indicates the language classification

Fig. 2

Phylogenetic relationship of 44 African and 32 west Eurasian populations determined by a neighbor joining analysis assuming no admixture. Here, the dots of each node represent bootstrap values and the color of each branch indicates language usage of each population. Human_AA human ancestral alleles

Fig. 3

Principal component analysis of 44 African and 32 west Eurasian populations using principal component analysis. Each dot represents an individual and color of dots represents language usage. PC1 separates the African and western Eurasian populations, with Middle-Eastern populations in between. PC2 distinguishes the San populations (both Khomani San and Juǀ’hoan) from other Africans. CRHG individuals (including both eastern and western CRHG) separate with other Africans at PC3

Fig. 4

ADMIXTURE analysis of 92 African and 62 West Eurasian individuals. Each bar is an individual and colors represent the proportion of inferred ancestry from K ancestral populations. The bottom bar shows the language classification of each individual. K = 2 separates the African and West Eurasian populations. African hunter-gatherer populations Khomani San, Ju|’hoan, Sandawe, Hadza, and CRHG populations are distinguished from the rest of the populations at K = 3 (yellow bar). From K = 5, CRHG populations emerge as a single cluster. With the increasing of K, the populations are largely grouped by their current language usage

Fig. 5

Effective population size inferred using MSMC. Each line represents the average effective population size per population, and the colors represent language usage, except for the CRHG populations. Here, we assume a mutation rate per generate (v) 1.25 × 10⁻⁸ and average generation time (g) 29 years. a–d The effective population size of Khoesan-, Niger-Congo-, Nilo-Saharan-, and Afroasiatic-speaking populations

Fig. 6

Relative cross-coalescence rate (RCCR) in African populations. Between the San and non-Khoesan-speaking populations (a); between the San and other African hunter-gatherer populations (b); between the CRHG populations and between the Hadza and Sandawe populations (c); between the Nilo-Saharan-, Niger-Congo-, and Afroasiatic-speaking populations (d)