On the edge of Bantu expansions: mtDNA, Y chromosome and lactase persistence genetic variation in southwestern Angola

Abstract

Background: Current information about the expansion of Bantu-speaking peoples is hampered by the scarcity of genetic data from well identified populations from southern Africa. Here, we fill an important gap in the analysis of the western edge of the Bantu migrations by studying for the first time the patterns of Y-chromosome, mtDNA and lactase persistence genetic variation in four representative groups living around the Namib Desert in southwestern Angola (Ovimbundu, Ganguela, Nyaneka-Nkumbi and Kuvale). We assessed the differentiation between these populations and their levels of admixture with Khoe-San groups, and examined their relationship with other sub-Saharan populations. We further combined our dataset with previously published data on Y-chromosome and mtDNA variation to explore a general isolation with migration model and infer the demographic parameters underlying current genetic diversity in Bantu populations.

Results: Correspondence analysis, lineage sharing patterns and admixture estimates indicate that the gene pool from southwestern Angola is predominantly derived from West-Central Africa. The pastoralist Herero-speaking Kuvale people were additionally characterized by relatively high frequencies of Y-chromosome (12%) and mtDNA (22%) Khoe-San lineages, as well as by the presence of the -14010C lactase persistence mutation (6%), which likely originated in non-Bantu pastoralists from East Africa. Inferred demographic parameters show that both male and female populations underwent significant size growth after the split between the western and eastern branches of Bantu expansions occurring 4000 years ago. However, males had lower population sizes and migration rates than females throughout the Bantu dispersals.

Conclusion: Genetic variation in southwestern Angola essentially results from the encounter of an offshoot of West-Central Africa with autochthonous Khoisan-speaking peoples from the south. Interactions between the Bantus and the Khoe-San likely involved cattle herders from the two groups sharing common aspects of their social organization. The presence of the -14010C mutation in southwestern Angola provides a link between the East and Southwest African pastoral scenes that might have been established indirectly, through migrations of Khoe herders across southern Africa. Differences in patterns of mtDNA and Y-chromosome intrapopulation diversity and interpopulation differentiation may be explained by contrasting demographic histories underlying the current female and male genetic variation.

Figure 1

Major ethnolingusitic groups from Angola and population samples used in this study. A) Map of Angola depicting the core areas of the country's major ethnolinguistic groups and sampled locations in the Namibe province (modified from [21]). The area encompassing the sampled locations is shaded. B) Map of Africa with the approximate locations of the population groups used in the present analysis. Populations are coded with numbers. The correspondence between numbers and populations is given in Additional files 4 and 5. Major geographic regions are encircled.

Figure 2

MtDNA haplogroup variation in southwestern Angola and other African populations. A) and B) Correspondence analysis plots based on haplogroup frequency profiles from several African populations (A) and different ethnolinguistic groups from Namibe (B). Percentages in parentheses indicate the total fraction of the genetic variation that was captured by each dimension. Geographic regions were defined as in Figure 1B. Populations from Mozambique and Zimbabwe were pooled into a single Southeast Africa group. Angola includes samples from Cabinda and Luanda. Namibe includes all groups sampled in this study. C) MtDNA haplogroup frequencies in the Namibe province and in other African population groups. D) MtDNA haplogroup frequencies in the four population groups sampled in the Namibe province. Haplogroup frequencies were broken down as in [25]. ANG = Angola (Luanda + Cabinda); WC = West-Central Africa; W = West Africa; E = East Africa; PYG = Pygmies; SAK = South Africa Khoe-San; SE = Southeast Africa; NAB = Namibe; KUV = Kuvale; OVI = Ovimbundu; NYA = Nyaneka-Nkhumbi; GANG = Ganguela.

Figure 3

Patterns of mtDNA lineage sharing. Lineage sharing between individual mtDNAs (A) and haplotypes (B) from southwestern Angola and from other population groups in Africa. Only mtDNAs and haplotypes found to be shared between Namibe and at least one other African population were included in the calculations. Abbreviations are the same as Figure 2.

Figure 4

Y-chromosome haplogroup variation in southwestern Angola and other African populations. A) and B) Correspondence analysis plots based on haplogroup frequency profiles from several African populations (A) and different ethnolinguistic groups from Namibe (B). Percentages in parentheses indicate the total fraction of the genetic variation that was captured by each dimension. Geographic regions were defined as in Figure 1B. Angola refers to a sample from Cabinda. Namibe includes all groups sampled in this study. C) Y-chromosome haplogroup frequencies in the Namibe province and in other African population groups. D) Y-chromosome haplogroup frequencies in the four population groups sampled in the Namibe province. Abbreviations are the same as Figure 2.

Figure 5

Patterns of Y-chromosome lineage sharing. Lineage sharing between individual Y chromosomes A) and haplotypes B) from southwestern Angola and from other population groups in Africa. Only Y chromosomes or haplotypes that were found to be shared between southwestern Angola and at least one other African population were included in the calculations. Haplotypes were defined by STR loci DYS19, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393. Abbreviations are the same as Figure 2.

Figure 6

Possible trajectories of the lactase persistence -14010C mutation from East to Southwest Africa. A) Major hypotheses about the migration of the -14010C mutation: a direct migratory link between East and Southwest Africa (violet arrow); a Khoe mediated link, with a first contact between East African pastoralists and the herding Khoe (blue arrow) followed by subsequent transfer to Southwest Bantu pastoralists through Bantu-Khoe interactions (green arrow). B-D) carrier frequencies of the -14010C mutation (B), and typical Khoe-San mtDNA (C) and NRY lineages (D) in major ethnolinguistic groups sampled in the Namibe province.