- Background: Humpless Bos taurus cattle are one of the earliest domestic cattle in Africa, followed by the arrival of humped Bos indicus cattle. - The diverse indigenous cattle breeds of Africa are derived from these migrations, with most appearing to be hybrids between Bos taurus and Bos indicus . - Methods: Data for ~ 40 k SNPs was obtained from previous projects for 4089 animals representing 35 African indigenous, 6 European Bos taurus , 4 Bos indicus, and 5 African crossbred cattle populations. - Results: The first two principal components differentiated Bos indicus from European Bos taurus , and African Bos taurus from other breeds. - indigenous breeds are either pure African Bos taurus or admixtures of African Bos taurus and Bos indicus. - The African zebu breeds had highest proportions of Bos indicus ancestry ranging from 70 to 90% or 60 to 75%, depending on the admixture model. - Other indigenous breeds that were not 100% African Bos taurus , ranged from 42 to 70% or 23 to 61% Bos indicus ancestry. - The African Bos taurus populations showed substantial genetic diversity, and other indigenous breeds show evidence of having more than one African taurine ancestor. - Conclusion: African indigenous cattle breeds have a large genetic diversity and are either pure African Bos taurus or admixtures of African Bos taurus and Bos indicus. - Keywords: Admixture, African crossbreds, African indigenous, Bos taurus , Bos indicus , Effective population size, Genetic differentiation, Linkage disequilibrium, SNPs. - Using genome-wide SNP data of 67 ancient Near Eastern Bos taurus and modern populations, Verdugo et al. - [4] suggested that the an- cient Levantine genome affinity with Moroccan aurochs implies that the distinct phenotypes and genotypes in African Bos taurus cattle may stem from roots in the southern Fertile Crescent. - In their review of the evi- dence, Stock and Gifford-Gonzalez [5] concluded that Bos taurus cattle likely spread across the Sinai and into the Nile Delta 7000 to 8000 BP, then across North Af- rica, and subsequently into the Nile and the then-grassy Sahara, possibly with additional inputs through the Horn of Africa. - Humpless, presumably Bos taurus cattle first appear to be present south of the Sahara about 4500 to 4000 BP [6, 7]. - A few depictions of Egyptian cattle show humped animals, which are claimed as evidence for the presence of Bos indicus cattle in Egypt from 3500 BP [8].. - The earliest evidence for Bos indicus cattle in sub- Saharan Africa is in East Africa, where all samples, that could be analyzed from two sites dated around 2000 to 2500 BP, were of Bos indicus or Sanga (a hybrid of Bos indicus and Bos taurus ) type [9]. - This suggests that Bos indicus genes were already predominant in the pastoral systems in this region. - Payne and Hodges [6] concluded that Bos taurus cattle, however, remained predominant in Ethiopia and East Africa until recently despite many waves of Bos indicus introductions to the region from about 2500 BP onwards.. - Rege and Tawah [11] sug- gested four categories of indigenous breeds: Bos taurus , Bos indicus (zebu), Sanga ( Bos taurus × Bos indicus hy- brid. - According to Lenstra and Bradley [12], African Bos taurus breeds are those that have short ears and no hump, while zebu breeds are those that have long floppy ears and a prom- inent hump. - Subsequent results based on molecular marker data [13] and results presented here show that the genetic diversity of African cattle is more complex than this, most particularly, no African indigenous breeds have been shown to be pure Bos indicus . - means that the breed has a hump, but it does not imply that the breed is pure Bos indicus , despite much of the literature using zebu and Bos indicus as synonymous when applied to African cattle.. - Studies of mitochondrial DNA (mtDNA) variation in- dicated that the two major groups of cattle, Bos taurus and Bos indicus, were genetically distinct before domes- tication [14–16]. - using genome sequence data on ancient cattle samples revealed that cattle origins consisted of two divergent aurochs populations that formed the basis of the Bos indicus and Bos taurus divide. - These authors also showed, using mtDNA sequence data, that there was male-driven Bos indicus introgression into the Near East Bos taurus populations. - Studies of microsatellite DNA and Y-chromosomal markers showed extensive intro- gression of male Bos indicus genes into existing African cattle populations [17–19], all of which currently carry Bos taurus mtDNA, indicating male-driven introgression of Bos indicus genes into the previously Bos taurus Afri- can cattle populations. - [13] showed that all indigenous cattle breeds from Tanzania, Kenya, Uganda, and Ethiopia were admixtures of Bos indicus and African Bos taurus.. - The first two components accounted for 88.7 and 5.7% of the total genetic variation, respectively, and differentiated the Bos indicus, European Bos taurus, and African Bos taurus breeds from each other as the apexes of a triangle in the plot area (Fig. - N’Dama2 and especially N’Dama3 appeared to include animals that spread towards the pooled Bos indicus reference breeds, showing that they are not pure African taurine breeds (Fig. - The Sheko1, Maure, Boran Ethiopia1, and Madagascar-zebu clustered further towards the Africa taurine breeds (i.e., lower Bos indicus admixture) and spread between the two axes that connect the indicine to the first African taurine group (axis 1) versus the second African taurine group (axis 2).. - Model 2 included an additional four African taurine reference breeds to differentiate the Afri- can Bos taurus background. - However, the West African breeds, espe- cially from Senegal, showed a wide range of Bos indicus ancestry. - The African taurine breeds N’Dama1, Lagune, Lagu- naire, and Baoule showed >. - Admixture Model 2, which included five African Bos taurus breeds as ancestral reference breeds, identified a difference in the assigned African taurine ancestry be- tween cattle breeds from East, South, and West Africa.. - Of the African. - taurine breeds that were not used as reference ancestral breeds, N’Dama2 appeared to be an admixture of all refer- ence African taurine breeds (N’Dama1 = 58.8%, Baoule = 15.7%, N’Dama = 15.3%, Somba = 2.1%, and Lagune = 4.0%) plus 4.1% Bos indicus ancestry. - N’Dama3 showed 94.2% N’Dama1 plus 5.2% Bos indicus ancestry. - Breed differentiation, as represented by F ST values, showed a strong divergence within different groups of breeds (European Bos taurus , African Bos taurus , zebu types, Sanga types including admixed breeds, and Bos indicus . - Ranked from lowest to highest genetic differentiation between breeds within groups are zebu types, Bos indicus , Sanga types, African Bos taurus, and lastly, European Bos taurus . - Some notable outliers within the breed groups are N’Dama3, which has high F ST with all other Africa Bos taurus breeds. - Ne was calculated for various generations in the past using r 2 and r 2 adj for the nine African indigenous breeds Table 1 Admixture proportions from supervised analyses (mean ± SD) of African indigenous breeds for indicine, African taurine and total European taurine ancestry. - EUT 5 European Bos taurus breeds, NDA1 N’Dama1, LAG Lagune, BAO Baoule. - in the analyses. - Depending on the used data and underlying assumption about biological clocks, estimates of divergence between Bos taurus and Bos indicus vary from approximately 200, 000 to 300,000 years BP to 575,000 to. - a East African crossbreds. - The PCA and F ST results showed a clear divergence between Bos indicus , African Bos taurus , and European Bos taurus reference breeds, which is in agreement with several previous studies [4, 26–32]. - As shown here and in other studies, the first two principal components differentiate the groups with the largest genetic differences (PC1 Bos taurus vs. - Bos indicus , PC2 European Bos taurus vs. - Africa Bos taurus. - Among the African cattle populations, there are no pure Bos indicus populations in our sample. - Based on the range of samples included in our study, it is un- likely that any indigenous breeds of Africa are pure Bos indicus. - As outlined in the background section, it has been assumed in the literature that the admixed indigenous breeds of Africa arose from Bos indicus cattle entering Africa and breeding with existing Afri- can Bos taurus populations [8, 9]. - Verdugo et al. - concluded that Bos taurus populations in the Near East became admixed with Bos indicus likely due to human migrations around 4200 years BP. - The popula- tions they sampled in the Levant, which were the closest samples to the putative first route of Bos indi- cus into Africa through Egypt, showed a Bos taurus genotype that was closest to modern African Bos taurus . - already have been hybrids between Bos taurus and Bos indicus rather than pure Bos indicus. - Our results show that, other than the pure African Bos taurus populations, all African indigenous cattle popula- tions are admixtures of Bos indicus and African Bos taurus , with West African and Southern African popula- tions showing lower Bos indicus admixture than East African populations consistent with recent studies by Pitt et al. - The PCA showed that the existing African Bos taurus populations and our reference European Bos taurus pop- ulations exhibit much greater diversity than the set of Bos indicus populations used in our analyses. - Studies that included much larger samples of European Bos taurus cattle similarly showed greater diversity among European Bos taurus versus Bos indicus cattle (e.g.. - Our re- sults indicate that the greater diversity of Bos taurus cat- tle extends to African Bos taurus in addition to European Bos taurus. - The distribution of indigenous breeds in the PC plots (Fig. - 1a, b) and the results from Admix- ture (Table 1, K = 11) suggest a different African Bos taurus ancestry for West African versus East African indigenous.. - Kuri is generally referred to as be- ing an African Bos taurus breed [42], but our results show that Kuri is an admixture between African Bos taurus and Bos indicus. - The Oulmes Zaer showed high heterozy- gosity consistent with its high European Bos taurus an- cestry and being an admixture between African and European Bos taurus . - Gautier and Naves [44], who ana- lyzed the same Oulmes Zaer samples as here but with a very different set of 23 other breeds, also found that Oulmes Zaer was of hybrid origin between African and European Bos taurus . - The rather dispersed cluster of the Oulmes Zaer samples in the PC plots suggests the possi- bility that the breed might have been deliberately created by the crossing of African and European Bos taurus cat- tle in relatively recent times.. - In the current study, the European dairy proportions found in East and West African crossbreds reflect the reported history of crossbreeding. - The European reference dairy breeds showed a higher level of LD across all inter- val sizes compared to Bos indicus reference breeds and most African indigenous breeds (Figure S3), reflecting that intensive selection has caused relatively low effective population sizes generating high LD in the European dairy breeds [52, 53].. - The Bos indicus reference breeds and all African indigenous populations, including the African Bos taurus breeds, show a substantially higher Ne 12,000 years ago ( Ne = 5000 to 7000) than the European Bos taurus breeds ( Ne = 2000 to 3500, Figure S4). - Given the admixed Bos indicus and African Bos taurus ancestry of most African indigenous breeds, a high Ne pre-domestication is not unexpected, but the higher Ne of Bos indicus and African Bos taurus com- pared to European Bos taurus suggest that European Bos taurus was domesticated from a smaller population than African Bos taurus and Bos indicus . - An alternative explanation of the in- crease in Ne about 200 generations ago might be a period of hybridization between existing indigenous pop- ulations and/or between indigenous populations and Bos indicus cattle, following the migration of Bantu-speaking agropastoralists from eastern to southern Africa around 1500 years BP [57], and the second wave of Bos indicus cattle that are believed to have entered Africa with the migration of Arab peoples starting around 1500 to 1300 years BP.. - Corbin et al. - African indigenous cattle are genetically diverse due to historical and highly diverse admixture of Bos indicus, African Bos taurus, and European Bos taurus. - In addition to the crossbreds, exotic reference breeds, one African synthetic breed, and one unclassified African indigenous breed were used, and 669 samples representing 33 breeds or populations within the three main African indigenous cattle breed groups of African Bos taurus , African zebu, and Sanga (Table 3). - Bos indicus and European Bos taurus breeds were in- cluded to represent the major known anchor points of global cattle diversity against which African cattle diver- sity can be assessed. - The European Bos taurus breeds were chosen because these breeds are known to have contributed to the crossbred dairy populations included in our study, allowing clearer interpretation of results than inclusion of other breeds or a larger sample of breeds. - The reference breeds included five African Bos taurus (N’Dama, N’Dama1, Lagune, Baoule, and Somba), four Bos indicus (Nelore, Sahiwal, Gir, and Guzerat), and. - Ankole-Watusi Sanga East African Ruanda 5 Decker et al. - Boran1 zebu East African Ethiopia 20 Decker et al. - Sheko Sanga East African Ethiopia 17 Decker et al. - six European Bos taurus dairy breeds (Guernsey, Holstein, Jersey, Canadian Ayrshire, British Friesian, and Montbeliarde). - Analysis of the genetic structure. - The second GRM was used to evaluate the genetic structure and diversity among the African taurine breeds to select the African Bos taurus reference populations to be used in the Ad- mixture analysis. - To investigate the genetic admixture of the indigenous and crossbred cattle populations, a maximum likelihood model implemented in the software ADMIXTURE 1.23 [64] was applied. - Also, prior literature [33, 66] and our analyses have previously demonstrated that there are three ancestral populations of African cattle (African Bos taurus , European Bos taurus, and Bos indicus. - A pooled sample of Bos indicus ref- erence (indicine) was created with eight animals per breed because of the four indicine reference breeds clus- tered very closely together in the PCA (Figure S1a). - (a) Expanded plot Bos indicus breeds section. - (b) Expanded plot African Bos taurus breeds section.. - PCA using African Bos taurus populations (a) Plot of PC1 vs PC2. - (a) Bos taurus dairy breeds. - (b) Bos indicus reference breeds. - (c) East and South African indigenous breeds. - (d) West African indigenous breeds.. - Effective population size over past generations using r 2 (log-scaled) for (a) Bos taurus dairy breeds, (b) Bos indicus breeds, (c) East and Southern African indigenous breeds, and (d) West African indigenous breeds.. - Rethinking the role of Bos indicus in sub-Saharan Africa. - Genetic structure and differentiation among African Bos taurus cattle breeds. - Pervasive introgression facilitated domestication and adaptation in the Bos species complex. - Complete mitochondrial genomes of Bos taurus and Bos indicus provide new insights into intra-species variation, taxonomy and domestication. - Footprints of selection in the ancestral admixture of a New World creole cattle breed. - Patterns of linkage disequilibrium in the human genome
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