Variation of Female and Male Lineages in Sub-Saharan Populations: the Importance of Sociocultural Factors

Abstract

In this paper, we present a study of genetic variation in sub-Saharan Africa, which is based on published and unpublished data on fast-evolving (hypervariable region 1 of mitochondrial DNA and six microsatellites of Y chromosome) and slow-evolving (haplogroup frequencies) polymorphisms of mtDNA and Y chromosome. Our study reveals a striking difference in the genetic structure of food-producer (Bantu and Sudanic speakers) and hunter-gatherer populations (Pygmies, Kung, and Hadza). In fact, the ratio of mtDNA to Y-chromosome Nupsilon is substantially higher in food producers than in hunter-gatherers as determined by fast-evolving polymorphisms (1.76 versus 0.11). This finding indicates that the two population groups differ substantially in female and male migration rate and/or effective size. The difference also persists when linguistically homogeneous populations are used and outlier populations are eliminated (1.78 vs 0.19) or when the jacknife procedure is applied to a paired population data set (1.32 to 7.84 versus 0.14 to 0.66). The higher ratio of mtDNA to Y-chromosome Nnu in food producers than in hunter-gatherers is further confirmed by the use of slow-evolving polymorphisms (1.59 to 7.91 versus 0.12 to 0.35). To explain these results, we propose a model that integrates demographic and genetic aspects and incorporates ethnographic knowledge. In such a model, the asymmetric gene flow, polyginy, and patrilocality play an important role in differentiating the genetic structure of sub-Saharan populations. The existence of an asymmetric gene flow is supported by the phylogeographic features of mtDNA and Y-chromosome haplogroups found in the two population groups. The role of polyginy and patrilocality is sustained by the evidence of a differential pressure of genetic drift and gene flow on maternal and paternal lineages of food producers and hunter-gatherers that is revealed through the analysis of mitochondrial and Y-chromosomal intrapopulational variation.

The impact of agricultural emergence on the genetic history of African rainforest hunter-gatherers and agriculturalists

“…AGR-to-RHG admixture rate estimates were thus on average 8.8 times larger than RHG-to-AGR estimates, supporting the occurrence of asymmetrical admixture from AGR to RHG populations. Furthermore, our comparison of ancestry proportions on the X chromosome and the autosomes in AGR and some RHG populations, and a large body of studies based on uniparentally inherited markers 18,38,39 , suggest that during the admixture process there has been preferential mating of AGR males with RHG females (Supplementary Note 2, Supplementary Fig. 7, Supplementary Tables 5 and 6).…”

“…First, we show that the bulk of the admixture between various groups of RHG and neighbouring AGR took place only recently, within the past B1,000 years. This indicates that the earliest phase of the diffusion of an agriculturebased lifestyle, where an avant-garde of farming communities in the Western (c. 3,000-5,000 YBP) and Eastern (c. 2,500-3,000 YBP) equatorial rainforest 3,6,15,54 promoted early socio-economic and cultural interactions with local RHG 2,3,7,8,11,[15][16][17][18][19] , was not accompanied by immediate, extensive genetic exchanges. Our results suggest instead that admixture started extensively at a later stage, well after the introduction of iron tools and plant cultivation and the subsequent rise of territorial chiefdoms, profoundly transforming the interactions between the two communities 15,42 .…”

“…As soon as farming communities penetrated the rainforest, extensive economic and technological exchange with local huntergatherers occurred, as attested by the appearance of pottery and polished stone tools within this time frame, together with the shared language families and oral traditions of the two communities 2,3,7,8,11,[15][16][17][18][19] . Such early interactions are further supported by a recent study that reports the acquisition of Helicobacter pylori bacteria strains by Western RHG through contacts with their AGR neighbours B4,500 YBP 20 .…”

Contrasting patterns of Y chromosome and mtDNA variation in Africa: evidence for sex-biased demographic processes

“…12,[31][32][33] The data set includes 39 populations from the major language groups: Khoisan (!Kung1, !Kung2, Khwe, Hadza), Nilo-Saharan (Kanuri, Songhai, Turkana, Nubian, Sudanese, Mbuti, Datoga), Afroasiatic (Moroccan Berber, non-Berber Moroccan, Egyptian, Algerian Mozabite, Tuareg, Somalian, Amhara, Hausa, Podokwo, Mandara, Uldeme, Iraqw), Niger-Congo non-Bantu (Fulbe ¼ Fulfulde, Yoruba, Serer, Wolof, Mandinka, Tupuri), and Niger-Congo Bantu (Bubi, Fang, Biaka, Kikuyu, Mozambique1, Mozambique2, Bakaka, Bassa, Mbenzele, Sukuma) ( Figure 1). Some populations represented in the original data sets 12,31 -33 were omitted because they are not found on the African mainland, are Cameroonian populations not represented in the Y chromosome data set, 33 or because linguistic designations could not be inferred.…”

“…The approximate location of 40 populations typed for Y chromosome markers in this study (K) and 39 populations surveyed for HVS1 sequence data 12,31,32,33 (J) are indicated. The distribution of the four African language families was constructed using Greenberg's 39 classifications and further refined with data from the ethnologue (http://www.ethnologue.com/).…”