The Genes of Freedom: Genome-Wide Insights into Marronage, Admixture and Ethnogenesis in the Gulf of Guinea

Abstract

The forced migration of millions of Africans during the Atlantic Slave Trade led to the emergence of new genetic and linguistic identities, thereby providing a unique opportunity to study the mechanisms giving rise to human biological and cultural variation. Here we focus on the archipelago of São Tomé and Príncipe in the Gulf of Guinea, which hosted one of the earliest plantation societies relying exclusively on slave labor. We analyze the genetic variation in 25 individuals from three communities who speak distinct creole languages (Forros, Principenses and Angolares), using genomic data from expanded exomes in combination with a contextual dataset from Europe and Africa, including newly generated data from 28 Bantu speakers from Angola. Our findings show that while all islanders display mixed contributions from the Gulf of Guinea and Angola, the Angolares are characterized by extreme genetic differentiation and inbreeding, consistent with an admixed maroon isolate. In line with a more prominent Bantu contribution to their creole language, we additionally found that a previously reported high-frequency Y-chromosome haplotype in the Angolares has a likely Angolan origin, suggesting that their genetic, linguistic and social characteristics were influenced by a small group of dominant men who achieved disproportionate reproductive success.

Keywords: African populations; São Tomé and Príncipe; WES; expanded exome sequences; slave trade; social selection.

Figure 1

Genetic structure in groups from São Tomé and Príncipe in relation to European and mainland African populations. (a) Geographic locations of sampled individuals from São Tomé and Príncipe, and populations on the African continent. In the inset, the distance between São Tomé (larger island) and Príncipe (smaller island) is not to scale. (b,c) Haplotype-based principal component analysis performed with CHROMOPAINTER/fineSTRUCTURE; (b) PC1 and PC2 plot; (c) PC1 and PC3 plot. (d) ADMIXTURE analysis assuming 4 clusters (K). Each individual is represented as a vertical line divided according to the proportion of its genome that is derived from the assumed genetic clusters. Although the lowest cross-validation error (CV) was associated with K = 2, the differentiation between African mainland populations is evident only from K = 4. Additional PCA and ADMIXTURE plots are shown in Supplementary Figures S2 and S3.

Figure 2

Ancestry inference in the studied populations. (a) CHROMOPAINTER coancestry matrix based on the number of haplotype segments (chromosome chunks) shared between donor (columns) and recipient (rows) populations. The copy profile of each recipient group is an average of the copy profiles of all individuals belonging to that group. (b) Matrix of pairwise TVDxy distances based on the ancestral profiles of the recipient groups in panel (a). The scales of chunk counts and TVDxy values are shown to the right of the matrices. (c) Neighbor-Joining (NJ) tree based on TVDxy distances. Values indicate the percentage of NJ partitions observed in 1000 replicas of the coancestry matrix, generated by sampling the individual copy profiles from each population with replacement. The NJ tree was rotated to fit the approximate geographic location of the recipient groups. Abbreviations: GWD (Mandinka), MSL (Mende), ESN (Esan), YRI (Yoruba), ANG (Angolares), BBS (Bubi), FOR (Forros), PRI (Principenses), GAN (Ganguela), HIM (Himba), KUV (Kuvale), NYK (Nyaneka), OVI (Ovimbundu).

Figure 3

Summary statistics of genetic diversity. (a) Boxplots representing the individual variation in the average size of runs of homozygosity (ROH), defined as the ratio between the total length of ROH (sROH) and the number of ROH (nROH). (b) Linkage disequilibrium (LD) decay with physical distance. (c) Boxplots representing the variation in individual observed heterozygosity per locus (Ho). (d) Site frequency spectra (SFS). For (b,d), populations were randomly downsampled (without replacement) to the smallest sample size, and the average over replicates is reported.

Figure 4

Network representing the haplotype variation in African-derived Y-chromosomes from São Tomé and Príncipe. Haplotypes were defined by using 10 microsatellite loci (DYS19, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393, DYS437, DYS438, DYS439). Locus DYS385 was excluded from the network because it is duplicated. The inset shows the descent cluster centered around the most frequent haplotype in the Angolares. Haplotypes from the Angolares (ANG) and from a sample of linguistically uncharacterized non-Angolar residents of São Tomé (Non-ANG) were previously reported [22]. The newly generated data on the Y-chromosome haplotypes from Príncipe (PRI) are shown in Table S4. Circles represent haplotypes, area is proportional to frequency, and colors represent populations. Lines represent microsatellite mutational differences.