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Population Structure and Infectious Disease Risk in Southern Africa

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Population Structure and Infectious Disease Risk in Southern Africa Mol Genet Genomics (2017) 292:499–509 DOI 10.1007/s00438-017-1296-2 REVIEW Population structure and infectious disease risk in southern Africa Caitlin Uren1 · Marlo Möller1 · Paul D. van Helden1 · Brenna M. Henn2 · Eileen G. Hoal1 Received: 12 August 2016 / Accepted: 1 February 2017 / Published online: 22 February 2017 © Springer-Verlag Berlin Heidelberg 2017 Abstract The KhoeSan populations are the earliest Keywords Population structure · Southern Africa · known indigenous inhabitants of southern Africa. The Disease susceptibility relatively recent expansion of Bantu-speaking agropasto- ralists, as well as European colonial settlement along the south–west coast, dramatically changed patterns of genetic Introduction diversity in a region which had been largely isolated for thousands of years. Owing to this unique history, popula- Southern Africa has a unique and complex human history tion structure in southern Africa refects both the underly- reaching back at least 100,000 years (Rito et al. 2013). The ing KhoeSan genetic diversity as well as diferential recent region spans southern Angola, Namibia, Botswana, South admixture. This population structure has a wide range of Africa, Zimbabwe, and Mozambique. Many diverse ethnic biomedical and sociocultural implications; such as changes groups are present in the area, including KhoeSan popu- in disease risk profles. Here, we consolidate information lations, Bantu-speaking populations, European-descent from various population genetic studies that characterize groups, and groups resulting from inter- and intra-continen- admixture patterns in southern Africa with an aim to bet- tal admixture such as the South African “Coloured” popu- ter understand diferences in adverse disease phenotypes lation (de Wit et al. 2010; Daya et al. 2013; Chimusa et al. observed among groups. Our review confrms that ancestry 2013). “Admixed” populations are the result of gene fow has a direct impact on an individual’s immune response to between distinct, historically divergent parental popula- infectious diseases. In addition, we emphasize the impor- tions, such as those from diferent continents like Asia and tance of collaborative research, especially for populations Africa. The rate, extent, and timing of gene fow between in southern Africa that have a high incidence of potentially genetically distinct populations have resulted in unique fatal infectious diseases such as HIV and tuberculosis. genetic complexity in almost all populations in southern Africa, as well as fne-scale genetic diferences between populations. Patterns of allele frequency diferences among populations are described as population structure and such allele frequency diferences can have subtle or profound Communicated by S. Hohmann. phenotypic efects, such as diferential susceptibility to infectious disease. * Eileen G. Hoal [email protected] The genetics underlying human disease phenotype vari- ation in African populations have been under-researched. 1 SA MRC Centre for TB Research, DST/NRF Centre However, the NIH and Wellcome Trust-funded initiative of Excellence for Biomedical Tuberculosis Research, named the Human Heredity and Health in Africa (H3Af- Division of Molecular Biology and Human Genetics, Faculty of Medical and Health Sciences, Stellenbosch University, rica) (Adoga et al. 2014; Ramsay 2015) aim to improve the Tygerberg, Parow 7500, South Africa health of all African populations by facilitating research 2 Department of Ecology and Evolution, Stony Brook in the area of genomic and environmental impacts on University, Stony Brook, NY 11794, USA common diseases such as trypanosomiasis, tuberculosis, Vol.:(0123456789)1 3 500 Mol Genet Genomics (2017) 292:499–509 rheumatic heart disease, schizophrenia, type 2 diabetes, and agriculturalists was followed by Arab traders who sailed other cardiometabolic diseases. We focus on recent genetic down the east coast at least as far as Sofala, Mozambique. investigations of the two infectious diseases with the big- The Portuguese (the frst European visitors to South Africa) gest impact on health in southern Africa, viz., tuberculosis encountered the San and Khoekhoen in Mossel Bay, South (TB) and the human immunodefciency virus (HIV). Africa in 1487, although this and subsequent encounters Tuberculosis (TB) and the human immunodefciency were brief due to confict with these indigenous groups. virus (HIV) have high incidence and mortality rates in The Dutch and other Europeans began a formal settlement southern Africa (WHO 2016). A major component of TB at the Cape of Good Hope (present-day Cape Town, South susceptibility is genetic, and recently, it has been estab- Africa) in 1652. Within a short period of time, Indian and lished that part of this susceptibility can be attributed to Asian slaves were brought to the area. These historical a particular ancestral population, which contributed to events are depicted in Fig. 1. Over time, the Bantu-speak- present populations (Daya et al. 2014a, b; Chimusa et al. ing, European, San, and Khoekhoen, all culturally distinct 2014). Understanding the role of ancestry in infectious groups, intermarried with one another, a fact evident not disease risk has manifold benefts, including the identifca- only from their genomes but also from resulting language tion of the most vulnerable populations, providing efective and cultural practices (Scheinfeldt et al. 2010). The Euro- and specialized drug therapies and/or vaccines; and in the pean and Bantu expansion into San and Khoekhoe territory highly probable case of the identifcation of novel suscep- resulted in the decline of the indigenous populations due tibility factors, aiding in the development of new therapies. to confict, disease, and resource scarcity (Fourie and van Here, we review the population structure and prehistory Zanden 2013). of southern African populations, as inferred from recent Archaeological and genetic evidence suggests that the genetic and genomic data sets, to provide a better under- modern human species originated within Africa, though standing of how population structure afects disease risk. the precise location of origin is widely contested due to the Thorough literature searches were performed using Pub- diversity of African populations and complexity of popu- med and Google Scholar to capture a wide array of the lat- lation history (Batini and Jobling 2011). One hypothesis est studies in the feld using “ancestry-related disease risk”, proposes that the earliest population divergence among “southern Africa population genetics”, and “TB and HIV in humans occurred within southern Africa based on the southern Africa” as keywords. exceptional genetic diversity present in KhoeSan groups (Henn et al. 2011). Demographic history within KhoeSan The genetic history of the KhoeSan populations has widely been investigated with particular reference to their origins and thus the origins of modern The KhoeSan are indigenous inhabitants of southern Africa humans. One such study included click-speaking Hadza and their ancestors may represent the earliest divergence and Sandawe individuals from Tanzania, ≠Khomani San among extant human populations (Chen et al. 2000; Ham- from South Africa as well as 24 other African popula- mer et al. 2001; Knight et al. 2003; Tishkof et al. 2007a; tions. Linkage disequilibrium and heterozygosity analysis Brown et al. 2009, 2012; Schlebusch et al. 2009; Naidoo from single nucleotide polymorphism (SNP) array data et al. 2010; Marean 2010; Henn et al. 2011). The genetic demonstrated that the ≠Khomani and other KhoeSan from origin of the KhoeSan can be traced back to the emergence Namibia are two of the most genetically diverse popula- of modern humans in southern Africa (Gronau et al. 2011; tions in the world (Henn et al. 2011). In conjunction with Henn et al. 2012). Prior to 2500 years ago, all KhoeSan Fst patterns (a measure of genetic distance between popu- populations in southern Africa hunted game or fshed, for- lations), their results suggested that humans originated aged for plants, and gathered natural products, hence the in southern Africa (Henn et al. 2011). This conclusion is anthropological term of hunter-gatherers. Some contempo- supported by microsatellite and indel data (Tishkof et al. rary KhoeSan populations continue to forage, while other 2009). It was found that the two southern African KhoeSan groups have transitioned to wage labour or stock farming. populations from this study clustered together when phylo- The Khoekhoen are pastoralists who derive their ancestry genetic trees were constructed from genetic distances (Fst) from the original hunter-gatherer KhoeSan, but adopted between populations. These populations were also the most sheep, goat, and cattle husbandry from east African pasto- distinct populations worldwide (Tishkof et al. 2009). This ralists approximately 2000 years ago (Pleurdeau et al. 2012; is broadly consistent with studies on mitochondrial DNA Uren et al. 2016; Montinaro et al. 2017). Bantu-speaking and Y chromosome, which indicated divergent genetic line- farmers arrived in southern Africa from approximately AD ages (Behar et al. 2012; Poznik et al. 2013). Studies investi- 600 onwards, having migrated down both the west and east gating the geographical origins of modern humans depend coasts of Africa, and subsequently impacted the Khoek- on contemporary populations which might not be truly hoe and San way of life. The expansion of Bantu-speaking representative of historical populations (Haber et al. 2016). 1 3 Mol Genet
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