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Previous Article | Next Article 
Journal of Virology, March 2001, p. 2729-2740, Vol. 75, No. 6
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
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.
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.
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.
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
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Virus sequences used in this
studya
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.| |
RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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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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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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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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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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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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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.
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ACKNOWLEDGMENT |
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We thank Lucy Phillips for editorial review.
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FOOTNOTES |
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* 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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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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