Post by Admin on May 23, 2023 20:03:34 GMT
Introduction
Africa exhibits vast cultural and linguistic diversity, including a wide range of subsistence strategies and ∼2,000 spoken languages. In addition, African populations harbor the greatest genetic diversity, exhibit the lowest levels of linkage disequilibrium (LD), have the largest long-term effective population sizes (Ne), and show the deepest split times of all human lineages (Tishkoff et al. 2009; Auton et al. 2015; Mallick et al. 2016; Bergström et al. 2020). For these reasons, Africa is commonly accepted as the cradle of humankind (Henn et al. 2018), and African population history is of exceptional interest to human evolution.
Most of our knowledge about African population history is derived from archeological and linguistic studies, as Africa has long been neglected in genetic studies (Popejoy and Fullerton 2016; Martin et al. 2018; Sirugo et al. 2019; Fatumo et al. 2022). However, archeological and linguistic studies are largely unable to disentangle cultural diffusion from demic diffusion, that is, movements of people (Robertson and Bradley 2000; Diamond and Bellwood 2003). By contrast, genetic studies are uniquely equipped to identify large-scale demic movements (e.g., Tishkoff et al. 2009). In the last decade, the importance of studying genetic variation in Africa has become more appreciated, and a heap of genetic studies of contemporary and ancient individuals has revealed complex population structure and history in Africa, complementing archeological and linguistic studies (e.g., Tishkoff et al. 2009; Schlebusch et al. 2012; Choudhury et al. 2020; Lipson et al. 2022).
In this review, we focus on genetic studies that uncovered extensive archaic, prehistoric, and recent gene flow that has occurred in Africa. We start by putting genetic variation in Africa into a global context and giving a brief overview of population structure in Africa inferred from ancient and extant genomes, focusing on hunter–gatherer groups and deep population structure in the continent. We then discuss how this population structure was shaped by archaic and recent admixture, moving from the deeper past to more recent times. Given the scope of this review paper, we cannot comprehensively review the evolutionary history of every population. Instead, we focus on representative examples of major migratory and admixture events. Finally, we briefly review the evidence for local adaption and discuss the biomedical implication of population structure in Africa. In light of this, we call for more (responsibly conducted) studies of genetic variation in Africa and research capacity building on the African continent. Note that we tried to refer to populations according to current naming conventions, and when we refer to admixture between specific populations, this does not necessarily imply the mixing of these exact populations, but rather the mixing of genetically similar populations.
Patterns of Genetic Variation in Africa
Compared with the rest of the world, each African genome harbors ∼25% more polymorphisms than each non-African genome (Auton et al. 2015; Mallick et al. 2016; Bergström et al. 2020). Furthermore, variants that are rare on a global level (<1% frequency) are more frequently found to be common in African populations, that is, there is an excess of variants exclusively found in Africans (Auton et al. 2015). Greater numbers of private African alleles are consistent with the out-of-Africa (OOA) model, as substantial numbers of polymorphisms were lost due to serial founder effects. In fact, the genetic variation found outside of Africa is largely a subset of African genetic diversity (Tishkoff et al. 2009; Lachance et al. 2012). Subsets of African genetic variation found outside of Africa also vary by region, indicating that multiple OOA migrations may have occurred (Rasmussen et al. 2011; Pagani et al. 2015). Additionally, African populations exhibit a faster decay of LD, leading to shorter haplotypes (Auton et al. 2015). This is of biomedical relevance (see below), and it also enables improved fine-mapping of causal variants in genome-wide association studies (GWAS) because casual variants are tagged by fewer other variants (Auton et al. 2015).
In line with the OOA model, many human populations experienced a major decline in Ne coinciding with the OOA migration 70–50 thousand years ago (kya) (Bergström et al. 2020). Concurrently, African populations experienced declines in Ne while maintaining consistently larger Ne than non-African populations (Auton et al. 2015; Mallick et al. 2016; Bergström et al. 2020). Thus, the higher genetic diversity and lower LD in African populations reflect historically larger Ne.
Deep Population Structure in Africa
Hunting and gathering was the predominant subsistence strategy prior to the introduction of agriculture and pastoralism during the Neolithic (i.e., 12–6.5 kya in Africa) (Marshall and Hildebrand 2002). Today, only a few traditional hunter–gatherer groups remain that live in small communities. Generally, it is assumed that they have either merged into or were replaced by neighboring agropastoral groups, obscuring some of the ancestral genetic variation and structure (Pagani et al. 2012; Schlebusch and Jakobsson 2018; Gopalan et al. 2022). Nevertheless, when accounting for recent admixture, studying the genetics of the traditional hunter–gatherer groups in Africa can provide a snapshot of deep population structure due to their long-term population continuity. Attempts to illuminate the deep population structure in Africa have been further aided by the emergence of ancient DNA from unadmixed hunter–gatherer individuals (e.g., Skoglund et al. 2017 and Lipson et al. 2022).
The remaining traditional hunter–gatherer groups in Africa can be broadly grouped into three major groups: Khoe-San, eastern African hunter–gatherers (EAHG), and rainforest hunter–gatherers (RHG). Khoe-San collectively refers to Khoisan-speaking San hunter–gatherers and Khoekhoe herders, who historically inhabit arid regions in southern Africa. Possibly, Khoe-San were the only inhabitants of southern Africa for much of its prehistory (Schlebusch et al. 2017; Skoglund et al. 2017; Vicente, Jakobsson, et al. 2019). Khoekhoe herders have adopted a pastoralist lifestyle only recently, likely after admixture with eastern African pastoralists over the past 1,500 years (Breton et al. 2014; Macholdt et al. 2014; Schlebusch et al. 2017). Similarly, EAHG groups, for example, the click-speaking Hadza and Sandawe in Tanzania and the Chabu in Ethiopia, are traditional foragers, who have practiced a hunter–gatherer lifestyle until recently or are still practicing it (Bower 1991; Prendergast 2020). These EAHG groups are more closely related to each other than to other African hunter–gatherer groups (Scheinfeldt et al. 2019). RHG groups comprise genetically diverse populations in equatorial Africa, which are often further subdivided into western (e.g., the Baka) and eastern (e.g., the Mbuti) RHG groups (Patin and Quintana-Murci 2018).
Many hunter–gatherer groups experienced declines in Ne during the Holocene and have small census population sizes today (Patin et al. 2014; Scheinfeldt et al. 2019; Bergström et al. 2020; Gopalan et al. 2022). Nevertheless, African hunter–gatherers have the highest level of genetic diversity of extant populations and represent the most deeply branching human lineages even after accounting for recent admixture (Henn et al. 2011; Barbieri et al. 2014; Schlebusch et al. 2020). Specifically, the Khoe-San exhibit the highest genetic diversity of all human lineages, with a mean heterozygosity of 1.154 × 10−3 compared with 1.09 × 10−3 in the Mandenka (Schlebusch et al. 2020). As their genetic diversity is still significantly higher after accounting for recent admixture with non–Khoe-San groups, it reflects their historically larger Ne (Kim et al. 2014; Fan et al. 2019; Schlebusch et al. 2020). The lineage leading to the Khoe-San is basal to all other human lineages with an estimated divergence time of 300–200 kya (e.g., the Ju|’Hoan with the lowest level of recent admixture diverged ∼270 ± 12 kya). Subsequently, the Mbuti (RHG) diverged ∼220 ± 10 kya from all other human lineages, forming a second basal lineage (Schlebusch et al. 2020) (fig. 1). These estimates may reflect lower bounds as recent admixture reduces divergence time estimates. For these reasons, assuming regional population continuity, it has been argued for a southern African origin of modern humans (Henn et al. 2011), although models involving eastern Africa and/or multiple geographic regions are also debated (Henn et al. 2018).
Africa exhibits vast cultural and linguistic diversity, including a wide range of subsistence strategies and ∼2,000 spoken languages. In addition, African populations harbor the greatest genetic diversity, exhibit the lowest levels of linkage disequilibrium (LD), have the largest long-term effective population sizes (Ne), and show the deepest split times of all human lineages (Tishkoff et al. 2009; Auton et al. 2015; Mallick et al. 2016; Bergström et al. 2020). For these reasons, Africa is commonly accepted as the cradle of humankind (Henn et al. 2018), and African population history is of exceptional interest to human evolution.
Most of our knowledge about African population history is derived from archeological and linguistic studies, as Africa has long been neglected in genetic studies (Popejoy and Fullerton 2016; Martin et al. 2018; Sirugo et al. 2019; Fatumo et al. 2022). However, archeological and linguistic studies are largely unable to disentangle cultural diffusion from demic diffusion, that is, movements of people (Robertson and Bradley 2000; Diamond and Bellwood 2003). By contrast, genetic studies are uniquely equipped to identify large-scale demic movements (e.g., Tishkoff et al. 2009). In the last decade, the importance of studying genetic variation in Africa has become more appreciated, and a heap of genetic studies of contemporary and ancient individuals has revealed complex population structure and history in Africa, complementing archeological and linguistic studies (e.g., Tishkoff et al. 2009; Schlebusch et al. 2012; Choudhury et al. 2020; Lipson et al. 2022).
In this review, we focus on genetic studies that uncovered extensive archaic, prehistoric, and recent gene flow that has occurred in Africa. We start by putting genetic variation in Africa into a global context and giving a brief overview of population structure in Africa inferred from ancient and extant genomes, focusing on hunter–gatherer groups and deep population structure in the continent. We then discuss how this population structure was shaped by archaic and recent admixture, moving from the deeper past to more recent times. Given the scope of this review paper, we cannot comprehensively review the evolutionary history of every population. Instead, we focus on representative examples of major migratory and admixture events. Finally, we briefly review the evidence for local adaption and discuss the biomedical implication of population structure in Africa. In light of this, we call for more (responsibly conducted) studies of genetic variation in Africa and research capacity building on the African continent. Note that we tried to refer to populations according to current naming conventions, and when we refer to admixture between specific populations, this does not necessarily imply the mixing of these exact populations, but rather the mixing of genetically similar populations.
Patterns of Genetic Variation in Africa
Compared with the rest of the world, each African genome harbors ∼25% more polymorphisms than each non-African genome (Auton et al. 2015; Mallick et al. 2016; Bergström et al. 2020). Furthermore, variants that are rare on a global level (<1% frequency) are more frequently found to be common in African populations, that is, there is an excess of variants exclusively found in Africans (Auton et al. 2015). Greater numbers of private African alleles are consistent with the out-of-Africa (OOA) model, as substantial numbers of polymorphisms were lost due to serial founder effects. In fact, the genetic variation found outside of Africa is largely a subset of African genetic diversity (Tishkoff et al. 2009; Lachance et al. 2012). Subsets of African genetic variation found outside of Africa also vary by region, indicating that multiple OOA migrations may have occurred (Rasmussen et al. 2011; Pagani et al. 2015). Additionally, African populations exhibit a faster decay of LD, leading to shorter haplotypes (Auton et al. 2015). This is of biomedical relevance (see below), and it also enables improved fine-mapping of causal variants in genome-wide association studies (GWAS) because casual variants are tagged by fewer other variants (Auton et al. 2015).
In line with the OOA model, many human populations experienced a major decline in Ne coinciding with the OOA migration 70–50 thousand years ago (kya) (Bergström et al. 2020). Concurrently, African populations experienced declines in Ne while maintaining consistently larger Ne than non-African populations (Auton et al. 2015; Mallick et al. 2016; Bergström et al. 2020). Thus, the higher genetic diversity and lower LD in African populations reflect historically larger Ne.
Deep Population Structure in Africa
Hunting and gathering was the predominant subsistence strategy prior to the introduction of agriculture and pastoralism during the Neolithic (i.e., 12–6.5 kya in Africa) (Marshall and Hildebrand 2002). Today, only a few traditional hunter–gatherer groups remain that live in small communities. Generally, it is assumed that they have either merged into or were replaced by neighboring agropastoral groups, obscuring some of the ancestral genetic variation and structure (Pagani et al. 2012; Schlebusch and Jakobsson 2018; Gopalan et al. 2022). Nevertheless, when accounting for recent admixture, studying the genetics of the traditional hunter–gatherer groups in Africa can provide a snapshot of deep population structure due to their long-term population continuity. Attempts to illuminate the deep population structure in Africa have been further aided by the emergence of ancient DNA from unadmixed hunter–gatherer individuals (e.g., Skoglund et al. 2017 and Lipson et al. 2022).
The remaining traditional hunter–gatherer groups in Africa can be broadly grouped into three major groups: Khoe-San, eastern African hunter–gatherers (EAHG), and rainforest hunter–gatherers (RHG). Khoe-San collectively refers to Khoisan-speaking San hunter–gatherers and Khoekhoe herders, who historically inhabit arid regions in southern Africa. Possibly, Khoe-San were the only inhabitants of southern Africa for much of its prehistory (Schlebusch et al. 2017; Skoglund et al. 2017; Vicente, Jakobsson, et al. 2019). Khoekhoe herders have adopted a pastoralist lifestyle only recently, likely after admixture with eastern African pastoralists over the past 1,500 years (Breton et al. 2014; Macholdt et al. 2014; Schlebusch et al. 2017). Similarly, EAHG groups, for example, the click-speaking Hadza and Sandawe in Tanzania and the Chabu in Ethiopia, are traditional foragers, who have practiced a hunter–gatherer lifestyle until recently or are still practicing it (Bower 1991; Prendergast 2020). These EAHG groups are more closely related to each other than to other African hunter–gatherer groups (Scheinfeldt et al. 2019). RHG groups comprise genetically diverse populations in equatorial Africa, which are often further subdivided into western (e.g., the Baka) and eastern (e.g., the Mbuti) RHG groups (Patin and Quintana-Murci 2018).
Many hunter–gatherer groups experienced declines in Ne during the Holocene and have small census population sizes today (Patin et al. 2014; Scheinfeldt et al. 2019; Bergström et al. 2020; Gopalan et al. 2022). Nevertheless, African hunter–gatherers have the highest level of genetic diversity of extant populations and represent the most deeply branching human lineages even after accounting for recent admixture (Henn et al. 2011; Barbieri et al. 2014; Schlebusch et al. 2020). Specifically, the Khoe-San exhibit the highest genetic diversity of all human lineages, with a mean heterozygosity of 1.154 × 10−3 compared with 1.09 × 10−3 in the Mandenka (Schlebusch et al. 2020). As their genetic diversity is still significantly higher after accounting for recent admixture with non–Khoe-San groups, it reflects their historically larger Ne (Kim et al. 2014; Fan et al. 2019; Schlebusch et al. 2020). The lineage leading to the Khoe-San is basal to all other human lineages with an estimated divergence time of 300–200 kya (e.g., the Ju|’Hoan with the lowest level of recent admixture diverged ∼270 ± 12 kya). Subsequently, the Mbuti (RHG) diverged ∼220 ± 10 kya from all other human lineages, forming a second basal lineage (Schlebusch et al. 2020) (fig. 1). These estimates may reflect lower bounds as recent admixture reduces divergence time estimates. For these reasons, assuming regional population continuity, it has been argued for a southern African origin of modern humans (Henn et al. 2011), although models involving eastern Africa and/or multiple geographic regions are also debated (Henn et al. 2018).