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1.  Evolutionary affinities of the enigmatic saola (Pseudoryx nghetinhensis) in the context of the molecular phylogeny of Bovidae. 
To elucidate the systematic status of the enigmatic saola (Pseudoryx nghetinhensis), a new bovid genus recently discovered in Vietnam, and to investigate phylogenetic relationships within the family Bovidae, four distinct DNA markers were sequenced. Complete mitochondrial cytochrome b (1143 bp) and 12S rRNA (956 bp) genes and non-coding regions from the nuclear genes for aromatase cytochrome P-450 (199 bp) and lactoferrin (338 bp) have been compared for 25 bovid species and three Cervidae and Antilocapridae outgroups. Independent and/or combined analyses of the four nucleotide matrices through maximum parsimony and maximum-likelihood methods indicated that Bovidae consists of two major lineages, i.e. Bovinac which contains the tribes Bovini, Boselaphini and Tragelaphini, and Antilopinae which encompasses all other bovids. Within Bovinae, the tribe Bovini is divided into buffalo Bovini (Bubalus and Syncerus) and cattle Bovini (Bos and Bison) and Tragelaphini are possibly related to Boselaphini. Pseudoryx is shown to be (i) robustly nested within Bovinae; (ii) strongly associated with Bovini; and (iii) tentatively sharing a sister-group relationship with cattle Bovini. Within Antilopinae, three robust clades are in evidence: (i) Hippotragus and Damaliscus are linked to Ovis; (ii) Aepyceros joins Neotragus; and (iii) Cephalophus clusters with Oreotragus.
PMCID: PMC1689916  PMID: 10380679
2.  Molecular evolution of the Bovini tribe (Bovidae, Bovinae): Is there evidence of rapid evolution or reduced selective constraint in Domestic cattle? 
BMC Genomics  2009;10:179.
If mutation within the coding region of the genome is largely not adaptive, the ratio of nonsynonymous (dN) to synonymous substitutions (dS) per site (dN/dS) should be approximately equal among closely related species. Furthermore, dN/dS in divergence between species should be equivalent to dN/dS in polymorphisms. This hypothesis is of particular interest in closely related members of the Bovini tribe, because domestication has promoted rapid phenotypic divergence through strong artificial selection of some species while others remain undomesticated. We examined a number of genes that may be involved in milk production in Domestic cattle and a number of their wild relatives for evidence that domestication had affected molecular evolution. Elevated rates of dN/dS were further queried to determine if they were the result of positive selection, low effective population size (Ne) or reduced selective constraint.
We have found that the domestication process has contributed to higher dN/dS ratios in cattle, especially in the lineages leading to the Domestic cow (Bos taurus) and Mithan (Bos frontalis) and within some breeds of Domestic cow. However, the high rates of dN/dS polymorphism within B. taurus when compared to species divergence suggest that positive selection has not elevated evolutionary rates in these genes. Likewise, the low rate of dN/dS in Bison, which has undergone a recent population bottleneck, indicates a reduction in population size alone is not responsible for these observations.
The effect of selection depends on effective population size and the selection coefficient (Nes). Typically under domestication both selection pressure for traits important in fitness in the wild and Ne are reduced. Therefore, reduced selective constraint could be responsible for the observed elevated evolutionary ratios in domesticated species, especially in B. taurus and B. frontalis, which have the highest dN/dS in the Bovini. This may have important implications for tests of selection such as the McDonald-Kreitman test. Surprisingly we have also detected a significant difference in the supposed neutral substitution rate between synonymous and noncoding sites in the Bovine genome, with a 30% higher rate of substitution at synonymous sites. This is due, at least in part, to an excess of the highly mutable CpG dinucleotides at synonymous sites, which will have implications for time of divergence estimates from molecular data.
PMCID: PMC2681479  PMID: 19393048
3.  Phylogenetic relationships and the primitive X chromosome inferred from chromosomal and satellite DNA analysis in Bovidae 
The early phylogeny of the 137 species in the Bovidae family is difficult to resolve; knowledge of the evolution and relationships of the tribes would facilitate comparative mapping, understanding chromosomal evolution patterns and perhaps assist breeding and domestication strategies. We found that the study of the presence and organization of two repetitive DNA satellite sequences (the clone pOaKB9 from sheep, a member of the 1.714 satellite I family and the pBtKB5, a 1.715 satellite I clone from cattle) on the X and autosomal chromosomes by in situ hybridization to chromosomes from 15 species of seven tribes, was informative. The results support a consistent phylogeny, suggesting that the primitive form of the X chromosome is acrocentric, and has satellite I sequences at its centromere. Because of the distribution of the ancient satellite I sequence, the X chromosome from the extant Tragelaphini (e.g. oryx), rather than Caprini (sheep), line is most primitive. The Bovini (cow) and Tragelaphini tribes lack the 1.714 satellite present in the other tribes, and this satellite is evolutionarily younger than the 1.715 sequence, with absence of the 1.714 sequence being a marker for the Bovini and Tragelaphini tribes (the Bovinae subfamily). In the other tribes, three (Reduncini, Hippotragini and Aepycerotini) have both 1.714 and 1.715 satellite sequences present on both autosomes and the X chromosome. We suggest a parallel event in two lineages, leading to X chromosomes with the loss of 1.715 satellite from the Bovini, and the loss of both 1.714 and 1.715 satellites in a monophyletic Caprini and Alcelaphini lineage. The presence and X chromosome distribution of these satellite sequences allow the seven tribes to be distributed to four groups, which are consistent with current diversity estimates, and support one model to resolve points of separation of the tribes.
PMCID: PMC1559903  PMID: 16191610
Bovidae; phylogeny; primitive X chromosome; satellite DNA
4.  Correlating Bayesian date estimates with climatic events and domestication using a bovine case study 
Biology Letters  2008;4(4):370-374.
The tribe Bovini contains a number of commercially and culturally important species, such as cattle. Understanding their evolutionary time scale is important for distinguishing between post-glacial and domestication-associated population expansions, but estimates of bovine divergence times have been hindered by a lack of reliable calibration points. We present a Bayesian phylogenetic analysis of 481 mitochondrial D-loop sequences, including 228 radiocarbon-dated ancient DNA sequences, using a multi-demographic coalescent model. By employing the radiocarbon dates as internal calibrations, we co-estimate the bovine phylogeny and divergence times in a relaxed-clock framework. The analysis yields evidence for significant population expansions in both taurine and zebu cattle, European aurochs and yak clades. The divergence age estimates support domestication-associated expansion times (less than 12 kyr) for the major haplogroups of cattle. We compare the molecular and palaeontological estimates for the Bison–Bos divergence.
PMCID: PMC2610130  PMID: 18426745
divergence times; demographic model; population expansion; ancient DNA; time dependency
5.  An examination of positive selection and changing effective population size in Angus and Holstein cattle populations (Bos taurus) using a high density SNP genotyping platform and the contribution of ancient polymorphism to genomic diversity in Domestic cattle 
BMC Genomics  2009;10:181.
Identifying recent positive selection signatures in domesticated animals could provide information on genome response to strong directional selection from domestication and artificial selection. With the completion of the cattle genome, private companies are now providing large numbers of polymorphic markers for probing variation in domestic cattle (Bos taurus). We analysed over 7,500 polymorphic single nucleotide polymorphisms (SNP) in beef (Angus) and dairy (Holstein) cattle and outgroup species Bison, Yak and Banteng in an indirect test of inbreeding and positive selection in Domestic cattle.
Outgroup species: Bison, Yak and Banteng, were genotyped with high levels of success (90%) and used to determine ancestral and derived allele states in domestic cattle. Frequency spectrums of the derived alleles in Angus and Holstein were examined using Fay and Wu's H test. Significant divergences from the predicted frequency spectrums expected under neutrality were identified. This appeared to be the result of combined influences of positive selection, inbreeding and ascertainment bias for moderately frequent SNP. Approximately 10% of all polymorphisms identified as segregating in B. taurus were also segregating in Bison, Yak or Banteng; highlighting a large number of polymorphisms that are ancient in origin.
These results suggest that a large effective population size (Ne) of approximately 90,000 or more existed in B. taurus since they shared a common ancestor with Bison, Yak and Banteng ~1–2 million years ago (MYA). More recently Ne decreased sharply probably associated with domestication. This may partially explain the paradox of high levels of polymorphism in Domestic cattle and the relatively small recent Ne in this species. The period of inbreeding caused Fay and Wu's H statistic to depart from its expectation under neutrality mimicking the effect of selection. However, there was also evidence for selection, because high frequency derived alleles tended to cluster near each other on the genome.
PMCID: PMC2681480  PMID: 19393053
6.  Divergent evolution in the cytoplasmic domains of PRLR and GHR genes in Artiodactyla 
Prolactin receptor (PRLR) and growth hormone receptor (GHR) belong to the large superfamily of class 1 cytokine receptors. Both of them have been identified as candidate genes affecting key quantitative traits, like growth and reproduction in livestock. We have previously studied the molecular anatomy of the cytoplasmic domain of GHR in different cattle breeds and artiodactyl species. In this study we have analysed the corresponding cytoplasmic signalling region of PRLR.
We sequenced PRLR gene exon 10, coding for the major part of the cytoplasmic domain, from cattle, American bison, European bison, yak, sheep, pig and wild boar individuals. We found different patterns of variation in the two receptors within and between ruminants and pigs. Pigs and bison species have no variation within GHR exon 10, but show high haplotype diversity for the PRLR exon 10. In cattle, PRLR shows lower diversity than GHR. The Bovinae PRLR haplotype network fits better the known phylogenetic relationships between the species than that of the GHR, where differences within cattle breeds are larger than between the different species in the subfamily. By comparison with the wild boar haplotypes, a high number of subsequent nonsynonymous substitutions seem to have accumulated in the pig PRLR exon 10 after domestication.
Both genes affect a multitude of traits that have been targets of selection after domestication. The genes seem to have responded differently to different selection pressures imposed by human artificial selection. The results suggest possible effects of selective sweeps in GHR before domestication in the pig lineage or species divergence in the Bison lineage. The PRLR results may be explained by strong directional selection in pigs or functional switching.
PMCID: PMC2720954  PMID: 19622175
7.  Origin of mitochondrial DNA diversity of domestic yaks 
The domestication of plants and animals was extremely important anthropologically. Previous studies have revealed a general tendency for populations of livestock species to include deeply divergent maternal lineages, indicating that they were domesticated in multiple, independent events from genetically discrete wild populations. However, in water buffalo, there are suggestions that a similar deep maternal bifurcation may have originated from a single population. These hypotheses have rarely been rigorously tested because of a lack of sufficient wild samples. To investigate the origin of the domestic yak (Poephagus grunnies), we analyzed 637 bp of maternal inherited mtDNA from 13 wild yaks (including eight wild yaks from a small population in west Qinghai) and 250 domesticated yaks from major herding regions.
The domestic yak populations had two deeply divergent phylogenetic groups with a divergence time of > 100,000 yrs BP. We here show that haplotypes clustering with two deeply divergent maternal lineages in domesticated yaks occur in a single, small, wild population. This finding suggests that all domestic yaks are derived from a single wild gene pool. However, there is no clear correlation of the mtDNA phylogenetic clades and the 10 morphological types of sampled yaks indicating that the latter diversified recently. Relatively high diversity was found in Qinghai and Tibet around the current wild distribution, in accordance with previous suggestions that the earliest domestications occurred in this region. Conventional molecular clock estimation led to an unrealistic early dating of the start of the domestication. However, Bayesian estimation of the coalescence time allowing a relaxation of the mutation rate are better in agreement with a domestication during the Holocene as supported by archeological records.
The information gathered here and the previous studies of other animals show that the demographic histories of domestication of livestock species were highly diverse despite the common general feature of deeply divergent maternal lineages. The results further suggest that domestication of local wild prey ungulate animals was a common occurrence during the development of human civilization following the postglacial colonization in different locations of the world, including the high, arid Qinghai-Tibetan Plateau.
PMCID: PMC1626082  PMID: 16995938
8.  Evolutionary patterns of two major reproduction candidate genes (Zp2 and Zp3) reveal no contribution to reproductive isolation between bovine species 
It has been established that mammalian egg zona pellucida (ZP) glycoproteins are responsible for species-restricted binding of sperm to unfertilized eggs, inducing the sperm acrosome reaction, and preventing polyspermy. In mammals, ZP apparently represents a barrier to heterospecific fertilization and thus probably contributes to reproductive isolation between species. The evolutionary relationships between some members of the tribe Bovini are complex and highly debatable, particularly, those involving Bos and Bison species for which interspecific hybridization is extensively documented. Because reproductive isolation is known to be a major precursor of species divergence, testing evolutionary patterns of ZP glycoproteins may shed some light into the speciation process of these species. To this end, we have examined intraspecific and interspecific genetic variation of two ZP genes (Zp2 and Zp3) for seven representative species (111 individuals) from the Bovini tribe, including five species from Bos and Bison, and two species each from genera Bubalus and Syncerus.
A pattern of low levels of intraspecific polymorphism and interspecific divergence was detected for the two sequenced fragments each for Zp2 and Zp3. At intraspecific level, none of neutrality tests detected deviations from neutral equilibrium expectations for the two genes. Several haplotypes in both genes were shared by multiple species from Bos and Bison.
Here we argue that neither ancestral polymorphism nor introgressive hybridization alone can fully account for haplotype sharing among species from Bos and Bison, and that both scenarios have contributed to such a pattern of haplotype sharing observed here. Additionally, codon-based tests revealed strong evidence for purifying selection in the Zp3 coding haplotype sequences and weak evidence for purifying selection in the Zp2 coding haplotype sequences. Contrary to a general genetic pattern that genes or genomic regions contributing to reproductive isolation between species often evolve rapidly and show little or no gene flow between species, these results demonstrate that, particularly, those sequenced exons of the Zp2 and the Zp3 did not show any contribution to reproductive isolation between the bovine species studied here.
PMCID: PMC3037879  PMID: 21266067
9.  Inferring the Phylogeny of Bovidae Using Mitochondrial DNA Sequences: Resolving Power of Individual Genes Relative to Complete Genomes 
Molecular techniques that assess biodiversity through the analysis of a small segment of mitochondrial genome have been getting wide attention for inferring the mammalian diversity. Due to their highly conserved nature, specific mitochondrial genes offer a promising tool for phylogenetic analysis. However, there is no established criteria for selecting the typical mitochondrial DNA (mtDNA) segments to achieve a greater resolving power. We therefore chose the family Bovidae as a model and compared the tree-topologies resulting from the commonly used and phylogenetically-informative genes including 16S rRNA, 12S rRNA, COI, Cyt b and D-loop with respect to complete mitochondrial genome. The tree topologies from the whole mitochondrial genome of 12 species were not identical albeit similar with those resulting from the five individual genes mentioned above. High bootstrap values were observed for mtDNA compared with that of any single gene. The average pair-wise sequence divergence using different genetic modes was found to be: D-loop (0.229) > Cyt b (0.159) > COI or complete mtDNA (0.143) > 12S rRNA (0.094) > 16S rRNA (0.091). The tree resulting from complete mtDNA clearly separated the 12 taxa of Bovidae into 3 major clusters, one cluster each for subfamily Cervinae and Bovinae and the third cluster comprised the distinctive clades of Caprinae and Antilopinae. However, jumping clades of Antilopinae were observed while using the individual genes. This study showed that Bison bison and Bos Taurus have very close phylogenetic relationship compared to Bubalus bubalis (Bovinae), irrespective of the method used. Our findings suggest that complete mtDNA genome provides most reliable understanding of complex phylogenetic relationships while the reliability of individual gene trees should be verified with high bootstrap support.
PMCID: PMC3290115  PMID: 22399841
bovidae; mitochondrial genome; 16S rRNA; 12S rRNA; cytochrome oxidase 1; cytochrome b; D-loop; phylogenetic analysis
10.  Molecular anatomy of the cytoplasmic domain of bovine growth hormone receptor, a quantitative trait locus 
Quantitative trait loci (QTL) studies have indicated growth hormone receptor (GHR) as a candidate gene affecting cattle milk yield and composition. In order to characterize genetic variation at GHR in cattle, we studied European and East African breeds with different histories of selection, and Bos grunniens, Ovis aries, Sus scrofa, Bison bison and Rangifer tarandus as references. We sequenced most of the cytoplasmic domain (900 bp of exon 10), 89 bp of exon 8, including the putative causative mutation for the QTL effect, and 390 bp of intron 8 for comparison. In the cytoplasmic domain, seven synonymous and seven non-synonymous single nucleotide polymorphisms (SNP) were identified in cattle. Three non-synonymous SNPs were found in sheep and one synonymous SNP in yak, while other studied species were monomorphic. Three major haplotypes were observed, one unique to African breeds, one unique to European breeds and one shared. Bison and yak haplotypes are derivatives of the European haplotype lineage. Most of the exon 10 non-synonymous cattle SNPs appear at phylogenetically highly conserved sites. The polymorphisms in exon 10 cluster around a ruminant-specific tyrosine residue, suggesting that this site may act as an additional signalling domain of GHR in ruminants. Alternative explanations for the persistent polymorphism include balancing selection, hitch-hiking, pleiotropic or sexually antagonistic fitness effects or relaxed functional constraints.
PMCID: PMC2602661  PMID: 18381258
growth hormone receptor; cattle; polymorphism; genetic variation; QTL; quantitative trait locus; GHR; growth hormone receptor; GH; growth hormone; SNP; single nucleotide polymorphism
11.  Resolving a zoological mystery: the kouprey is a real species 
The kouprey is a rare and enigmatic forest ox discovered by scientists in Cambodia only in 1937. Numerous morphological hypotheses have been proposed for the origin of the kouprey: that it is a species closely related to banteng and gaur, two other wild oxen of southeast Asia; a morphologically divergent species placed in a separate genus, named Novibos; a wild species linked to aurochs and domestic cattle; a vicariant population of banteng; a feral cattle; or a hybrid of banteng with either zebu cattle, gaur or water buffalo.
In a recent paper, which gained a lot of media coverage, Galbreath et al. analysed mitochondrial DNA sequences and concluded that the kouprey never existed as a wild, natural species, and that it was a feral hybrid between banteng and zebu cattle.
Here we analyse eight DNA markers—three mitochondrial regions and five nuclear fragments—representing an alignment of 4582 nucleotides for the holotype of the kouprey and all related species. Our results demonstrate that the kouprey is a real and naturally occurring species, and show that Cambodian populations of banteng acquired a mitochondrial genome of kouprey by natural introgressive hybridization during the Pleistocene epoch.
PMCID: PMC2288688  PMID: 17848372
kouprey; Bos sauveli; Bos javanicus; introgression; hybridization; conservation
12.  Evolutionary history of bovine endogenous retroviruses in the Bovidae family 
Endogenous retroviruses (ERVs) are genomic elements of retroviral origin that are present in the genomes of almost all vertebrates. In cattle, more than 13,000 elements related to ERVs have been detected, and based on the pol gene, 24 families or groups of bovine ERVs have been described. However, information about ERVs in other bovids and the presence of families of related bovine ERVs in different species of the Bovidae family is scarce.
The 24 families of bovine ERVs previously detected in cattle (Bos taurus) were also detected in zebus (Bos indicus) and yaks (Bos grunniens). In addition, six new families, named BoERV25 to BoERV30, were detected in the three Bos species. Five more ruminant species were screened for related ERVs: 26 families were detected in these species, but four families (BoERV24, BoERV26, BoERV28 and BoERV29) were specific to cattle, zebus, yaks and buffalo. An analysis of the homology of the ERVs of cattle, zebus and yaks revealed that the level of LTR divergence was similar between ERVs from cattle and zebus but was less similar between with ERVs from cattle and yaks. In addition, purifying selection was detected in the genes and retroviral regions of clusters of ERVs of cattle, zebus and yaks.
In this work, the 24 ERV families previously identified in cattle were also found in two other species in the Bos genus. In addition, six new bovine ERV families were detected. Based on LTR divergence, the most recently inserted families are from Class II. The divergence of the LTR, used as an indirect estimate of the ERV insertion time, seemed to be influenced by the differences in genome evolution since the divergence of the species. In addition, purifying selection could be acting on clusters of ERVs from different species.
PMCID: PMC3879100  PMID: 24256121
13.  Dispersal of an ancient retroposon in the TP53 promoter of Bovidae: phylogeny, novel mechanisms, and potential implications for cow milk persistency 
BMC Genomics  2015;16(1):53.
In recent years, the perception of transposable genetic elements has changed from “junk DNA” to a focus of interest when appearing near or inside genes. Bov-A2 is a short interspersed nuclear element (SINE) that was first found in Bovidae and later in other ruminants. This retroposon is mostly used as a marker for phylogenetic analysis.
We describe insertions of Bov-A2 in the promoter region of TP53, a key tumor suppressor gene that is indispensable for diverse developmental processes, in Antilopinae and Tragelaphini (belonging to the Bovinae subfamily). In Tragelaphini two Bov-A2 elements were inserted sequentially, whereas in 5 tribes of Antilopinae only one Bov-A2 element was inserted, in a different site and reverse orientation. The entrance site in both cases employed short palindromes that can form hairpin secondary structures. Interestingly, mutations that create or disrupt base pairing in the palindrome sequence dictated the presence or absence of Bov-A2, such as in the domestic cow and buffalo, which lack Bov-A2. Transcription factor binding site analysis revealed unique binding sites for STAT3 and NFκB within the Bov-A2 sequence, which together with TP53 itself are known to play a crucial role in mammary involution.
This report demonstrates how short palindromes serve as hot spots for Bov-A2 retroposon insertion into the mammalian genome. The strict correlation between point mutation in the palindromes and the presence/absence of Bov-A2 retroposon insertions, questions the use of singular insertion events as valid phylogenetic markers inside families. Bov-A2 insertion into the TP53 promoter in Antilopinae and Tragelaphini may not only provide a genetic network that regulates mammary involution, but can also answer the need for rapid mammary involution in Savanna antelopes after weaning, partially in response to predation stress. The absence of Bov-A2 in domestic bovids may constitute the molecular background for greater lactation persistency.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-1235-8) contains supplementary material, which is available to authorized users.
PMCID: PMC4324840  PMID: 25653076
TP53 Promoter; Bov-A2; Molecular Phylogeny; Milk Persistency; Palindrome
14.  Maternal Phylogeny of a Newly-Found Yak Population in China 
The Jinchuan yak is a new yak population identified in Sichuan, China. This population has a special anatomical characteristic: an additional pair of ribs compared with other yak breeds. The genetic structure of this population is unknown. In the present study, we investigated the maternal phylogeny of this special yak population using the mitochondrial DNA variation. A total of 23 Jinchuan yaks were sequenced for a 823-bp fragment of D-loop control region and three individuals were sequenced for the whole mtDNA genome with a length of 16,371-bp. To compare with the data from other yaks, we extracted sequence data from Genebank, including D-loop of 398 yaks (from 12 breeds) and 55 wild yaks, and whole mitochondrial genomes of 53 yaks (from 12 breeds) and 21 wild yaks. A total of 127 haplotypes were defined, based on the D-loop data. Thirteen haplotypes were defined from 23 mtDNA D-loop sequences of Jinchuan yaks, six of which were shared only by Jinchuan, and one was shared by Jinchuan and wild yaks. The Jinquan yaks were found to carry clades A and B from lineage I and clade C of lineage II, respectively. It was also suggested that the Jinchuan population has no distinct different phylogenetic relationship in maternal inheritance with other breeds of yak. The highly haplotype diversity of the Pali breed, Jinchuan population, Maiwa breed and Jiulong breed suggested that the yak was first domesticated from wild yaks in the middle Himalayan region and the northern Hengduan Mountains. The special anatomic characteristic that we found in the Jinchuan population needs further studies based on nuclear data.
PMCID: PMC3472757  PMID: 23109865
Bos grunniens; Jinchuan yak population; mtDNA control region; mitochondrial genome; genetic diversity; phylogeny
15.  Assessment of cattle genetic introgression into domestic yak populations using mitochondrial and microsatellite DNA markers 
Animal Genetics  2010;41(3):242-252.
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 (mYcattle = 2.66 ± 0.53% and Qcattle = 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.
PMCID: PMC2878598  PMID: 19917041
admixture analysis; cattle; introgression; Qinghai-Tibetan Plateau; yak
16.  Ruminal ciliated protozoa in bison. 
Applied and Environmental Microbiology  1988;54(11):2733-2736.
Ruminal contents from 79 slaughtered bison and 2 ruminally cannulated bison were collected to obtain information on total numbers and species distribution of ciliated protozoa. The bison originated from numerous herds throughout the Great Plains and were grouped into three dietary categories: (i) only forage; (ii) forage with moderate levels of supplementation; and (iii) feedlot concentrate-silage diet. Total ciliate counts were highest in bison receiving grain supplementation (210.1 x 10(4)/g) and lowest in bison consuming only forage (27.1 x 10(4)/g). All protozoan species found in bison have been reported in domestic livestock, although Ophryoscolex sp., a relatively common protozoan in cattle, was detected at low concentrations in only eight bison. The uncommon holotrich Microcetus lappus was present in five bison in concentrations reaching 8.4% of the total ciliate population. Charonina ventriculi, another infrequently observed species, was present in 18 bison, with the highest concentrations in forage-fed animals. Thirty bison possessed a type B protozoan population, characterized by Epidinium sp., Eudiplodinium maggii, and Eudiplodinium bovis. Thirty-eight bison possessed a mixed A-B population, characterized by Polyplastron sp. coexisting with low numbers of Eudiplodinium maggii or Epidinium sp. or both. Thirteen bison possessed populations lacking any remnant type B ciliate species. At least 29 of the bison possessing Polyplastron sp. were known to have been in contact with cattle, whereas all bison isolated from cattle had type B populations. The reduction of type B populations in bison becomes increasingly likely as bison production expands into areas inhabited by domestic livestock.
PMCID: PMC204364  PMID: 3145709
17.  Comparison of methanogen diversity of yak (Bos grunniens) and cattle (Bos taurus) from the Qinghai-Tibetan plateau, China 
BMC Microbiology  2012;12:237.
Methane emissions by methanogen from livestock ruminants have significantly contributed to the agricultural greenhouse gas effect. It is worthwhile to compare methanogen from “energy-saving” animal (yak) and normal animal (cattle) in order to investigate the link between methanogen structure and low methane production.
Diversity of methanogens from the yak and cattle rumen was investigated by analysis of 16S rRNA gene sequences from rumen digesta samples from four yaks (209 clones) and four cattle (205 clones) from the Qinghai-Tibetan Plateau area (QTP). Overall, a total of 414 clones (i.e. sequences) were examined and assigned to 95 operational taxonomic units (OTUs) using MOTHUR, based upon a 98% species-level identity criterion. Forty-six OTUs were unique to the yak clone library and 34 OTUs were unique to the cattle clone library, while 15 OTUs were found in both libraries. Of the 95 OTUs, 93 putative new species were identified. Sequences belonging to the Thermoplasmatales-affiliated Linage C (TALC) were found to dominate in both libraries, accounting for 80.9% and 62.9% of the sequences from the yak and cattle clone libraries, respectively. Sequences belonging to the Methanobacteriales represented the second largest clade in both libraries. However, Methanobrevibacter wolinii (QTPC 110) was only found in the cattle library. The number of clones from the order Methanomicrobiales was greater in cattle than in the yak clone library. Although the Shannon index value indicated similar diversity between the two libraries, the Libshuff analysis indicated that the methanogen community structure of the yak was significantly different than those from cattle.
This study revealed for the first time the molecular diversity of methanogen community in yaks and cattle in Qinghai-Tibetan Plateau area in China. From the analysis, we conclude that yaks have a unique rumen microbial ecosystem that is significantly different from that of cattle, this may also help to explain why yak produce less methane than cattle.
PMCID: PMC3502369  PMID: 23078429
18.  Molecular investigation of bovine viral diarrhea virus infection in yaks (Bos gruniens) from Qinghai, China 
Virology Journal  2014;11:29.
Bovine viral diarrhea virus (BVDV) is a pestivirus which infects both domestic animals and wildlife species worldwide. In China, cattle are often infected with BVDV of different genotypes, but there is very limited knowledge regarding BVDV infection in Chinese yaks and the genetic diversity of the virus. The objectives of this study were to detect viral infection in yaks in Qinghai, China and to determine the genotypes of BVDV based on analysis of the 5′untranslated region (5′UTR) and N-terminal protease (Npro) region.
Between 2010 and 2012, 407 blood samples were collected from yaks with or without clinical signs in six counties of Qinghai Province. Ninety-eight samples (24%) were found to be positive by reverse transcription polymerase chain reaction (RT-PCR) targeting a conserved region of BVDV-1 and BVDV-2. The nucleotide sequences of the 5′UTR and complete Npro region were determined for 16 positive samples. Phylogenetic reconstructions demonstrated that all 16 samples belong to subgenotypes BVDV-1b, BVDV-1d and BVDV-1q.
This study provides, for the first time, molecular evidence for BVDV infection in yaks in Qinghai involving multiple subgenotypes of BVDV-1. This may have occurred under three possible scenarios: interspecies transmission, natural infection, and the use of vaccines contaminated with BVDV. The results have important implications for yak production and management in China, and specifically indicate that unscientific vaccination practices should be stopped and bio-security increased.
PMCID: PMC3926853  PMID: 24524442
Bovine viral diarrhea virus; Yak; 5′UTR; Npro; Phylogeny
19.  A mobile element-based evolutionary history of guenons (tribe Cercopithecini) 
BMC Biology  2007;5:5.
Guenons (tribe Cercopithecini) are a species-rich group of primates that have attracted considerable attention from both primatologists and evolutionary biologists. The complex speciation pattern has made the elucidation of their relationships a challenging task, and many questions remain unanswered. SINEs are a class of non-autonomous mobile elements and are essentially homoplasy-free characters with known ancestral states, making them useful genetic markers for phylogenetic studies.
We identified 151 novel Alu insertion loci from 11 species of tribe Cercopithecini, and used these insertions and 17 previously reported loci to infer a phylogenetic tree of the tribe Cercopithecini. Our results robustly supported the following relationships: (i) Allenopithecus is the basal lineage within the tribe; (ii) Cercopithecus lhoesti (L'Hoest's monkey) forms a clade with Chlorocebus aethiops (African green monkey) and Erythrocebus patas (patas monkey), supporting a single arboreal to terrestrial transition within the tribe; (iii) all of the Cercopithecus except C. lhoesti form a monophyletic group; and (iv) contrary to the common belief that Miopithecus is one of the most basal lineages in the tribe, M. talapoin (talapoin) forms a clade with arboreal members of Cercopithecus, and the terrestrial group (C. lhoesti, Chlorocebus aethiops and E. patas) diverged from this clade after the divergence of Allenopithecus. Some incongruent loci were found among the relationships within the arboreal Cercopithecus group. Several factors, including incomplete lineage sorting, concurrent polymorphism and hybridization between species may have contributed to the incongruence.
This study presents one of the most robust phylogenetic hypotheses for the tribe Cercopithecini and demonstrates the advantages of SINE insertions for phylogenetic studies.
PMCID: PMC1797000  PMID: 17266768
20.  An update of the goat genome assembly using dense radiation hybrid maps allows detailed analysis of evolutionary rearrangements in Bovidae 
BMC Genomics  2014;15(1):625.
The domestic goat (Capra hircus), an important livestock species, belongs to a clade of Ruminantia, Bovidae, together with cattle, buffalo and sheep. The history of genome evolution and chromosomal rearrangements on a small scale in ruminants remain speculative. Recently completed goat genome sequence was released but is still in a draft stage. The draft sequence used a variety of assembly packages, as well as a radiation hybrid (RH) map of chromosome 1 as part of its validation.
Using an improved RH mapping pipeline, whole-genome dense maps of 45,953 SNP markers were constructed with statistical confidence measures and the saturated maps provided a fine map resolution of approximate 65 kb. Linking RH maps to the goat sequences showed that the assemblies of scaffolds/super-scaffolds were globally accurate. However, we observed certain flaws linked to the process of anchoring chromosome using conserved synteny with cattle. Chromosome assignments, long-range order, and orientation of the scaffolds were reassessed in an updated genome sequence version. We also present new results exploiting the updated goat genome sequence to understand genomic rearrangements and chromosome evolution between mammals during species radiations. The sequence architecture of rearrangement sites between the goat and cattle genomes presented abundant segmental duplication on regions of goat chromosome 9 and 14, as well as new insertions in homologous cattle genome regions. This complex interplay between duplicated sequences and Robertsonian translocations highlights the rearrangement mechanism of centromeric nonallelic homologous recombination (NAHR) in mammals. We observed that species-specific shifts in ANKRD26 gene duplication are coincident with breakpoint reuse in divergent lineages and this gene family may play a role in chromosome stabilization in chromosome evolution.
We generated dense maps of the complete whole goat genome. The chromosomal maps allowed us to anchor and orientate assembled genome scaffolds along the chromosomes, annotate chromosome rearrangements and thereby get a better understanding of the genome evolution of ruminants and other mammals.
Electronic supplementary material
The online version of this article (doi:10.1186/1471-2164-15-625) contains supplementary material, which is available to authorized users.
PMCID: PMC4141111  PMID: 25052253
Goat; Radiation hybrid map; Genomic rearrangements; Gene duplication
21.  Microsatellite markers of water buffalo, Bubalus bubalis - development, characterisation and linkage disequilibrium studies 
BMC Genetics  2009;10:68.
Microsatellite markers are highly polymorphic and widely used in genome mapping and population genetic studies in livestock species. River buffalo, Bubalus bubalis is an economically important livestock species, though only a limited number of microsatellite markers have been reported thus far in this species.
In the present study, using two different approaches 571 microsatellite markers have been characterized for water buffalo. Of the 571 microsatellite markers, 498 were polymorphic with average heterozygosity of 0.51 on a panel of 24 unrelated buffalo. Fisher exact test was used to detect LD between the marker pairs. Among the 137550 pairs of marker combination, 14.58% pairs showed significant LD (P < 0.05). Further to check the suitability of these microsatellite markers to map these on a radiation hybrid map of buffalo genome, the markers were tested on Chinese hamster genomic DNA for amplification. Only seven of these markers showed amplification in Chinese hamster, and thus 564, of these can be added to the radiation hybrid map of this species.
The high conservation of cattle microsatellite loci in water buffalo promises the usefulness of the cattle microsatellites markers on buffalo. The polymorphic markers characterised in this study will contribute to genetic linkage and radiation hybrid mapping of water buffalo and population genetic studies.
PMCID: PMC2773805  PMID: 19843347
22.  First molecular characterization of Cryptosporidium and Giardia from bovines (Bos taurus and Bubalus bubalis) in Sri Lanka: unexpected absence of C. parvum from pre-weaned calves 
Parasites & Vectors  2014;7:75.
The genetic characterization of Cryptosporidium and Giardia has important implications for investigating their epidemiology and underpins their control. We undertook the first molecular epidemiological survey of domestic bovids in selected regions of Sri Lanka to establish whether they excreted Cryptosporidium and/or Giardia with zoonotic potential.
Faecal samples were collected from dairy calves (n = 340; Bos taurus; < 3 months of age; weekly sampling for six weeks) and water buffaloes (n = 297; Bubalus bubalis; <6 months and ≥6 months of age; one sampling) from seven different farms in Sri Lanka. Genomic DNAs were extracted from individual faecal samples and then tested for the presence of parasite DNA using a PCR-based mutation scanning-targeted sequencing-phylogenetic approach, employing genetic markers within the small subunit of nuclear ribosomal RNA and 60 kDa glycoprotein genes (designated pSSU and pgp60, respectively) for Cryptosporidium, and within the triose phosphate isomerise (ptpi) gene for Giardia.
Based on pSSU sequence data, C. bovis, C. ryanae and six new genotypes that were genetically similar but not identical to C. andersoni (n = 1), C. bovis (n = 1), C. ryanae (n = 3) and C. suis (n = 1) were recorded in cattle. For pSSU, two other, new genotypes were defined in water buffalo, which were genetically most similar to Cryptosporidium genotypes recorded previously in this host species in other countries including Australia. Consistent with the findings for pSSU, no species or genotypes of Cryptosporidium with zoonotic potential were detected using pgp60. Based on ptpi sequence data, G. duodenalis assemblages A and E were detected in four and 137 samples from cattle, respectively, and assemblage E in two samples from water buffaloes.
The present study showed that C. parvum, the most commonly reported zoonotic species of Cryptosporidium recognised in bovine calves globally, was not detected in any of the samples from pre-weaned calves tested in the present study. However, eight new genotypes were recorded. Future studies of different host species in various regions are required to investigate the molecular epidemiology of cryptosporidiosis and giardiasis in Sri Lanka and neighbouring countries in South Asia.
PMCID: PMC4015788  PMID: 24559043
Bos taurus; Bubalus bubalis; Cryptosporidium; Giardia; Single-strand conformation polymorphism (SSCP) analysis; Restriction endonuclease fingerprinting (REF); Sri Lanka
23.  A possible case of caprine-associated malignant catarrhal fever in a domestic water buffalo (Bubalus bubalis) in Switzerland 
Malignant catarrhal fever (MCF) is a fatal herpesvirus infection, affecting various wild and domestic ruminants all over the world. Water buffaloes were reported to be particularly susceptible for the ovine herpesvirus-2 (OvHV-2) causing the sheep-associated form of MCF (SA-MCF). This report describes the first case of possibly caprine-associated malignant catarrhal fever symptoms in a domestic water buffalo in Switzerland.
Case presentation
The buffalo cow presented with persistent fever, dyspnoea, nasal bleeding and haematuria. Despite symptomatic therapy, the buffalo died and was submitted to post mortem examination. Major findings were an abomasal ulceration, a mild haemorrhagic cystitis and multifocal haemorrhages on the epicardium and on serosal and mucosal surfaces. Eyes and oral cavity were not affected. Histopathology revealed a mild to moderate lymphohistiocytic vasculitis limited to the brain and the urinary bladder. Although these findings are typical for MCF, OvHV-2 DNA was not detected in peripheral blood lymphocytes or in paraffin-embedded brain, using an OvHV-2 specific real time PCR. With the aid of a panherpesvirus PCR, a caprine herpesvirus-2 (CpHV-2) sequence could be amplified from both samples.
To our knowledge, this is the first report of malignant catarrhal fever in the subfamily Bovinae, where the presence of CpHV-2 could be demonstrated. The etiological context has yet to be evaluated.
PMCID: PMC3259070  PMID: 22132808
24.  Mapping whole genome shotgun sequence and variant calling in mammalian species without their reference genomes 
F1000Research  2013;2:244.
Genomics research in mammals has produced reference genome sequences that are essential for identifying variation associated with disease.  High quality reference genome sequences are now available for humans, model species, and economically important agricultural animals.  Comparisons between these species have provided unique insights into mammalian gene function.  However, the number of species with reference genomes is small compared to those needed for studying molecular evolutionary relationships in the tree of life.  For example, among the even-toed ungulates there are approximately 300 species whose phylogenetic relationships have been calculated in the 10k trees project.  Only six of these have reference genomes:  cattle, swine, sheep, goat, water buffalo, and bison.  Although reference sequences will eventually be developed for additional hoof stock, the resources in terms of time, money, infrastructure and expertise required to develop a quality reference genome may be unattainable for most species for at least another decade.  In this work we mapped 35 Gb of next generation sequence data of a Katahdin sheep to its own species’ reference genome ( Ovis aries Oar3.1) and to that of a species that diverged 15 to 30 million years ago ( Bos taurus UMD3.1).  In total, 56% of reads covered 76% of UMD3.1 to an average depth of 6.8 reads per site, 83 million variants were identified, of which 78 million were homozygous and likely represent interspecies nucleotide differences. Excluding genome repeat regions and sex chromosomes, approximately 3.7 million heterozygous sites were identified in this animal vs. bovine UMD3.1, representing polymorphisms occurring in sheep.  Of these, 41% could be readily mapped to orthologous positions in ovine Oar3.1 with 80% corroborated as heterozygous.  These variant sites, identified via interspecies mapping could be used for comparative genomics, disease association studies, and ultimately to understand mammalian gene function.
PMCID: PMC4103496  PMID: 25075278
25.  Mapping whole genome shotgun sequence and variant calling in mammalian species without their reference genomes 
F1000Research  2014;2:244.
Genomics research in mammals has produced reference genome sequences that are essential for identifying variation associated with disease.  High quality reference genome sequences are now available for humans, model species, and economically important agricultural animals.  Comparisons between these species have provided unique insights into mammalian gene function.  However, the number of species with reference genomes is small compared to those needed for studying molecular evolutionary relationships in the tree of life.  For example, among the even-toed ungulates there are approximately 300 species whose phylogenetic relationships have been calculated in the 10k trees project.  Only six of these have reference genomes:  cattle, swine, sheep, goat, water buffalo, and bison.  Although reference sequences will eventually be developed for additional hoof stock, the resources in terms of time, money, infrastructure and expertise required to develop a quality reference genome may be unattainable for most species for at least another decade.  In this work we mapped 35 Gb of next generation sequence data of a Katahdin sheep to its own species’ reference genome ( Ovis aries Oar3.1) and to that of a species that diverged 15 to 30 million years ago ( Bos taurus UMD3.1).  In total, 56% of reads covered 76% of UMD3.1 to an average depth of 6.8 reads per site, 83 million variants were identified, of which 78 million were homozygous and likely represent interspecies nucleotide differences. Excluding repeat regions and sex chromosomes, nearly 3.7 million heterozygous sites were identified in this animal vs. bovine UMD3.1, representing polymorphisms occurring in sheep.  Of these, 41% could be readily mapped to orthologous positions in ovine Oar3.1 with 80% corroborated as heterozygous.  These variant sites, identified via interspecies mapping could be used for comparative genomics, disease association studies, and ultimately to understand mammalian gene function.
PMCID: PMC4103496  PMID: 25075278

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