A comprehensive evaluation of cattle introgression into US federal bison herds

Genetic introgression, especially from interspecies hybridization, is a significant threat to species conservation worldwide. In this study, 11 US federal bison populations were comprehensively examined for evidence of both mitochondrial and nuclear domestic cattle (Bos taurus) introgression. Mitochondrial introgression was examined using established polymerase chain reaction methods and confirmed through analysis of D-loop sequences. Nuclear introgression was assessed in 14 chromosomal regions through examination of microsatellite electromorph and sequence differences between bison and domestic cattle. Only one population was identified with domestic cattle mitochondrial DNA introgression. In contrast, evidence of nuclear introgression was found in 7 (63.6%) of the examined populations. Historic accounts of bison transfers among populations were corroborated with evidence of introgressed DNA transmission. While neither nuclear nor mitochondrial domestic cattle introgression was detected in bison from Grand Teton National Park, Sully's Hill National Game Preserve, Wind Cave National Park, or Yellowstone National Park, adequate sample sizes were available only from the last 2 populations to allow for statistical confidence (>90%) in nuclear introgression detection limits. The identification of genetically unique and undisturbed populations is critical to species conservation efforts, and this study serves as a model for the genetic evaluation of interspecies introgression.     

Conservation genomics: disequilibrium mapping of domestic cattle chromosomal segments in North American bison populations

Introgressive hybridization is one of the major threats to species conservation, and is often induced by human influence on the natural habitat of wildlife species. The ability to accurately identify introgression is critical to understanding its importance in evolution and effective conservation management of species. Hybridization between North American bison (Bison bison) and domestic cattle (Bos taurus) as a result of human activities has been recorded for over 100 years, and domestic cattle mitochondrial DNA was previously detected in bison populations. In this study, linked microsatellite markers were used to identify domestic cattle chromosomal segments in 14 genomic regions from 14 bison populations. Cattle nuclear introgression was identified in five populations, with an average frequency per population ranging from 0.56% to 1.80%. This study represents the first use of linked molecular markers to examine introgression between mammalian species and the first demonstration of domestic cattle nuclear introgression in bison. To date, six public bison populations have been identified with no evidence of mitochondrial or nuclear domestic cattle introgression, providing information critical to the future management of bison genetic resources. The ability to identify even low levels of introgression resulting from historic hybridization events suggests that the use of linked molecular markers to identify introgression is a significant development in the study of introgressive hybridization across a broad range of taxa.     

Differential introgression of uniparentally inherited markers in bison populations with hybrid ancestries

Historical hybridization between Bison bison (bison) and Bos taurus (cattle) has been well documented and resulted in cattle mitochondrial DNA (mtDNA) introgression, previously identified in six different bison populations. In order to examine Y chromosome introgression, a microsatellite marker (BYM-1) with non-overlapping allele size distributions in bison and cattle was isolated from a bacterial artificial chromosome (BAC) clone, and was physically assigned to the Y chromosome by fluorescence in situ hybridization. BYM-1 genotypes for a sample of 143 male bison from 10 populations, including all six populations where cattle mtDNA haplotypes were previously identified, indicated that cattle Y chromosome introgression had not occurred in these bison populations. The differential permeability of uniparentally inherited markers to introgression is consistent with observations of sterility among first generation hybrid males and a sexual asymmetry in the direction of hybridization favouring matings between male bison and female cattle.     

Phylogenies using mtDNA and SRY provide evidence for male-mediated introgression in Asian domestic cattle

Using nucleotide sequences of the mitochondrial DNA (mtDNA) cytochrome b and SRY genes, we examined the genetic status of two major groups of domestic cattle, the humpless taurine (Bos taurus) and humped zebu (B. indicus), using 10 cattle populations in Asia. Several sequence polymorphisms specific for each major group were found, although the frequency of these polymorphisms varied in each population. Six major mtDNA-SRY composite types were observed. The Mishima, Mongolian, Korean, Chinese Yellow and Sri Lanka cattle populations had a full match between the mtDNA and SRY sequences, specifically the taurine/taurine type or zebu/zebu type. A non-match type (zebu/taurine type) was found at a high frequency in the Bangladesh (83.4%) and Nepal populations (83.3%). Our results suggest that these non-match type populations developed from genetic hybridization of different strains. Also, the domestication history of modern Asian domestic cattle could be explained by male-mediated introgression. Additionally, our results suggest the occurrence of introgression of mtDNA from other Bibos or Poephagus species into native cattle populations. The existence of other mtDNA-SRY composite types, such as the Bali-zebu and yak-zebu types in Indonesia (85.7%) and Nepal (16.7%), respectively, suggests that genetic introgression also occurred from other genera into domestic cattle during the process of domestication.     

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.     

Genome-wide genetic diversity,population structure and admixture analysis in African and Asian cattle breeds

Knowledge about genetic diversity and population structure is useful for designing effective strategies to improve the production, management and conservation of farm animal genetic resources. Here, we present a comprehensive genome-wide analysis of genetic diversity, population structure and admixture based on 244 animals sampled from 10 cattle populations in Asia and Africa and genotyped for 69 903 autosomal single-nucleotide polymorphisms (SNPs) mainly derived from the indicine breed. Principal component analysis, STRUCTURE and distance analysis from high-density SNP data clearly revealed that the largest genetic difference occurred between the two domestic lineages (taurine and indicine), whereas Ethiopian cattle populations represent a mosaic of the humped zebu and taurine. Estimation of the genetic influence of zebu and taurine revealed that Ethiopian cattle were characterized by considerable levels of introgression from South Asian zebu, whereas Bangladeshi populations shared very low taurine ancestry. The relationships among Ethiopian cattle populations reflect their history of origin and admixture rather than phenotype-based distinctions. The high within-individual genetic variability observed in Ethiopian cattle represents an untapped opportunity for adaptation to changing environments and for implementation of within-breed genetic improvement schemes. Our results provide a basis for future applications of genome-wide SNP data to exploit the unique genetic makeup of indigenous cattle breeds and to facilitate their improvement and conservation.     

Genetic Analysis of the Henry Mountains Bison Herd

Wild American plains bison (Bison bison) populations virtually disappeared in the late 1800s, with some remnant animals retained in what would become Yellowstone National Park and on private ranches. Some of these private bison were intentionally crossbred with cattle for commercial purposes. This forced hybridization resulted in both mitochondrial and nuclear introgression of cattle genes into some of the extant bison genome. As the private populations grew, excess animals, along with their history of cattle genetics, provided founders for newly established public bison populations. Of the US public bison herds, only those in Yellowstone and Wind Cave National Parks (YNP and WCNP) appear to be free of detectable levels of cattle introgression. However, a small free-ranging population (~350 animals) exists on public land, along with domestic cattle, in the Henry Mountains (HM) of southern Utah. This isolated bison herd originated from a founder group translocated from YNP in the 1940s. Using genetic samples from 129 individuals, we examined the genetic status of the HM population and found no evidence of mitochondrial or nuclear introgression of cattle genes. This new information confirms it is highly unlikely for free-living bison to crossbreed with cattle, and this disease-free HM bison herd is valuable for the long-term conservation of the species. This bison herd is a subpopulation of the YNP/WCNP/HM metapopulation, within which it can contribute significantly to national efforts to restore the American plains bison to more of its native range.     

Taurine and zebu admixture in Near Eastern cattle: a comparison of mitochondrial, autosomal and Y-chromosomal data

Eight Bos taurus cattle breeds from the Near East region were screened with a Bos indicus (zebu)-diagnostic Y-specific microsatellite (INRA124) to estimate the proportion of zebu Y chromosomes in each population. This value was compared with previously published values for zebu introgression for both the mitochondrial and autosomal gene pools of the same breeds. All breeds revealed considerable levels of introgression from B. indicus cattle when the autosomal data were taken into consideration; this was particularly apparent in cattle populations from Iraq in the east, and declined in the populations further west towards Anatolia. This non-random pattern of introgression and admixture is suggestive of the introduction of zebu cattle from the region corresponding to present-day Iran and northern Pakistan. In addition, the maternal and paternal markers demonstrate that the movement of cattle into and within the Near East was complex.     

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.     

Predominant African-derived mtDNA in Caribbean and Brazilian Creole cattle is also found in Spanish cattle (Bos taurus)

African-derived mitochondrial DNA (mtDNA) have been described in South American and Caribbean native cattle populations, which could have been introduced into America from Iberia or by direct importation from Africa. However, the similarity among described haplotypes is not known. We examined mtDNA variation in Guadeloupe Creole and Spanish cattle in an attempt to identify African-derived mtDNA haplotypes and compare them with those previously described. Eleven haplotypes clustered into the European taurine haplogroup (T3), two haplotypes into the African taurine (T1) haplogroup, and three haplotypes into the African-derived American haplogroup (AA). The AA1 and Eucons haplotypes were the most frequently observed. The presence of the AA haplogroup in Spanish cattle confirms historical records and genetic evidence of Iberian cattle as the main source of American native cattle origin. The possible origin of African-derived mitochondrial haplotypes in Iberian and Creole cattle is discussed, and the accumulated evidence does not support a founder effect from African ancestral cattle by direct importations. The presence of taurine AA and T3 haplotypes in Brazilian Nellore may indicate introgression by local European-derived cattle. Data presented in this work will contribute to the understanding of the origin of Guadeloupe Creole cattle.     

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.     

On the Origin of Indonesian Cattle

Background

Two bovine species contribute to the Indonesian livestock, zebu (Bos indicus) and banteng (Bos javanicus), respectively. Although male hybrid offspring of these species is not fertile, Indonesian cattle breeds are supposed to be of mixed species origin. However, this has not been documented and is so far only supported by preliminary molecular analysis.

Methods and Findings

Analysis of mitochondrial, Y-chromosomal and microsatellite DNA showed a banteng introgression of 10–16% in Indonesian zebu breeds. East-Javanese Madura and Galekan cattle have higher levels of autosomal banteng introgression (20–30%) and combine a zebu paternal lineage with a predominant (Madura) or even complete (Galekan) maternal banteng origin. Two Madura bulls carried taurine Y-chromosomal haplotypes, presumably of French Limousin origin. In contrast, we did not find evidence for zebu introgression in five populations of the Bali cattle, a domestic form of the banteng.

Conclusions

Because of their unique species composition Indonesian cattle represent a valuable genetic resource, which potentially may also be exploited in other tropical regions.     

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.     

Microsatellite analysis reveals substantial genetic differentiation between contemporary New World and Old World Holstein Friesian populations

Genotypic data from 39 microsatellite loci typed in 211 animals were used to assess the genetic differentiation between Old World and New World Holstein Friesian cattle populations. Gene diversities were similar in all five Holstein Friesian populations surveyed, ranging from 0.43 to 0.48. A tree of individuals based on the proportion of shared alleles indicated a clear distinction between Old World and New World Holstein Friesian populations. Similarly, genetic differentiation between populations, as measured by FST, was highly significant. Using the split decomposition method, we were able to visualize the significant introgression of New World Holstein Friesian into European Holstein Friesian populations.     

Genomewide introgressive hybridization patterns in wild Atlantic salmon influenced by inadvertent gene flow from hatchery releases

Many salmonid fish populations are threatened by genetic homogenization, primarily due to introgressive hybridization with hatchery‐reared conspecifics. By applying genomewide analysis using two molecular marker types (1986 SNPs and 17 microsatellites), we assessed the genetic impacts of inadvertent gene flow via straying from hatchery releases on wild populations of Atlantic salmon in the Gulf of Finland, Baltic Sea, over 16 years (1996–2012). Both microsatellites and SNPs revealed congruent population genetic structuring, indicating that introgression changed the genetic make‐up of wild populations by increasing genetic diversity and reducing genetic divergence. However, the degree of genetic introgression varied among studied populations, being higher in the eastern part and lower in the western part of Estonia, which most likely reflects the history of past stocking activities. Using kernel smoothing and permutation testing, we detected considerable heterogeneity in introgression patterns across the genome, with a large number of regions exhibiting nonrandom introgression widely dispersed across the genome. We also observed substantial variation in nonrandom introgression patterns within populations, as the majority of genomic regions showing elevated or reduced introgression were not consistently detected among temporal samples. This suggests that recombination, selection and stochastic processes may contribute to complex nonrandom introgression patterns. Our results suggest that (i) some genomic regions in Atlantic salmon are more vulnerable to introgressive hybridization, while others show greater resistance to unidirectional gene flow; and (ii) the hybridization of previously separated populations leads to complex and dynamic nonrandom introgression patterns that most likely have functional consequences for indigenous populations.     

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.     

Genomic Diversity in Pig (Sus scrofa) and its Comparison with Human and other Livestock

We have reviewed the current pig (Sus scrofa) genomic diversity within and between sites and compared them with human and other livestock. The current Porcine 60K single nucleotide polymorphism (SNP) panel has an average SNP distance in a range of 30 - 40 kb. Most of genetic variation was distributed within populations, and only a small proportion of them existed between populations. The average heterozygosity was lower in pig than in human and other livestock. Genetic inbreeding coefficient (F(IS)), population differentiation (F(ST)), and Nei's genetic distance between populations were much larger in pig than in human and other livestock. Higher average genetic distance existed between European and Asian populations than between European or between Asian populations. Asian breeds harboured much larger variability and higher average heterozygosity than European breeds. The samples of wild boar that have been analyzed displayed more extensive genetic variation than domestic breeds. The average linkage disequilibrium (LD) in improved pig breeds extended to 1 - 3 cM, much larger than that in human (~ 30 kb) and cattle (~ 100 kb), but smaller than that in sheep (~ 10 cM). European breeds showed greater LD that decayed more slowly than Asian breeds. We briefly discuss some processes for maintaining genomic diversity in pig, including migration, introgression, selection, and drift. We conclude that, due to the long time of domestication, the pig possesses lower heterozygosity, higher F(IS), and larger LD compared with human and cattle. This implies that a smaller effective population size and less informative markers are needed in pig for genome wide association studies.     

Genetic polymorphism in varietal identification and genetic improvement

Summary New sources of genetic polymorphisms promise significant additions to the number of useful genetic markers in agricultural plants and animals, and prompt this review of potential applications of polymorphic genetic markers in plant and animal breeding. Two major areas of application can be distinguished. The first is based on the utilization of genetic markers to determine genetic relationships. These applications include varietal identification, protection of breeder's rights, and parentage determination. The second area of application is based on the use of genetic markers to identify and map loci affecting quantitative traits, and to monitor these loci during introgression or selection programs. A variety of breeding applications based on these possibilities can be envisaged for Selfers, particularly for those species having a relatively small genome size. These applications include: (i) screening genetic resources for useful quantitative trait alleles, and introgression of chromosome segments containing these alleles from resource strain to commercial variety; (ii) development of improved pure lines out of a cross between two existing commercial varieties; and (iii) development of crosses showing increased hybrid vigor. Breeding applications in segregating populations are more limited, particularly in species with a relatively large genome size. Potential applications, however, include: (i) preliminary selection of young males in dairy cattle on the basis of evaluated chromosomes of their proven sire; (ii) genetic analysis of resource strains characterized by high values for a particular quantitative trait, and introgression of chromosome segments carrying alleles contributing to the high values from resource strain to recipient strain.Contribution from The Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel, No. 767-E, 1983 Series     

Paternally inherited markers in bovine hybrid populations

The genetic integrity of crossfertile bovine- or cattle-like species may be endangered by species hybridization. Previously, amplified fragment length polymorphism, satellite fragment length polymorphism and microsatellite assays have been used to analyze the species composition of nuclear DNA in taurine cattle, zebu, banteng and bison populations, while mitochondrial DNA reveals the origin of the maternal lineages. Here, we describe species-specific markers of the paternally transmitted Y-chromosome for the direct detection of male-mediated introgression. Convenient PCR-restriction fragment length polymorphism and competitive PCR assays are shown to differentiate the Y-chromosomes of taurine cattle, American bison and European bison, and to detect the banteng origin of Indonesian Madura and Bali cattle bulls.