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1 Immunology–Vaccinology (B43b), Department of Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, Belgium
2 Institute of Genetics, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK
Correspondence
Alain Vanderplasschen
A.vdplasschen{at}ulg.ac.be
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the nucleotide sequences determined in this work are AY847305 [GenBank] –AY847311 [GenBank] and AY847322 [GenBank] –AY847348 [GenBank] .
Supplementary tables with primer details and GenBank accession numbers for the BoHV-4 sequenced regions are available in JGV Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Markine-Goriaynoff et al., 2003b; Thiry et al., 1992). The widespread distribution of BoHV-4 in cattle (Bos taurus and Bos indicus) populations justified the conclusion that the bovine species is the natural host; hence the nomenclature of the virus. However, BoHV-4 has also been detected in a variety of other ruminants (Todd & Storz, 1983; Van Opdenbosch et al., 1986). In particular, BoHV-4 infection is very common among wild African buffalo (Syncerus caffer). An early survey performed mainly within one reserve in Kenya revealed that BoHV-4 can be isolated from the blood of healthy wild African buffaloes with a high frequency (25 %) and that almost all (94 %) animals tested had antibodies against BoHV-4 (Rossiter et al., 1989). More recently, our seroprevalence study of 400 sera from wild African buffaloes from numerous locations in eastern and southern Africa revealed that, independent of their geographical origin, members of this species exhibit a seroprevalence of anti-BoHV-4 antibodies of around 70 % (Dewals et al., 2005), a rate much higher than is generally observed in cattle populations (16–18 %) (Wellenberg et al., 1999). These observations suggest that African buffalo may be the original host species of BoHV-4 and that other species, including domestic cattle, may have acquired the virus more recently.
An independent observation supports the role of the African buffalo as the original host species of BoHV-4. The Bo17 gene of BoHV-4 is the only viral gene known to date that encodes a homologue of the cellular core 2 
-1,6-N-acetylglucosaminyltransferase-mucin type (Vanderplasschen et al., 2000). Our phylogenetic study demonstrated that the Bo17 gene is related significantly more closely to the cellular homologue from African buffalo than to that from cattle, indicating that the viral gene was acquired from a recent ancestor of the African buffalo (Markine-Goriaynoff et al., 2003a). Furthermore, the gene-acquisition event was dated at around 1.5 million years ago, long after the separation of the Bos and Syncerus lineages and long before the domestication of cattle. The sequences of the Bo17 gene from nine BoHV-4 strains, three from African buffalo and six from cattle, were split into two clades according to the species of origin (Markine-Goriaynoff et al., 2003a), consistent with restriction-profile analyses showing a clear differentiation between BoHV-4 strains isolated from the two species (Bublot et al., 1991; Markine-Goriaynoff et al., 2003a; Rossiter et al., 1989). For Bo17, the divergence between the two viral lineages was estimated to have occurred about 0.7 million years ago, suggesting a relatively ancient transmission of BoHV-4 from the ancestor of the African buffalo to Bos primigenius, the wild ancestor of domesticated cattle. Among the cattle strains, the one isolated from zebu (B. indicus) formed an outgroup to those from the taurine cattle (B. taurus) lineage and the split was estimated to have occurred at about the same time as the divergence of the ancestors of B. taurus and B. indicus, around 0.2–0.3 million years ago, consistent with a host-dependent split between zebu and taurine BoHV-4 strains. Thus, whilst these data indicated that BoHV-4 has been co-evolving with the African buffalo for at least the last 1.5 million years, they also pointed to infection of cattle since long before they were domesticated, around 10 000 years ago.
These interpretations of the evolutionary history of BoHV-4 must be treated with caution because they rely on the analysis of a single gene, Bo17. Recombination has been reported in numerous species of herpesviruses (Burrows et al., 1996; Norberg et al., 2004; Poole et al., 1999; Thiry et al., 2005; Walling & Raab-Traub, 1994). The consequence of recombination is that different genes may have different evolutionary histories. Therefore, we set out to investigate the phylogenetic relationships among the nine BoHV-4 strains that were used in our former study (Markine-Goriaynoff et al., 2003a) by characterizing four more gene sequences from three different regions distributed across the genome. The results demonstrate that BoHV-4 evolution has indeed involved recombination among divergent strains and that the evolutionary history of the Bo17 gene is not typical of that of the genome as a whole. These data necessitate a new interpretation of the origins of the various lineages of BoHV-4 distributed worldwide among cattle.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The complete sequence of strain 66-p-347 has been published previously (Zimmermann et al., 2001). Sequences from the other eight strains were obtained in this study.
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and the primers used for the amplifications are given in Supplementary Table S1 (available in JGV Online). PCR products were subsequently purified (Wizard PCR Preps DNA purification system; Promega) and sequenced by primer walking using a BigDye Terminator v3.1 cycle sequencing kit (Applied Biosystems). An ABI Prism 3730 DNA Analyser (Applied Biosystems) was used for analysis of samples.
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Sequence analysis.
Sequences were aligned by using CLUSTAL W (Thompson et al., 1994), with minor manual adjustment. The numbers of non-synonymous (KA) and synonymous (KS) substitutions per site were estimated by the method of Li (1993). Phylogenetic trees were estimated from nucleotide sequences by the neighbour-joining (NJ) method (Saitou & Nei, 1987), using distances corrected by Kimura's two-parameter method and 1000 bootstrap replicates, as implemented in CLUSTAL W. Phylogenetic trees were also estimated by the maximum-likelihood (ML) method, implemented using DNAML from the PHYLIP package (J. Felsenstein; http://evolution.genetics.washington.edu/phylip.html). No significant differences were found between the NJ and ML trees; the results from the NJ analyses are presented. For most of the sequences analysed, there was no suitable outgroup available and, so, each tree was rooted at its midpoint; for the one case where an outgroup was available (the Bo17 gene), midpoint rooting yielded the same result as outgroup rooting (Markine-Goriaynoff et al., 2003a). Observed substitution rates were consistent with midpoint rooting for the other genes. Recombination was inferred from topological differences between the trees for different genes and was not dependent on the position of the root (except in one case, discussed specifically). Mosaicism of sequences due to recombination was investigated by analysis of phylogenetically informative sites; the statistical significance of putative recombination breakpoints was assessed by a permutation test (Hatwell & Sharp, 2000).
The protein encoded by the Bo10 gene was found to contain a highly variable, Ser-rich region that was difficult to align with confidence. This region, corresponding to codons 38–94 in the 66-p-347 Bo10 sequence, was excluded from the comparative analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) were compared for four different regions distributed across the genome (Fig. 1). Three strains were isolated from buffalo in Kenya, five from taurine cattle from Europe or North America and one from zebu cattle in India; these nine strains are representative of the three groups of BoHV-4 strains defined on the basis of restriction profiles. From left to right, the genomic regions selected for this study were ORF 16, the Bo10 ORF, ORF 71–ORF 73 and the previously characterized Bo17 ORF. The ORF 71–ORF 73 region includes two genes and the region between them (IG 71–73). A putative 74 codon ORF, called Bo13, overlapping ORF 71 and ORF 73 and thus spanning the IG 71–73 region, has been described in the genome of strain 66-p-347 (Zimmermann et al., 2001). However, we found an insertion of 1 nt within IG 71–73, resulting in a frameshift, in six of the nine viral strains. Also, in a comparison of strains 66-p-347 and M40 (the latter lacks the frameshift), there was an excess of non-synonymous over synonymous substitutions. These observations suggest that this ORF does not function as a gene.
In each region, the three European strains (V. test, MOVAR and LVR 140) were very similar, differing by no more than 2 nt and showing overall diversity (summed across regions) of <0.1 %, consistent with the similarity of the EcoRI restriction profiles of the genomes of these three strains (Markine-Goriaynoff et al., 2003a). Similarly, the two North American strains (DN599 and 66-p-347) differed by only 1 nt in each of two regions, again consistent with their restriction profiles. In contrast, the three buffalo strains (108, 130 and Buf.) differed from each other by up to 2.5 % overall. The most divergent strain was M40 from zebu, differing on average at 4.7 % of sites. Phylogenetic analysis of a concatenated alignment of all four regions (a total of 4093 sites compared) yielded a tree in which the European and North American strains from taurine cattle clustered, the three African buffalo strains clustered and the Indian zebu strain appeared to be the outgroup (Fig. 2a). This tree differed from that found previously from analysis of the Bo17 gene alone (Markine-Goriaynoff et al., 2003a), where the M40 strain grouped quite close to the taurine cattle virus clade. Therefore, phylogenetic analyses of each of the individual regions were compared.
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). Significant topological differences among the trees must reflect recombination during the divergence of the BoHV-4 strains. In comparison to the tree from the concatenated sequences, only the IG 71–73 tree was similar, but each of the gene trees differed with respect to the position of only one or a small number of strains. This suggests that the tree from the concatenated sequences reflects the clonal evolution of the viral strains, whereas the trees from individual sequences indicate the impact of occasional inter-strain recombination events. To facilitate interpretation of the differences among the trees, the extent of synonymous nucleotide substitution (KS) between pairs of strains was calculated for each gene. Synonymous-substitution rates are expected to be similar for different genes and, so, differences among genes in KS values for the same pair of strains may reflect differences in the time since common ancestry, due to recombination.
The ORF 16 tree differed from the concatenated tree in that the topological positions of the 130 and Buf. strains switched (Fig. 2b). The extent of synonymous substitution between Buf. and 108 was lower than for any other gene (Table 2), suggesting that the ancestor of the Buf. strain acquired DNA by recombination from a recent ancestor of the 108 strain. The Bo10 tree differed from the concatenated tree in two, more subtle, ways. First, the North American strains were very close to the European strains, with KS values less than half those seen for other genes, suggesting that a recombination event occurred between the ancestors of the two groups. Second, midpoint rooting placed the 130, 108 and Buf. strains together with M40 on one side of the root. Although an alternative rooting with the same topology as the concatenated tree is possible, the KS values for Bo10 between M40 and the buffalo strains are lower than those for other genes (except Bo17) and lower than those for Bo10 between M40 and the taurine strains. This suggests the occurrence of a recombination event between the ancestor of the buffalo strains and an ancestor of the M40 strain. However, the KS values do not provide a clear indication of the direction of the exchange in this case. In the ORF 71 tree, the North American strains clustered within the African buffalo clade (Fig. 2b), suggesting that the ancestor of the North American strains acquired the ORF 71 sequence from an ancestor of the 108 and 130 strains. In the ORF 73 tree, the three buffalo strains did not form a monophyletic clade. This topology could be explained as the result of an acquisition of sequence by an ancestor of the 108 and 130 strains from the common ancestor of the European and North American strains, but further investigation of this region (see below) revealed a complex mosaic of evolutionary histories within this gene. Finally, the Bo17 tree differed from all others in placing the M40 strain close to the clade of taurine cattle viruses, and Bo17 KS values between M40 and the five taurine viruses were unusually low. This suggests that an ancestor of the M40 strain acquired sequence encompassing the Bo17 ORF from a common ancestor of the North American and European strains.
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). It is now apparent that the unclassifiable strains are not a true group, as they are much more heterogeneous than the two other groups, are not monophyletic and have complex relationships due to interlineage recombination (Fig. 2).
The ORF 71–73 region of the BoHV-4 genome contains recombination breakpoints
The three contiguous genomic regions ORF 71, IG 71–73 and ORF 73 yielded three different trees (Fig. 2), suggesting the presence of (at least) two recombination breakpoints within this ORF 71–73 region. As recombination need not occur at the boundaries of genes, the distribution of informative sites within this region was examined in order to localize the putative breakpoints. The three European strains were considered as a single taxon, as were the two North American strains and two of the buffalo strains (108 and 130); thus, together with strains Buf. and M40, there were five taxa in the analysis, which may be connected by 15 possible unrooted tree topologies (Fig. 3). There were 24 phylogenetically informative sites, including a tetranucleotide at position 976–979 (GTCT in Buf. and M40; ACAA in the other strains) that we considered as a single site (Table 3). Each informative site was consistent with, i.e. would require a single mutation on, three of the 15 possible topologies; any of the 12 other topologies would require two mutations at the same site on different branches of the tree. Within ORF 71, there were five (of seven) informative sites consistent with topology 12, the tree found for ORF 71 (Fig. 2b); across the rest of the region, there was only one other such site, at the far end of ORF 73. Over the intergenic region and ORF 73, 12 (of 17) informative sites were consistent with topology 1, the tree found for ORF 73 (Fig. 2b). In a permutation test, this array of informative sites for topologies 1 and 12 was significantly non-random (P<0.01). These data suggest that a recombination breakpoint occurred between the informative sites at 514 and 591, close to the end of ORF 71.
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), corresponds to topology 3. Many of the informative sites across IG 71–73 and ORF 73 consistent with topology 1 were also consistent with topology 3 (Table 3). However, within the region from 930 to 1202 were four sites consistent with topology 1, but not with topology 3; these include the tetranucleotide site, which seems unlikely to have undergone similar mutations in two different branches of the tree. In this context, the important difference between the two topologies is whether the three buffalo strains cluster (as in topology 3) or not (topology 1). Phylogenetic analysis of the region from 901 to 1230 (from the middle of ORF 73) yielded a tree (Fig. 4b) in which strains 108 and 130 fell within the clade of taurine cattle viruses, with strong bootstrap support; this tree matches topology 4. In contrast, a tree (Fig. 4a) based on a concatenation of regions 550–900 and 1231–1456 (IG 71–73 plus the two ends of ORF 73) was the same as the overall concatenated tree (Fig. 2a). Thus, the earlier tree for ORF 73 (Fig. 2b) does not appear to reflect the evolutionary history of any sequence within that gene, but was a compromise between the two histories for different segments within the gene (Fig. 4). Simultaneous analysis for two breakpoints within the array of the informative sites supporting topology 3 or topology 4 across IG 71–73 and ORF 73 yielded significant (P=0.005) results in a permutation test. These data suggest that there are two recombination breakpoints within ORF 73, representing the introduction of an internal segment of the gene from an ancestor of the European strains into the ancestor of strains 108 and 130.
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Estimation of divergence time between BoHV-4 phylogeographical clades
In the concatenated sequence tree inferred above to reflect the evolutionary history of the clonal backbone of the BoHV-4 genome (Fig. 2a), the various strains form phylogeographical clades. To estimate the divergence times of these clades, average KS values across the five gene sequences were calculated for each pairwise comparison of strains (Table 2). As genes involved in recombination events would have different times of divergence from those genes inherited clonally, a corrected average was calculated, excluding pairwise comparisons involving sequences that may have been acquired by recombination. Mean corrected averages were then calculated for groups of pairwise comparisons that diverged at the same point in the tree. Assuming a rate of evolution of 5x10–8 substitutions per site per year for BoHV-4 (Markine-Goriaynoff et al., 2003a), estimated times of divergence between the different clades were calculated from the mean corrected KS values. These data suggest that the initial split of the M40 strain lineage from the ancestor of the other strains occurred around 850 000 years ago, whilst the last common ancestor of the taurine and buffalo strains existed around 730 000 years ago. The separation between the European and North American clades was estimated at around 260 000 years ago, whilst the last common ancestor of the buffalo strains existed around 280 000 years ago. These estimates of the divergence times between the clades, as well as the various recombination events detected in the present study, are summarized in Fig. 5.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; McGeoch, 2001; McGeoch et al., 1995; Sharp, 2002). Nevertheless, there are clear instances where cross-species transmission must have occurred in the past, for example to give rise to bovine and wallaby viruses that lie within the radiation of primate alphaherpesviruses. Whilst evolving with their hosts, gammaherpesviruses have captured a variety of genes from their genomes (McGeoch, 2001; Shackelton & Holmes, 2004). In an investigation of the origin of one such gene, the Bo17 gene of BoHV-4, we found that the gene was acquired from the genome of African buffalo, indicating that BoHV-4 had been transmitted from buffalo to cattle at some time after the gene-acquisition event (Markine-Goriaynoff et al., 2003a). Nevertheless, phylogenetic analyses of the Bo17 genes from various cattle and buffalo strains of BoHV-4 suggested that the cross-species transmission event could have occurred up to 0.7 million years ago and that the virus may have been co-evolving with cattle since then (Markine-Goriaynoff et al., 2003a). For the same group of strains, we have now analysed sequences of four other genes from locations across the BoHV-4 genome. These data provide evidence of a number of recombination events during the divergence of the strains, including one involving the Bo17 gene, so that it is now apparent that the evolutionary history of the BoHV-4 strains is very different from that inferred previously.
Although a number of recombination events were detected, such that none of the trees for the five genes investigated here were the same, it is clear that recombination between divergent strains has been relatively infrequent during the diversification of BoHV-4. With even a modest rate of recurrent recombination, the evolutionary histories of different genes would become quite scrambled. However, here it was possible to discern the underlying tree reflecting the clonal evolution of strains, upon which the recombination events have been superimposed (Fig. 5). In that tree, the cattle strains do not form a single clade, but rather the M40 strain from zebu represents the earliest-diverging lineage. From this tree alone, the most-parsimonious interpretation would be a single transmission from cattle to African buffalo. However, the estimated divergence times for the various lineages in the tree do not correspond well with the evolutionary history of domestic cattle. Although these dates rely on the use of a synonymous-substitution rate estimated for the Bo17 gene (Markine-Goriaynoff et al., 2003a), other BoHV-4 genes seem (as expected) to have a similar rate (Table 2). Estimates of the synonymous-substitution rate for herpes simplex viruses (3x10–8; Hatwell & Sharp, 2000) and during the divergence of Epstein–Barr virus and Cercopithecine herpesvirus 12 (2x10–8–4x10–8; Hughes, 2002) are a little lower than, but of the same order as, that used here for BoHV-4 (5x10–8); thus, the estimated dates are unlikely to be substantially wrong, but must be taken with some caution. Thus, the split between the M40 strain and others, at around 850 000 years ago, greatly predates the estimated time of divergence between the ancestors of zebu and taurine cattle, placed at 275 000 years ago (Bradley et al., 1996). Similarly, the split between the European and North American BoHV-4 strains from taurine cattle was estimated at around 260 000 years ago, whereas taurine cattle were domesticated about 10 000 years ago and the ancestors of the North American domestic cattle were taken there from Europe less than 500 years ago. These observations suggest strongly that BoHV-4 has not been co-evolving with cattle during most of the evolutionary history portrayed in the tree. Taken together with our previous conclusion that BoHV-4 infected African buffalo around 1.5 million years ago, when the Bo17 gene was acquired (Markine-Goriaynoff et al., 2003a), and the observation that the prevalence of BoHV-4 infection is higher in buffalo than in cattle (Dewals et al., 2005), these data point to the African buffalo as the original BoHV-4 reservoir, implying at least three recent cross-species transmissions to cattle to give rise to the lineages seen in zebu and in European and North American taurine cattle.
In this interpretation, the overall tree reflects divergence of, and recombination between, BoHV-4 strains infecting African buffalo over the last million years. However, the three strains isolated from buffalo form a subclade within the tree, with a much more recent coalescence time (around 280 000 years ago) than the tree as a whole (around 850 000 years ago). Buffalo are distributed widely across sub-Saharan Africa, but all three strains analysed here were sampled from Kenya and, so, it is possible that more divergent strains of BoHV-4 infect buffalo elsewhere in Africa. However, the great rinderpest epidemic of the 1890s caused mortality levels reaching 80–90 % among African ruminant species, notably causing a crash in the African buffalo population (Mack, 1970; Wenink et al., 1998). It would not be surprising if this led to a dramatic reduction in the diversity of buffalo BoHV-4 lineages. Thus, the various cattle strains of BoHV-4 would reflect more divergent lineages that survived because they were transmitted from buffalo to other species before the rinderpest epidemic. Further isolation and phylogenetic analysis of buffalo BoHV-4 strains in various sub-Saharan areas are required to test these two hypotheses.
The transmission of BoHV-4 from buffalo to cattle probably involved intermediate host species. It has been shown that BoHV-4 is able to replicate in a broad range of mammal species both in vivo and in vitro (Gillet et al., 2004). Certainly, any transmission prior to the domestication of cattle is unlikely to have been direct, as their ancestor, B. primigenius, was found only in Eurasia and North Africa (Troy et al., 2001), whereas African buffalo are restricted to sub-Saharan Africa (Simonsen et al., 1998; Van Hooft et al., 2002). Also, the relatively large divergence between North American and European BoHV-4 strains, estimated to have diverged around 260 000 years ago, is surprising if both lineages had an origin in European cattle. No North American-type BoHV-4 strains have ever been described in Europe (Bublot et al., 1990, 1991), whereas European-type BoHV-4 strains have been described in North American cattle (Henry et al., 1986; Shen et al., 1992). Thus, it seems more likely that the divergence of North American strains reflects a host jump in prehistory followed by a recent transmission to cattle. North American-like strains of BoHV-4 have been recovered from the North American bison (Bison bison) (Todd & Storz, 1983) and it is plausible that bison were the reservoir for the ancestors of the North American strains. Bison are believed to have first entered eastern Beringia from Asia during the middle Pleistocene (300 000–130 000 years ago) and then moved southward into central North America around 130 000–75 000 years ago (Shapiro et al., 2004). This scenario argues for a very recent cross-species transmission from bison to cattle, whilst the European-like strains in North America are probably due to the recent wide flow of livestock breeds associated with modern selective breeding. It would be interesting to isolate a collection of BoHV-4 strains from bison and cattle populations in North America and to establish the proportion and the distribution of North American-type and European-type BoHV-4 strains. European bison became extinct in the wild in 1919; attempts to detect evidence of BoHV-4 infection in a reintroduced population from a single area have proved unsuccessful (Borchers et al., 2002).
In conclusion, taken together with recent serological and viral isolation data (Dewals et al., 2005; Rossiter et al., 1989), the present study further supports the role of the African buffalo as the original natural host species of BoHV-4. It suggests that while BoHV-4 has been coevolving with the African buffalo for at least the last 1.5 million years, it has been transmitted to cattle on at least three independent occasions, and via intermediate species much more recently.
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ACKNOWLEDGEMENTS |
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Received 9 December 2005;
accepted 17 February 2006.
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