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Journal of Virology, November 2000, p. 10401-10406, Vol. 74, No. 22
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Toward a Comprehensive Phylogeny for Mammalian and
Avian Herpesviruses
Duncan J.
McGeoch,*
Aidan
Dolan, and
Adam C.
Ralph
Medical Research Council Virology Unit,
Institute of Virology, Glasgow G11 5JR, United Kingdom
Received 17 July 2000/Accepted 22 August 2000
 |
ABSTRACT |
With the aim of deriving a definitive phylogenetic tree for as many
mammalian and avian herpesvirus species as possible, alignments were
made of amino acid sequences from eight conserved and ubiquitously present genes of herpesviruses, with 48 virus species each represented by at least one gene. Phylogenetic trees for both single-gene and
concatenated alignments were evaluated thoroughly by maximum-likelihood methods, with each of the three herpesvirus subfamilies (the
Alpha-, Beta-, and
Gammaherpesvirinae) examined independently. Composite trees
were constructed starting with the top-scoring tree based on the
broadest set of genes and supplemented by addition of virus species
from trees based on narrower gene sets, to give finally a 46-species
tree; branching order for three regions within the tree remained
unresolved. Sublineages of the Alpha- and
Betaherpesvirinae showed extensive cospeciation with host
lineages by criteria of congruence in branching patterns and
consistency in extent of divergence. The Gammaherpesvirinae
presented a more complex picture, with both higher and lower
substitution rates in different sublineages. The final tree obtained
represents the most detailed view to date of phylogenetic relationships
in any family of large-genome viruses.
| |
INTRODUCTION |
The Herpesviridae are a
numerous family of large DNA viruses which have as their natural hosts
humans, other mammals and vertebrates, and in one described case, an
invertebrate (11, 16). The genomes of herpesviruses of
mammals and birds clearly evince descent from a common ancestor, but
with a great range of variation in terms of nucleotide substitution,
gene content, and genomic arrangement (15). The
Herpesviridae have been divided into three subfamilies, the
Alpha-, Beta-, and Gammaherpesvirinae,
initially from their distinct biological properties and latterly more
precisely on the basis of their genomic attributes (16).
Over the last two decades an extensive body of herpesvirus DNA sequence
data has been built up, from single-gene analyses to studies of whole
genomes (in the range 120 to 240 kbp). Phylogenetic studies using
herpesvirus sequences have been undertaken, demonstrating clear
division into the three subfamilies and, in some sublineages, patterns
of divergence consistent with cospeciation of virus and host (7,
9, 13, 14). Herpesviruses of fish (2, 3), amphibians
(4), and invertebrates (A. J. Davison, personal
communication) are only remotely related to the mammalian and avian
viruses, while certain turtle viruses (the only reptile herpesviruses
for which some sequence is known) probably group with the mammalian and avian viruses (18).
We describe in this report a major update of herpesvirus phylogenetic
analysis, using the greatly increased number of gene sequences now
available from a wide range of mammalian and avian herpesviruses, and
enabled by advances both in processing power of modern computers and in
methods for analysis of relationships among gene sequences. We aimed to
produce by good current practice a single phylogenetic tree that would
be thoroughly justified, be accurate in terms of branch patterns and
relative branch lengths, and contain as many mammalian and avian
herpesviruses as possible.
| |
MATERIALS AND METHODS |
Amino acid sequences and alignments.
Coding sequences of
herpesvirus genes were provided by colleagues and collected from the
literature and the EMBL data library until December 1999. Table
1 lists abbreviations for viruses and
sources for genes orthologous to HSV1 genes UL2, UL5, UL15, UL19, UL27,
UL28, UL29, and UL30 (the set used in this study). Only complete gene
sequences were used with the exception of the UL15 entry for PRV, for
which only the second exon sequence (of two) was available. Sequence
files were manipulated in Alpha (Open VMS and Unix) systems using
Genetics Computer Group software (version 10). Amino acid sequences
were aligned by each of the programs CLUSTAL W (20),
Dialign2 (17), and PRRP (6), which use distinct
algorithmic approaches and have been evaluated as good performers
(21). Default values of program parameters were used. Combined alignments were produced by reextracting the individual sequences from these three alignment versions, with retention of the
gapping characters introduced by each program, and then making a new
alignment from this whole triple set of sequences using the program
Pileup. All positions in the combined alignment that had a gap in any
sequence were then excised, thus deleting both unanimously placed gaps
and sections where the three primary alignments were in conflict.
Regions regarded as unalignable were also removed (14).
Phylogenetic trees.
Trees were investigated in three stages.
Preliminary examination used the neighbor-joining method with
bootstrapping (programs Seqboot, Protdist, Neighbor, and Consense from
the PHYLIP package, version 3.572 [5]). In the second
stage of analysis, particular parts in the total tree were varied
separately and examined with the maximum-likelihood program Protml from
the MOLPHY package (1), which imposed a single rate of
change on all sites in each sequence. We were able to examine up to
104 tree topologies for each subset of species by this
approach. For each topology, Protml computed a log-likelihood (lnL)
value, a bootstrap value, and a set of branch lengths. Final evaluation of high-scoring topologies and derivation of branch lengths were made
with the maximum-likelihood program Codeml of the PAML package (version
2) (24), which allowed a distribution of rates of change across sites, in up to eight rate classes assigned by the program in a
discrete gamma distribution (23); for each topology, Codeml computed lnL and branch lengths. Up to 20 trees for each data set were
examined by this computer-intensive method. Substitution probabilities
for Protml and Codeml were from reference 8. These
maximum-likelihood trees are presented (see Fig. 2 and 3) in a rooted
format with root locus as the midpoint of the distance from the mean
position of branch tips in the Alphaherpesvirinae subfamily
to the mean position of branch tips in the Beta- plus Gammaherpesvirinae subfamilies (i.e., the root is taken to
lie on the branch from the Alphaherpesvirinae to the other
subfamilies [14]). For purposes of presentation and
for combining data from different trees, top-scoring tree topologies
were input to Codeml to recompute branch lengths with overall rate
constancy maintained among lineages; we refer to such trees as MC
(molecular clock) trees. Minitab was used for analysis of numerical
data. Details of alignments and trees are available by anonymous FTP
from zippy.vir.gla.ac.uk/public/mcgeoch/.
| |
RESULTS AND DISCUSSION |
Aligning amino acid sequences.
The gene complements of
mammalian and avian herpesviruses contain a subset of some 30 genes
that have homologues with clearly conserved encoded amino sequences in
all of the genomes sequenced. In previous work on herpesvirus
phylogeny, we used collections of eight genes from this set to build
phylogenetic trees (14). As a preliminary to the present
analysis, and with the greater number of herpesvirus gene sequences now
available, we examined alignments of additional gene collections whose
amino acid sequences were relatively highly conserved; however, we
concluded that in all of these cases the alignment process introduced
too many gapping characters for them to be useful for tree inference
across the whole herpesvirus family. Table 1 summarizes sequences for
the eight-gene set used for the present study. Forty-eight viruses were
represented with at least one gene sequence, and 19 had data for all
eight genes. HHV6 variants A and B were very close by applicable
criteria, and only variant A was included in the analysis. Our goal was
to infer from these various sequences a single integrated, well-founded
phylogenetic tree.
The wide divergences among herpesvirus gene sequences require that the
appropriate level for examining phylogeny based on
molecular sequence
comparison is that of the amino acid, rather
than nucleotide, sequences
(
13). Alignments for amino acid sequences
from each of the
eight gene sets were constructed with each of
three programs that used
distinct computational approaches. Alignments
from the three programs
were identical in regions that were of
uniform length in all sequences,
but placements of gaps by the
programs in regions that exhibited length
inequalities among sequences
often differed. Inappropriate gap
placement represents a potential
source of noise or bias for subsequent
phylogenetic analysis;
therefore, these contentious regions were
removed via a procedure
involving a further alignment of
alignments.
Inference of phylogenetic trees.
We aimed to carry through the
phylogenetic analysis as thoroughly as practicable with the best
currently available approach, which we judged to comprise
maximum-likelihood evaluation of sets of candidate trees with provision
for different rates of evolutionary change at different sites in the
alignment. Limitations are that this method is relatively
computationally intensive and that the number of possible trees to be
evaluated rapidly becomes gigantic as number of species increases. We
therefore proceeded by establishing a small subset of candidate best
trees using more rapid methods and then subjecting only this subset to
the most time-consuming computation. Preliminary analysis by the
neighbor-joining method with bootstrapping demonstrated that, as
expected, for all sets of sequences individual viruses were
assigned unambiguously to one of the three subfamilies of the
Alpha-, Beta-, and Gammaherpesvirinae; that is, it was reasonable to pursue maximum-likelihood evaluation independently within each subfamily, much reducing the search space.
Tree topologies for each of the eight sets of genes were found to be
closely similar in most respects; a notable exception was the variable
locus for MHV4 within the Gammaherpesvirinae. We next chose
a set of alignments, including concatenated alignments (containing
sequences from all eight genes down to two-gene sets) and UL2, UL27,
and UL30 single-gene alignments, to give the maximum representation for
the greatest number of species (Table 2). For each data set, tree topologies within each subfamily were evaluated
as exhaustively as possible with Protml while holding the pattern in
the two other subfamilies constant (initially in the topology derived
by neighbor joining). We were able to handle up to seven operational
taxonomic units in a subfamily, requiring analysis of 10,395 trees. For
those cases where the subfamily contained more than seven species, we
proceeded either by treating closely related species together in
uncontentious cases (e.g., putting HSV1 and HSV2 into one operational
taxonomic unit) or by analyzing separately parts of the subfamily that
we were confident were distinct. The trees examined by Protml were
ranked by their lnL scores and then evaluated by lnL differences and
the bootstrap value. The top trees (typically 10 to 20) were then taken
for examination by Codeml, with relative rates of change at individual alignment sites assigned to one of eight values by the program. Evidently this procedure relies on Protml and Codeml yielding similar
rankings of trees, and in practice this was observed to be so with no
major discordances. Top topologies derived for subsets of virus species
were then brought together, and branch lengths for the overall best
topology were obtained with Codeml. The final outcome for a given set
of aligned sequences was (i) identification of the top-scoring
topology; (ii) evaluation of the robustness of each branch point
obtained from comparison with scores of runner-up trees; and (iii) a
set of branch lengths for the top-scoring tree.
To combine the various top-scoring trees (which contained distinct
subsets of the 48 virus species) into one composite tree,
we first used
Codeml to compute for each top-scoring topology
a rooted
maximum-likelihood tree with molecular clock imposed.
This gave a tree
with branch tips in register, in contrast to
the unconstrained rate
tree that was the direct output of the
topology evaluation process (see
Fig.
2). These MC trees could
then be used straightforwardly to add
locations for additional
virus species successively to the MC tree
based on the largest
gene set, by interpolation and scaling into the
appropriate locus.
We emphasize that the use of MC trees is primarily a
simplifying
and presentational device, justified pragmatically in the
present
work but readily alterable. Figure
1 presents a flow diagram for
the
composite-tree derivation process. The eight-gene set gave
a 19-species
tree that was unambiguous except for the location
of MHV4 (a single,
robust, equivalent tree was obtained when MHV4
was excluded) (Fig.
1,
top left). With a gene set that omitted
only UL15 exon 1, a 20-species
tree (including PRV) was obtained
that was topologically equivalent and
very close in branch lengths
to the eight-gene trees, and this
20-species tree was therefore
used as the starting point for building
composite trees. Reducing
the number of genes to five (UL2, UL5, UL27,
UL29, and UL30) allowed
addition of ILTV. An alignment containing UL27
plus UL30 sequences
increased the number of species in the MC tree to
28. Four alignments
(UL15 plus UL27, and single-gene alignments for
UL27, UL30, and
UL2) then independently added species to the 28-species
MC tree
to give a 46-species MC tree. These later additions were
facilitated
by the distribution of species in different trees; for
instance,
all but one of the species represented by UL27 alone
were alphaherpesviruses,
while no UL30-only species were from
this subfamily. Finally,
the 46-species MC tree was reduced to a
multifurcated form that
eliminated branching uncertainties at three
loci (Fig.
1, bottom
right).
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FIG. 1.
Flow diagram for creation of composite trees. The box at
top left indicates the starting maximum-likelihood tree based on the
eight-gene alignment; the other boxes represent trees that contributed
to building composite trees. Successive composite MC trees are shown as
circles with numbers of species added from different data sets shown
above arrows; the final 46-species multifurcated tree is shown at
bottom right.
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|
Figures
2 to
4 illustrate selected stages
in the above process. Figure
2A depicts the unconstrained
maximum-likelihood tree
with 20 species. The atypical excess length of
the terminal branch
for MHV4 is striking, while EBV has a short
terminal branch. Figure
2B shows the corresponding maximum-likelihood
MC tree. In view
of the unusual behavior of MHV4, we excluded this
species when
computing MC trees and placed it in the 20-species MC tree
by
interpolation from the unconstrained tree's data. Figure
3 shows
the 28-species tree as obtained
from the analytical process and
used to compute an MC tree to add seven
species to the 21-species
MC tree. We emphasize that in this and the
other trees from narrower
gene sets not illustrated, congruence of
branching pattern for
virus subfamilies that added new species with the
equivalent parts
of the 20-species tree emerged from the analysis as
distinct from
being imposed via the topologies chosen for evaluation.
Figure
4A shows the final 46-species MC
tree constructed, and Fig.
4B
shows the subfamily portions of the same
tree with three regions
of uncertain branching order drawn as
unresolved multifurcations;
major sublineages in each subfamily,
taxonomically equivalent
to genera (
16), are labeled for the
following discussion. Two
of the starting 48 virus species, SCMV and
CRHV, were withheld
from the final tree. SCMV, for which only gene UL29
was available,
locates to a position in the
1 lineage equivalent to
that of
RHCM in Fig.
4 but not resolved from RHCM because that species
was represented by only UL27 and UL30. The only CRHV sequence
was that
for the short UL2 gene. Our analysis placed CRHV near
the clade
occupied by HHV8 through to HVS in the
2 sublineage
(Fig.
4) but
lacked resolution in what is also in other respects
a problematic
locality (see below).
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FIG. 2.
The 20-species phylogenetic trees. (A) Unconstrained
maximum-likelihood tree obtained using Codeml and with alignment sites
in eight rate classes. The tree is shown in a rooted format as
specified in Materials and Methods, and the mean position of branch
tips is indicated by the dashed line. (B) Equivalent rooted MC tree.
Divergence scale (substitutions/site) for both is at the bottom.
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FIG. 3.
The 28-species phylogenetic tree. The unconstrained
maximum-likelihood tree from the UL27-plus-UL30 alignment is shown as
for Fig. 1A, with species contributed to the 28-species composite tree
marked with circles.
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FIG. 4.
The 46-species composite trees. (A) The 46-species
composite MC tree. (B) Subfamily portions of the same tree with regions
of uncertain branching drawn as multifurcations (heavy lines).
Subfamily and sublineage designations are at the right.
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|
Characteristics of the herpesvirus phylogenetic tree.
The
final tree obtained in this work is consistent with less populated
trees derived previously by less rigorous methods (13, 14).
We consider that the present tree is likely to be accurate in almost
all of its topology, while estimates of branch lengths specific to the
many viruses that are represented by one- or two-gene data sets must be
relatively imprecise. We believe that this analysis sets a presently
unequaled standard in phylogenetic analysis of large-genome virus families.
We previously discussed for a smaller data set the high level of
congruence between the herpesvirus phylogenetic tree and
that of the
virus hosts' lineages, indicating that cospeciation
has been a
prominent feature in herpesvirus evolution (
13,
14),
and the
46-species tree now provides fuller evidence of this trend.
The most
cogent examples of congruence are in the
2 sublineage,
involving
primate, perissodactyl, carnivore, and artiodactyl viruses,
and in the
1 sublineage, with primate, rodent, and tree shrew
viruses. The Old
and New World primate viruses in the
1 sublineage
provide another
example. Other features in the
Alphaherpesvirinae,
i.e., the
locations of BHV2, WHV1, and WHV2 and (from consideration
of
branch lengths) the
3 and
4 avian viruses, clearly do not
represent cospeciation. We postpone discussion of the
Gammaherpesvirinae.
For the
2 and
1 examples noted
above, we plotted selected pairs
of divergence values for virus
lineages present in the 20-species
tree (i.e., those with the best
quantitative support) against
host lineage divergence times as shown in
Fig.
5. The host datings
are from a
recent analysis using DNA sequences of vertebrate genes
(
10). The straight line indicates an overall consistency of
divergences with cospeciation and a global substitution rate of
3 × 10
9 substitutions per site per year in each lineage
for the sets
of amino acid sequences used. Further
1,
2, and
1
divergence
values based on shorter alignments are consistent with an
equivalent
overall rate but greater variability.
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FIG. 5.
Comparison between divergences for branch points in the
herpesvirus tree and dates of corresponding events in mammalian
evolution. The graph compares divergence values (substitutions/site in
one lineage) for features in the composite tree (Fig. 4) with dates of
possible equivalents in host evolution (10) in millions of
years before the present (My). Filled symbols, data from 20-species MC
tree; open symbols, data from 46-species tree; squares, 2
sublineage; triangles, 1 sublineage. The line was drawn through the
origin and the four highest-value filled symbols. Divergence events and
times for filled symbols: humans/chimpanzees, 5.5 My; suidae/ruminants,
64.7 My; artiodactyls/perissodactyls, 83.4 My; primates/ungulates, 92.0 My; primates/rodents, (sciurognathi), 112 My. Similarly for open
symbols: human/cercopithecidae, 23.3 My; mice/rats, 40.7 My;
feliformia/caniformia, 46.2 My; carnivores/perissodactyls, 74.0 My.
Dates in reference 10 included error estimates.
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|
The phylogeny of the
Gammaherpesvirinae presents the most
complex and least interpretationally satisfactory region in the
herpesvirus tree and thus is also of particular interest. The
exact
phylogenetic loci for MHV4 and the associated BHV4 remain
unresolved,
but a cospeciational history is not indicated. From
Fig.
2 and
3, the
MHV4 lineage has been evolving at a higher rate
than other species (a
phenomenon not visible with MCMV, the other
rodent virus studied with
the full data set), while the
1 EBV
lineage may have a lower
evolutionary rate. The branching pattern
for separation of Old from New
World primate
2 viruses is consistent
with a cospeciational
process, but the magnitude of divergence
between these groups
would then imply a rate of change about twice
that seen for the
Alpha- and
Betaherpesvirinae in Fig.
5, possibly
another indication of more rapid evolution in the
2 group.
Separately,
the perissodactyl and artiodactyl
2 viruses do not form
a clade
(as seen in the
2 viruses and there taken to indicate a
cospeciational
history); this finding could be genuine or possibly an
artifact
of tree inference associated with aberrant substitution rates.
It may be possible to improve resolution in
-only or
2-only
phylogenetic analyses with an enlarged gene
set.
The final tree gives an integrated view of many features
of herpesvirus phylogeny. It will be of utility for
illuminating
evolutionary and functional relationships among
herpesvirus species
and in developing taxonomy. The procedures we have
described should
represent a route for future analysis of the
Herpesviridae with
additional sequences. There are other
herpesviruses, not included
in this study, for which the only sequences
available are of gene
fragments, often obtained via PCR (
18,
22). We consider that
inferring phylogenetic trees de novo from
such limited data is
an uncertain undertaking, but that the extensive,
high-quality
tree now available should allow an alternative approach,
namely,
varying the locus of the test species on the standard topology
and comparing
likelihoods.
| |
ACKNOWLEDGMENTS |
We thank A. J. Davison for a critical review, and we thank
B. Ehlers, T. M. Rose, and the CCMV Genome Sequence Group for
early sight of data.
This work was supported by the UK Medical Research Council.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: MRC Virology
Unit, Institute of Virology, Church St., Glasgow G11 5JR, United
Kingdom. Phone: (44) 141 330 4645. Fax: (44) 141 337 2236. E-mail:
d.mcgeoch{at}vir.gla.ac.uk.
| |
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Journal of Virology, November 2000, p. 10401-10406, Vol. 74, No. 22
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
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