https://orcid.org/0000-0002-9310-5009
Abstract
The Sahel/Savannah belt of Africa is a contact zone between two subsistence systems (nomadic pastoralism and sedentary farming) and of two groups of populations, namely Eurasians penetrating from northern Africa southwards and sub-Saharan Africans migrating northwards. Because pastoralism is characterized by a high degree of mobility, it leaves few significant archaeological traces. Demographic history seen through the lens of population genetic studies complements our historical and archaeological knowledge in this African region. In this review, we highlight recent advances in our understanding of demographic history in the Sahel/Savannah belt as revealed by genetic studies. We show the impact of food-producing subsistence strategies on population structure and the somewhat different migration patterns in the western and eastern part of the region. Genomic studies show that the gene pool of various groups of Sahelians consists in a complex mosaic of several ancestries. We also touch upon various signals of genetic adaptations such as lactase persistence, taste sensitivity and malaria resistance, all of which have different distribution patterns among Sahelian populations. Overall, genetic studies contribute to gain a deeper understanding about the demographic and adaptive history of human populations in this specific African region and beyond.
Introduction
Sahel region is a semi-desert zone of northern Africa that stretches from the Atlantic Ocean to the Red Sea coast. From west to east, it spans over ~ 5500 km, and in total, it covers an area of some 3 million km2 (Fig. 1). From an ecological point of view, the Sahelian landscape is a mosaic of grasses and shrubs with few trees south of Sahara (1). The northern boundary of the Sahel—and thus also of sub-Saharan Africa as a whole—starts at the isohyet of 100 mm (Fig. 1A), where grasses such as Cenchrus biflorus begin to grow; in the past, they were an important food source not only for animals but also for humans. At its southern edge, Sahel passes at isohyet of 250 mm first into the Sudanese savannah, where annual precipitation reaches 500 mm, and further south to Guinean savannah with 1000 mm of rainfall a year, where up to 80% of land is covered with forests (Fig. 1A). Overall, the Sahel and adjacent savannahs, i.e. the Sahel/Savannah belt, produce a large number of wild grasses with nutritionally rich edible seeds for wild and domestic ruminants (2) but also for humans.
Vegetation cover in northern Africa. (A) present day; (B) early Holocene.
In the past, Africa had experienced a number of harsh climate changes that had a profound impact on natural conditions and the landscape (3). During the Last Glacial Maximum, some 20–18 thousand years ago (kya) the region of the Sahel was void of human populations and the occupation limited only to sites close to permanent water sources. These climatic oscillations may have caused increased competition for food resources that would have manifested itself, by more frequent conflicts among hunter-gatherers, as evidenced for example by traumas found in almost half of the skeletons buried in the Jebel Sahaba cemetery in northern Sudan (4). In fact, it seems that hunter-gatherers occupying the Sahel still before the Last Glacial Maximum retreated to more hospitable places either close to Mediterranean Sea, where cultures such as Iberomaurusian and Capsian are known, Nile Valley with Early Khartoum and sites such as Wadi Kubbaniya and Nazlet Khater or further south to places near the equator (e.g. Iwo Eleru and Shum Laka).
More peaceful time came during the Holocene, some 11.5 kya when not only Sahel but whole Sahara was repopulated by ancestors of the present populations. The impact of climate changes during this period is clearly visible in the Lake Chad, which currently covers an area of ~ 20 000 km2, but estimates of its size during the Early Holocene range between 350 000–400 000 km2 and show the lake as the largest freshwater area in the whole of Africa (5,6). This stage of its development is commonly referred to as Lake Mega-Chad, which was formed by a runoff from a permanent (and still existing) southern reservoir that led northwards through Bahr el-Ghazal and to the Bodélé Depression in northern Chad. The humid period from ~ 11.5 to ~ 5.5 kya is known as Green Sahara, when lush vegetation, large bodies of water, permanent rivers and tropical rainfall characterized the climate of entire northern Africa (Fig. 1B) (7).
Today, populations from the Sahel/Savannah belt have different food-producing practices and lifestyles. To better understand their demographic histories and genetic adaptations to environmental and cultural factors, here we review first their food-producing practices, complex patterns of genetic diversity, population structure and admixture, and then discuss recent findings about their genetic and genomic adaptations.
Food-Producing Practices and Lifestyles
Cattle (Bos taurus), the most important domestic animal for Sahelian pastoralists, was first introduced to northeastern Africa from the Near East ~ 10 kya via the Nile Valley, from where it later spread further to Central Sahara by Nile tributaries such as Wadi Howar (8–10). It is possible that along this way, cattle mixed with wild aurochs (Bos primigenius), which at this time still lived in northern Africa (11). Although the favourable climate of the Early Holocene created a suitable natural setting for terrestrial ungulates (2), the first African herders supplemented their diet by wild grasses and hunting of wild game (12,13). Later on, zebu cattle (Bos indicus), more resilient to parasites than B. taurus, was introduced to Africa from India <2 kya and contributed significantly to the repertoire of domesticated animals of nomadic pastoralists (14).
Although a majority of current African livestock, including sheep and goats, was introduced from the southwestern Asia (9), Sahel and the Sahara became the cradle of sub-Saharan plant domestication. Recent genomic studies of pearl millet (Pennisetum glaucum), African rice (Oryza glaberrima) and African yam (Dioscorea rotundata) show that the origins of their cultivation centre around the Inner Niger Delta (15–17). The results of genomic analyses of pearl millet domestication are consistent with archaeological findings, which indicate its presence at ~ 4.5 kya in Tilemsi Valley in northeastern Mali (18). Cereal domestication, however, did not take place only in western Africa. Another crop typical for the Sahel is sorghum (Sorghum bicolor), whose relatively long transformation into a domesticated form took place in Sudan, where the process started ~ 6 kya (19,20).
Nowadays, the Sahel/Savannah belt is inhabited by populations practicing two subsistence strategies: nomadic pastoralists and sedentary farmers. The former keep large numbers of domestic animals who feed on natural vegetation that requires seasonal movements to pastures and water resources—so-called ‘transhumance’ (21). Herders thus differ from farmers by a much higher degree of mobility, which also means that any remains of their temporary camps quickly disappear. Famers, on the other hand, live in villages, where waste is accumulated and families stay in one place for generations. This is naturally an oversimplification. In reality, there are numerous semi-pastoralist groups whose mode of subsistence involves only part of the family engaged in transhumance. Nevertheless, this dual distinction does capture a real phenomenon, reflects a long tradition in the region, and to a large degree coincides also with local people’s ethnic identity.
There are two main groups of traditional pastoralists in the Sahel/Savanna belt: the Fulani in its western part, and the Arabs in the eastern part. The Fulani have a long tradition of cattle herding and their features often seem to indicate non-sub-Saharan origin, which inspired many researchers to look for their origin in northern Africa and even Eurasia (22). The Arabs, on the other hand, are descendants of Bedouin tribes that have been migrating from Arabia to northern Africa since the early middle ages and penetrated further south into the Sahel (23). Originally, they were camel herders but some of their groups—currently usually known under an Arabic term ‘Baggara’, meaning ‘cow’—began to specialize in cattle breeding. This probably happened after they contacted Fulani pastoralists residing at the west of Lake Chad. This process is generally known as ‘Baggarisation’ (24).
Patterns of Genetic Diversity in Uniparental Markers
For the past 20 years, our team has been studying the population history of the Sahel/Savannah region (25). We first focused on populations living in the Lake Chad Basin (26–29), and later we expanded our area of interest to neighbouring regions to better understand the peopling of the entire Sahel/Savannah belt (30–33). Initially, we studied uniparental markers with either maternal (mitochondrial DNA henceforth referred as mtDNA) or paternal (Y chromosome) inheritance. We detected the presence of some specific mtDNA-haplogroups with age estimates falling mostly to the Early Holocene, such as L3f3 or L3e5 (34,35), which confirms the importance of this period in shaping the demographic history of this region. Interestingly, we also found that while non-sub-Saharan haplogroups are much more frequent among pastoralists than among farmers (36–40), they are not associated with any specific morphometric pattern (41).
In the western part of the Sahel, our genetic studies of Fulani pastoralists have shown that they mainly have haplogroups of western African ancestry; however, some northern African (36,39) and east African ancestry (30) were also detected. In the eastern part of the Sahel, we investigated the genetic patterns in Arab pastoralists, and our results of both uniparental markers supported the possibility of the earlier-mentioned Baggarization process (32), besides biological contacts between the Fulani and Arabs must have been rather infrequent. This is also evident from the investigation of lactase persistence alleles described later (33,42,43).
Using genetic information of a hypervariable region in the mtDNA known as the D-loop, we tested migration events between pastoralists and farmers in both the eastern and western parts of the Sahel/Savannah belt and found different trends in the Fulani and the Arabs (31). In the eastern part of Sahel, the inferred best-fitting model indicated a more intensive gene flow between the two groups, especially in the direction from sub-Saharan farmers to Arabic-speaking pastoralists. Limited gene flow took place in the west as well, but it was more pronounced only among some Fulani sub-populations (31). In addition, asymmetric gene flow, that is, differences in the migration pattern of male versus female subpopulations, was observed as well (32). It has also been established that factors other than the mode of subsistence help account for the population structure across the Sahel belt, whereas for pastoralists, the main factor is their linguistic affiliation, and for farmers, it is their geographical location.
Genomic Patterns of Population Structure and Admixture
In genomic studies of Sahelian populations, we observed differences between the western and eastern Sahelian groups (44), largely explained by a genetic exchange with populations of non-sub-Saharan ancestry observed in the eastern parts and diseases that could have led to local adaptations in the western parts of the region (45). Previously, we analysed dense genome-wide genotype data of 13 Sahelian populations covering western, central and eastern Sahel (44). The results highlighted a strong population structure in both west and central African populations, which was confirmed by recent genome-wide studies (46). Population-genetic analyses, such as principal component analysis (PCA) (47) and ADMIXTURE analysis (48), of Sahelian populations together with worldwide reference populations (44,49–55) further highlight complex patterns of admixture (Fig. 2). More admixed groups in the Sahel/Savannah belt received gene flow from Middle Eastern and European sources, whereas their African sources have different ancestral origins, e.g. the African ancestry in Fulani populations is from west African populations, whereas Arab groups received genetic admixtures from central and eastern African groups.
Population structure and complex admixture patterns across the Sahel belt. (A) Geographical locations of selected populations from publicly available previous studies (44,49–55). The analysed dataset included 262 245 genetic variants and 2108 individuals after quality control and LD-pruning steps. (B) Admixture proportions across Sahelian and reference populations estimated on the basis of a four-way admixture model using unsupervised clustering ADMIXTURE analysis at K = 4 (48). For better visualization of the results, we used the AncestryPainter (75) with segment size of each population equal regardless of its sample size. (C) A distribution of admixture patterns across Sahelian and reference populations is plotted on a geographic map using the Kriging method and estimated admixture proportions. (D) PCA plot showing a strong population structure among Sahelian populations from Sudan and Chad. PCA coordinates were estimated using smartpca (47). Figure 2A and C also show latitude and longitude coordinates of selected populations.
The Arab expansion had a large impact on population history of both northern Africa and the Sahel/Savannah belt. In this context, dense genome-wide exome data of various linguistic groups in Sudan and South Sudan (49) revealed a strong genetic differentiation among northeastern African groups. This differentiation process was driven by an influx of people of Eurasian origin who probably followed the Nile Valley southwards. Its timing coincides with Arab expansion into northern Africa (see purple component in Fig. 2C). It was estimated that a major admixture event took place ~700 years ago (ya), coinciding with the fall of Dongola, a Christian Nubian kingdom, and the beginning of reign of the first Muslim ruler of this region in 1315/1316 CE, and later a wave of admixture that reached the Kordofanian populations some 400–200 ya (49). Nowadays, most populations from Sudan (such as the Nubian, Arab, and Beja) have some ancestry from southwestern and western Asia and/or northeastern Africa (Fig. 2). Other populations in Sudan have only little admixture of Eurasian origin, coming from recent migrants from Egypt (e.g. the Copts), suggesting a long-term isolation in some groups from this African region (49). Likewise, Nilo-Saharan-speaking populations from southern Sudan and northern Chad (see dark-blue component in Fig. 2C) have low or null contributions from Afro–Asiatic-speaking groups or other sources. In agreement, a recent genomic study (56) of Nilo-Saharan groups highlighted a notable genetic differentiation between Nilo-Saharan populations and Afro–Asiatic or Niger–Congo populations, as well as within Nilo-Saharan populations, e.g. the Lugbara from Uganda and the Gumuz from Ethiopia have greater genetic differentiation than between any two Afro–Asiatic or Niger–Congo populations (56).
The Fulani are a large and widely dispersed population of both nomadic herders and sedentary farmers, who speak a Niger-Congo language and live in the Sahel/Savannah belt. Nowadays, they are scattered all the way from Senegal in the west to the Blue Nile area of Sudan in the east. More recently, a genome-wide study of a Fulani community from Burkina Faso inferred two major admixture events in this group, dating to ~1800 and 300 ya (50). The first admixture event took place between west African ancestors of the Fulani and ancestral north African nomadic groups (see results for ‘Burkina_Faso_Fulani_V’ in Fig. 2B), which probably coincided with a change of lifestyle and adaptation to milk consumption and subsequently led to Fulani expansion throughout the Sahel/Savannah belt. The timing also coincides with the beginnings of pastoralism in western Africa, especially in northern Burkina Faso, which archaeozoological evidence dates to ~ 2 kya (57). The second admixture event, relatively recent, inferred a source from southwestern Europe, which suggests either a gene flow between the Fulani and northern African groups, who carry considerable admixture proportions from Europeans due to trans-Gibraltar gene flow (51), or the influence of European colonial expansion into Africa, both implying maritime travels (50).
Future research involving numerous Fulani and Arab communities from different regions would help us to further investigate and reconstruct more complex admixture scenarios among these groups, and to better understand the factors that led to extensive spread of these groups across the Sahel/Savannah belt.
Genomic Patterns of Local Adaptations
Sahelian populations have been constantly adapting to the unique environmental conditions of their challenging environment (44,58). Changes in subsistence mode in conjunction with numerous migrations meant that populations were repeatedly exposed to new diets and new pathogens (59). This created a selective pressure that increased the frequency of advantageous genomic variants, whereby particularly useful were the variants that confer resistance to infectious diseases and ability to digest new types of food (60).
A well-documented example of genomic adaptation in the Sahel is the prevalence of lactase persistence (furthermore referred to as LP) in populations with a tradition of animal husbandry (33). Fresh milk is an excellent source of sugar, fats and proteins, but the production of lactase, an enzyme needed to digest milk sugar, is usually suppressed in adults. Because the domestication of cattle approximately 10 kya (61), several human populations acquired mutations in the genomic region upstream of the lactase-encoding (LCT) gene, which ensure that the production of lactase continues throughout adulthood (62). At least four different mutations in the LCT region are known to cause LP in African populations. Two of them (variants −14 010*C and − 13 907*G) originated in eastern Africa (63), one (−13 915*G) in the Middle East (42,64) and one (−13 910*T) in Europe (65). Each of these variants emerged independently and on a different haplotype background (66).
In the eastern part of the Sahel, the LP phenotype is common among Arabic pastoralists who migrated to Africa in multiple waves from Arabia and introduced variant −13 915*G into the region (43). This variant has also been reported in Afro–Asiatic-speaking Beja pastoralists among whom the exclusively east African variant −13 907*G is also found (33,66). In the western part of the Sahel/Savannah belt, LP is frequent among Fulani pastoralists (33,50), in whom it is rather interestingly determined by the same −13 910*T allele as in Europeans and present within a demonstrably European haplotype background (50).
Because of the historical admixture events, Fulani genomic diversity is a mosaic of African and Eurasian haplotypes (30,44). In genomic regions where a particular haplotype provides an evolutionary advantage, such as the LCT region, the ratio between African and Eurasian haplotypes in the population is skewed due to selective pressures, which increased the frequency of the advantageous haplotype. As a result, the European LP haplotype is present in approximately one half of Fulani from Ziniaré (Burkina Faso) (50), which is significantly higher than the genome-wide average amount of European ancestry in the Fulani population in general (33).
The ability to detect bitter compounds in food is mediated by bitter taste receptors encoded by a wide range of genes belonging to the TAS2R family. Because bitter taste often indicates the presence of potentially harmful substances, such as alkaloids, the ability to detect bitter taste is considered a protective evolutionary feature. A strong signature of positive selection on the TAS2R16 gene has been reported not only in Eurasian populations (67) but also in east African populations and in Fulani from Cameroon (68). A special role of TAS2R receptors in the Fulani is also reflected in an enrichment of Eurasian haplotypes in the TAS2R genes on chromosome 12 (44), although the driver of the natural selection remains unclear. One possible explanation is that during particular rituals (69,70), the Fulani consume substances containing various alkaloids and TAS2R receptors might play a role in the process of ingestion of these potions (44).
Malaria has long been one of the most serious health hazards in Africa, including the Sahel belt. Plasmodium vivax, the causative agent of a less serious form of malaria, uses Duffy antigens located on the surface of erythrocytes as a receptor for invasion. Point mutations in the DARC gene lead to an absence of Duffy antigen on the surface of erythrocytes, which makes the host resistant to P. vivax (71). Duffy-negative phenotype is therefore advantageous in regions where P. vivax malaria is endemic. Its prevalence among sub-Saharan African populations ranges between 80 and 100% (72), whereas outside of Africa the prevalence is much lower, or non-existent (73,74). It is therefore likely that Eurasian populations that migrated into the Sahel/Savannah belt from the Near East lacked Duffy-negative variants in their gene pool. Local ancestry analysis of genomic segments in the Arabs and Nubians from Sudan revealed that alleles responsible for Duffy-negative phenotype in these populations were acquired through an adaptive admixture with autochthonous African populations (44). Thanks to a subsequent selective sweep, present-day populations of non-African origin in Sudan have an African haplotype in the DARC gene and consequently also exhibit resistance to P. vivax malaria.
Conclusions
The climate of the African Sahel/Savannah belt is and was always highly variable, therefore creating an ecologically fragile environment that poses challenges to long-term continuous survival of human populations. Nevertheless, Sahelians have successfully adapted to their harsh climate and environmental limitations in a number of cultural and biological ways. Recent advances in genetics and genomics have shown that the history of human populations in this region is highly complex and characterized by numerous demographic expansions, mass migrations, admixture events and adaptations linked especially with environmental changes since the Early Holocene until today. Overall, there is a clear distinction between western and eastern part of the Sahel/Savannah belt with the centre of gravity in Lake Chad Basin. In this review, we highlighted some of the key insights into the demographic history of this region and illustrated how genetic studies contribute to a better understanding of the prehistory of this vast and in many ways under-investigated part of Africa. For further insight into the complex demographic history of the Sahel/Savannah belt populations, future genomic studies ought to include more groups of different linguistic affiliations, geographic locations and modes of subsistence, an undertaking that would require international collaborations and cross-disciplinary approaches.
Acknowledgements
We thank the editors for the invitation to participate in this special issue. The authors would like to thank Anna Pilatová, PhD for proofreading the manuscript.
Conflict of Interest statement. None declared.
Funding
V.Č. and P.T. were supported by the Czech Science Foundation (grant no. 18-23889S). C.F.-L. was supported by the European Research Council (ERC StG AfricanNeo, grant no. 759933), Marcus Borgström Foundation for Genetic Research, Bertil Lundman’s Fund for Anthropological Studies, and Sven and Lilly Lawski’s Foundation (Postdoctoral scholarship).
References
Author notes
Cesar Fortes-Lima and Petr Tříska contributed equally to this work.
