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. Electronic supplementary material The online version of this article (10.1186/s13059-019-1679-2) contains supplementary material, which is available to authorized users.

Ancient Admixture into Africa from the ancestors of non-Africans

“…Consistent with previous analyses conducted with MSMC2, our estimates show high RCCR in the Late Middle Pleistocene in both the SGDP and the HGDP ( Fig. 1c,d) [48,50]. These observations confirm the existence of a substantial pulse of ancient gene flow between Eurasians (Han Chinese) and Africans.…”

“…Populations in the Afroasiatic language group show evidence of large amounts of directional migration in the Holocene (Supplemental Fig. S2), which is consistent with previous findings of relatively recent European introgression into these populations [32,50].…”

“…To validate the existence of the migration pulse, though not its direction, we next analyzed the same data using MSMC, which is widely used to estimate gene flow in the ancient past by estimating the relative cross-coalescent rate (RCCR) between two populations [22,26,28,50]. We use the updated implementation MSMC2 recommended by the authors and first published in [34].…”

“…Further clarity on the early structure and diversification of hunter-gatherer populations are necessary to interpret their interactions with Eurasian migrants. The Afroasiatic populations on the other hand show high levels of admixture, which also appears to be of much more recent origin, and it appears likely that this is the result of extensive admixture from Eurasian populations during the Holocene [32,50].…”

Acoustic regularities in infant-directed speech and song across cultures

“…Second, people with genomic imprinting disorders, which are characterized by altered parental investment behaviors, such as those related to food consumption 53,54 , also have altered music perception ability and responses to music 55,56 . Last, consistent with classic ideas in the psychology of music 57–59 substantial evidence demonstrates that lullabies, one typical form of infant-directed song, are a human universal: singing is associated with infant care across the ethnographies of a representative sample of human small-scale societies, even after correcting for reporting biases 21 , and parents use singing to calm infants in several of the most genetically distant human societies, the Hadza, Mbuti, and !Kung San hunter-gatherers of East, Central, and South Africa 60–62 . Other forms of infant-directed song, like excitatory play songs and singing games for children, also appear to be widespread 21,63 , and parents produce them often 64 .…”