Genetic diversity and admixture of indigenous cattle from North Ethiopia: implications of historical introgressions in the gateway region to Africa

Microsatellite variation was surveyed to determine the genetic diversity, population structure and admixture of seven North Ethiopian cattle breeds by combining multiple microsatellite data sets of Indian and West African zebu, and European, African and Near-Eastern taurine in genetic analyses. Based on allelic distribution, we identified four diagnostic alleles (HEL1-123 bp, CSSM66-201 bp, BM2113-150 bp and ILSTS6-285 bp) specific to the Near-Eastern taurine. Results of genetic relationship and population structure analyses confirmed the previously established marked genetic distinction between taurine and zebu, and indicated further divergence among the bio-geographical groupings of breeds such as North Ethiopian, Indian and West African zebu, and African, European and Near-Eastern taurine. Using the diagnostic alleles for bio-geographical groupings and a Bayesian method for population structure inference, we estimated the genetic influences of major historical introgressions in North Ethiopian cattle. The breeds have been heavily (>90%) influenced by zebu, followed by African, European and the Near-Eastern taurine. Overall, North Ethiopian cattle show a high level of within-population genetic variation (e.g. observed heterozygosity = 0.659-0.687), which is in the upper range of that reported for domestic cattle and indicates their potential for future breeding applications, even in a global context. Rather low but significant population differentiation (F(ST) = 1.1%, P < 0.05) was recorded as a result of multiple introgression events and strong genetic exchanges among the North Ethiopian breeds.     

Genetic characterization of Argentine and Bolivian Creole cattle breeds assessed through microsatellites

In the present report, the polymorphisms from 9 microsatellites were used to assess genetic diversity and relationships in 4 Creole cattle breeds from Argentina and Bolivia, 4 European taurine breeds, and 2 American zebu populations. The Creole populations display a relatively high level of genetic variation as estimated by allelic diversity and heterozygosity, whereas the British breeds displayed reduced levels of genetic diversity. The analysis of molecular variance indicated that 7.8% of variance can be explained by differences among taurine and zebu breeds. Consistent with these results, the first principal component (PC), which comprised the 40% of the total variance, clearly distinguishes these 2 groups. In addition, all constructed phylogenetic trees cluster together Nelore and Brahman breeds with robust bootstrap values. Only 1% of variance was due to difference between American Creole and European taurine cattle. Although this secondary split was supported by the classical genetic distance and the second PC (15%), the topology of trees is not particularly robust. The presence of zebu-specific alleles in Creole cattle allowed estimating a moderate degree of zebu admixture. When these data were compared with mitochondrial and Y chromosomal studies, a clear pattern of male-mediated introgression was revealed. The results presented here contribute to the understanding of origin and history of the American Creole cattle.     

Reduced genetic structure of north Ethiopian cattle revealed by Y-chromosome analysis

Ethiopia is considered to be a putative migratory corridor for both Near-East Bos taurine and Arabian and Indian B. indicus cattle into East Africa. African pastoralism, which is associated with adaptation to specific habitats and farming systems, has contributed to the composite constitution of Ethiopian cattle. We analyse, for the first time, five Y-chromosome microsatellite markers from seven north Ethiopian cattle populations, using a European Holstein-Friesian population as a reference, to assess the paternal gene pool and to explore the mechanisms behind the genetic structure. Our results reveal that the indicine alleles predominate in the present populations, with only one animal in the Arado carrying the taurine alleles. The north Ethiopian cattle populations with one exception (Abergelle) are characterized by a general low Y-chromosome haplotype diversity, as well as by a reduced interpopulation variance (Phi(ST)=4.0%), which can be a result of strong male-mediated selective sweeps. Population structure revealed by multidimensional-scaling analysis differentiates two populations (Arado and Abergelle) from the rest. Analysis of molecular variance does not lend support to the traditional classification for the populations, which is mainly based on physical characteristics. A network analysis indicates two closely related founding haplotypes accounting for a large proportion (50.0% in Abergelle and 85.0-94.7% in others) of north Ethiopian cattle Y-chromosomes. Our findings point to a common, but limited, paternal origin of the north Ethiopian cattle populations and strong male-mediated gene flow among them. The findings also provide insight into the historical immigration of cattle into East Africa.     

Genome-wide analysis reveals the ancient and recent admixture history of East African Shorthorn Zebu from Western Kenya

The Kenyan East African zebu cattle are valuable and widely used genetic resources. Previous studies using microsatellite loci revealed the complex history of these populations with the presence of taurine and zebu genetic backgrounds. Here, we estimate at genome-wide level the genetic composition and population structure of the East African Shorthorn Zebu (EASZ) of western Kenya. A total of 548 EASZ from 20 sub-locations were genotyped using the Illumina BovineSNP50 v. 1 beadchip. STRUCTURE analysis reveals admixture with Asian zebu, African and European taurine cattle. The EASZ were separated into three categories: substantial (⩾12.5%), moderate (1.56%<X<12.5%) and non-introgressed (⩽1.56%) according to the European taurine genetic proportion. The non-European taurine introgressed animals (n=425) show an unfluctuating zebu and taurine ancestry of 0.84±0.009 s.d. and 0.16±0.009 s.d., respectively, with significant differences in African taurine (AT) and Asian zebu backgrounds across chromosomes (P<0.0001). In contrast, no such differences are observed for the European taurine ancestry (P=0.1357). Excluding European introgressed animals, low and nonsignificant genetic differentiation and isolation by distance are observed among sub-locations (F_st=0.0033, P=0.09; r=0.155, P=0.07). Following a short population expansion, a major reduction in effective population size (N_e) is observed from approximately 240 years ago to present time. Our results support ancient zebu × AT admixture in the EASZ population, subsequently shaped by selection and/or genetic drift, followed by a more recent exotic European cattle introgression.     

Microsatellite DNA Variation and the Evolution, Domestication and Phylogeography of Taurine and Zebu Cattle (Bos Taurus and Bos Indicus)

Genetic variation at 20 microsatellite loci was surveyed to determine the evolutionary relationships and molecular biogeography of 20 different cattle populations from Africa, Europe and Asia. Phylogenetic reconstruction and multivariate analysis highlighted a marked distinction between humpless (taurine) and humped (zebu) cattle, providing strong support for a separate origin for domesticated zebu cattle. A molecular clock calculation using bison (Bison sp.) as an outgroup gave an estimated divergence time between the two subspecies of 610,000-850,000 years. Substantial differences in the distribution of alleles at 10 of these loci were observed between zebu and taurine cattle. These markers subsequently proved very useful for investigations of gene flow and admixture in African populations. When these data were considered in conjunction with previous mitochondrial and Y chromosomal studies, a distinctive male-mediated pattern of zebu genetic introgression was revealed. The introgression of zebu-specific alleles in African cattle afforded a high resolution perspective on the hybrid nature of African cattle populations and also suggested that certain West African populations of valuable disease-tolerant taurine cattle are under threat of genetic absorption by migrating zebu herds.     

Satellite DNA polymorphisms and AFLP correlate with Bos indicus-taurus hybridization

We describe satellite DNA variation that detects hybridization of Bos indicus (zebu or indicine cattle) and Bos taurus (taurine cattle) in African cattle populations. On Southern blots hybridized to a satellite III probe, relative intensities of Hinfl fragments correlated with the taurine-zebu composition in hybrid animals as deduced from AFLP genotyping of the same animals and previous data on microsatellite allele frequencies. Similar results were obtained by PCR-RFLP analysis of a zebu-specific mutation in the repeat unit of satellite 1.711b. Analysis of individuals from 20 African cattle breeds indicate that the centromeric satellites of the sanga breeds are of the taurine type and that several East-African zebu breeds are hybrids between taurine and zebu. These satellite RFLP, or SFLP, markers provide a fast method to screen the genetic makeup of African cattle.     

Geographic distribution and frequency of a taurine Bos taurus and an indicine Bos indicus Y specific allele amongst sub-saharan African cattle breeds

We report for the first time, and for the whole of sub-Saharan Africa, the geographical distribution and the frequency of an indicine and a taurine Y specific allele amongst African cattle breeds. A total of 984 males from 69 indigenous African populations from 22 countries were analysed at the microsatellite locus INRA 124. The taurine allele is probably the oldest one on the continent. However, the taurine and the indicine alleles were present in 291 males (30%), and 693 males (70%), respectively. More particularly, 96% of zebu males (n = 470), 50% of taurine males (n = 263), 29% of sanga males (crossbreed Bos taurus x Bos indicus, n = 263) and 95% of zebu x sanga crossbred males (n = 56) had the indicine allele. The Borgou, a breed classified as zebu x taurine cross showed only the zebu allele (n = 12). The indicine allele dominates today in the Abyssinian region, a large part of the Lake Victoria region and the sahelian belt of West Africa. All the sanga males (n = 64) but only one from the Abyssinian region had the indicine allele. The taurine allele is the commonest only among the sanga breeds of the southern African region and the trypanotolerant taurine breeds of West Africa. In West Africa and in the southern Africa regions, zones of introgression were detected with breeds showing both Y chromosome alleles. Our data also reveal a pattern of male zebu introgression in Mozambique and Zimbabwe, probably originating from the Mozambique coast. The sanga cattle from the Lake Victoria region and the Kuri cattle of Lake Chad, cattle populations surrounded by zebu breeds were, surprisingly, completely devoid of the indicine allele. Human migration, phenotypic preferences by the pastoralists, adaptation to specific habitats and to specific diseases are the main factors explaining the present-day distribution of the alleles in sub-Saharan Africa.     

Assessing introgression of Sahelian zebu genes into native Bos taurus breeds in Burkina Faso

A total of 350 samples were analyzed to estimate zebu gene proportions into two different taurine cattle breeds of Burkina Faso (Lobi and N’Dama) using 38 microsatellites and various statistical methodologies. West African and East African zebu samples were sequentially used as reference parental populations. Furthermore, N’Dama cattle from Congo, the composite South African Bonsmara cattle breed and a pool of European cattle were used successively as second parental populations. Independently of the methodology applied: (a) the use of West African zebu samples gave higher admixture coefficients than the East African zebu; (b) the higher zebu proportions were estimated when the European cattle was used as parental population 2; and (c) the use of the N’Dama population from Congo as parental population 2 gave the more consistent zebu proportion estimates for both the Lobi and the N’Dama breeds. In any case, the zebu admixture proportions estimated were not negligible and were always higher in the N’Dama cattle than in the Lobi cattle of Burkina Faso. This suggested that the introgression of Sahelian zebu genes into the taurine cattle of Southern West Africa can follow a complex pattern that can depend on local agro-ecological features. The current research pointed out that the estimation of admixture coefficients is highly dependent on both the assumptions underlying the methodologies applied and the selection of parental populations. Our analyses suggest that either too high or nil genetic identity between the parental and the expectedly derived populations must be avoided.     

Polymorphisms in Blood Proteins of Bos indicus and Bos taurus Cattle Breeds of Cameroon and Nigeria, and Description of New Albumin Variants

Polymorphisms in the five blood protein loci albumin (ALB), carbonic anhydrase (CA II), vitamin D binding protein (GC), haemoglobin (HBB), and transferrin (TF) were investigated in 520 individuals from 12 cattle populations (Bos indicus and Bos taurus) in Cameroon and Nigeria by isoelectric focusing with carrier ampholytes in ultrathin polyacrylamide gels (PAG-IEF) and by linear gradient polyacrylamide gel electrophoresis (PAGE). While all loci in nine populations were polymorphic with up to six alleles at the ALB and TF loci: the Namchi population showed monomorphism at the CA II locus and Muturu at the ALB, CA II, and HBB loci. There was a clear distinction between Bos indicus and Bos taurus breeds at the ALB locus with ALBB predominating in indicine and ALBA predominating in taurtine breeds. CA IIS, GCA, and HBBA were the most commonly occurring alleles in all populations. Two variants not described before were demonstrated by PAG-IEF at the ALB locus and named ALBJ and ALBK. Mean effective number of alleles as measure of intrabreed diversity was higher in zebu populations (2.040-2.288) as compared to taurine breeds (1.349-1.836). Significant deviations from Hardy-Weinberg equilibrium occurred in some populations at the HBB and TF loci. More haplotypes of ALB/GC occurred in the zebu than taurine breeds. ALBAGCA predominated in the taurine populations and ALBBGCA in the indicine populations. Influence of zebu genes on the Namchi and N'Dama taurine breeds was detected at the ALB, CA II, HBB, and TF loci, and estimated at 61.5% and 5.7%, respectively. The high resolution of PAG-IEF in screening for polymorphisms within diversity studies was demonstrated.     

Microsatellite analysis reveals high genetic diversity but low genetic structure in Ethiopian indigenous cattle populations

Ethiopian cattle are under threat from uncontrolled mating practices and are at high risk of becoming genetically homogeneous. Therefore, to evaluate genetic diversity, population structure and degree of admixture, 30 microsatellite markers were genotyped using 351 DNA samples from 10 Ethiopian cattle populations and the Holstein breed. The mean number of alleles per cattle population ranged from 6.93 ± 2.12 in Sheko to 7.50 ± 2.35 in Adwa. The mean observed and expected heterozygosities were 0.674 ± 0.015 and 0.726 ± 0.019 respectively. Ethiopian cattle populations have maintained a high level of within-population genetic differentiation (98.7%), the remainder being accounted for by differentiation among populations (1.3%). A highly significant deficiency in heterozygotes was detected within populations ( F _IS = 0.071; P  <   0.001) and total inbreeding ( F _IT = 0.083; P  <   0.001). The study populations were highly admixed but distinct from pure Bos taurus and Bos indicus breeds. The various levels of admixture and high genetic diversity make Ethiopian cattle populations suitable for future genetic improvement and utilization under a wide range of agro-ecologies in Ethiopia.     

Classification of the southern African sanga and East African shorthorned zebu

Humped African cattle, which are differentiated into zebu and sanga types, have traditionally been classified as Bos indicus . This paper discusses existing evidence and presents new evidence supporting the classification of southern African sangas as Bos taurus and East African zebus as ' taurindicus '. Classification is based on karyotype, frequencies of DNA markers and protein polymorphisms. The Boran, an East African zebu, has an acrocentric Y chromosome typical of Bos indicus . The southern African sanga breeds have a submetacentric Y chromosome typical of Bos taurus . Frequencies of four DNA markers support the hypothesis that the Tuli, a southern African sanga, had taurine ancestors and the Boran had both taurine and indicine ancestors. Frequencies for several protein polymorphisms strongly suggest that southern African sangas have more in common with taurine than with indicine breeds, while East African zebus are an admixture of African taurine and Asian indicine breeds.     

Low levels of taurine introgression in the current Brazilian Nelore and Gir indicine cattle populations

Background

Nelore and Gir are the two most important indicine cattle breeds for production of beef and milk in Brazil. Historical records state that these breeds were introduced in Brazil from the Indian subcontinent, crossed to local taurine cattle in order to quickly increase the population size, and then backcrossed to the original breeds to recover indicine adaptive and productive traits. Previous investigations based on sparse DNA markers detected taurine admixture in these breeds. High-density genome-wide analyses can provide high-resolution information on the genetic composition of current Nelore and Gir populations, estimate more precisely the levels and nature of taurine introgression, and shed light on their history and the strategies that were used to expand these breeds.

Results

We used the high-density Illumina BovineHD BeadChip with more than 777 K single nucleotide polymorphisms (SNPs) that were reduced to 697 115 after quality control filtering to investigate the structure of Nelore and Gir populations and seven other worldwide populations for comparison. Multidimensional scaling and model-based ancestry estimation clearly separated the indicine, European taurine and African taurine ancestries. The average level of taurine introgression in the autosomal genome of Nelore and Gir breeds was less than 1% but was 9% for the Brahman breed. Analyses based on the mitochondrial SNPs present in the Illumina BovineHD BeadChip did not clearly differentiate taurine and indicine haplotype groupings.

Conclusions

The low level of taurine ancestry observed for both Nelore and Gir breeds confirms the historical records of crossbreeding and supports a strong directional selection against taurine haplotypes via backcrossing. Random sampling in production herds across the country and subsequent genotyping would be useful for a more complete view of the admixture levels in the commercial Nelore and Gir populations.

Electronic supplementary material

The online version of this article (doi:10.1186/s12711-015-0109-5) contains supplementary material, which is available to authorized users.     

Paternal origins of Chinese cattle

To determine the genetic diversity and paternal origin of Chinese cattle, 302 males from 16 Chinese native cattle breeds as well as 30 Holstein males and four Burma males as controls were analysed using four Y‐SNPs and two Y‐STRs. In Chinese bulls, the taurine Y1 and Y2 haplogroups and indicine Y3 haplogroup were detected in seven, 172 and 123 individuals respectively, and these frequencies varied among the Chinese cattle breeds examined. Y2 dominates in northern China (91.4%), and Y3 dominates in southern China (90.8%). Central China is an admixture zone, although Y2 predominates overall (72.0%). The geographical distributions of the Y2 and Y3 haplogroup frequencies revealed a pattern of male indicine introgression from south to north China. The three Y haplogroups were further classified into one Y1 haplotype, five Y2 haplotypes and one Y3 haplotype in Chinese native bulls. Due to the interplay between taurine and indicine types, Chinese cattle represent an extensive reservoir of genetic diversity. The Y haplotype distribution of Chinese cattle exhibited a clear geographical structure, which is consistent with mtDNA, historical and geographical information.     

Association between Sscp Haplotypes at the Bovine Growth Hormone Gene and Milk Protein Percentage

The bovine Growth Hormone gene (bGH) is an attractive candidate gene for milk production in cattle. Single-strand conformation polymorphisms at bGH were identified and used to define haplotype configurations at this gene in the Israeli Holstein dairy cattle population (Bos taurus) and in the parent animals of the International Bovine Reference Family Panel (a collection of B. taurus and B. indicus crosses). B. taurus and B. indicus haplotypes at the bGH gene differed qualitatively, confirming the previously proposed long evolutionary separation of these cattle subraces. Only a small number of bGH haplotypes were present in the Israel Holstein population. One of the haplotypes, apparently of B. indicus origin, was found to have a highly significant positive effect on milk protein percentage. This illustrates the utility of the haplotype approach for uncovering candidate gene involvement in quantitative genetic variation in agricultural populations. The strong effect of an indicine haplotype in a taurine background raises the possibility that indicine alleles at other candidate genes may comprise a genetic resource for improvement of taurine populations. It is proposed that haplotype analysis may be a useful adjunct to measures of genetic distance for evaluating rare breeds with respect to gene conservation.     

On the origin of cattle: How aurochs became cattle and colonized the world

Since their domestication in the Neolithic, cattle have belonged to our cultural heritage. The reconstruction of their history is an active field of research 1 that contributes to our understanding of human history. Archeological data are now supplemented by analyses of modern and ancient samples of cattle with DNA markers of maternal, paternal, or autosomal inheritance. The most recent genetic data suggest that maternal lineages of taurine cattle originated in the Fertile Crescent with a possible contribution of South‐European wild cattle populations, while zebu cattle originate from the Indus Valley. Subsequently, cattle accompanied human migrations, which led to the dispersal of domestic cattle of taurine, indicine, or mixed origin over Asia, Africa, Europe, and the New World. This has resulted in their adaptation to different environments and considerable variation in appearance and performance. More recently, rational management of breeding led to international movements of sires, which again changed the global patterns of genetic diversity.     

Genetic diversity of Chinese cattle revealed by Y‐SNP and Y‐STR markers

With its vast territory and complex natural environment, China boasts rich cattle genetic resources. To gain the further insight into the genetic diversity and paternal origins of Chinese cattle, we analyzed the polymorphism of Y‐SNPs (UTY19 and ZFY10) and Y‐STRs (INRA189 and BM861) in 34 Chinese cattle breeds/populations, including 606 males representative of 24 cattle breeds/populations collected in this study as well as previously published data for 302 bulls. Combined genotypic data identified 14 Y‐chromosome haplotypes that represented three haplogroups. Y2‐104‐158 and Y2‐102‐158 were the most common taurine haplotypes detected mainly in northern and central China, whereas the indicine haplotype Y3‐88‐156 predominates in southern China. Haplotypes Y2‐108‐158, Y2‐110‐158, Y2‐112‐158 and Y3‐92‐156 were private to Chinese cattle. The population structure revealed by multidimensional scaling analysis differentiated Tibetan cattle from the other three groups of cattle. Analysis of molecular variance showed that the majority of the genetic variation was explained by the genetic differences among groups. Overall, our study indicates that Chinese cattle retain high paternal diversity (H = 0.607 ± 0.016) and probably much of the original lineages that derived from the domestication center in the Near East without strong admixture from commercial cattle carrying Y1 haplotypes.     

Genetic diversity,introgression and relationships among West/Central African cattle breeds

Genetic diversity, introgression and relationships were studied in 521 individuals from 9 African Bos indicus and 3 Bos taurus cattle breeds in Cameroon and Nigeria using genotype information on 28 markers (16 microsatellite, 7 milk protein and 5 blood protein markers). The genotypes of 13 of the 16 microsatellite markers studied on three European (German Angus, German Simmental and German Yellow) and two Indian (Nelore and Ongole) breeds were used to assess the relationships between them and the African breeds. Diversity levels at microsatellite loci were higher in the zebu than in the taurine breeds and were generally similar for protein loci in the breeds in each group. Microsatellite allelic distribution displayed groups of alleles specific to the Indian zebu, African taurine and European taurine. The level of the Indian zebu genetic admixture proportions in the African zebus was higher than the African taurine and European taurine admixture proportions, and ranged from 58.1% to 74.0%. The African taurine breed, Muturu was free of Indian zebu genes while its counter Namchi was highly introgressed (30.2%). Phylogenic reconstruction and principal component analysis indicate close relationships among the zebu breeds in Cameroon and Nigeria and a large genetic divergence between the main cattle groups – African taurine, European taurine and Indian zebu, and a central position for the African zebus. The study presents the first comprehensive information on the hybrid composition of the individual cattle breeds of Cameroon and Nigeria and the genetic relationships existing among them and other breeds outside of Africa. Strong evidence supporting separate domestication events for the Bos species is also provided.     

A microsatellite survey of cattle from a centre of origin: the Near East

Eight humpless cattle breeds from the Near East, three from Europe, one from West Africa and two zebu breeds from India were screened with 20 microsatellite loci. Breeds from the Near East revealed considerable levels of introgression from zebu cattle, which was apparent most in populations from the East and which declined in populations further West. This nonrandom pattern is suggestive of the introduction of zebu cattle from the East. Notwithstanding the overlay of zebu alleles, it was possible to demonstrate that Near Eastern cattle exhibited significantly higher levels of allelic diversity than breeds from other regions, which is consistent with the view that this region represents a primary domestication centre for Bos taurus cattle. The hypothesis that B. taurus and B. indicus cattle have separate domestic origins is also supported by the survey, a large genetic divergence being apparent between the nonhybrid taurine and zebu groups.     

Genome-wide insights into population structure and genetic history of tunisian local cattle using the illumina bovinesnp50 beadchip

Background

Tunisian local cattle populations are at risk of extinction as they were massively crossed with imported breeds. Preservation of indigenous livestock populations is important because each of them comprises a unique set of genes resulting from a local environment-driven selection that occurred over hundreds of years. The diversity and genetic structure of Tunisian local cattle populations are poorly understood. However, such information is crucial to the conservation and sustainable use of genetic resources.In addition, comparing the genomic structure of population sets from different parts of the world could help yield insight into their origin and history.In the present study, we provide a detailed assessment of the population structure of the three Tunisian local cattle populations using various methods, and we highlight their origin and history by investigating approximately ~38,000 SNPs in a broad panel of 878 individuals from 37 worldwide cattle breeds representative of African, European and indicine populations.

Results

Our study revealed a low level of divergence and high genetic diversity in Tunisian local cattle reflecting low levels of genetic drift. A Comparison with the worldwide cattle panel pinpointed the admixed origin of the genome of the three Tunisian populations with the two main European and African ancestries. Our results were in agreement with previous historical and archaeological reports about the past gene flow that existed between North African and South European breeds, in particular with Iberian cattle. We also detected a low-level indicine introgression in the three Tunisian populations and we inferred that indicine ancestry was inherited via African ancestors.

Conclusions

Our results represent the first study providing genetic evidence about the origin and history of Tunisian local cattle. The information provided by the fine-scale genetic characterization of our study will enhance the establishment of a national conservation strategy for these populations. These results may enable the identification of genetic variants involved in adaptation to harsh environmental conditions.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1638-6) contains supplementary material, which is available to authorized users.