scholarly journals Microevolution of bank voles (Myodes glareolus) at neutral and immune-related genes during multiannual dynamic cycles: Consequences for Puumala hantavirus epidemiology

2016 ◽  
Author(s):  
Dubois Adelaïde ◽  
Maxime Galan ◽  
Jean-François Cosson ◽  
Bertrand Gauffre ◽  
Heikki Henttonen ◽  
...  

ABSTRACTUnderstanding how host dynamics, including variations of population size and dispersal, may affect the epidemiology of infectious diseases through ecological and evolutionary processes is an active research area. Here we focus on a bank vole (Myodes glareolus) metapopulation surveyed in Finland between 2005 and 2009. Bank vole is the reservoir of Puumala hantavirus (PUUV), the agent of nephropathia epidemica (NE, a mild form of hemorrhagic fever with renal symptom) in humans.M glareoluspopulations experience multiannual density fluctuations that may influence the level of genetic diversity maintained in bank voles, PUUV prevalence and NE occurrence. We examine bank vole metapopulation genetics at presumably neutral markers and immune-related genes involved in susceptibility to PUUV (Tnf-promoter,Mhc-Drb, Tlr4,Tlr7andMx2gene) to investigate the links between population dynamics, microevolutionary processes and PUUV epidemiology. We show that genetic drift slightly and transiently affects neutral and adaptive genetic variability within the metapopulation. Gene flow seems to counterbalance its effects during the multiannual density fluctuations. The low abundance phase may therefore be too short to impact genetic variation in the host, and consequently viral genetic diversity. Environmental heterogeneity does not seem to affect vole gene flow, which might explain the absence of spatial structure previously detected in PUUV in this area. Besides, our results suggest the role of vole dispersal on PUUV circulation through sex-specific and density-dependent movements. We find little evidence of selection acting on immune-related genes within this metapopulation. Footprint of positive selection is detected atTlr-4gene in 2008 only. We observe marginally significant associations betweenMhc-Drbhaplotypes and PUUV serology, and betweenMx2genotype and PUUV genogroups. These results show that microevolutionary changes and PUUV epidemiology in this metapopulation are mainly driven by neutral processes, although the relative effects of neutral and adaptive forces could vary temporally with density fluctuations.

2008 ◽  
Vol 89 (7) ◽  
pp. 1649-1660 ◽  
Author(s):  
Maria Razzauti ◽  
Angelina Plyusnina ◽  
Heikki Henttonen ◽  
Alexander Plyusnin

The genetic diversity of Puumala hantavirus (PUUV) was studied in a local population of its natural host, the bank vole (Myodes glareolus). The trapping area (2.5×2.5 km) at Konnevesi, Central Finland, included 14 trapping sites, at least 500 m apart; altogether, 147 voles were captured during May and October 2005. Partial sequences of the S, M and L viral genome segments were recovered from 40 animals. Seven, 12 and 17 variants were detected for the S, M and L sequences, respectively; these represent new wild-type PUUV strains that belong to the Finnish genetic lineage. The genetic diversity of PUUV strains from Konnevesi was 0.2–4.9 % for the S segment, 0.2–4.8 % for the M segment and 0.2–9.7 % for the L segment. Most nucleotide substitutions were synonymous and most deduced amino acid substitutions were conservative, probably due to strong stabilizing selection operating at the protein level. Based on both sequence markers and phylogenetic clustering, the S, M and L sequences could be assigned to two groups, ‘A’ and ‘B’. Notably, not all bank voles carried S, M and L sequences belonging to the same group, i.e. SAMALA or SBMBLB. A substantial proportion (8/40, 20 %) of the newly characterized PUUV strains possessed reassortant genomes such as SBMALA, SAMBLB or SBMALB. These results suggest that at least some of the PUUV reassortants are viable and can survive in the presence of their parental strains.


Author(s):  
Johann Vulin ◽  
Séverine Murri ◽  
Sarah Madrières ◽  
Maxime Galan ◽  
Caroline Tatard ◽  
...  

AbstractPuumala orthohantavirus (PUUV) causes a mild form of hemorrhagic fever with renal syndrome (HFRS) named nephropathia epidemica (NE), regularly diagnosed in Europe. France represents the Western frontier of NE expansion in Europe with two distinct areas: the endemic area (Northeast) where PUUV circulates in rodent populations and where many cases of NE are detected in humans and non-endemic area (Southwest) where the virus is not detected and only a few human cases have been reported. The country is a pertinent target to study factors that influence the evolution of PUUV distribution. In this study, we describe for the first time the isolation of two PUUV strains from two distinct French geographical areas: Ardennes (endemic area) and Loiret (non-endemic area). To isolate PUUV efficiently, we selected wild rodents (Myodes glareolus, the specific reservoir of PUUV) from these areas that were seronegative for anti-PUUV IgG (ELISA) but associated with viral RNA load in lung (qRT-PCR). With this design, we are able to cultivate and maintain these two strains in VeroE6 cells but also to propagate efficiently and rapidly both strains in a bank vole colony. Complete coding sequences of S and M segments were determined by Sanger sequencing of RNA extracted from positive bank voles (naturally and experimentally infected) and from supernatant of Vero E6. For the M segment, nucleotidic sequences were 100% identical for both strains. For the S segment, the amino acid sequences from each strain revealed one mismatch between sequences obtained from tissue and from supernatant, revealing a “bank vole” and a “cell” signature. High throughput sequencing confirmed Sanger results, and provided a better assessment of the impact of isolation methods on intra-host viral diversity.


Viruses ◽  
2021 ◽  
Vol 13 (7) ◽  
pp. 1258
Author(s):  
Julia Schneider ◽  
Bernd Hoffmann ◽  
Cristina Fevola ◽  
Marie Luisa Schmidt ◽  
Christian Imholt ◽  
...  

The development of new diagnostic methods resulted in the discovery of novel hepaciviruses in wild populations of the bank vole (Myodes glareolus, syn. Clethrionomys glareolus). The naturally infected voles demonstrate signs of hepatitis similar to those induced by hepatitis C virus (HCV) in humans. The aim of the present research was to investigate the geographical distribution of bank vole-associated hepaciviruses (BvHVs) and their genetic diversity in Europe. Real-time reverse transcription polymerase chain reaction (RT-qPCR) screening revealed BvHV RNA in 442 out of 1838 (24.0%) bank voles from nine European countries and in one of seven northern red-backed voles (Myodes rutilus, syn. Clethrionomys rutilus). BvHV RNA was not found in any other small mammal species (n = 23) tested here. Phylogenetic and isolation-by-distance analyses confirmed the occurrence of both BvHV species (Hepacivirus F and Hepacivirus J) and their sympatric occurrence at several trapping sites in two countries. The broad geographical distribution of BvHVs across Europe was associated with their presence in bank voles of different evolutionary lineages. The extensive geographical distribution and high levels of genetic diversity of BvHVs, as well as the high population fluctuations of bank voles and occasional commensalism in some parts of Europe warrant future studies on the zoonotic potential of BvHVs.


2009 ◽  
Vol 59 (2) ◽  
pp. 169-187 ◽  
Author(s):  
Michal Kozakiewicz ◽  
Alicja Gryczyńska–Siemiątkowska ◽  
Hanna Panagiotopoulou ◽  
Anna Kozakiewicz ◽  
Robert Rutkowski ◽  
...  

AbstractHabitat barriers are considered to be an important factor causing the local reduction of genetic diversity by dividing a population into smaller sections and preventing gene flow between them. However, the “barrier effect” might be different in the case of different species. The effect of geographic distance and water barriers on the genetic structure of populations of two common rodent species – the yellow-necked mouse (Apodemus flavicollis) and the bank vole (Myodes glareolus) living in the area of a lake (on its islands and on two opposite shores) was investigated with the use of microsatellite fragment analysis. The two studied species are characterised by similar habitat requirements, but differ with regard to the socio-spatial structure of the population, individual mobility, capability to cross environmental barriers, and other factors. Trapping was performed for two years in spring and autumn in north-eastern Poland (21°E, 53°N). A total of 160 yellow-necked mouse individuals (7 microsatellite loci) and 346 bank vole individuals (9 microsatellite loci) were analysed. The results of the differentiation analyses (FST and RST) have shown that both the barrier which is formed by a ca. 300 m wide belt of water (between the island and the mainland) and the actual distance of approximately 10 km in continuous populations are sufficient to create genetic differentiation within both species. The differences between local populations living on opposite lake shores are the smallest; differences between any one of them and the island populations are more distinct. All of the genetic diversity indices (the mean number of alleles, mean allelic richness, as well as the observed and expected heterozygosity) of the local populations from the lakeshores were significantly higher than of the small island populations of these two species separated by the water barrier. The more profound “isolation effect” in the case of the island populations of the bank vole, in comparison to the yellow-necked mouse populations, seems to result not only from the lower mobility of the bank vole species, but may also be attributed to other differences in the animals' behaviour.


Pathogens ◽  
2021 ◽  
Vol 10 (9) ◽  
pp. 1169
Author(s):  
Yuriy N. Davidyuk ◽  
Emmanuel Kabwe ◽  
Anton F. Shamsutdinov ◽  
Anna V. Knyazeva ◽  
Ekaterina V. Martynova ◽  
...  

In the European part of Russia, the highest number of hemorrhagic fever with renal syndrome (HFRS) cases are registered in the Volga Federal District (VFD), which includes the Republic of Tatarstan (RT). Puumala orthohantavirus (PUUV) is the main causative agent of HFRS identified in the RT. The goal of the current study is to analyze the genetic variations of the PUUV strains and possible presence of chimeric and reassortant variants among the PUUV strains circulating in bank vole populations in the Trans-Kama area of the RT. Complete S segment CDS as well as partial M and L segment coding nucleotide sequences were obtained from 40 PUUV-positive bank voles and used for the analysis. We found that all PUUV strains belonged to RUS genetic lineage and clustered in two subclades corresponding to the Western and Eastern Trans-Kama geographic areas. PUUV strains from Western Trans-Kama were related to the previously identified strain from Teteevo in the Pre-Kama area. It can be suggested that the PUUV strains were introduced to the Teteevo area as a result of the bank voles’ migration from Western Trans-Kama. It also appears that physical obstacles, including rivers, could be overcome by migrating rodents under favorable circumstances. Based on results of the comparative and phylogenetic analyses, we propose that bank vole distribution in the Trans-Kama area occurred upstream along the river valleys, and that watersheds could act as barriers for migrations. As a result, the diverged PUUV strains could be formed in closely located populations. In times of extensive bank vole population growth, happening every 3–4 years, some regions of watersheds may become open for contact between individual rodents from neighboring populations, leading to an exchange of the genetic material between divergent PUUV strains.


Parasitology ◽  
2017 ◽  
Vol 145 (3) ◽  
pp. 393-407 ◽  
Author(s):  
A. DUBOIS ◽  
G. CASTEL ◽  
S. MURRI ◽  
C. PULIDO ◽  
J.-B. PONS ◽  
...  

SUMMARYEcoevolutionary processes affecting hosts, vectors and pathogens are important drivers of zoonotic disease emergence. In this study, we focused on nephropathia epidemica (NE), which is caused by Puumala hantavirus (PUUV) whose natural reservoir is the bank vole,Myodes glareolus. We questioned the possibility of NE emergence in a French region that is considered to be NE-free but that is adjacent to a NE-endemic region. We first confirmed the epidemiology of these two regions and we demonstrated the absence of spatial barriers that could have limited dispersal, and consequently, the spread of PUUV into the NE-free region. We next tested whether regional immunoheterogeneity could impact PUUV chances to circulate and persist in the NE-free region. We showed that bank voles from the NE-free region were sensitive to experimental PUUV infection. We observed high levels of immunoheterogeneity between individuals and also between regions. Antiviral gene expression (TnfandMx2) reached higher levels in bank voles from the NE-free region. During experimental infections, anti-PUUV antibody production was higher in bank voles from the NE-endemic region. These results indicated a lower susceptibility to PUUV for bank voles from this NE-free region, which might limit PUUV persistence and therefore, the risk of NE.


Viruses ◽  
2019 ◽  
Vol 12 (1) ◽  
pp. 44 ◽  
Author(s):  
Jenni Kesäniemi ◽  
Anton Lavrinienko ◽  
Eugene Tukalenko ◽  
Tapio Mappes ◽  
Phillip C. Watts ◽  
...  

Bank voles (Myodes glareolus) are host to many zoonotic viruses. As bank voles inhabiting areas contaminated by radionuclides show signs of immunosuppression, resistance to apoptosis, and elevated DNA repair activity, we predicted an association between virome composition and exposure to radionuclides. To test this hypothesis, we studied the bank vole virome in samples of plasma derived from animals inhabiting areas of Ukraine (contaminated areas surrounding the former nuclear power plant at Chernobyl, and uncontaminated areas close to Kyiv) that differed in level of environmental radiation contamination. We discovered four strains of hepacivirus and four new virus sequences: two adeno-associated viruses, an arterivirus, and a mosavirus. However, viral prevalence and viral load, and the ability to cause a systemic infection, was not dependent on the level of environmental radiation.


Viruses ◽  
2020 ◽  
Vol 12 (2) ◽  
pp. 237
Author(s):  
Saskia Weber ◽  
Kathrin Jeske ◽  
Rainer G. Ulrich ◽  
Christian Imholt ◽  
Jens Jacob ◽  
...  

Cowpox virus (CPXV) belongs to the genus Orthopoxvirus in the Poxviridae family and is endemic in western Eurasia. Based on seroprevalence studies in different voles from continental Europe and UK, voles are suspected to be the major reservoir host. Recently, a CPXV was isolated from a bank vole (Myodes glareolus) in Germany that showed a high genetic similarity to another isolate originating from a Cotton-top tamarin (Saguinus oedipus). Here we characterize this first bank vole-derived CPXV isolate in comparison to the related tamarin-derived isolate. Both isolates grouped genetically within the provisionally called CPXV-like 3 clade. Previous phylogenetic analysis indicated that CPXV is polyphyletic and CPXV-like 3 clade represents probably a different species if categorized by the rules used for other orthopoxviruses. Experimental infection studies with bank voles, common voles (Microtus arvalis) and Wistar rats showed very clear differences. The bank vole isolate was avirulent in both common voles and Wistar rats with seroconversion seen only in the rats. In contrast, inoculated bank voles exhibited viral shedding and seroconversion for both tested CPXV isolates. In addition, bank voles infected with the tamarin-derived isolate experienced a marked weight loss. Our findings allow for the conclusion that CPXV isolates might differ in their replication capacity in different vole species and rats depending on their original host. Moreover, the results indicate host-specific differences concerning CPXV-specific virulence. Further experiments are needed to identify individual virulence and host factors involved in the susceptibility and outcome of CPXV-infections in the different reservoir hosts.


2017 ◽  
Author(s):  
Audrey Rohfritsch ◽  
Maxime Galan ◽  
Mathieu Gautier ◽  
Karim Gharbi ◽  
Gert Olsson ◽  
...  

AbstractInfectious pathogens are major selective forces acting on individuals. The recent advent of high-throughput sequencing technologies now enables to investigate the genetic bases of resistance/susceptibility to infections in non-model organisms. From an evolutionary perspective, the analysis of the genetic diversity observed at these genes in natural populations provides insight into the mechanisms maintaining polymorphism and their epidemiological consequences. We explored these questions in the context of the interactions between Puumala hantavirus (PUUV) and its reservoir host, the bank vole Myodes glareolus. Despite the continuous spatial distribution of M. glareolus in Europe, PUUV distribution is strongly heterogeneous. Different defence strategies might have evolved in bank voles as a result of co-adaptation with PUUV, which may in turn reinforce spatial heterogeneity in PUUV distribution. We performed a genome scan study of six bank vole populations sampled along a North/South transect in Sweden, including PUUV endemic and non-endemic areas. We combined candidate gene analyses (Tlr4, Tlr7, Mx2 genes) and high throughput sequencing of RAD (Restriction-site Associated DNA) markers. We found evidence for outlier loci showing high levels of genetic differentiation. Ten outliers among the 52 that matched to mouse protein-coding genes corresponded to immune related genes and were detected using ecological associations with variations in PUUV prevalence. One third of the enriched pathways concerned immune processes, including platelet activation and TLR pathway. In the future, functional experimentations should enable to confirm the role of these these immune related genes with regard to the interactions between M. glareolus and PUUV.


Open Biology ◽  
2017 ◽  
Vol 7 (9) ◽  
pp. 170135 ◽  
Author(s):  
Grace M. Loxley ◽  
Jennifer Unsworth ◽  
Michael J. Turton ◽  
Alexandra Jebb ◽  
Kathryn S. Lilley ◽  
...  

The urine of bank voles ( Myodes glareolus ) contains substantial quantities of a small protein that is expressed at much higher levels in males than females, and at higher levels in males in the breeding season. This protein was purified and completely sequenced at the protein level by mass spectrometry. Leucine/isoleucine ambiguity was completely resolved by metabolic labelling, monitoring the incorporation of dietary deuterated leucine into specific sites in the protein. The predicted mass of the sequenced protein was exactly consonant with the mass of the protein measured in bank vole urine samples, correcting for the formation of two disulfide bonds. The sequence of the protein revealed that it was a lipocalin related to aphrodisin and other odorant-binding proteins (OBPs), but differed from all OBPs previously described. The pattern of secretion in urine used for scent marking by male bank voles, and the similarity to other lipocalins used as chemical signals in rodents, suggest that this protein plays a role in male sexual and/or competitive communication. We propose the name glareosin for this novel protein to reflect the origin of the protein and to emphasize the distinction from known OBPs.


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