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History and genetics of African cattle domestication




Case Type: 


This project will contribute new genetic evidence towards debates on the origins and spread of African cattle by sequencing complete mitochondrial genomes of cattle herds in Southern Africa. In contrast to early and mid-Holocene fauna from Egypt and Eastern Africa, the best-preserved and dated faunal samples come from early farmer sites in southern Africa. Yet, these remains have not been subject to ancient DNA analyses. The only study of complete mitochondrial genomes from modern Nguni cattle in South Africa by Horsburgh has shown that Nguni sequences are substantially different from cattle in Egypt and Ethiopia and outside Africa. Paired with further study of modern cattle, we propose to examine pre-colonial cattle remains to compare with modern and mtDNA data previously collected from Egypt and Eastern Africa. This permit is for the export and analysis of teeth from the 18th C site of Nqabeni.


The History and Genetics of African Cattle Domestication: Insights from Southern African Cattle Breeds 1. Issues and Objectives Animal domestication is one of the key transitions in human history. It stimulated a transformation of economic and social relations in human societies and how people thought about and utilized landscapes. However, the process of animal domestication and social transformation was not uniform. Rather, archaeological, environmental, linguistic and genetic evidence demonstrate the processes are complex and nuanced, and had different long-term effects on the development of complex societies globally. The domestication and spread of cattle in Africa represent one of the most controversial transitions (Gifford-Gonzalez, 2013). There is no agreement on how many domestication events occurred across the continent’s diverse biomes and there is a deficit of genetic evidence from eastern sub-equatorial Africa, a region with the best preserved archaeological and linguistic evidence for the spread of distinctive mixed-farming societies between 3000 and 1300 years ago. Collaboration between archaeologists and genetic researchers working in Africa lags far behind the efforts of researchers on animal domestication in Eurasia (Gifford-Gonzalez, 2013). The purpose of this project is to contribute new genetic evidence towards debates on the origins and spread of African cattle by sequencing complete mitochondrial genomes of cattle herds in Southern Africa. Our general objective is to utilize these new data to address three specific issues confronting the application of genetic data to understand the origin, spread, and development of cattle pastoralism in Eurasia and Africa: (1) the spread cattle domestication from Eastern Africa, (2) the late precolonial introduction of cattle from the Indian sub-continent, and (3) the effects of a continent-wide panzootic on indigenous cattle genetic diversity. 2. Issues in the study of African cattle pastoralism Present-day African cattle represent a unique population particularly adapted to the challenging conditions of semi-arid and sub-tropical environments. It comprises nearly 356 million animals and more than 150 different breeds (Glatzel et al. 2020), which fall into three groups: taurine, indicine, and hybrid. The question of their origins, antiquity, and spread on the continent has been debated for the last 50 years by archaeologists, and in the last quarter century by both archaeologists and geneticists. 2.1 Origins and spread of cattle pastoralism Domestic cattle have their ancestry among wild aurochs (Bos primigenius), a taxon naturally distributed across northern Africa, Eurasia and India, which became extinct in the 17th century (Van Vuure, 2005). Modern domesticated cattle comprise two distinct, though completely interfertile groups: taurine and indicine cattle. Taurine cattle (Bos taurus) account for most of the herds in the temperate regions of Europe, Western Africa and northern Asia. Indicine cattle (Bos indicus) are phenotypically identifiable by the presence of a substantial cervicothoracic hump and are better adapted to arid conditions and dominate across the Indian sub-continent (Caramelli, 2006). Presently, the origins debate in Africa centers on whether wild cattle were first independently domesticated in southwestern Asia (taurine) and south-central Asia (indicine) 8,000-9,000 years ago and brought to Africa, or whether Africa represents a third and separate taurine domestication event some 7,000 years ago (Bonfiglio et al., 2012; Caramelli, 2006). Evidence of domesticated cattle in Africa by about 7,400 years ago includes rock art in what is now the Sahara Desert (Muzzolini, 2000) and archaeological remains attributed to domestic stock based on their bone morphology (Clutton-Brock, 1989; Smith, 1980; Smith, 1986). Cattle based pastoralism, including dairying (Dunne et al., 2012), was probably practiced throughout northern Africa by about 6,000 years ago and gradually moved south, pushed by desire to escape the increasingly hostile climate of the Sahara. Herders with cattle, sheep and goats spread into eastern Africa (Kenya and Tanzania) shortly before 4,000 years ago and had become widespread across the region by 3,000 years ago (Lane, 2013). Debate on the spread of cattle pastoralism across Africa hinges on whether people moved with cattle west and south from Eastern Africa 3,000 years ago (demic diffusion) or whether cattle were instead initially involved in exchange networks thereby spreading cattle into new areas independently of pastoralists (trans-cultural diffusion). Archaeological, genetic and linguistic data only support a model of demic expansion of culturally and linguistically distinct Bantu-speaking farmers into northeastern river valleys and southeastern coastlands through a series of migrations from Eastern Africa in the early centuries of the first millennium AD (50-350 AD) (Mitchell, 2002). They carried with them the remainder of the founding population of East African cattle that were tolerant to trypanosomiasis (sleeping sickness), as well as other domestic plants and animals (sheep, goat, chickens), metallurgy, and distinctive ceramics (Huffman, 2007; Williamson and Blench, 2000). Researchers fixed in these debates have attempted to reconcile evidence from ancient animal remains, ecology, linguistics, and genetics. Sometimes these data complement each other, but often they do not (Stock and Gifford-Gonzalez, 2013). Early and mid-Holocene faunal remains are often poorly preserved, making the identification of domesticates through bone morphology difficult or impossible. Most remains are indirectly dated at archaeological sites, some with very complex, and others with non-existent, stratigraphic sequences, which can under-estimate the age of the remains. Chronologies provided by historical linguistics are controversial, only rarely aligning with archaeological dating frameworks (Stock and Gifford-Gonzalez, 2013). It is widely acknowledged that the best preserved and dated faunal samples come from early farmer sites in southern Africa. 2.2 The genetic data The genomes of modern cattle populations play a central role in reconstructing the history of their domestication because their mitochondrial and Y-chromosome DNA holds the ancestry of the original founder populations that no longer exist. Recovery and analysis of mtDNA from archaeological cattle bones from East, West, and southern African sites, and comparison of these lineages with those of modern humped cattle in East Africa, is necessary to elucidate these questions. Today, hybrids of taurine and indicine types are found throughout sub- Saharan Africa (Bradley et al., 1998; Clutton-Brock, 1989). Regardless of their morphology, however, modern African cattle all possess mitochondrial haplotypes derived from non-humped taurine ancestors (Bradley et al., 1996; Dadi et al., 2009) although many possess indicine Y-chromosomes (Hanotte et al., 2000). The majority of taurine cattle are members of mitochondrial macro-haplogroup T, comprising haplogroups T1– T5, although taurine members of haplogroups P, Q and R also exist in much lower frequencies (Achilli et al., 2009). It has been shown, however, that while T1, T2 and T4 belong to the same taxon and share a common ancestor (monophyletic), T and T3 do not (Ho et al., 2008; Troy et al., 2001). Nearly all modern African cattle carry haplogroup T1 (Ho et al., 2008; Troy et al., 2001; Cymbron et al., 1999), which is further subdivided into six subhaplogroups T1a – T1f (Bonfiglio et al., 2012). These subhaplogroups are largely defined by mutations that fall outside the frequently sequenced control region, making the sequencing of complete mitochondrial genomes crucial for advancing our understanding of the phylogeography of T1 cattle in general, and African cattle in particular. The major deficit in ancient DNA research, which has now largely overcome problems of accuracy, is sampling bias. Complete mitochondrial genomes of cattle have only been published from herds in Egypt and Ethiopia (Bonfiglio et al., 2012) and a single modern herd of cattle in the southern third of the continent (Horsburgh et al., 2013). These limited genetic data contribute toward the bias of European cattle breeds into estimates of genetic distance (Decker et al., 2009), and limit the possibility of testing whether there was a unique African domestication trajectory. More importantly, the African genetic data add little to debate over the spread of pastoralism because the effects of two historical circumstances on modern cattle population genetics remain unclear: (1) the potential hybridization introduced from indicine cattle traded into eastern and southern Africa from the Indian subcontinent in the later precolonial era (Anderung et al., 2007; Freeman et al., 2004; Hanotte et al., 2002; Huffman, 2007; MacHugh et al., 1997; Mitchell and Whitelaw, 2005), and (2) the repopulation of southern taurine herds from those in Eastern Africa and Europe due to the rinderpest panzootic in the 1890s that killed most cattle in sub- Saharan Africa (Mack, 1970). 2.3 The potential contribution of southern African cattle The only study of complete mitochondrial genomes from Nguni cattle in South Africa (Horsburgh et al., 2013) has shown that the Nguni sequences are substantially different from cattle found in Egypt and Ethiopia and outside Africa. All are members of subhaplogroup T1b, and most display a previously uncharacterized variation in T1b1. They also demonstrate nucleotide diversity lower than in Ethiopia, which is likewise lower than in Egypt. It is unknown if this pattern is a consequence of isolation by distance, or if other environmental and/or historical factors account for the breeding isolation of founding cattle populations as they spread from north to south. 3. Research Design In this project, we have developed an interdisciplinary program of genetic and archaeological research to contribute towards each of these issues. This study will characterize the complete mitochondrial genomes of cattle from both modern Nguni cattle herds and historically recent Nguni cattle remains from 18th and 19th century archaeological sites in southeastern Africa. The sites have well preserved cattle remains and are well understood from a combination of archaeological research, oral and documentary historical evidence, and later ethnography of descendant populations. We focus on the Nguni breed to try to reconstruct the history of cattle expansion because they represent a distinctive, conserved phenotype widely recognized by local farmers, and because there are no modern breeds with direct association with the earliest pastoralists in the region during the first millennium AD, although there are archaeological specimens of these stock. The Nguni cattle breed is named for their historical association with speakers of Nguni languages, one branch of the Bantu language family, which includes the languages of Zulu, Xhosa, Ndebele, and Swazi peoples. Ancestors of Nguni speaking peoples first entered Southern Africa at the turn of the second millennium AD (Huffman, 2004). Today, Nguni speakers comprise the bulk of African populations from Zimbabwe in the north to the eastern Cape in South Africa. The specific objectives of our project are to 1. provide the first data on the genetic diversity of modern Nguni cattle based upon the study of complete mitochondrial genomes from multiple herds of known ancestry; 2. provide the first comparison of modern and pre-rinderpest domesticated cattle samples in southern Africa; 3. utilize new data from the modern and historically recent samples to contribute towards current debates on the origins and spread of African cattle by focusing on breeds with superior disease tolerance, higher calving rates, and the ability to walk long distances. We think that this approach begs fewer conceptual questions about the significance and meaning of genetic data in social and historical terms because it does not historically decontextualize the genetic data nor ignore the influence of people and their practices on herd management and composition. By combining genetic data with a rich archaeological and historical record, we will contribute toward both the major issues confronting the integration of genetic data into debate over the origin and spread of domesticated cattle and provide a deeper and more nuanced understanding of the specific pastoral practices of Nguni speaking people prior to European colonization. Furthermore, we follow others in contending that a deeper understanding of domestic animals’ coevolution with humans “and their resultant genomes, can offer a vast amount of historical information that may be especially relevant to modern African communities dealing with social and environmental changes” (Gifford-Gonzalez, 2013:16). 3. Methods 3.1 Data Sets The proposed project is based upon the study of two data sets: hair samples from modern Nguni cattle and fauna from 19th century and 18th century archaeological sites. The hair samples will be collected from 300 head across a minimum of five herds of Nguni cattle from the province of KwaZulu-Natal in South Africa. We are working closely with the KZN Nguni club of the Nguni Cattle Breeders’ Society of South Africa (NCBS) to obtain access to herds. These efforts are being coordinated by Fowler and Mr. Nico Harris, Chairman of KZN Nguni and Vice-President (Technical) of the NCBS. For the archaeological sample, we will turn to two significant later precolonial sites in northern KwaZulu-Natal. The first is the site of uMgungundlovu, the royal ikhanda, or capital, of the Zulu king Dingane from 1828-1839 (Parkington and Cronin, 1979; Plug and Roodt, 1990; Roodt, 1993). We currently have access to 58 cattle specimens from the site (43 cattle teeth, 15 bones) which were obtained on permanent export for destructive analysis in 2016. This sample has been micro drilled for strontium isotope analysis leaving the teeth and bone completely intact and viable for future studies (Fowler et al., 2020). The second sample will come from the 18th century AD site of Nqabeni (Hall and Maggs, 1979). This is the name-site of the Nqabeni phase (1700-1850 AD) in the eastern lowland cultural-historical framework (Huffman, 2004). Based on excavation records, dental material was best preserved at the site although there are identifiable post-cranial remains of cattle. A total of 76 cattle teeth were documented. We expect to examine 30 teeth and 20 bone fragments from Nqabeni. From this total sample we will run 100 specimens for mitochondrial DNA analysis. 3.2 Data Collection DNA will be extracted from the modern hair samples using the Monarch Genomic DNA Purification Kit (New England BioLabs Inc). PCR amplification of the mitochondrial genome will be undertaken in two or four fragments depending on the quality of the extracted DNA using previously published primers (Horsburgh et al., 2013) and KAPA HiFi HS DNA Polymerase (Roche, Ltd). Following clean up (DNA Clean and Concentrator-5, Zymo Research, Ltd), DNA will be fragmented and barcoded Illumina sequencing libraries constructed using NEBNext Ultra FS DNA Library Prep Kit (New England BioLabs, Ltd). Pooled, normalized libraries will be sequenced with 100PE reads at the University of Chicago Genomics Facility Sequencing Core on the Illumina HiSeq 4000. All ancient DNA laboratory work will be undertaken in the dedicated and purpose-built ancient DNA suite of the Southern Methodist University Molecular Anthropology Laboratories. Ancient DNA will be extracted using a modified silica and guanidinium thiocyanate protocol (Allentoft et al., 2015) and barcoded Illumina sequencing libraries constructed using SRSLY PicoPlus NGS Library Prep Kit (Claret Bioscience). The manufacturers library preparation protocol will be modified only by exchanging the kit’s DNA polymerase for KAPA’s HiFi Uracil+ enzyme (Roche, Ltd) which can read through cytosine residues that have been deaminated to uracil, a common form of damage observed in ancient DNA (Dabney et al., 2013). We will therefore retain deaminated molecules and increase DNA recovery rate. DNA sequencing libraries will be enriched for the mitochondrial genome using MyBaits probes designed for cattle (MYcroarray Ltd) following the manufacturer’s protocol for low quantity and low quality targets. Enriched sequencing libraries will be qualified by quantitative PCR using Bio- Rad’s CFX96 Touch Real Time PCR Detection System and the NEBNext Library Quant Kit for Illumina (New England BioLabs, Ltd). After pooling in equimolar ratios, libraries will be sequenced with 100PE reads at the University of Chicago Genomics Facility Sequencing Core on the Illumina HiSeq 4000. 3.3 Data Analysis Modern genetic data will be mapped to the compete mitochondrial genome of Bos taurus (GenBank V00654.1) using the Burrows-Wheeler Alignment tool (Li and Durbin, 2009). Ancient genetic data will be processed to remove sequences with stretches of Ns, low quality scores or short read lengths, then mapped using the Burrows-Wheeler Alignment tool, with ancient DNA settings. Samtools (http://samtools.sourceforge.net/samtools-c.shtml) will be used to remove PCR duplicates, and mapDamage (Jónsson et al., 2013) to assess damage patterns characteristic of genuinely ancient DNA. Coverage plots, used to assess mean coverage across the mitochondrial genome, will be generated using the R package ggplot2. Phylogenetic relationships within and between our samples and previously sequenced African cattle will be assessed by calculating maximum likelihood trees in PhyML 3.0 (Lefort et al., 2017). Demographic history will be calculated using Bayesian Skyline plot analyses implemented in BEAST 2.5 (Bouckaert et al., 2019). These analyses permit estimates of the effective population sizes over time, the relationships between different groups of cattle, and the timing of divergences of populations. 4. Significance and potential impact This research project is significant because it will vastly expand our present understanding of the genetic heritage of African cattle breeds and the history of animal domestication. These new data will impact current theories of wild cattle domestication in Asia, Europe and Africa, by isolating variants of haplogroup T1 in southern African cattle breeds. More specifically, this study will impact theories of the spread and adaptations by wild cattle within eastern African savannah and savannah-woodland biomes by providing a clearer understanding of eastern African cattle founder populations though an expansion of the existing database of subhaplogroup T1b cattle populations. Genetic research on modern and ancient African cattle breeds also hold tremendous potential to safeguard food security globally, and, specifically, in arid and semiarid environments with lower quality pastureland and high disease loads. Modern African cattle breeds represent a unique genetic resource adapted to these conditions at a juncture when there is an urgent need to improve livestock productivity for the benefit of the present and future human generations. These kinds of data are extremely valuable to present-day Nguni breeders and, as such, regularly feature in publications such as the Nguni Journal (e.g., Sholtz, 2020). Domestic cattle continue to hold deep economic and symbolic significance for African peoples (e.g., Bollig et al. 2013). This study introduces new genetic evidence to our understanding of that value system and the intimate role cattle have played in human relationships across Africa for seven millennia. 5. Timeline This project’s timeline has been impacted by the Covid-19 pandemic. A revised timeline sanctioned by the Social Sciences and Humanities Council of Canada (SSHRC) is presented below. This timeline will see sample collection and the beginning of data analyses in 2022, the analyses completed in 2023 and the first two of four planned publications completed that year. A public outcome publication, and planned fourth paper, and conference presentations are scheduled for 2023, at which time the archaeological sample will be returned to the Amafa and Research Institute repository in Pietermaritzburg. 6. References Cited Achilli, A. et al. (2009) The multifaceted origin of taurine cattle reflected by the mitochondrial genome. PLOS ONE, 4, e5753. Allentoft, M.E. et al. (2015) Population genomics of bronze age Eurasia. Nature, 522, 167-172. 7 Anderung, C. et al. (2007) Investigation of X‐ and Y‐specific single nucleotide polymorphisms in taurine (Bos taurus) and indicine (Bos indicus) cattle. Animal Genetics, 38, 595-600. Bollig, M., Schnegg, M. & Wotzka, H.-P. (Eds.) (2013) Pastoralism in Africa: Past, present and future. Berghahan, New York/Oxford. Bonfiglio, S. et al. (2012) Origin and spread of Bos taurus: new clues from mitochondrial genomes belonging to haplogroup T1. PLOS ONE, 7, e38601. Bouckaert, R. et al. (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLOS Computational Biology, 15, e1006650. 10.1371/journal.pcbi.1006650. Bradley, D.G. et al. (1998) Genetics and domestic cattle origins. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews, 6, 79-86. Bradley, D.G. et al. (1996) Mitochondrial diversity and the origins of African and European cattle. Proceedings of the National Academy of Sciences, 93, 5131-5135. Caramelli, D. (2006) The origins of domesticated cattle. Human Evolution, 21, 107-122. Clutton-Brock, J. (1989) Cattle in ancient North Africa. In The walking larder: Patterns of domestication, pastoralism, and predation, (Ed, Clutton-Brock, J.) Allen & Unwin Australia, pp. 200-206. Cymbron, T. et al. (1999) Mitochondrial sequence variation suggests an African influence in Portuguese cattle. Proceedings of the Royal Society B, 266, 597-603. Dabney, J., Meyer, M. & Pääbo, S. (2013) Ancient DNA damage. Cold Spring Harbor Perspectives in Biology, 5, a012567. Dadi, H. et al. (2009) Variation in mitochondrial DNA and maternal genetic ancestry of Ethiopian cattle populations. Animal Genetics, 40, 556-559. Decker, J.E. et al. (2009) Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proceedings of the National Academy of Sciences, 106, 18644-18649. Dunne, J. et al. (2012) First dairying in green Saharan Africa in the fifth millennium BC. Nature, 390- 394. Fowler, K.D., Yang, P. & Halden, N.M. (2020) The provisioning of nineteenth century Zulu capitals, South Africa: Insights from strontium isotope analysis of cattle remains. Journal of Archaeological Science: Reports, 31, 10.1016/j.jasrep.2020.102306. Freeman, A.R. et al. (2004) Admixture and diversity in West African cattle populations. Molecular Ecology, 13, 3477-3487. Glatzel, K. et al. (2020) Meat, milk and more: Policy innovations to shepherd inclusive and sustainable livestock systems in Africa. Malabo Montpellier Panel Report 2020. Gifford-Gonzalez, D. (2013) Animal genetics and African archaeology: why it matters. African Archaeological Review, 30, 1-20. Hall, M. & Maggs, T. (1979) Nqabeni, a Later Iron Age site in Zululand. South African Archaeological Society Goodwin Series, 3, 159-176. Hanotte, O. et al. (2002) African pastoralism: Genetic imprints of origins and migrations. Science, 296, 336-339. Hanotte, O. et al. (2000) Geographic distribution and frequency of a taurine Bos taurus and an indicine Bos indicus Y specific allele amongst sub‐Saharan African cattle breeds. Molecular Ecology, 9, 387-396. Ho, S.Y.W. et al. (2008) Correlating Bayesian date estimates with climatic events and domestication using a bovine case study. Biology Letters, 4, 370-374. Horsburgh, K.A. et al. (2013) The genetic diversity of the Nguni breed of African cattle (Bos spp.): Complete mitochondrial genomes of Haplogroup T1. PLOS ONE, 8, e71956. 10.1371/journal.pone.0071956. 8 Huffman, T.N. (2004) The archaeology of the Nguni past. Southern African Humanities, 16, 79-111. Huffman, T.N. (2007) A handbook to the Iron Age: The archaeology of pre-colonial farming societies in southern Africa. University of KwaZulu-Natal Press, Pietermaritzburg. Jónsson, H. et al. (2013) mapDamage2. 0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics, 29, 1682-1684. Lane, P.J. (2013) The archaeology of pastoralism and stock-keeping in East Africa. In The Oxford handbook of African archaeology, (Eds, Mitchell, P. & Lane, P.J.) Oxford University Press, Oxford, pp. 585-601. Lefort, V., Longueville, J.-E. & Gascuel, O. (2017) SMS: smart model selection in PhyML. Molecular biology and evolution, 34, 2422-2424. Li, H. & Durbin, R. (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. bioinformatics, 25, 1754-1760. MacHugh, D.E. et al. (1997) Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). Genetics, 146, 1071-1086. Mack, R. (1970) The great African cattle plague epidemic of the 1890s. Tropical Animal Health and Production, 2, 210-219. Mitchell, P. & Whitelaw, G. (2005) The archaeology of southernmost Africa from c. 2000 BP to the early 1800s: a review of recent research. The Journal of African History, 46, 209-241. Mitchell, P. (2002) The archaeology of Southern Africa. Cambridge University Press, Cambridge. Muzzolini, A. (2000) Livestock in Saharan rock art. In The origins and development of African livestock: archaeology, genetics, linguistics and ethnography, (Eds, Blench, R. & MacDonald, K.) Routlege, London/New York, pp. 87-110. Parkington, J. & Cronin, M. (1979) The size and layout of uMgungundlovu: 1829-1839. South African Archaeological Society Goodwin Series, 3, 133-148. Plug, I. & Roodt, F. (1990) The faunal remains from recent excavations at uMgundgundlovu. The South African Archaeological Bulletin, 45, 47-52. Roodt, F.R. (1993) ‘n Rekonstruksie van geelkoperbwerking by Mgundgundlovu. Master of Arts thesis, University of Pretoria. Sholtz, M.M. (2020) The origin and genetic composition of Nguni cattle in South Africa. Nguni Journal, 17, 30-36. Smith, A.B. (1980) Domesticated cattle in the Sahara and their introduction into West Africa. In Quaternary environments and prehistoric occupation in northern Africa, (Eds, Williams, M.A.J. & Faure, H.) pp. 489-503. Smith, A.B. (1986) Cattle domestication in North Africa. African Archaeological Review, 4, 197-203. Stock, F. & Gifford-Gonzalez, D. (2013) Genetics and African cattle domestication. African Archaeological Review, 30, 51-72. Troy, C.S. et al. (2001) Genetic evidence for Near-Eastern origins of European cattle. Nature, 410, 1088-1091. Van Vuure, C. (2005) Retracing the aurochs: History, morphology and ecology of extinct wild ox. Pensoft Publishers, Sofia, Bulgaria. Williamson, K. & Blench, R. (2000) Niger-Congo. In African languages: An introduction, (Eds, Heine, B. & Nurse, D.) Cambridge University Press, pp. 11-42.


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