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1 Department of Biology, Museum of Southwestern Biology (MSB), The University of New Mexico, Albuquerque, NM 87131, USA
2 Department of Biological Sciences, Oswego State University, Oswego, NY 13126, USA
3 School of Medicine, The University of New Mexico, Albuquerque, NM 87131, USA
4 Laboratorio de Evolución, Facultad de Ciencias, Universidad de la República, Iguá 4225, Montevideo 11400, Uruguay
Correspondence
Jerry W. Dragoo
jdragoo{at}unm.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are DQ385624–DQ385827.
A table showing specimens of Peromyscus examined and the Nexus file used to generate Fig. 1
are available as supplementary material in JGV Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). SNV, first discovered in 1993 (Nichol et al., 1993), has been responsible for 416 instances of hantavirus cardiopulmonary syndrome (HCPS) in humans in the USA until January 2006 (CDC, 2005a), of which about 36 % were fatal. The majority of HCPS cases have occurred in western North America, but cases throughout the range of deer mice have been documented.
Hantaviruses (family Bunyaviridae) are RNA viruses that are suspected to have co-evolved with their murid rodent hosts. Pathogens causing persistent infections are more likely to co-evolve with their host through vicariance (co-speciation) than through dispersal (Holmes, 2004). Chronic infection by these viruses may contribute to the observed pattern of tight co-evolution with murid rodents, although further tests are needed to explore temporal and spatial aspects of this phenomenon more rigorously (Holmes, 2004). Analyses of the RNA sequence of SNV indicated that this virus was not introduced from the Old World recently, but instead has a long evolutionary history in North America (Yates et al., 2002).
Several investigators (e.g. Plyusnin & Morzunov, 2001) found substantial concordance between phylogenies of New World hantaviruses and their murid reservoirs, whereas others reported substantial geographical variation within a particular hantavirus that apparently reflects the evolutionary and biogeographical history of the respective host (Asikainen et al., 2000). Instances of host switching, although demonstrated (Morzunov et al., 1998; Vapalahti et al., 1999), are not common. Recognition of this co-evolutionary process stimulated the rapid identification of other suspected hosts of novel hantaviruses. Delineation of viral and rodent phylogenies at the interspecific and intraspecific levels provides a framework for predicting the discovery of novel viruses (Yates et al., 2002) and hosts (Salazar-Bravo et al., 2002). For example, knowledge of the phylogenetic relationships of these rodent hosts focused survey efforts in the Americas subsequent to the 1993 discovery of SNV, and this knowledge, enabled by samples archived in museum collections, led quickly to the discovery of the first hantaviruses known from Central (Hjelle et al., 1995) and South (Hjelle et al., 1996) America. In the past dozen years, 28 new hantaviruses have been described from the western hemisphere; at least 16 are pathogenic to humans (Jentes & Mills, 2003). New hantaviruses continue to be discovered (Rosa et al., 2005) and significant advances in our understanding of viral occurrence, evolution, epidemiology and transmission are on the horizon.
Intraspecific variation of either host or virus, however, has received less attention, but phylogeographical studies could be as informative as phylogenetic studies in understanding viral evolution. P. maniculatus is a widespread species with considerable documented geographical variation (Carleton, 1989). Substantial geographical variation within a viral host is probably reflected in substantial genetic structure within the presumably co-adapting virus, especially given the high rates of molecular evolution characteristic of viruses. P. maniculatus harbours at least two hantaviruses: SNV, primarily in the western United States, and Monongahela virus (MONV) in the eastern United States and Canada, suggesting a phylogeographical split in both host and virus. Herein, we use molecular phylogeography to elucidate population structure among deer mice and to develop a predictive framework for discovering novel SNV variants.
Previous efforts to document geographical variation in deer mice demonstrated marked phylogeographical structure and raised awareness of the possibility that this nominal species may represent a complex of closely related species (Avise et al., 1983; Hogan et al., 1993, 1997; Lansman et al., 1983). We extended earlier studies by sequencing the entire mitochondrial cytochrome b gene across a more extensive geographical sample of deer mice and by including as outgroups closely related species to provide a context for identifying significant geographical variation in P. maniculatus. Additionally, we used more advanced methods for phylogeographical and population analyses than were available in previous studies. Bayesian analyses, for example, suggest significant phylogeographical structure and population expansion among phylogeographical lineages of the host, thereby providing clues to the uneven prevalence and transmissibility of viruses such as SNV. Expanding populations might create identifiable contact zones of interest for discovering novel strains of hantaviruses.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) ranging from Labrador, Canada, to Baja California, Mexico. Within the USA, populations from Washington to Tennessee and from southern California to Maine were sampled (see Supplementary Table S1, available in JGV Online, for specimens examined). Tissue samples were archived at the MSB, University of New Mexico, Albuquerque, USA, the Carnegie Museum of Natural History, Pittsburgh, USA, and Oswego State University, Oswego, New York, USA.
DNA sequences.
Total genomic DNA was extracted from frozen tissues or tissues stored in 70 % ethanol by using a Qiagen DNeasy tissue kit. Double-stranded symmetrical amplification and sequencing of the complete mitochondrial cytochrome b gene were performed via PCR with the primers L14724
[GenBank]
and H15915
[GenBank]
(Irwin et al., 1991). Cleaned PCR products were sequenced by using BigDye Terminator Cycle Sequencing Ready Reaction mix v. 1.1 (Applied Biosystems). PCR products were run on an ABI 3100 automated DNA sequencer in the Molecular Biology Facility, Biology Department, University of New Mexico, Albuquerque, USA.
Analyses.
Sequences were analysed by PAUP* (Swofford, 2002) using the MrModeltest block (24 evolutionary models) and model scores were submitted to MrModeltest v. 2.2 (Nylander, 2004) to determine the best model to use for Bayesian reconstruction. MrBayes (v. 3.1.1; Huelsenbeck & Ronquist, 2001) was used to conduct analyses using a GTR+
+I model determined from MrModeltest to ascertain phylogenetic relationships. Four consecutive Markov chain Monte Carlo Metropolis coupling (MCMCMC) computations were run for 1 million generations, with tree sampling every 100 generations. A burn-in period of 250 000 generations was discarded for each run prior to calculating consensus trees. Trees were rooted by using P. gossypinus, a member of the Peromyscus leucopus species group (Musser & Carleton, 2005), as the outgroup. Only unique cytochrome b sequences within a population were included in phylogenetic analyses, but all samples were used for neutrality and population-expansion analyses.
Possible historical changes in population size or selective regimes were examined in clades with sample sizes >10. The null assumptions of neutrality and constant population size were tested with Tajima's D test of selective neutrality (Tajima, 1989) and Fu's Fs test of neutrality (Fu, 1997). Fs P values for clades were estimated from 1000 replicates with ARLEQUIN (v. 2.000; Schneider et al., 2000) and DnaSP (Rozas et al., 2003).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). These results indicate that the nominal species P. maniculatus, as currently recognized by Musser & Carleton (2005), is paraphyletic with respect to P. keeni and P. melanotis and may represent at least four distinct species. One lineage (clade 1, Fig. 1) includes samples from Rocky Mountain states, including northern and central New Mexico, and closely related forms from Washington, northern California and Michigan (Isle Royale). A second lineage (clade 2, Fig. 1) is represented by individuals from the Plains states. A third (clade 3, Fig. 1) includes populations along the Pacific Coast region from Washington to Baja California; this lineage also consists of mice recognized as P. keeni. A fourth (clade 4, Fig. 1) comprises mice from southern New Mexico and Mexico. A fifth lineage (clade 5, Fig. 1) is represented by mice from north-eastern USA and eastern Canada. The sixth lineage (clade 6, Fig. 1) occurs in north-eastern and north-central USA and south-central Canada (Fig. 2).
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) with larger sample sizes and multiple geographical locations. Three smaller lineages within the Rocky Mountain clade (clades 1b, 1c and 1d), consisting of mice from Washington, Michigan and northern California, were not analysed due to small sample sizes. Two eastern lineages (clade 5 and 6) were analysed separately, as were the lineages found in the Plains states and the Rocky Mountains. Three of the major lineages analysed showed signs of demographic expansion and/or departures from strict neutrality (Table 1). Tajima's D and Fu's Fs test values for the lineages representing the Rocky Mountains (clade 1, Fig. 1), Plains states (clade 2, Fig. 1) and north-eastern USA and Canada (clade 6, Fig. 1) populations are both negative and significant and the mismatch distributions are unimodal (Fig. 3). However, the north-east central lineage (clade 5, Fig. 1) shows a negative and significant Fs value, but D is not significant and the mismatch distribution is bimodal.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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), is a complex of several deeply divergent phylogeographical lineages. Some of these lineages may represent distinct species. Second, the deepest genetic divergence occurs between the eastern clades (5 and 6; Fig. 1) and the western clades (1–4; Fig. 1), corresponding roughly to the geographical ranges of MONV and SNV. Drebot et al. (2001) provided similar results from Canada and suggested that P. maniculatus was separated into two distinct haplotypes corresponding to genetic divergence seen in SN-like viruses. Finally, post-Pleistocene population expansion has created zones of potential contact between members of divergent host clades, potentially stimulating recombination of closely related viruses.
Phylogeographical implications
Data provided here suggest that P. maniculatus is paraphyletic with respect to other recognized species. The type locality for P. maniculatus is the Moravian settlements of Labrador, Canada (Musser & Carleton, 2005); this taxon herein is restricted to mice from the north-eastern and central clades (clades 5 and 6; Fig. 1). This mouse harbours MONV, a virus related closely to the New York virus carried by P. leucopus (Song et al., 1996). MONV has been found in P. maniculatus from Canada and throughout the eastern USA (Monroe et al., 1999). Our data restrict the distribution of P. maniculatus to Canada, east of approximately the Manitoba–Saskatchewan border [but possibly as far west as the coastal region of British Columbia, as mapped by Hall (1981)] and southward through the eastern USA (Fig. 2).
Given the foregoing implications, our data suggest that populations in the western United States and Mexico may represent a previously described taxon, Peromyscus sonoriensis (Le Conte, 1853). The phylogeographical lineage represented by these mice is the host of SNV and would comprise the Rocky Mountain clade (clade 1a, Fig. 1), including north-western New Mexico, where SNV was first discovered. Three of the major lineages of deer mice meet in the south-western USA (clades 1a, 2 and 4, Figs 1 and 2). One lineage occurs in eastern New Mexico, extends into the Plains states (clade 2, Fig. 1) and may be conspecific (as a closely related sister clade) with mice from the Rocky Mountain clade (1a, Fig. 1). Mice from south-western New Mexico (clade 4) at the base of the western radiation may represent a different, formerly recognized species, Peromyscus blandus (Osgood, 1904). This taxon has been reported to occur from the southern to the eastern part of the state and into Mexico and the Trans-Pecos of Texas (Hall, 1981). The extent of sympatry and interbreeding, if any, among these lineages is unknown.
Cryptic species of Peromyscus have been detected in other regions within the range of P. maniculatus. Previous work hypothesized a connection between P. keeni of the Pacific North-West and Peromyscus sejugis (which we have not analysed), an island form from Baja California del Sur (Hogan et al., 1997). Those two species are allied closely with P. maniculatus coolidgei from Baja California (Hogan et al., 1997). Our data also place P. keeni and P. maniculatus coolidgei in the same clade and suggest that our Pacific Coast clade can be linked, along with P. sejugis, as a distinctive coastal form. Lucid & Cook (2004) suggested that P. keeni survived the ice age in coastal refugia in south-east Alaska and thus were in the Pacific North-West prior to the arrival of P. maniculatus. Populations of deer mice along the Pacific coast are more similar to P. keeni/sejugis than to P. maniculatus and may represent a distinct species. Avise et al. (1983) found P. maniculatus to be paraphyletic with respect to Peromyscus polionotus. P. polionotus may be sister species to P. maniculatus gambeli from southern California (Avise et al., 1983). We analysed the 321 bp of cytochrome b sequence available from GenBank for P. polionotus (X89792
[GenBank]
) and the results suggest a close relationship with the Californian samples, represented by P. maniculatus gambeli, P. maniculatus coolidgei and P. keeni, from our study (results not shown). Avise et al. (1983) suggested that P. polionotus is a peripheral population of P. maniculatus that underwent speciation approximately 1.5 million years ago. This is approximately the time period suggested by other authors for P. polionotus, as well as P. melanotis and P. sejugis, based on morphology (Blair, 1950; Hooper, 1968), chromosomes and protein electrophoresis (Bowers et al., 1973; Greenbaum et al., 1978).
Population expansion
The pattern of phylogeographical structure found in P. maniculatus corresponds to hypothesized Pleistocene expansion in other mammalian taxa (Brant & Ortí, 2003; Hayes & Harrison, 1992; Runck & Cook, 2005). Those studies uncovered genetic signals of postglacial colonization among members of distinct clades found in eastern and western regions of the USA and Canada. These studies and others suggest that mammalian populations (and their respective viruses) were isolated in refugia during the Pleistocene glacial periods and later expanded to their current distributions. Three of the four lineages of Peromyscus that we analysed show genetic signatures of geographical expansion similar to that seen in other mammalian taxa (Lessa et al., 2003). The lack of expansion signature in clade 6 (Fig. 1) is intriguing, although not completely surprising. Some clades cover fairly broad areas that include both recolonized and refugial areas. The prominent genetic breaks among lineages, as reported here for deer mice, suggest a history of allopatric divergence (Avise, 2000).
Deer mice from the Rocky Mountain lineage (clade 1a, Fig. 1) probably represent an expanding population (Fig. 3). In general, genetic evidence of expanding populations would persist for about 1.5xNfe generations (Nfe being the female effective population size), although the pattern is also consistent with a departure from strict neutrality. Sample sizes prevented testing for population expansion along the Pacific Coast. The north-east central clade (clade 6, Fig. 1) does not appear to have undergone historical population expansion, which could be a result of the minor phylogeographical break between clades 6a and 6b obscuring the detection of expansion, whereas the Rocky Mountain and Plains states clades do appear to have undergone population expansion (Table 1). Members of these clades intersect in Michigan (Fig. 2).
Potential contact zones
Zones of contact among divergent viral elements may increase the possibility of formation of recombinant variants. For example, Klempa et al. (2003) reported that Dobrava virus, which occurs in two species of Apodemus (Apodemus agrarius and Apodemus flavicollis), is separated into two distinct lineages. There is evidence of reassortment in a small area where the two viral lineages come into contact in Slovakia. Schmaljohn et al. (1995) reported new hantavirus variants from P. maniculatus of northern California in the zone that we identified as potentially being a region of sympatry among distinctive deer-mice lineages (Fig. 2). Genomic reassortment apparently distinguished these variants from SNV. These two lineages may contact in the Pacific North-West (Fig. 2) and additional sampling across Oregon and northern California would help to determine the geographical range of each taxon and reveal the extent of variation in associated hantaviruses.
Within the deer-mouse complex, distinct geographical populations of mice (and their associated viruses) have different evolutionary trajectories. The focus of new hantavirus discovery to date has been at the interspecific level, but new viral strains may emerge within currently recognized species that span broad geographical ranges and cross-ecological boundaries, such as we have identified in the large complex of deer mice. In addition, hantaviruses may undergo recombination when closely related viruses come into contact within the same individual host (Plyusnin, 2002). Thus, zones of sympatry should be productive areas to survey for recombinant viruses.
Our samples from Isle Royale (clade 1d, Fig. 1) clustered with the Rocky Mountain clade, whilst samples from central Michigan clustered in the north-east central clade. Lansman et al. (1983) reported specimens from northern Michigan clustering with mice from eastern states and mice from southern Michigan clustering more with the western mice. Thus, New Mexico, northern California and Michigan are areas where different lineages of deer mice are potentially in sympatry or at least in parapatry.
Many of the cases of HCPS in the eastern states were confirmed serologically, but actual viruses were not genotyped by RNA sequencing (CDC, 2005b). It is possible that these cases may actually represent exposure to MONV rather than SNV. The apparent presence of multiple, closely related species in the P. maniculatus complex merits more rigorous identification of geographical variation in hantaviruses. In addition to highlighting the significance of systematic and phylogeographical work for understanding the co-evolution of viruses and their hosts, this study points to several areas that require attention. For instance, distinctiveness of these phylogroups should be analysed more thoroughly with additional individuals and independent molecular markers (nuclear gene sequences, microsatellites or single-nucleotide polymorphisms) to characterize levels of gene flow among divergent populations of deer mice.
Additionally, co-evolutionary histories of viruses and their hosts should be examined in more detail, especially in areas of potential contact between hosts and associated viral strains. Evidence of population expansion of some of the host units raises the intriguing issue of a corresponding expansion of particular viral strains. Repeated cycles of range expansion and contraction (as during the Pleistocene glacial stages) might have made a substantial contribution to viral diversity. Phylogeographical and population-level analyses may provide key insight into situations that promote the emergence of novel viral elements.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Received 1 October 2005;
accepted 4 March 2006.
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