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Journal of Virology, March 2001, p. 2729-2740, Vol. 75, No. 6
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.6.2729-2740.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Evolutionary Relationships among Parvoviruses: Virus-Host
Coevolution among Autonomous Primate Parvoviruses and Links
between Adeno-Associated and Avian Parvoviruses
Vladimir V.
Lukashov* and
Jaap
Goudsmit
Department of Human Retrovirology, Academic
Medical Center, University of Amsterdam, 1105 AZ Amsterdam, and
Amsterdam Institute of Viral Genomics, 1105 BA Amsterdam, The
Netherlands
Received 25 October 2000/Accepted 4 December 2000
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ABSTRACT |
The current classification of parvoviruses is based on
virus host range and helper virus dependence, while little data on evolutionary relationships among viruses are available. We identified and analyzed 472 sequences of parvoviruses, among which there were
(virtually) full-length genomes of all 41 viruses currently recognized
as individual species within the family Parvoviridae. Our
phylogenetic analysis of full-length genomes as well as open reading
frames distinguished three evolutionary groups of parvoviruses from
vertebrates: (i) the human helper-dependent adeno-associated virus
(AAV) serotypes 1 to 6 and the autonomous avian parvoviruses; (ii) the
bovine, chipmunk, and autonomous primate parvoviruses, including human
viruses B19 and V9; and (iii) the parvoviruses from rodents (except for
chipmunks), carnivores, and pigs. Each of these three evolutionary
groups could be further subdivided, reflecting both virus-host
coevolution and multiple cross-species transmissions in the
evolutionary history of parvoviruses. No parvoviruses from
invertebrates clustered with vertebrate parvoviruses. Our analysis
provided evidence for negative selection among parvoviruses, the
independent evolution of their genes, and recombination among parvoviruses from rodents. The topology of the phylogenetic tree of
autonomous human and simian parvoviruses matched exactly the topology
of the primate family tree, as based on the analysis of primate
mitochondrial DNA. Viruses belonging to the AAV group were not
evolutionarily linked to other primate parvoviruses but were linked to
the parvoviruses of birds. The two lineages of human parvoviruses may
have resulted from independent ancient zoonotic infections. Our results
provide an argument for reclassification of Parvovirinae
based on evolutionary relationships among viruses.
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INTRODUCTION |
The virus family
Parvoviridae comprises small animal viruses with linear
single-stranded DNA genomes. The genomes of parvoviruses are about 5 kb
in length and contain two large open reading frames (ORFs). The first
codes for two nonstructural proteins, NS-1 and NS-2, while the second
encodes coat proteins VP-1 to VP-3 (or two of them), which have
substantial amino acid identity, being derived from overlapping reading
frames (for a review, see reference 12).
As now classified, the family Parvoviridae contains two
subfamilies: the Parvovirinae, or viruses from vertebrates,
and the Densovirinae, or viruses from insects and
(tentatively) other arthropods (62). The subfamily
Parvovirinae contains three genera: Parvovirus,
comprising most parvoviruses from vertebrates; Erythrovirus, comprising B19 and V9 parvoviruses as well as parvoviruses from rhesus and pig-tailed macaques, and Dependovirus,
which comprises adeno-associated viruses (AAV). The last two genera
include human viruses: the B19 and V9 parvoviruses
(Erythrovirus) and AAV serotypes 1 to 6 (Dependovirus). Within Densovirinae, four genera
are recognized. The current classification of parvoviruses is based
primarily on their host range and their dependence on help from other
viruses for replication, according to the traditional separation of
parvoviruses into three types: (i) autonomous viruses of vertebrates,
(ii) helper-dependent viruses of vertebrates, and (iii) autonomous viruses of insects (62).
The relationships among parvoviruses have been extensively studied by
using serological methods as well as DNA hybridization and restriction
mapping analyses. A relatively high sequence homology of goose and
Muscovy duck autonomous parvoviruses (GPV and MDPV, respectively) with
helper-dependent AAV-2, but not with other autonomous parvoviruses, has
been documented (18, 68). Although direct data on sequence
homology of GPV and MDPV to AAV serotypes other than AAV-2 were not
available, DNA cross hybridization data have suggested that GPV is even
more similar to AAV-1 and AAV-3 (18). On the other hand,
little similarity between the two groups of human parvoviruses, B19 and
AAV, has been observed (68). Feline panleukopenia
virus, canine parvovirus, and mink enteritis virus (MEV) are
highly homologous and classified as host range variants of the
feline parvovirus (FelinePV) (reviewed in reference 46),
but another mink parvovirus, the Aleutian mink disease virus (AMDV),
has little homology with MEV (14). These observations prompted the suggestion that the original hypothesis of a
host-dependent evolution of parvoviruses (8) may have
limited value both within and among genera (49, 68).
Furthermore, autonomous parvoviruses are dependent on helper functions
that are transiently expressed in host cells, and helper viruses
can substantially increase their replication, while helper-dependent
viruses can replicate autonomously under certain conditions
(12). These observations together with genetic
homology between some autonomous and helper-dependent viruses
resulted in the validity of the other main criterion for classification of parvoviruses, dependence on helper viruses, also
being questioned (18, 68). The distinction that autonomous parvoviruses encapsidate primarily DNA strands that are complementary to mRNA, whereas AAV encapsidate strands of either polarity with equal
frequency, is also far from absolute. For instance, bovine parvovirus
encapsidates up to 30% of DNA strands with the same polarity as that
of mRNA. In certain hosts, the autonomous parvovirus LuIII encapsidates
strands with either polarity in equal measure (12).
Over the last decade, a massive amount of genetic information has been
obtained for various virus groups. For several groups, including the
human immunodeficiency viruses (HIV) and hepatitis C viruses, genetic
classifications that reflect evolutionary relationships have been
developed (38, 39, 57). However, no systematic and
explicit study on evolutionary relationships among
Parvoviridae has yet been performed, although (virtually)
full-length genomes of several members of each of the recognized genera
are available. Such a study is essential to elucidate the principal
issues of parvovirus biology, including the evolutionary relationships
both among and within subfamilies and genera, the driving forces of parvovirus evolution, and possible cross-species transmissions. In the
present study, we address these basic issues and analyze currently
available sequence information on parvoviruses by using phylogenetic methods.
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MATERIALS AND METHODS |
Sequences.
In the GenBank, we identified 472 sequences of
parvoviruses for use in this study. They were retrieved by using Batch
Entrez software, which allows a search for sequences belonging to a
specified organism (http://www.ncbi.nlm.nih.gov/Entrez/batch.html).
We specified Parvoviridae as the organism name, according to
the taxonomy database at the National Center for Biotechnology
Information, and performed an additional search for
Parvovirus. We used the classification of parvoviruses
accepted by the International Committee on Taxonomy of Viruses
(http://www.ncbi.nlm.nih.gov/htbin-post/Taxonomy/). The viruses we
studied are referred to by their descriptive name (e.g., FelinePV) or
trivial name (e.g., B19), as it is used in the nomenclature of
parvoviruses (62). The sequences are referred to by their
GenBank accession numbers, and the reference information is provided in
Table 1.
Sequence analysis.
The BioEdit, version 4.8.6, software
(28) was used to manipulate the retrieved sequences. The
alignment of sequences was performed by using the ClustalW software
(60). For full-length genomes as well as noncoding
regions, nucleotide sequences were aligned. For coding regions, the
alignment was performed for amino acid sequences.
Phylogenetic analysis was performed by using several methods. For all
methods, positions containing an alignment gap were
excluded from
pairwise sequence comparisons. Bootstrap resampling
was performed for
each analysis (100 replications). Nucleotide
distances were analyzed by
using the neighbor-joining algorithm
as implemented in the PHYLIP
package (NEIGHBOR), based on the
Kimura two-parameter distance
estimation method or the proportion
of differences (p distance). For
coding regions, additional analyses
of nonsynonymous and synonymous
nucleotide substitutions (those
which change or do not change the amino
acid, respectively) was
performed by using the MEGA software
(
37). Estimation of both
synonymous distances (Ds) and
nonsynonymous distances (Da) was
based on the Nei-Gojobori method
(
37). The ratios of synonymous
to nonsynonymous
substitutions (Ds/Da) were calculated (
41).
Recombination analysis was performed by using the bootscanning
method as implemented in the SimPlot software (available at
http://www.med.jhu.edu/deptmed/sray/).
Many viruses are represented in the GenBank by single full-length
genome sequences, but more than one sequence are available
for several
viruses. For B19 virus, we used full-length sequences
but also about
200 shorter sequences, typically a few hundred
nucleotides in length.
These partial genomes were aligned with
all full-length genome
sequences, and the B19 consensus sequence
was calculated as the
arithmetic mean of all nucleotides or amino
acids at a particular
position (
39,
42). This consensus sequence
was used in the
analyses together with the individual full-length
genomes.
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RESULTS |
Identification of phylogenetic groups within
Parvovirinae.
To identify groups of phylogenetically
related viruses within Parvovirinae, we analyzed (virtually)
full-length genomes of all members of the three genera that are
distinguished by the International Committee on Taxonomy of
Viruses as distinct virus species. Parvovirus species
included were bovine, simian (from the cynomolgus [long-tailed]
macaque), Manchurian chipmunk, canine, feline
panleukopenia, Georgian raccoon (only a partial sequence of 2,410 nucleotides in length is available), porcine, mice minute, mouse 1, mouse 1b, mouse 1c, rat 1a, Kilham rat, hamster, LuIII, Barbarie duck, and H1 parvoviruses as well as MEV, AMDV, GPV, and MDPV.
Erythrovirus species included an individual B19 virus and
the consensus of 215 B19 sequences and V9 and rhesus and pig-tailed macaque parvoviruses. Dependovirus species
included AAV serotypes 1 to 6. The list of sequences analyzed is
provided in Table 1.
In total, genomic sequences of 32 virus species were aligned. Based on
phylogenetic analysis, they fell into three groups
(Fig.
1): (i) AAV serotypes 1 to 6 and GPV,
Barbarie duck parvovirus,
and MDPV; (ii) primate (B19, V9, and
three viruses from macaques),
chipmunk, and bovine parvoviruses; (iii)
parvoviruses from all
rodents (except for chipmunks), carnivores,
and pigs.
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FIG. 1.
The three evolutionary groups of
Parvovirinae. The neighbor-joining phylogenetic tree is
based on the analysis of (virtually) full-length genomes of all members
of the Parvovirinae subfamily that are recognized as
individual virus species, one sequence per species (except for the B19
virus, for which a consensus, ConsB19, of 215 available sequences is
also included). For RaccoonPV, only a shorter sequence is available.
Bootstrap values are shown (100 replications). Sequences used in this
analysis are in boldface in Table 1. For virus abbreviations, see Table
1.
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Additionally, we analyzed viruses from the
Densovirinae
subfamily (Table
1). None of viruses from the
Densovirinae
clustered
together with
Parvovirinae (data not
shown).
AAV and avian parvoviruses.
To analyze phylogenetic
relationships among AAV and avian parvoviruses, we aligned sequences of
viruses belonging to this phylogenetic group. The analyses were based
on nucleotide distances as well as, for coding regions, Ds and Da.
Irrespective of the phylogenetic model and genomic region used, the
three avian parvoviruses clustered together and separately
from AAV,
with a bootstrap value of 100 (Fig.
2).
The two viruses
from ducks were virtually identical, with their Ds and
Da being
0.01 for orf1 and 0.00 for orf2. Among AAV, two
pairs of closely
related viruses were found. Besides the two
sequences belonging
to viruses from the same serotype (AAV-3 and
AAV-3B), AAV-1 and
AAV-6 also clustered together. Although these two
viruses are
defined as separate AAV serotypes, the vast majority of
nucleotide
substitutions between AAV-1 and AAV-6 are synonymous, with
Ds
being 0.07 and 0.11 for orf1 and orf2, respectively, and Da being
0.00 for both ORFs. AAV-3 and AAV-3B, AAV-1 and AAV-6, and AAV-2
were
approximately equidistant from each other as well as from
AAV-5, which
appeared to be the most distantly related to other
AAV (Fig.
2). Within
this virus group, branching orders of two
viruses, AAV-2 and AAV-4,
varied with the genetic region analyzed.
The orf1 sequence of AAV-4
clustered together with AAV-3 and AAV-3B,
AAV-1 and AAV-6, and AAV-2
and was most closely related to AAV-3
(Fig.
2B to D), whereas the orf2
sequence of AAV-4 branched out
between AAV-5 and the main cluster of
AAV (Fig.
2E to G). The
position of AAV-2 (within or outside the AAV-3
and AAV-3B and
AAV-1 and AAV-6 clusters) also depended upon the genetic
region
(Fig.
2).
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FIG. 2.
Phylogenetic relationships among the AAV serotypes 1 to
6 and parvoviruses from GPV, Barbarie duck parvovirus (BarbduckPV), and
MDPV (MuscduckPV). Bootstrap values are shown (100 replications). (A)
Relationships based on nucleotide p distances among full-length genome
sequences; (B to D) relationships based on nucleotide Kimura
two-parameter distances, Ds, and Da, respectively, for orf1; (E to G)
nucleotide distances, Ds, and Da, respectively, for orf2. For panels B
and E, positions of AAV-2 and AAV-4 are marked. Virus abbreviations are
listed in Table 1.
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For all pairwise sequence comparisons, the Ds/Da ratios were markedly
higher than 1. The Da between any two sequences did
not exceed 0.39 (AAV-1 and AAV-6 versus avian parvoviruses; orf1),
but the vast
majority of pairwise Ds were higher (Fig.
2D and
G versus C and F).
Remarkable differences between the Ds and Da
were observed for GPV
versus duck parvoviruses, for which the
Ds were 0.58 to 0.59, compared
to Da of 0.06 to 0.07. Among AAV,
the most remarkable differences
between Ds and Da were observed
for the comparisons of AAV-2 and AAV-4
in orf1, 0.44 versus 0.07,
and AAV-1 and AAV-6 and AAV-3 and AAV-3B in
orf 2, 0.52 to 0.57
versus 0.08 to 0.09 (Fig.
2).
Autonomous primate, chipmunk, and bovine parvoviruses.
In
addition to a single B19 individual sequence and the B19 consensus, we
analyzed all 12 individual B19 sequences for which both orf1 and orf2
regions are available.
For this group of viruses, topologies of phylogenetic trees were
virtually identical when based on full-length sequence analysis
or Da
in orf1 and orf2 (Fig.
3). B19 and V9
clustered together,
as did the simian parvoviruses, whereas chipmunk
and bovine parvoviruses
(ChipmunkPV and BovinePV) were outliers.
Among B19 viruses, high
genetic homogeneity was observed. Within the
two ORFs, the mean
Ds among B19 viruses were 0.022 (range, 0.007 to 0.034) and 0.035
(range, 0.007 to 0.054) and the mean Da were 0.003 (range, 0.001
to 0.005) and 0.002 (range, 0.001 to 0.005), resulting in
the
mean Ds/Da ratios of 7.3 and 17.5 for orf1 and orf2, respectively.
Negative selection was even more evident in our comparison of
the two
human parvoviruses: while the Ds between the V9 sequence
and the
B19 consensus were 0.40 and 0.45, the Da were 0.03 and
0.02 (Fig.
3B to
E), resulting in mean Ds/Da ratios of 13.3 and
22.5 for orf1 and orf2,
respectively. Pairwise Ds between human
and simian parvoviruses were
also markedly higher than Da (Fig.
3). Moreover, phylogenetic
analysis of orf2 based on Ds resulted
in virtually complete loss of
tree structure as B19 and V9, the
three macaque viruses, ChipmunkPV,
and BovinePV were equidistant
from each other (Fig.
3D).
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FIG. 3.
Phylogenetic relationships among the autonomous primate,
chipmunk, and bovine parvoviruses. In addition to sequences used in
Fig. 1, 11 more sequences of B19 are included (labeled by their GenBank
accession numbers). Bootstrap values above 70 are shown (100 replications). (A) Relationships based on nucleotide p distances among
full-length genome sequences; (B and C) relationships based on Ds and
Da, respectively, for orf1; (D and E) relationships based on Ds and Da,
respectively, for orf2. Branches between the B19 cluster and V9 are in
boldface (B to E). Virus abbreviations are in Table 1.
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Parvoviruses from rodents, carnivores, and pigs.
For several
viruses within this evolutionary group, more than one
full-length sequence were available, permitting study of genetic heterogeneity within virus species. We included five
strains of minute virus of mice (MVM), two Kilham rat parvoviruses
(KilhamRatPV), three FelinePV, three canine parvoviruses
(CaninePV), five porcine parvoviruses (PorcinePV), and three AMDV
sequences in the analysis.
Our analysis distinguished four major subgroups of evolutionarily
related viruses: (i) viruses from rodents and unknown natural
hosts,
(ii) viruses from carnivores, except for AMDV, (iii) PorcinePV,
and
(iv) AMDV, which was the most distantly related to all other
viruses in
this group (Fig.
4A). The
four subgroups were observed
in all phylogenetic trees (Fig.
4), but their branching order
varied. Based on Da, viruses of rodents,
carnivores, and pigs
clustered together and were approximately
equidistant from each
other (Fig.
4D and G), while AMDV
appeared to be an outlier. Based
on synonymous distances, all
four subgroups were equidistant from
each other (Fig.
4C and F).
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FIG. 4.
Phylogenetic relationships among parvoviruses from
rodents, carnivores, and pigs. The four phylogenetic subgroups are
shown. (A) All full-length sequences available for each virus species
are included (labeled by their virus names and the GenBank accession
numbers). Bootstrap values above 70 are shown (100 replications). (A)
relationships based on nucleotide p distances among full-length genome
sequences; (B to D) relationships based on the nucleotide Kimura
two-parameter distances, Ds, and Da, respectively, for orf1; (E to G)
relationships based on nucleotide Kimura two-parameter distances, Ds,
and Da, respectively, for orf2. In orf1 (B to D), MousePV,
HamsterPV, and MVM form a homogeneous cluster (B, grey box), to
which LuIII (arrow) is an outlier. In contrast, in orf2 (E to G),
MousePV and HamsterPV (E, open box) cluster with LuIII (arrow)
and not with MVM (grey box). Virus abbreviations are in Table 1.
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Similar to what was observed for AAV, avian parvoviruses, and primate
parvoviruses, the mean Ds/Da ratios for pairwise
comparisons
within groups were above 1 (range: 1.3 to 10.3),
except for PorcinePV
in orf2, a reflection of its extreme genetic
homogeneity (Ds =
0.002, Da = 0.003). The largest Ds/Da ratio
was observed for the
comparisons of mouse and hamster viruses with
LuIII in orf1: 0.30/0.04
(Fig.
4C and
D).
Among the rodent viruses, we identified three subclusters, which
comprised (i) LuIII and viruses from mice and hamsters, (ii)
KilhamRatPV and H1, and (iii) the most distantly related rat parvovirus
(RatPV) (Fig.
4). The second subgroup of viruses from various
natural
hosts, viruses from carnivores, and the two subgroups
of viruses from
single hosts, PorcinePV and AMDV, were much more
homogeneous. Among
viruses from carnivores, the FelinePV, raccoon
parvovirus (RaccoonPV),
and MEV clustered together and separately
from CaninePV when Da were
analyzed (Fig.
4D and G). This trend
was less pronounced for Ds (Fig.
4C and F). Genetic heterogeneity
in FelinePV was higher than that in
CaninePV. The mean Ds/Da ratios
among FelinePV and CaninePV and between
these two viruses were
0.016/0.004, 0.008/0.001, and 0.023/0.004,
respectively, for orf1
and 0.016/0.004, 0.004/0.002, and
0.023/0.007, respectively, for
orf2. Within these three
subgroups, both the mean Ds and Da were
generally below 0.02.
For the three subclusters of rodent parvoviruses, RatPV was an outlier
in all phylogenetic trees. For the other two subclusters,
remarkable
patterns were identified. For the H1-KilhamRatPV subcluster,
we
observed a great difference in the evolutionary distances between
the
two viruses for the two ORFs. Within orf1, the mean Da and
Ds between
H1 and the two KilhamRatPV were 0.004 and 0.044, respectively,
while
the Da and Ds within orf2 were 34 and 9 times greater and
equal to
0.135 and 0.388, respectively (Fig.
4).
For the mouse-hamster-LuIII subcluster, even more complex
relations among viruses were found. In orf1, MVM, mouse
parvovirus
(MousePV), and hamster parvovirus (HamsterPV)
represented an extremely
homogeneous (mean Da = 0.01, Ds = 0.11) monophyletic group, to
which LuIII was an outlier (Fig.
4B to D;
bootstrap value of 100).
Within this cluster, sequences belonging
to distinct virus species
were intermixed (Fig.
4B). In contrast, our
analysis of orf2 revealed
that MousePV and HamsterPV
cluster together with LuIII and are
distant (mean Da = 0.18, Ds = 0.56) from MVM (Fig.
4E to G; bootstrap
value of 100). In
orf2, sequences belonging to all recognized
virus species
represented monophyletic groups (Fig.
4E to G).
Yet no host-related
clustering was observed, as sequences of MousePV
clustered together
with HamsterPV and LuIII and not with sequences
of another mouse
virus, MVM. The mosaicism of virus genomes within
this subcluster was
further supported by our analysis of full-length
sequences with the
bootscanning method (Fig.
5). In this
analysis,
MousePV-1, -1B, -1C, and HamsterPV (query group) were
compared
to five full-length sequences of MVM (comparison group 1) and
LuIII (comparison group 2), whereas the sequence of H1 was used
as
an outgroup. While the left part (positions 1 to 2600) of the
MousePV and HamsterPV genomes clustered together with MVM, the
right part of the genomes clustered together with LuIII and not
with
MVM (Fig.
5).
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FIG. 5.
Bootscan analysis of the phylogenetic relationships
among LuIII and parvoviruses from mice and hamsters. The three
MousePV and HamsterPV were used as a query sequence group in
comparison to the five MVM (comparison group 1), LuIII (comparison
group 2), and H1 (outgroup). Analysis settings were as follows: window
size, 400 nucleotides; step 100 nucleotides; bootstrap resampling, 100;
distance, Kimura two-parameter distance; transitions/transversions
ratio, 2. Arrow, recombination site.
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DISCUSSION |
Currently, the GenBank database contains sequences of about 500 viruses from the Parvoviridae family. The vast majority of them are vertebrate viruses, while for viruses of invertebrates only a
dozen sequences are available.
So far, no systematic evolutionary study has been performed on
parvoviruses. Typically, earlier studies focused on describing the
amino acid identities of a new virus with a few of the most closely
related sequences (5, 6, 9, 27, 53, 67, 68). To the best
of our knowledge, the only parvoviruses for which evolutionary issues
have been specifically addressed by analyzing full-length genomes are
FelinePV and CaninePV (35). Due to the lack of
systematically analyzed data, genetic information was not used as the
basis for parvovirus classification.
In the present study, we used all available sequence information and
powerful phylogenetic methods to learn whether the
Parvoviridae are evolutionarily related viruses and whether
their current classification into subfamilies and genera truly reflects
the evolutionary relationships among viruses. Moreover, we attempted to
study how and to what degree various evolutionary factors, such as
positive or negative selection, recombinations, host-dependent
evolution, cross-species transmissions, and the independent evolution
of genomic regions, were operational during the evolution of parvoviruses.
Toward the evolutionary classification of
Parvovirinae.
Our analysis of the genomes of 32 parvoviruses, all recognized virus species for which (virtually)
full-length genome sequences are available, revealed the existence of
three groups of evolutionarily related viruses (Fig. 1 to 4): (i) AAV
and all three known avian parvoviruses; (ii) all five known autonomous
primate parvoviruses, ChipmunkPV, and the outlier BovinePV; (iii)
parvoviruses from rodents (except for chipmunks), carnivores, and pigs,
with AMDV being an outlier.
These findings indicate that the current classification of viruses
within
Parvovirinae (
62) does not always
reflect their
evolutionary relationships. The first discrepancy was
found for
avian parvoviruses, now classified as members of the
Parvovirus genus but revealed by our analysis to be linked
evolutionarily
to AAV rather than to any autonomous parvoviruses (Fig.
1 and
2). Our results concur with an observation on the relatively high
homology between GPV, MDPV, and AAV-2 (18, 68) but do not show
that GPV
is even closer to AAV-1 and AAV-3, an earlier notion
based on DNA
cross-hybridization data (
18). We found that all
serotypes
of AAV are equidistant from each of the three avian
parvoviruses (Fig.
2).
Other discrepancies were found for the simian parvovirus from the
long-tailed macaque, ChipmunkPV, and BovinePV. While these
three
viruses are classified as members of the
Parvovirus genus,
their evolutionary linkage to all known autonomous primate
parvoviruses,
and not to any known nonprimate parvoviruses, was
revealed in
our study (Fig.
1 and
3). Our observations concur
with recent
data on the genetic homology of primate
(
27) and chipmunk (
67)
parvoviruses to
B19.
A reliable analysis of phylogenetic relationships among the three
identified groups of
Parvovirinae (Fig.
1) was obstructed
by
the high evolutionary distances. The topology of the phylogenetic
tree,
in which all three groups of
Parvovirinae branch out from
basically a single phylogenetic node, is likely to reflect the
saturation of nucleotide substitutions among the groups. In contrast
to
intergroup relationships, intragroup relationships could be
analyzed in
detail.
Another important issue of parvovirus classification is related to the
recognition of individual virus species. For several
other viruses,
such as HIV type 1 (HIV-1), genetic distances among
isolates can be
higher than 0.3 (
38,
39,
41) and biological
and
immunological characteristics of virus isolates are highly
variable
(for review, see reference
40). Nevertheless, all HIV-1
strains are considered to belong to the same virus species based
on
their common evolutionary origin. This principle is used for
some
parvoviruses but not for others. For example, all five available
full-length genome sequences of MVM are considered to be derived
from a
single species, while the three available genome sequences
of
MousePV are classified as belonging to three different species,
MousePV-1, -1b, and -1c, even though genetic heterogeneity in
MVM
is actually much higher than in MousePV (Fig.
4). Similarly,
the
genetic distances among AMDV isolates, which are considered
to belong
to a single species, are not different from or even
higher than those
between the two duck parvoviruses or between
AAV-3 and -3B or
among parvoviruses from carnivores: FelinePV,
CaninePV,
RaccoonPV, and MEV. The parvoviruses of carnivores have
been considered
as (host range) variants of a single virus species
(
46),
and our data suggest similar consideration for MousePV-1,
-1b, and
-1c, the two duck parvoviruses, AAV-3 and -3b, and possibly
AAV-1 and
-6.
Driving forces of parvovirus evolution.
To study evolutionary
forces that are operational among parvoviruses, we analyzed synonymous
versus nonsynonymous nucleotide substitutions in the two ORFs.
Nonsynonymous substitutions, as they change the amino acids, are
generally subjected to strong positive or negative selection pressure.
In contrast, synonymous substitutions, which preserve amino acids, are
supposed to be subjected to a weaker selection pressure or to none.
Since the mutation rates at synonymous and nonsynonymous sites should
be the same, Ds and Da, as well as their ratios, indicate the direction and intensity of selection in the evolutionary history of a group of
species. For instance, the Ds/Da ratios among HIV-1 polymerase sequences are well above 1, since most nonsynonymous substitutions within this gene are deleterious (23). In contrast,
short-term intrahost evolution of the HIV-1 envelope gene is
characterized by mean Ds/Da ratios of 0.4, reflecting the advantageous
character of amino acid changes in this immunogenic region
(41). For long-term evolution, as the separation among
HIV-1 subtypes, the Ds/Da ratios within the env gene are
generally above 1 (39), reflecting accumulation of
synonymous substitutions with time (26).
For all pairwise sequence comparisons, except for the extremely
homogeneous PorcinePV, we found Ds/Da ratios above 1. The
most
extreme case of negative selection was observed for the separation
between the B19 and V9 lineages, apparently an ancient event.
While
these two viruses were extremely homologous at the amino
acid level,
with the mean Da between them not exceeding 0.03,
the mean Ds were 0.40 to 0.45 resulting in Ds/Da ratios of up
to 22.5 (Fig.
3). The Ds/Da
ratios were above 1 even for recent
evolutionary events, such as the
cross-species transmission of
FelinePV to dogs (
35,
46,
49), when an increase of nonsynonymous
substitutions during
virus adaptation to a new host could be expected.
We did observe a
two- to four-times-lower genetic heterogeneity
among
CaninePV than among FelinePV, a likely indication of a recent
transmission bottleneck. At the same time, the mean Ds/Da ratios
were
5.8 for orf1 and 3.3 for orf2 for the comparisons of CaninePV
to
FelinePV. Among CaninePV, the mean Ds/Da ratios were 8.0 for
orf1
and 2.0 for orf2, compared to a mean ratio of 4.0 for both
ORFs
among FelinePV. While these data do not exclude the possibility
that
certain nonsynonymous substitutions were selected for during
the
adaptation of FelinePV to dogs (
35), they indicate that
the influence of positive selection during this recent cross-species
transmission was extremely
limited.
In contrast to that for the cross-species transmissions of FelinePV to
dogs (
46), the time scales for separation between
and
diversification within other virus species are not known.
Since little
is known about the evolution rate of parvoviruses,
precise dating
of those events is currently not possible. CaninePV
has been
shown to evolve in a linear fashion over time with the
mean evolution
rate of 10
4 nucleotides per year (
35), which
would require 100 years of
independent evolution for the evolutionary
distance of 0.01 between
two lineages. Apparently, this evolution rate
has to be considered
maximal, since it is measured during a short
period of virus adaptation
to a new host. Moreover, we demonstrated
that the evolution rate
of parvoviruses is far from being uniform for
synonymous and nonsynonymous
positions.
Our analysis provided evidence for both host-dependent and independent
evolution in the history of parvoviruses. Within two
phylogenetic
groups, the autonomous primate parvoviruses and AAV
and avian
parvoviruses, the phylogenetic relationships were host
dependent. For
instance, the relationships among B19, V9, and
parvoviruses from three
macaque species matched exactly the relationships
among their hosts,
according to an earlier analysis of primate
mitochondrial DNA
(
30). On the other hand, human B19 and V9
viruses and AAV
were evolutionarily related to simian and avian
parvoviruses,
respectively, rather than to each other. For the
third phylogenetic
group, in the homogeneous subgroup of viruses
from carnivores and, most
remarkably, the heterogeneous subgroup
of rodent viruses, no
host-specific clusters were observed (Fig.
4). While, unlike what was
found for viruses from carnivores (
46),
there is no
epidemiological evidence for cross-species transmissions
of rodent
parvoviruses, many of them are able to experimentally
infect different
hosts. For instance, LuIII can establish infection
in hamsters
(
59). The absence of host-specific clusters and
genetic mosaicism of rodent parvoviruses suggest that cross-species
transmissions may have occurred among
rodents.
For most virus comparisons, the topologies of phylogenetic trees were
similar in both ORFs, with two exceptions. First, the
positions of
AAV-2 and AAV-4 in the phylogenetic trees varied
in relation to the
genomic region analyzed (Fig.
2B to D versus
E to G). Taken with our
observations of pairwise Da among various
viruses being drastically
higher or lower within orf1 than within
orf2, this finding suggests
that the selection pressure on the
two genomic regions differs among
distinct lineages, which could
be related to functional difference
between the two
ORFs.
The second case of tree incongruity was observed among
parvoviruses from mice and hamsters. MousePV and
HamsterPV were evolutionary
related to MVM within orf1 and to
LuIII within orf2 (Fig.
4).
Since this incongruity was observed for
both nonsynonymous and
synonymous substitutions, it is unlikely to be
the result of convergent
evolution. We demonstrated that this genomic
mosaicism is likely
to be the result of a recombination that
occurred among lineages
within this group (Fig.
5).
Traditionally, MousePV and HamsterPV
should be considered the
recombinants between MVM and LuIII-related
viruses. However, one cannot
exclude the possibility that the
recombination event involved a
yet-undiscovered
parvovirus.
| |
ACKNOWLEDGMENT |
We thank Lucy Phillips for editorial review.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Human Retrovirology, Academic Medical Center, University of Amsterdam, Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands. Phone: (31-20) 566 5861. Fax: (31-20) 691 6531. E-mail:
v.lukashov{at}amc.uva.nl.
| |
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Zadori, Z.,
R. Stefancsik,
T. Rauch, and J. Kisary.
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Analysis of the complete nucleotide sequences of goose and muscovy duck parvoviruses indicates common ancestral origin with adeno-associated virus 2.
Virology
212:562-573[CrossRef][Medline].
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Journal of Virology, March 2001, p. 2729-2740, Vol. 75, No. 6
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.6.2729-2740.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
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