Whole-genome sequencing of Bantu-speakers from Angola and Mozambique reveals complex dispersal patterns and interactions throughout sub-Saharan Africa

Abstract

As the continent of origin for our species, Africa harbours the highest levels of diversity anywhere on Earth. This trove of diversity provides rich opportunities to discover unknown genomic variation and explore how human populations have moved and interacted on the continent over thousands of years. However, many regions of Africa remain under-sampled. Here we present the first collection of whole genomes from Angola and Mozambique, enabling the construction of a high-quality reference variation catalogue including three million novel SNPs. Leveraging the power and flexibility of whole-genome sequencing data, we model the development and continuity of Bantu-population structure through time, admixture events involving source populations from these regions across sub-Saharan Africa, and the heterogeneous population histories of Western and South-Eastern Bantu-speakers. In contrast to depictions of the Bantu expansion as a single, continuous macro-event, we recover evidence of admixture among distinct Bantu-speaking groups in South-Eastern Africa and bring together concordant patterns from linguistics and archaeology to paint a more complex picture of Iron-Age migrations into the region. Moreover, we generate reference panels that better represents the complete diversity of African populations involved in the Atlantic slave trade, improving imputation accuracy in African Americans and Brazilians over the 1000 Genomes Project panel alone. This study fills important gaps in the current record of global genetic diversity and informs on the most significant demographic events in the recent history of Africa. We anticipate that our collection of genomes will form the foundation for future genomic healthcare initiatives involving under-represented communities in Angola and Mozambique.

Evolutionary Genetics and Admixture in African Populations

“…Furthermore, uniparental markers and X chromosomal and autosomal data suggest male-biased seBSPs contributions and female-biased Khoe-San contributions ( Bajić et al 2018 ; Sengupta et al 2021 ). In contrast to the admixture in South Africa, seBSPs appeared to have replaced resident hunter–gatherer populations in Malawi and Mozambique with present-day individuals deriving ≥97% of their ancestry from the Bantu expansion ( Skoglund et al 2017 ; Tallman et al 2022 ). Overall, this suggests multiple migration waves of Bantu speakers or that Khoe-San admixture did not occur immediately.…”

“…In South Africa, seBSPs received between 1.5% (e.g., the Tsonga) and 20% (e.g., the Tswana) gene flow from Khoe-San groups during independent admixture events ( Sengupta et al 2021 ). The exact admixture timings differ between populations (1.7 kya–700 ya), with northern groups showing older dates than southern groups ( Sengupta et al 2021 ; Tallman et al 2022 ). However, Tallman et al (2022) also reported an older Khoe-San admixture event in the Zulu ∼3 kya.…”

“…The exact admixture timings differ between populations (1.7 kya–700 ya), with northern groups showing older dates than southern groups ( Sengupta et al 2021 ; Tallman et al 2022 ). However, Tallman et al (2022) also reported an older Khoe-San admixture event in the Zulu ∼3 kya. Furthermore, uniparental markers and X chromosomal and autosomal data suggest male-biased seBSPs contributions and female-biased Khoe-San contributions ( Bajić et al 2018 ; Sengupta et al 2021 ).…”

“…In western Africa, wBSPs asymmetrically mixed with resident RHG groups, with RHG groups receiving higher amounts of gene flow from wBSPs ( Jarvis et al 2012 ; Hsieh, Veeramah, et al 2016 ; Patin et al 2017 ; Lopez et al 2018 ). wBSPs in Angola have small amounts of RHG-related ancestry from an admixture event that occurred after the split of BSPs ∼800 ya ( Patin et al 2017 ), although a recent study inferred a more ancient admixture date of ∼1.9 kya for Bantu speakers in Cabinda, Angola ( Tallman et al 2022 ). The amount of gene flow from wBSPs into individual RHG groups varied.…”

“…Genetic studies of uniparental and autosomal markers initially suggested that BSPs are largely genetically homogenous groups of people (i.e., F ST ≤ 0.02) ( Coelho et al 2009 ; Ansari-Pour et al 2013 ; Gurdasani et al 2015 ; Busby et al 2016 ). Despite the modest F ST values, fine-scale population structure of BSPs has recently been emphasized ( Semo et al 2020 ; Sengupta et al 2021 ; Tallman et al 2022 ). Semo et al (2020) showed that eBSPs from Mozambique and Angola form a North–South genetic cline of relatedness along the coast from Kenya/Tanzania to South Africa.…”