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.     

Phylogenetic relationships of Malayan gaur with other species of the genus Bos based on cytochrome b gene DNA sequences

The Malayan gaur (Bos gaurus hubbacki) is one of the three subspecies of gaurs that can be found in Malaysia. We examined the phylogenetic relationships of this subspecies with other species of the genus Bos (B. javanicus, B. indicus, B. taurus, and B. grunniens). The sequence of a key gene, cytochrome b, was compared among 20 Bos species and the bongo antelope, used as an outgroup. Phylogenetic reconstruction was employed using neighbor joining and maximum parsimony in PAUP and Bayesian inference in MrBayes 3.1. All tree topologies indicated that the Malayan gaur is in its own monophyletic clade, distinct from other species of the genus Bos. We also found significant branching differences in the tree topologies between wild and domestic cattle.     

Complete mitochondrial genomes of Bos taurus and Bos indicus provide new insights into intra-species variation, taxonomy and domestication

The taurine and zebuine cattle breeds comprise the majority of the world cattle population but their taxonomic status is still controversial. The two forms of cattle are currently classified as Bos taurus and Bos indicus species and are differentiated primarily by the presence or absence of a hump. However, these two species hybridize readily, producing fully fertile offspring. We have determined and analyzed complete B. taurus and B. indicus mitochondrial genome sequences to investigate the extent of sequence divergences and to study their taxonomic status by molecular dating. The sequences encompassed 16,338 and 16,339 nucleotides, respectively, and differed at 237 positions. Estimated divergence times indicated that the two cattle lineages separated 1.7-2.0 million years ago. Combined phylogenetic analyses of 18 new and 130 previously reported extant B. taurus and B. indicus control region sequences with data from 32 archaeological specimens of the extinct wild aurochs (Bos primigenius) identified four major maternal lineages. B. primigenius haplotypes were present in all but the B. indicus lineage, and one B. taurus sequence clustered with B. primigenius P haplotypes that were not previously linked with domestic cattle. The B. indicus cluster and a recently reported new B. primigenius haplotype that represents a new lineage were approximately equidistant from the B. taurus cluster. These data suggest domestications from several differentiated populations of B. primigenius and a subspecies status for taurine (B. primigenius taurus) and zebuine (B. primigenius indicus) cattle.     

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.     

Assessment of cattle genetic introgression into domestic yak populations using mitochondrial and microsatellite DNA markers

Hybridization between yak Poephagus grunniens and taurine Bos taurus or indicine B. indicus cattle has been widely practiced throughout the yak geographical range, and gene flow is expected to have occurred between these species. To assess the impact of cattle admixture on domestic yak, we examined 1076 domestic yak from 29 populations collected in China, Bhutan, Nepal, India, Pakistan, Kyrgyzstan, Mongolia and Russia using mitochondrial DNA and 17 autosomal microsatellite loci. A cattle diagnostic marker‐based analysis reveals cattle‐specific mtDNA and/or autosomal microsatellite allele introgression in 127 yak individuals from 22 populations. The mean level of cattle admixture across the populations, calculated using allelic information at 17 autosomal microsatellite loci, remains relatively low (mY_cattle = 2.66 ± 0.53% and Q_cattle = 0.69 ± 2.58%), although it varies a lot across populations as well as among individuals within population. Although the level of cattle admixture shows a clear geographical structure, with higher levels of admixture in the Qinghai‐Tibetan Plateau and Mongolian and Russian regions, and lower levels in the Himalayan and Pamir Plateau region, our results indicate that the level of cattle admixture is not significantly correlated with the altitude across geographical regions as well as within geographical region. Although yak‐cattle hybridization is primarily driven to produce F₁ hybrids, our results show that the subsequent gene flow between yak and cattle took place and has affected contemporary genetic make‐up of domestic yak. To protect yak genetic integrity, hybridization between yak and cattle should be tightly controlled.     

Evolution of the bovine TLR gene family and member associations with Mycobacterium avium subspecies paratuberculosis infection

Members of the Toll-like receptor (TLR) gene family occupy key roles in the mammalian innate immune system by functioning as sentries for the detection of invading pathogens, thereafter provoking host innate immune responses. We utilized a custom next-generation sequencing approach and allele-specific genotyping assays to detect and validate 280 biallelic variants across all 10 bovine TLR genes, including 71 nonsynonymous single nucleotide polymorphisms (SNPs) and one putative nonsense SNP. Bayesian haplotype reconstructions and median joining networks revealed haplotype sharing between Bos taurus taurus and Bos taurus indicus breeds at every locus, and specialized beef and dairy breeds could not be differentiated despite an average polymorphism density of 1 marker/158 bp. Collectively, 160 tagSNPs and two tag insertion-deletion mutations (indels) were sufficient to predict 100% of the variation at 280 variable sites for both Bos subspecies and their hybrids, whereas 118 tagSNPs and 1 tagIndel predictively captured 100% of the variation at 235 variable sites for B. t. taurus. Polyphen and SIFT analyses of amino acid (AA) replacements encoded by bovine TLR SNPs indicated that up to 32% of the AA substitutions were expected to impact protein function. Classical and newly developed tests of diversity provide strong support for balancing selection operating on TLR3 and TLR8, and purifying selection acting on TLR10. An investigation of the persistence and continuity of linkage disequilibrium (r2≥0.50) between adjacent variable sites also supported the presence of selection acting on TLR3 and TLR8. A case-control study employing validated variants from bovine TLR genes recognizing bacterial ligands revealed six SNPs potentially eliciting small effects on susceptibility to Mycobacterium avium spp paratuberculosis infection in dairy cattle. The results of this study will broadly impact domestic cattle research by providing the necessary foundation to explore several avenues of bovine translational genomics, and the potential for marker-assisted vaccination.     

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.     

Extensive MHC class II DRB3 diversity in African and European cattle

Genetic deversity at the highly polymorphic BoLA-DRB3 locus was investigated by DNA sequence analyses of 18 African cattle from two breeds representing the two subspecies of cattle, Bos primigenius indicus and Bos primigenius taurus. Yhe polymorphism was compared with that found in a sample ofd 32 European cattle from four breeds, all classified as B. p. taurus. Particularly extensive genetic diversity was found among African cattle, in which as many as 18 alleles were recognized in this small random sample of animals from two breeds. The observed similarity in allele frequency distribution between the two African populations, N'Dama and Zebu cattle, is consistent with the recent recognition of gene flow between B. p. indicus and B. P taurus cattle in Africa. A total of 30 DRB3 alleles were documented and as many as 26 of these were classified as major allelic types showing at least five amino acid substitutions compared with other major types. The observation of extensive genetic diversity at MHC loci in cattle, as well as in other farm animals, provides a compelling argument against matin-type preferences as a primary cause in maintaining major histocompatibility complex diversity, since the reproduction of these animals has been controlled by humans for many generations.The nucleotide sequence data reported in this paper have been submitted to the EMBL nucleotide sequence database and have been given the accession numbers X87641-X87670     

The Complete Mitochondrial DNA Sequence of the Domestic Sheep (Ovis aries) and Comparison with the Other Major Ovine Haplotype

The complete mitochondrial DNA (mtDNA) molecule of the domestic sheep, Ovis aries, was sequenced, together with part of the mtDNA of a specimen representing the other major O. aries haplotype group. The length of the complete ovine mtDNA presented is 16,616 nucleotides (nt). This length is not absolute, however, due to heteroplasmy caused by the occurrence of different numbers of a 75-nt-long tandem repeat in the control region. The sequence data were included in analyses of intraspecific ovine molecular differences, molecular comparisons with bovine mtDNAs, and phylogenetic analyses based on complete mtDNAs. The comparisons with bovine mtDNAs were based on the central domains of the ovine control regions, representing both major ovine haplotype groups, and the corresponding domains of Bos taurus and B. indicus. The comparisons showed that the difference between the bovids was 1.4 times greater than the intraspecific ovine difference. These findings suggest that the strains of wild sheep from which domestic sheep originated were more closely related than were the B. primigenius subspecies which gave rise to B. indicus and B. taurus cattle. Datings based on complete mtDNAs suggest that the bovine and ovine lineages diverged about 30 million years before present. This dating is considerably earlier than that proposed previously. Received: 5 September 1997 / Accepted: 5 May 1998     

DNA Fingerprinting of Individual Species and Intergeneric and Interspecific Hybrids of the Genera Bos and Bison, Subfamily Bovinae

Genome fingerprinting with a hypervariable minisatellite sequence of phage M13 DNA was used to study the genetic variation in individual species of the genera Bosand Bison(subfamily Bovinae) and in their interspecific and intergeneric hybrids. DNA fingerprints were obtained for domestic cow Bos taurus primigenius, vatussy Bos taurus macroceros, banteng Bos javanicus, gaur Bos gaurus, wisent Bison bonasus, bison Bison bison, and for the interspecific and intergeneric hybrids. Compared with the original species, most hybrids showed a greater variation in number and size of hybridization fragments. An association was revealed between the number of hybridization fragments and degree of consanguinity of interspecific hybrids resulting from unique crossing of domestic cow and banteng. Pairwise similarity coefficients were calculated to construct a dendrogram of genetic similarity, which reflected the relationships between the parental species and hybrids varying in degree of consanguinity. The applicability of the method for identifying interspecific and intergeneric hybrids and for studying the consequences of hybridization in the subfamily Bovinae is discussed.     

Nucleotide Sequence and Variation of IGF2 Gene Exon 6 in Bos Taurus and Bos Indicus Cattle

The major assumption of this study is that polymorphism of a gene could be used to investigate its allele-specific expression as well as its methylation and imprinting status. Therefore, the aim of this study was to analyze the polymorphism of the coding region of the bovine IGF2 gene and to determine the sequence of its gene exon 6 in Bos taurus and Bos indicus cattle. A single nucleotide “C” deletion/insertion polymorphism was found in both cattle subspecies and a G/T transversion (RFLP-MboII) in the Bos indicus IGF2 gene. A 407-bp fragment of bovine IGF2 exon 6 was sequenced and the sequences (including variable nucleotides) were deposited in the GenBank database. A comparative analysis was performed for this fragment from different species; 99.5% identity was found between Bos taurus and Bos indicus cattle.     

Nucleotide sequence and variation of IGF2 gene exon 6 in Bos taurus and Bos indicus cattle

The major assumption of this study is that polymorphism of a gene could be used to investigate its allele-specific expression as well as its methylation and imprinting status. Therefore, the aim of this study was to analyze the polymorphism of the coding region of the bovine IGF2 gene and to determine the sequence of its gene exon 6 in Bos taurus and Bos indicus cattle. A single nucleotide "C" deletion/insertion polymorphism was found in both cattle subspecies and a G/T transversion (RFLP-MboII) in the Bos indicus IGF2 gene. A 407-bp fragment of bovine IGF2 exon 6 was sequenced and the sequences (including variable nucleotides) were deposited in the GenBank database. A comparative analysis was performed for this fragment from different species; 99.5% identity was found between Bos taurus and Bos indicus cattle.     

Crested gibbon (Hylobates [Nomascus]) identification using noninvasively obtained DNA

The development of captive breeding programs for the crested gibbons (Hylobates [Nomascus]) of Indochina is hindered by the difficulty of sorting individuals into their correct species and subspecies groups. We describe taxon-specific DNA sequence variation in a 252-base pair region of the mitochondrial cytochrome b gene, which can be used to identify individuals of the three taxa of crested gibbon commonly found in Western zoos. These molecular genetic markers can be amplified from plucked hair and will permit the identification of morphologically similar females and crested gibbons of either sex of unknown origin. Noninvasive genotyping of captive animals will facilitate the genetic management of these critically endangered primates. © 1994 Wiley-Liss, Inc.     

Mitochondrial DNA variation and evolution of Japanese black cattle (Bos taurus).

This article describes complete mitochondrial DNA displacement loop sequences from 32 Japanese Black cattle and the analysis of these data in conjunction with previously published sequences from African, European, and Indian subjects. The origins of North East Asian domesticated cattle are unclear. The earliest domestic cattle in the region were Bos taurus and may have been domesticated from local wild cattle (aurochsen; B. primigenius), or perhaps had an origin in migrants from the early domestic center of the Near East. In phylogenetic analyses, taurine sequences form a dense tree with a center consisting of intermingled European and Japanese sequences with one group of Japanese and another of all African sequences, each forming distinct clusters at extremes of the phylogeny. This topology and calibrated levels of sequence divergence suggest that the clusters may represent three different strains of ancestral aurochs, adopted at geographically and temporally separate stages of the domestication process. Unlike Africa, half of Japanese cattle sequences are topologically intermingled with the European variants. This suggests an interchange of variants that may be ancient, perhaps a legacy of the first introduction of domesticates to East Asia.     

Prion gene sequence variation within diverse groups of U.S. sheep,beef cattle,and deer

Prions are proteins that play a central role in transmissible spongiform encephalopathies in a variety of mammals. Among the most notable prion disorders in ungulates are scrapie in sheep, bovine spongiform encephalopathy in cattle, and chronic wasting disease in deer. Single nucleotide polymorphisms in the sheep prion gene (PRNP) have been correlated with susceptibility to natural scrapie in some populations. Similar correlations have not been reported in cattle or deer; however, characterization of PRNP nucleotide diversity in those species is incomplete. This report describes nucleotide sequence variation and frequency estimates for the PRNP locus within diverse groups of U.S. sheep, U.S. beef cattle, and free-ranging deer (Odocoileus virginianus and O. hemionus from Wyoming). DNA segments corresponding to the complete prion coding sequence and a 596-bp portion of the PRNP promoter region were amplified and sequenced from DNA panels with 90 sheep, 96 cattle, and 94 deer. Each panel was designed to contain the most diverse germplasm available from their respective populations to facilitate polymorphism detection. Sequence comparisons identified a total of 86 polymorphisms. Previously unreported polymorphisms were identified in sheep (9), cattle (13), and deer (32). The number of individuals sampled within each population was sufficient to detect more than 95% of all alleles present at a frequency greater than 0.02. The estimation of PRNP allele and genotype frequencies within these diverse groups of sheep, cattle, and deer provides a framework for designing accurate genotype assays for use in genetic epidemiology, allele management, and disease control.     

Admixture analysis of South Asian cattle

We present population genetic analysis of microsatellite variation in seven Bos indicus cattle breeds from a variety of locations in South Asia. This is the first such study focusing within this area, which is one of the postulated centres of origin of domestic cattle. An estimate of the influence of Bos taurus ancestry was carried out using three approaches: by the systematic selection of population-associated alleles for B. taurus and examination of their frequency; by examining the truncation of genetic distances from European populations; and by a model-based Bayesian admixture analysis. These analyses revealed a B. taurus influence in the Indian subcontinent; part of a gradation which stretches from Europe through the Near East towards Indian and which may be of ancient origin.     

Mitochondrial DNA sequence diversity and origin of Chinese domestic yak

In order to clarify the origin and genetic diversity of yak in China, we analysed mitochondrial DNA (mtDNA) control region sequences (approximately 891 bp) in 52 individuals from four domestic yak (Poephagus grunniens) breeds, as well as from a hybrid between yak and cattle (Pianniu). Twenty-five samples were further selected for partial (420 bp) cytochrome b sequencing based on control region sequence information. Two yak samples shared sequences with Chinese cattle (Bos taurus); the remaining yak mtDNAs converged into two major clades in the phylogenetic analysis. Genetic diversity varied substantially among the breeds, with the hybrid Pianniu yak demonstrating the highest diversity. Our results suggest that the Chinese yak was domesticated from two distinct matrilineal sources or from a heterogeneous pool containing both divergent lineages, with occasional gene introgression from cattle.     

Cot-based sampling of genomes for polymorphic low-copy DNA

DNA polymorphisms are powerful tools for many evolutionary and genomic studies in plants including molecular breeding. Single nucleotide polymorphisms (SNPs) are the most elemental DNA marker for genomic studies, but even with advances in DNA sequencing technology, SNP discovery remains costly and computationally demanding, especially in large genomes that are rich in repetitive DNA such as those of many plants. Here we report a method using DNA renaturation kinetics (Cot techniques), sequencing, and BLAST-based screening to identify low-copy, non-coding DNA sequences that were subsequently found to be relatively rich in polymorphisms. A total of of 63 such fragments isolated from a diploid D genome cotton species (Gossypium raimondii) revealed a higher frequency of polymorphisms than that observed for cotton expressed sequence tags or hypomethylated (PstI-susceptible) genomic DNA. While microsatellite-derived loci show still higher polymorphism rates, they often fall in repetitive elements and their sequence analysis is often complicated by alignment difficulties. The potential applications of Cot-filtered noncoding (CFNC) DNA in development of DNA markers are discussed.     

Genomic divergence of zebu and taurine cattle identified through high-density SNP genotyping

Background

Natural selection has molded evolution across all taxa. At an arguable date of around 330,000 years ago there were already at least two different types of cattle that became ancestors of nearly all modern cattle, the Bos taurus taurus more adapted to temperate climates and the tropically adapted Bos taurus indicus. After domestication, human selection exponentially intensified these differences. To better understand the genetic differences between these subspecies and detect genomic regions potentially under divergent selection, animals from the International Bovine HapMap Experiment were genotyped for over 770,000 SNP across the genome and compared using smoothed F_ST. The taurine sample was represented by ten breeds and the contrasting zebu cohort by three breeds.

Results

Each cattle group evidenced similar numbers of polymorphic markers well distributed across the genome. Principal components analyses and unsupervised clustering confirmed the well-characterized main division of domestic cattle. The top 1% smoothed F_ST, potentially associated to positive selection, contained 48 genomic regions across 17 chromosomes. Nearly half of the top F_ST signals (n = 22) were previously detected using a lower density SNP assay. Amongst the strongest signals were the BTA7:~50 Mb and BTA14:~25 Mb; both regions harboring candidate genes and different patterns of linkage disequilibrium that potentially represent intrinsic differences between cattle types. The bottom 1% of the smoothed F_ST values, potentially associated to balancing selection, included 24 regions across 13 chromosomes. These regions often overlap with copy number variants, including the highly variable region at BTA23:~24 Mb that harbors a large number of MHC genes. Under these regions, 318 unique Ensembl genes are annotated with a significant overrepresentation of immune related pathways.

Conclusions

Genomic regions that are potentially linked to purifying or balancing selection processes in domestic cattle were identified. These regions are of particular interest to understand the natural and human selective pressures to which these subspecies were exposed to and how the genetic background of these populations evolved in response to environmental challenges and human manipulation.

Electronic supplementary material

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