Publications by authors named "Gerald Heckel"

65 Publications

FREQUENT LEPTOSPIRA SPP. DETECTION BUT ABSENCE OF TULA ORTHOHANTAVIRUS IN MICROTUS SPP. VOLES, NORTHWESTERN SPAIN.

J Wildl Dis 2021 Jul 28. Epub 2021 Jul 28.

Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Südufer 10, 17493 Greifswald-Insel Riems, Germany.

The common vole (Microtus arvalis) is a major agricultural pest in Europe and is a reservoir for several zoonotic agents, such as Leptospira spp. and Tula orthohantavirus (TULV). However, little is known about the occurrence of those pathogens in voles from Spain, where the species has largely expanded its distribution range in the past decades, causing agricultural pests and zoonotic diseases. For a molecular survey, 580 common voles and six Lusitanian pine voles (Microtus lusitanicus) were collected in 26 localities from four provinces of northwestern Spain. We assessed the presence of Leptospira spp. DNA in kidney tissue by PCR targeting the lipL32 gene, detecting a prevalence of 7.9% (95% confidence interval, 5.9-10.4) for common voles and of 33.3% (95% confidence interval, 4.3-77.7) for Lusitanian pine voles. We identified Leptospira kirschneri in 24 animals and Leptospira borgpetersenii in two animals, using secY gene-specific PCR. We analyzed environmental and demographic factors (such as age class, weight, and sex) and population dynamics data for their potential effect on the Leptospira spp. prevalence in those voles. The Leptospira spp. DNA detection rate in common voles increased significantly with maximum air temperature, vole weight, and amount of accumulated rainfall during the 90 d before capture and within the peak phase of the population cycle. We assessed the presence of TULV in lung tissue of 389 voles by reverse-transcription PCR, with no positive results. The absence of TULV might be explained by the evolutionary isolation of the common vole in Spain. The detection of two Leptospira genomospecies underlines the necessity for further typing efforts to understand the epidemiology of leptospiral infection in the common vole and the potential risk for human health in Spain.
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http://dx.doi.org/10.7589/JWD-D-20-00109DOI Listing
July 2021

Spatial and Temporal Dynamics and Molecular Evolution of in German Vole Populations.

Viruses 2021 06 11;13(6). Epub 2021 Jun 11.

Institute for Plant Protection in Horticulture and Forests, Julius Kühn-Institute (JKI), 48161 Münster, Germany.

Tula orthohantavirus (TULV) is a rodent-borne hantavirus with broad geographical distribution in Europe. Its major reservoir is the common vole (), but TULV has also been detected in closely related vole species. Given the large distributional range and high amplitude population dynamics of common voles, this host-pathogen complex presents an ideal system to study the complex mechanisms of pathogen transmission in a wild rodent reservoir. We investigated the dynamics of TULV prevalence and the subsequent potential effects on the molecular evolution of TULV in common voles of the Central evolutionary lineage. Rodents were trapped for three years in four regions of Germany and samples were analyzed for the presence of TULV-reactive antibodies and TULV RNA with subsequent sequence determination. The results show that individual (sex) and population-level factors (abundance) of hosts were significant predictors of local TULV dynamics. At the large geographic scale, different phylogenetic TULV clades and an overall isolation-by-distance pattern in virus sequences were detected, while at the small scale (<4 km) this depended on the study area. In combination with an overall delayed density dependence, our results highlight that frequent, localized bottleneck events for the common vole and TULV do occur and can be offset by local recolonization dynamics.
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http://dx.doi.org/10.3390/v13061132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8231151PMC
June 2021

A Putative Novel Hepatitis E Virus Genotype 3 Subtype Identified in Rabbit, Germany 2016.

Viruses 2021 06 3;13(6). Epub 2021 Jun 3.

Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, 17493 Greifswald-Insel Riems, Germany.

Hepatitis E is an emerging viral disease that is the leading cause of viral hepatitis in the world. The vast majority of hepatitis E cases in developed countries are caused by zoonotic genotypes 3 and 4 of hepatitis E virus (HEV) for which pig and wild boar and to lesser extent rabbits are the main reservoir. According to recent reports rabbits are a source of human HEV infection and highlight the risk of zoonotic foodborne transmission. Here we report the molecular analysis of a novel HEV strain identified in a rabbit during a countrywide surveillance of rabbits and hares in Germany, 2016. The analysis of the complete genome reveals characteristics of a putative novel recombinant subtype of the species within the clade of genotype 3 but not closely related to any known subtypes. Importantly, the genome of this strain possesses a nucleotide exchange in the overlapping region of open reading frames ORF2/ORF3 interfering with a broadly applied diagnostic real-time RT-PCR. In conclusion, a new type of HEV strain was identified in a German rabbit with atypical and novel sequence characteristics.
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http://dx.doi.org/10.3390/v13061065DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8228152PMC
June 2021

Geographical Distribution and Genetic Diversity of Bank Vole Hepaciviruses in Europe.

Viruses 2021 06 28;13(7). Epub 2021 Jun 28.

Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, 17493 Greifswald-Insel Riems, Germany.

The development of new diagnostic methods resulted in the discovery of novel hepaciviruses in wild populations of the bank vole (, syn. ). 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 (, syn. ). 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 ( and ) 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.
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http://dx.doi.org/10.3390/v13071258DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8310187PMC
June 2021

Genomic insight into diet adaptation in the biological control agent Cryptolaemus montrouzieri.

BMC Genomics 2021 Feb 25;22(1):135. Epub 2021 Feb 25.

State Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen University, Guangzhou, Guangdong, China.

Background: The ladybird beetle Cryptolaemus montrouzieri Mulsant, 1853 (Coleoptera, Coccinellidae) is used worldwide as a biological control agent. It is a predator of various mealybug pests, but it also feeds on alternative prey and can be reared on artificial diets. Relatively little is known about the underlying genetic adaptations of its feeding habits.

Results: We report the first high-quality genome sequence for C. montrouzieri. We found that the gene families encoding chemosensors and digestive and detoxifying enzymes among others were significantly expanded or contracted in C. montrouzieri in comparison to published genomes of other beetles. Comparisons of diet-specific larval development, survival and transcriptome profiling demonstrated that differentially expressed genes on unnatural diets as compared to natural prey were enriched in pathways of nutrient metabolism, indicating that the lower performance on the tested diets was caused by nutritional deficiencies. Remarkably, the C. montrouzieri genome also showed a significant expansion in an immune effector gene family. Some of the immune effector genes were dramatically downregulated when larvae were fed unnatural diets.

Conclusion: We suggest that the evolution of genes related to chemosensing, digestion, and detoxification but also immunity might be associated with diet adaptation of an insect predator. These findings help explain why this predatory ladybird has become a successful biological control agent and will enable the optimization of its mass rearing and use in biological control programs.
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http://dx.doi.org/10.1186/s12864-021-07442-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7905881PMC
February 2021

Zoonotic pathogen screening of striped field mice (Apodemus agrarius) from Austria.

Transbound Emerg Dis 2021 Feb 3. Epub 2021 Feb 3.

Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Greifswald-Insel Riems, Germany.

The striped field mouse (Apodemus agrarius) is known to carry several zoonotic pathogens, including Leptospira spp. and Dobrava-Belgrade orthohantavirus (DOBV). Since its first detection in 1996 in south-east Austria, the striped field mouse has further expanded its range in Austria. Here, we screened 35 striped field mice collected in an Austrian region near the Hungarian border for DOBV, Leptospira spp. and seven vector-borne pathogens. Hantavirus RT-PCR screening and DOBV IgG ELISA analysis led to the detection of two DOBV-positive striped field mice. The complete coding sequences of all three genome segments of both strains were determined by a combination of target enrichment and next-generation sequencing. Both complete coding S segment sequences clustered within the DOBV genotype Kurkino clade with the highest similarity to a sequence from Hungary. In one of 35 striped field mice, Leptospira borgpetersenii sequence type (ST) 146 was detected. Bartonella spp., Borrelia miyamotoi and Neoehrlichia mikurensis DNA was detected in four, one and two of 32 mice, respectively. Babesia, Anaplasma, Ehrlichia and Rickettsia specific DNA was not detected. Future investigations will have to determine the prevalence and invasion of these pathogens with the ongoing range expansion of the striped field mouse in Austria.
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http://dx.doi.org/10.1111/tbed.14015DOI Listing
February 2021

Identification of a novel hantavirus strain in the root vole (Microtus oeconomus) in Lithuania, Eastern Europe.

Infect Genet Evol 2021 06 3;90:104520. Epub 2020 Sep 3.

Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Südufer 10, 17493 Greifswald-Insel Riems, Germany. Electronic address:

Hantaviruses are zoonotic pathogens that can cause subclinical to lethal infections in humans. In Europe, five orthohantaviruses are present in rodents: Myodes-associated Puumala orthohantavirus (PUUV), Microtus-associated Tula orthohantavirus, Traemmersee hantavirus (TRAV)/ Tatenale hantavirus (TATV)/ Kielder hantavirus, rat-borne Seoul orthohantavirus, and Apodemus-associated Dobrava-Belgrade orthohantavirus (DOBV). Human PUUV and DOBV infections were detected previously in Lithuania, but the presence of Microtus-associated hantaviruses is not known. For this study we screened 234 Microtus voles, including root voles (Microtus oeconomus), field voles (Microtus agrestis) and common voles (Microtus arvalis) from Lithuania for hantavirus infections. This initial screening was based on reverse transcription-polymerase chain reaction (RT-PCR) targeting the S segment and serological analysis. A novel hantavirus was detected in eight of 79 root voles tentatively named "Rusne virus" according to the capture location and complete genome sequences were determined. In the coding regions of all three genome segments, Rusne virus showed high sequence similarity to TRAV and TATV and clustered with Kielder hantavirus in phylogenetic analyses of partial S and L segment sequences. Pairwise evolutionary distance analysis confirmed Rusne virus as a strain of the species TRAV/TATV. Moreover, we synthesized the entire nucleocapsid (N) protein of Rusne virus in Saccharomyces cerevisiae. We observed cross-reactivity of antibodies raised against other hantaviruses, including PUUV, with this new N protein. ELISA investigation of all 234 voles detected Rusne virus-reactive antibodies exclusively in four of 79 root voles, all being also RNA positive, but not in any other vole species. In conclusion, the detection of Rusne virus RNA in multiple root voles at the same trapping site during three years and its absence in sympatric field voles suggests root voles as the reservoir host of this novel virus. Future investigations should evaluate host association of TRAV, TATV, Kielder virus and the novel Rusne virus and their evolutionary relationships.
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http://dx.doi.org/10.1016/j.meegid.2020.104520DOI Listing
June 2021

Assessing Genome-Wide Diversity in European Hantaviruses through Sequence Capture from Natural Host Samples.

Viruses 2020 07 11;12(7). Epub 2020 Jul 11.

Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.

Research on the ecology and evolution of viruses is often hampered by the limitation of sequence information to short parts of the genomes or single genomes derived from cultures. In this study, we use hybrid sequence capture enrichment in combination with high-throughput sequencing to provide efficient access to full genomes of European hantaviruses from rodent samples obtained in the field. We applied this methodology to Tula (TULV) and Puumala (PUUV) orthohantaviruses for which analyses from natural host samples are typically restricted to partial sequences of their tri-segmented RNA genome. We assembled a total of ten novel hantavirus genomes with very high coverage (on average >99%) and sequencing depth (average >247×). A comparison with partial Sanger sequences indicated an accuracy of >99.9% for the assemblies. An analysis of two common vole () samples infected with two TULV strains each allowed for the assembly of all four TULV genomes. Combining the novel sequences with all available TULV and PUUV genomes revealed very similar patterns of sequence diversity along the genomes, except for remarkably higher diversity in the non-coding region of the S-segment in PUUV. The genomic distribution of polymorphisms in the coding sequence was similar between the species, but differed between the segments with the highest sequence divergence of 0.274 for the M-segment, 0.265 for the S-segment, and 0.248 for the L-segment (overall 0.258). Phylogenetic analyses showed the clustering of genome sequences consistent with their geographic distribution within each species. Genome-wide data yielded extremely high node support values, despite the impact of strong mutational saturation that is expected for hantavirus sequences obtained over large spatial distances. We conclude that genome sequencing based on capture enrichment protocols provides an efficient means for ecological and evolutionary investigations of hantaviruses at an unprecedented completeness and depth.
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http://dx.doi.org/10.3390/v12070749DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7412162PMC
July 2020

Spatial and Temporal Evolutionary Patterns in Puumala Orthohantavirus (PUUV) S Segment.

Pathogens 2020 Jul 8;9(7). Epub 2020 Jul 8.

Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, 17493 Greifswald-Insel Riems, Germany.

The S segment of bank vole ()-associated Puumala orthohantavirus (PUUV) contains two overlapping open reading frames coding for the nucleocapsid (N) and a non-structural (NSs) protein. To identify the influence of bank vole population dynamics on PUUV S segment sequence evolution and test for spillover infections in sympatric rodent species, during 2010-2014, 883 bank voles, 357 yellow-necked mice (), 62 wood mice (), 149 common voles () and 8 field voles () were collected in Baden-Wuerttemberg and North Rhine-Westphalia, Germany. In total, 27.9% and 22.3% of bank voles were positive for PUUV-reactive antibodies and PUUV-specific RNA, respectively. One of eight field voles was PUUV RNA-positive, indicating a spillover infection, but none of the other species showed evidence of PUUV infection. Phylogenetic and isolation-by-distance analyses demonstrated a spatial clustering of PUUV S segment sequences. In the hantavirus outbreak years 2010 and 2012, PUUV RNA prevalence was higher in our study regions compared to non-outbreak years 2011, 2013 and 2014. NSs amino acid and nucleotide sequence types showed temporal and/or local variation, whereas the N protein was highly conserved in the NSs overlapping region and, to a lower rate, in the N alone coding part.
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http://dx.doi.org/10.3390/pathogens9070548DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7400055PMC
July 2020

Field vole-associated Traemmersee hantavirus from Germany represents a novel hantavirus species.

Virus Genes 2019 Dec 1;55(6):848-853. Epub 2019 Oct 1.

Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, Südufer 10, 17493, Greifswald-Insel Riems, Germany.

Vole-associated hantaviruses occur in the Old and New World. Tula orthohantavirus (TULV) is widely distributed throughout the European continent in its reservoir, the common vole (Microtus arvalis), but the virus was also frequently detected in field voles (Microtus agrestis) and other vole species. TULV and common voles are absent from Great Britain. However, field voles there harbor Tatenale and Kielder hantaviruses. Here we screened 126 field voles and 13 common voles from Brandenburg, Germany, for hantavirus infections. One common vole and four field voles were anti-TULV antibody and/or TULV RNA positive. In one additional, seropositive field vole a novel hantavirus sequence was detected. The partial S and L segment nucleotide sequences were only 61.1% and 75.6% identical to sympatrically occurring TULV sequences, but showed highest similarity of approximately 80% to British Tatenale and Kielder hantaviruses. Subsequent determination of the entire nucleocapsid (N), glycoprotein (GPC), and RNA-dependent RNA polymerase encoding sequences and determination of the pairwise evolutionary distance (PED) value for the concatenated N and GPC amino acid sequences confirmed a novel orthohantavirus species, tentatively named Traemmersee orthohantavirus. The identification of this novel hantavirus in a field vole from eastern Germany underlines the necessity of a large-scale, broad geographical hantavirus screening of voles to understand evolutionary processes of virus-host associations and host switches.
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http://dx.doi.org/10.1007/s11262-019-01706-7DOI Listing
December 2019

Genomic and spatial variability of a European common vole hepevirus.

Arch Virol 2019 Nov 9;164(11):2671-2682. Epub 2019 Aug 9.

Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, Südufer 10, 17493, Greifswald-Insel Riems, Germany.

Rodents host different orthohepeviruses, namely orthohepevirus C genotype HEV-C1 (rat hepatitis E virus, HEV) and the additional putative genotypes HEV-C3 and HEV-C4. Here, we screened 2,961 rodents from Central Europe by reverse transcription polymerase chain reaction (RT-PCR) and identified HEV RNA in 13 common voles (Microtus arvalis) and one bank vole (Myodes glareolus) with detection rates of 2% (95% confidence interval [CI]: 1-3.4) and 0.08% (95% CI: 0.002-0.46), respectively. Sequencing of a 279-nucleotide RT-PCR amplicon corresponding to a region within open reading frame (ORF) 1 showed a high degree of similarity to recently described common vole-associated HEV (cvHEV) sequences from Hungary. Five novel complete cvHEV genome sequences from Central Europe showed the typical HEV genome organization with ORF1, ORF2 and ORF3 and RNA secondary structure. Uncommon features included a noncanonical start codon in ORF3, multiple insertions and deletions within ORF1 and ORF2/ORF3, and the absence of a putative ORF4. Phylogenetic analysis showed all of the novel cvHEV sequences to be monophyletic, clustering most closely with an unassigned bird-derived sequence and other sequences of the species Orthohepevirus C. The nucleotide and amino acid sequence divergence of the common vole-derived sequences was significantly correlated with the spatial distance between the trapping sites, indicating mostly local evolutionary processes. Detection of closely related HEV sequences in common voles in multiple localities over a distance of 800 kilometers suggested that common voles are infected by cvHEV across broad geographic distances. The common vole-associated HEV strain is clearly divergent from HEV sequences recently found in narrow-headed voles (Microtus gregalis) and other cricetid rodents.
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http://dx.doi.org/10.1007/s00705-019-04347-1DOI Listing
November 2019

Genetic, phenotypic and ecological differentiation suggests incipient speciation in two Charadrius plovers along the Chinese coast.

BMC Evol Biol 2019 06 27;19(1):135. Epub 2019 Jun 27.

State Key Laboratory of Biocontrol, Department of Ecology, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China.

Background: Speciation with gene flow is an alternative to the nascence of new taxa in strict allopatric separation. Indeed, many taxa have parapatric distributions at present. It is often unclear if these are secondary contacts, e.g. caused by past glaciation cycles or the manifestation of speciation with gene flow, which hampers our understanding of how different forces drive diversification. Here we studied genetic, phenotypic and ecological aspects of divergence in a pair of incipient shorebird species, the Kentish (Charadrius alexandrinus) and the White-faced Plovers (C. dealbatus), shorebirds with parapatric breeding ranges along the Chinese coast. We assessed divergence based on molecular markers with different modes of inheritance and quantified phenotypic and ecological divergence in aspects of morphometric, dietary and climatic niches.

Results: Our integrative analyses revealed small to moderate levels of genetic and phenotypic distinctiveness with symmetric gene flow across the contact area at the Chinese coast. The two species diverged approximately half a million years ago in dynamic isolation with secondary contact occurring due to cycling sea level changes between the Eastern and Southern China Sea in the mid-late Pleistocene. We found evidence of character displacement and ecological niche differentiation between the two species, invoking the role of selection in facilitating divergence despite gene flow.

Conclusion: These findings imply that ecology can indeed counter gene flow through divergent selection and thus contributes to incipient speciation in these plovers. Furthermore, our study highlights the importance of using integrative datasets to reveal the evolutionary history and assist the inference of mechanisms of speciation.
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http://dx.doi.org/10.1186/s12862-019-1449-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598359PMC
June 2019

Genomic changes in the biological control agent associated with introduction.

Evol Appl 2019 Jun 11;12(5):989-1000. Epub 2019 Feb 11.

State Key Laboratory of Biocontrol, Ecology and Evolution, School of Life Sciences Sun Yat-sen University Guangzhou Guangdong China.

Biological control is the main purpose of intentionally introducing non-native invertebrate species. The evolutionary changes that occur in the populations of the introduced biological control agents may determine the agent's efficiency and the environmental safety. Here, to explore the pattern and extent of potential genomic changes in the worldwide introduced predatory ladybird beetle , we used a reduced-representation sequencing method to analyze the genome-wide differentiation of the samples from two native and five introduced locations. Our analyses based on a total of 53,032 single nucleotide polymorphism loci showed that beetles from the introduced locations in Asia and Europe exhibited significant reductions in genetic diversity and high differentiation compared with the samples from the native Australian range. Each introduced population belonged to a unique genetic cluster, while the beetles from two native locations were much more similar. These genomic patterns were also detected when the dataset was pruned for genomic outlier loci (52,318 SNPs remaining), suggesting that random genetic drift was the main force shaping the genetic diversity and population structure of this biological control agent. Our results provide a genome-wide characterization of polymorphisms in a biological control agent and reveal genomic differences that were influenced by the introduction history. These differences might complicate assessments of the efficiency of biological control and the invasion potential of this species but also indicate the feasibility of selective breeding.
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http://dx.doi.org/10.1111/eva.12774DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6503826PMC
June 2019

Secondary contact between diverged host lineages entails ecological speciation in a European hantavirus.

PLoS Biol 2019 02 20;17(2):e3000142. Epub 2019 Feb 20.

Institute of Ecology and Evolution, University of Bern, Switzerland.

The diversity of viruses probably exceeds biodiversity of eukaryotes, but little is known about the origin and emergence of novel virus species. Experimentation and disease outbreak investigations have allowed the characterization of rapid molecular virus adaptation. However, the processes leading to the establishment of functionally distinct virus taxa in nature remain obscure. Here, we demonstrate that incipient speciation in a natural host species has generated distinct ecological niches leading to adaptive isolation in an RNA virus. We found a very strong association between the distributions of two major phylogenetic clades in Tula orthohantavirus (TULV) and the rodent host lineages in a natural hybrid zone of the European common vole (Microtus arvalis). The spatial transition between the virus clades in replicated geographic clines is at least eight times narrower than between the hybridizing host lineages. This suggests a strong barrier for effective virus transmission despite frequent dispersal and gene flow among local host populations, and translates to a complete turnover of the adaptive background of TULV within a few hundred meters in the open, unobstructed landscape. Genetic differences between TULV clades are homogenously distributed in the genomes and mostly synonymous (93.1%), except for a cluster of nonsynonymous changes in the 5' region of the viral envelope glycoprotein gene, potentially involved in host-driven isolation. Evolutionary relationships between TULV clades indicate an emergence of these viruses through rapid differential adaptation to the previously diverged host lineages that resulted in levels of ecological isolation exceeding the progress of speciation in their vertebrate hosts.
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http://dx.doi.org/10.1371/journal.pbio.3000142DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6382107PMC
February 2019

Effects of the Mitochondrial and Nuclear Genomes on Nonshivering Thermogenesis in a Wild Derived Rodent.

Integr Comp Biol 2018 09;58(3):532-543

Computational and Molecular Population Genetics, Institute of Ecology and Evolution, University of Bern, Hochschulstrasse 6, CH-3012 Bern, Switzerland.

A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardized conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western [W] and Central [C]), we show that W voles had greater NST than C voles. By introgressing those two lineages over at least nine generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the W mitochondrial genotype being associated with higher NST and the W nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate (RMR). Hybrid voles were lighter and had higher RMR. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.
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http://dx.doi.org/10.1093/icb/icy072DOI Listing
September 2018

Hepatitis E virus in feral rabbits along a rural-urban transect in Central Germany.

Infect Genet Evol 2018 07 26;61:155-159. Epub 2018 Mar 26.

Friedrich-Loeffler-Institut, Institute of Novel and Emerging Infectious Diseases, Greifswald-Insel Riems, Germany; German Center for Infection Research (DZIF), Partner Site Hamburg-Luebeck-Borstel-Insel Riems, Germany. Electronic address:

Rabbit associated genotype 3 hepatitis E virus (HEV) strains were detected in feral, pet and farm rabbits in different parts of the world since 2009 and recently also in human patients. Here, we report a serological and molecular survey on 72 feral rabbits, collected along a rural-urban transect in and next to Frankfurt am Main, Central Germany. ELISA investigations revealed in 25 of 72 (34.7%) animals HEV-specific antibodies. HEV derived RNA was detected in 18 of 72 (25%) animals by reverse transcription-polymerase chain reaction assay. The complete genomes from two rabbitHEV-strains, one from a rural site and the other from an inner-city area, were generated by a combination of high-throughput sequencing, a primer walking approach and 5'- and 3'- rapid amplification of cDNA ends. Phylogenetic analysis of open reading frame (ORF)1-derived partial and complete ORF1/ORF2 concatenated coding sequences indicated their similarity to rabbit-associated HEV strains. The partial sequences revealed one cluster of closely-related rabbitHEV sequences from the urban trapping sites that is well separated from several clusters representing rabbitHEV sequences from rural trapping sites. The complete genome sequences of the two novel strains indicated similarities of 75.6-86.4% to the other 17 rabbitHEV sequences; the amino acid sequence identity of the concatenated ORF1/ORF2-encoded proteins reached 89.0-93.1%. The detection of rabbitHEV in an inner-city area with a high human population density suggests a high risk of potential human infection with the zoonotic rabbitHEV, either by direct or indirect contact with infected animals. Therefore, future investigations on the occurrence and frequency of human infections with rabbitHEV are warranted in populations with different contact to rabbits.
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http://dx.doi.org/10.1016/j.meegid.2018.03.019DOI Listing
July 2018

Spatial and temporal genetic dynamics of the grasshopper revealed by museum genomics.

Ecol Evol 2018 02 29;8(3):1480-1495. Epub 2017 Dec 29.

Department of Ecology and Evolution University of Lausanne Lausanne Switzerland.

Analyzing genetic variation through time and space is important to identify key evolutionary and ecological processes in populations. However, using contemporary genetic data to infer the dynamics of genetic diversity may be at risk of a bias, as inferences are performed from a set of extant populations, setting aside unavailable, rare, or now extinct lineages. Here, we took advantage of new developments in next-generation sequencing to analyze the spatial and temporal genetic dynamics of the grasshopper , a steppic Southwestern-Palearctic species. We applied a recently developed hybridization capture (hyRAD) protocol that allows retrieving orthologous sequences even from degraded DNA characteristic of museum specimens. We identified single nucleotide polymorphisms in 68 historical and 51 modern samples in order to (i) unravel the spatial genetic structure across part of the species distribution and (ii) assess the loss of genetic diversity over the past century in Swiss populations. Our results revealed (i) the presence of three potential glacial refugia spread across the European continent and converging spatially in the Alpine area. In addition, and despite a limited population sample size, our results indicate (ii) a loss of allelic richness in contemporary Swiss populations compared to historical populations, whereas levels of expected heterozygosities were not significantly different. This observation is compatible with an increase in the bottleneck magnitude experienced by central European populations of following human-mediated land-use change impacting steppic habitats. Our results confirm that application of hyRAD to museum samples produces valuable information to study genetic processes across time and space.
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http://dx.doi.org/10.1002/ece3.3699DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792620PMC
February 2018

Introgressive replacement of natives by invading Arion pest slugs.

Sci Rep 2017 11 2;7(1):14908. Epub 2017 Nov 2.

Computational and Molecular Population Genetics, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012, Bern, Switzerland.

Hybridization with invasive species is one of the major threats to the phenotypic and genetic persistence of native organisms worldwide. Arion vulgaris (syn. lusitanicus) is a major agricultural pest slug that successfully invaded many European countries in recent decades, but its impact on closely related native species remains unclear. Here, we hypothesized that the regional decline of native A. rufus is connected with the spread of invasive A. vulgaris, and tested whether this can be linked to hybridization between the two species by analyzing 625 Arion sp. along altitudinal transects in three regions in Switzerland. In each region, we observed clear evidence of different degrees of genetic admixture, suggesting recurrent hybridization beyond the first generation. We found spatial differences in admixture patterns that might reflect distinct invasion histories among the regions. Our analyses provide a landscape level perspective for the genetic interactions between invasive and native animals during the invasion. We predict that without specific management action, A. vulgaris will further expand its range, which might lead to local extinction of A. rufus and other native slugs in the near future. Similar processes are likely occurring in other regions currently invaded by A. vulgaris.
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http://dx.doi.org/10.1038/s41598-017-14619-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5668256PMC
November 2017

Detection of rat hepatitis E virus in wild Norway rats (Rattus norvegicus) and Black rats (Rattus rattus) from 11 European countries.

Vet Microbiol 2017 Sep 4;208:58-68. Epub 2017 Jul 4.

Friedrich-Loeffler-Institut, Institute of Novel and Emerging Infectious Diseases, Südufer 10, 17493 Greifswald-Insel Riems, Germany; German Center for Infection Research (DZIF), Partner Site Hamburg-Luebeck-Borstel-Insel Riems, Germany. Electronic address:

Rat hepatitis E virus (HEV) is genetically only distantly related to hepeviruses found in other mammalian reservoirs and in humans. It was initially detected in Norway rats (Rattus norvegicus) from Germany, and subsequently in rats from Vietnam, the USA, Indonesia, China, Denmark and France. Here, we report on a molecular survey of Norway rats and Black rats (Rattus rattus) from 12 European countries for ratHEV and human pathogenic hepeviruses. RatHEV-specific real-time and conventional RT-PCR investigations revealed the presence of ratHEV in 63 of 508 (12.4%) rats at the majority of sites in 11 of 12 countries. In contrast, a real-time RT-PCR specific for human pathogenic HEV genotypes 1-4 and a nested broad-spectrum (NBS) RT-PCR with subsequent sequence determination did not detect any infections with these genotypes. Only in a single Norway rat from Belgium a rabbit HEV-like genotype 3 sequence was detected. Phylogenetic analysis indicated a clustering of all other novel Norway and Black rat-derived sequences with ratHEV sequences from Europe, the USA and a Black rat-derived sequence from Indonesia within the proposed ratHEV genotype 1. No difference in infection status was detected related to age, sex, rat species or density of human settlements and zoological gardens. In conclusion, our investigation shows a broad geographical distribution of ratHEV in Norway and Black rats from Europe and its presence in all settlement types investigated.
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http://dx.doi.org/10.1016/j.vetmic.2017.07.001DOI Listing
September 2017

Revised time scales of RNA virus evolution based on spatial information.

Proc Biol Sci 2017 Aug;284(1860)

Computational and Molecular Population Genetics, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland

The time scales of pathogen evolution are of major concern in the context of public and veterinary health, epidemiology and evolutionary biology. Dating the emergence of a pathogen often relies on estimates of evolutionary rates derived from nucleotide sequence data. For many viruses, this has yielded estimates of evolutionary origins only a few hundred years in the past. Here we demonstrate through the incorporation of geographical information from virus sampling that evolutionary age estimates of two European hantaviruses are severely underestimated because of pervasive mutational saturation of nucleotide sequences. We detected very strong relationships between spatial distance and genetic divergence for both Puumala and Tula hantavirus-irrespective of whether nucleotide or derived amino acid sequences were analysed. Extrapolations from these relationships dated the emergence of these viruses most conservatively to at least 3700 and 2500 years ago, respectively. Our minimum estimates for the age of these hantaviruses are ten to a hundred times older than results from current non-spatial methods, and in much better accordance with the biogeography of these viruses and their respective hosts. Spatial information can thus provide valuable insights on the deeper time scales of pathogen evolution and improve our understanding of disease emergence.
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http://dx.doi.org/10.1098/rspb.2017.0857DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563803PMC
August 2017

A highly divergent Puumala virus lineage in southern Poland.

Arch Virol 2017 May 16;162(5):1177-1185. Epub 2017 Jan 16.

Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute for Novel and Emerging Infectious Diseases, Südufer 10, Greifswald-Insel Riems, 17493, Germany.

Puumala virus (PUUV) represents one of the most important hantaviruses in Central Europe. Phylogenetic analyses of PUUV strains indicate a strong genetic structuring of this hantavirus. Recently, PUUV sequences were identified in the natural reservoir, the bank vole (Myodes glareolus), collected in the northern part of Poland. The objective of this study was to evaluate the presence of PUUV in bank voles from southern Poland. A total of 72 bank voles were trapped in 2009 at six sites in this part of Poland. RT-PCR and IgG-ELISA analyses detected three PUUV positive voles at one trapping site. The PUUV-infected animals were identified by cytochrome b gene analysis to belong to the Carpathian and Eastern evolutionary lineages of bank vole. The novel PUUV S, M and L segment nucleotide sequences showed the closest similarity to sequences of the Russian PUUV lineage from Latvia, but were highly divergent to those previously found in northern Poland, Slovakia and Austria. In conclusion, the detection of a highly divergent PUUV lineage in southern Poland indicates the necessity of further bank vole monitoring in this region allowing rational public health measures to prevent human infections.
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http://dx.doi.org/10.1007/s00705-016-3200-5DOI Listing
May 2017

Host-Associated Absence of Human Puumala Virus Infections in Northern and Eastern Germany.

Emerg Infect Dis 2017 01;23(1):83-86

Human hantavirus disease cases, caused by Puumala virus (PUUV), are mainly recorded in western and southern areas of Germany. This bank vole reservoir survey confirmed PUUV presence in these regions but its absence in northern and eastern regions. PUUV occurrence is associated with the presence of the Western bank vole phylogroup.
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http://dx.doi.org/10.3201/eid2301.160224DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5176216PMC
January 2017

Phylogeographic past and invasive presence of Arion pest slugs in Europe.

Mol Ecol 2016 Nov 18;25(22):5747-5764. Epub 2016 Oct 18.

Computational and Molecular Population Genetics, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012, Bern, Switzerland.

Arion vulgaris (syn. A. lusitanicus) is the most destructive pest slug in Europe. The species has been regarded a classic case of an ongoing biological invasion with negative economic and ecological impact in many European countries, but this status has recently been contested. In this study, we assessed mitochondrial and autosomal genetic diversity in populations of A. vulgaris across the entire distribution range in order to characterize its evolutionary history. Mitochondrial diversity in A. vulgaris was strongly reduced compared with the closely related and largely codistributed noninvasive species A. rufus and A. ater, indicating a very rapid spread of A. vulgaris through Europe. Autosomal diversity assessed in 632 individuals from 32 populations decreased towards eastern and northern Europe which is consistent with the reported expansion of the species towards these regions in the last decades. Demographic simulations supported very recent population founding events in most of the European range. The short periods between the first detection of A. vulgaris in different countries and only a very weak association of genetic structuring among populations with geographical distances suggest a human contribution in the ongoing expansion of the slug. We propose that this contribution may ultimately prevent the exact localization of the debated region of origin of A. vulgaris. However, the reclassification of A. vulgaris as noninvasive would be premature. Without counter measures, the Eastern and Northern European countries can expect to see this biological invasion continued in the future.
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http://dx.doi.org/10.1111/mec.13860DOI Listing
November 2016

High genetic structuring of Tula hantavirus.

Arch Virol 2016 May 30;161(5):1135-49. Epub 2016 Jan 30.

Federal Research Institute for Animal Health, OIE Collaborating Centre for Zoonoses in Europe, Institute for Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Suedufer 10, 17493, Greifswald, Insel Riems, Germany.

Tula virus (TULV) is a vole-associated hantavirus with low or no pathogenicity to humans. In the present study, 686 common voles (Microtus arvalis), 249 field voles (Microtus agrestis) and 30 water voles (Arvicola spec.) were collected at 79 sites in Germany, Luxembourg and France and screened by RT-PCR and TULV-IgG ELISA. TULV-specific RNA and/or antibodies were detected at 43 of the sites, demonstrating a geographically widespread distribution of the virus in the studied area. The TULV prevalence in common voles (16.7 %) was higher than that in field voles (9.2 %) and water voles (10.0 %). Time series data at ten trapping sites showed evidence of a lasting presence of TULV RNA within common vole populations for up to 34 months, although usually at low prevalence. Phylogenetic analysis demonstrated a strong genetic structuring of TULV sequences according to geography and independent of the rodent species, confirming the common vole as the preferential host, with spillover infections to co-occurring field and water voles. TULV phylogenetic clades showed a general association with evolutionary lineages in the common vole as assessed by mitochondrial DNA sequences on a large geographical scale, but with local-scale discrepancies in the contact areas.
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http://dx.doi.org/10.1007/s00705-016-2762-6DOI Listing
May 2016

Tracing reinforcement through asymmetrical partner preference in the European common vole Microtus arvalis.

BMC Evol Biol 2015 Aug 25;15:170. Epub 2015 Aug 25.

Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH 3012, Bern, Switzerland.

Background: The mechanistic basis of speciation and in particular the contribution of behaviour to the completion of the speciation process is often contentious. Contact zones between related taxa provide a situation where selection against hybridization might reinforce separation by behavioural mechanisms, which could ultimately fully isolate the taxa. One of the most abundant European mammals, the common vole Microtus arvalis, forms multiple natural hybrid zones where rapidly diverging evolutionary lineages meet in secondary contact. Very narrow zones of hybridization spanning only a few kilometres and sex-specific gene flow patterns indicate reduced fitness of natural hybrids and incipient speciation between some of the evolutionary lineages. In this study, we examined the contribution of behavioural mechanisms to the speciation process in these rodents by fine-mapping allopatric and parapatric populations in the hybrid zone between the Western and Central lineages and experimental testing of the partner preferences of wild, pure-bred and hybrid female common voles.

Results: Genetic analysis based on microsatellite markers revealed the presence of multiple parapatric and largely non-admixed populations at distances of about 10 km at the edge of the area of natural hybridization between the Western and Central lineages. Wild females from Western parapatric populations and lab-born F1 hybrids preferred males from the Western lineage whereas wild females of Central parapatric origin showed no measurable preference. Furthermore, wild and lab-born females from allopatric populations of the Western or Central lineages showed no detectable preference for males from either lineage.

Conclusions: The detected partner preferences are consistent with asymmetrical reinforcement of pre-mating reproductive isolation mechanisms in the European common vole and with earlier results suggesting that hybridization is more detrimental to the Western lineage. As a consequence, these differences in behaviour might contribute to a further geographical stabilization of this moving hybrid zone. Such behavioural processes could also provide a mechanistic perspective for frequently-detected asymmetrical introgression patterns in the largely allopatrically diversifying Microtus genus and other rapidly speciating rodents.
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http://dx.doi.org/10.1186/s12862-015-0455-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4548911PMC
August 2015

Spatiotemporal dynamics of Puumala hantavirus associated with its rodent host, Myodes glareolus.

Evol Appl 2015 Jul 29;8(6):545-59. Epub 2015 May 29.

Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern Bern, Switzerland ; Swiss Institute of Bioinformatics Lausanne, Switzerland.

Many viruses significantly impact human and animal health. Understanding the population dynamics of these viruses and their hosts can provide important insights for epidemiology and virus evolution. Puumala virus (PUUV) is a European hantavirus that may cause regional outbreaks of hemorrhagic fever with renal syndrome in humans. Here, we analyzed the spatiotemporal dynamics of PUUV circulating in local populations of its rodent reservoir host, the bank vole (Myodes glareolus) during eight years. Phylogenetic and population genetic analyses of all three genome segments of PUUV showed strong geographical structuring at a very local scale. There was a high temporal turnover of virus strains in the local bank vole populations, but several virus strains persisted through multiple years. Phylodynamic analyses showed no significant changes in the local effective population sizes of PUUV, although vole numbers and virus prevalence fluctuated widely. Microsatellite data demonstrated also a temporally persisting subdivision between local vole populations, but these groups did not correspond to the subdivision in the virus strains. We conclude that restricted transmission between vole populations and genetic drift play important roles in shaping the genetic structure and temporal dynamics of PUUV in its natural host which has several implications for zoonotic risks of the human population.
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http://dx.doi.org/10.1111/eva.12263DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4479511PMC
July 2015

Complete genome of a Puumala virus strain from Central Europe.

Virus Genes 2015 Apr 28;50(2):292-8. Epub 2014 Dec 28.

Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, OIE Collaborating Centre for Zoonoses in Europe, Institute for Novel and Emerging Infectious Diseases, Südufer 10, 17493, Greifswald - Insel Riems, Germany.

Puumala virus (PUUV) is one of the predominant hantavirus species in Europe causing mild to moderate cases of haemorrhagic fever with renal syndrome. Parts of Lower Saxony in north-western Germany are endemic for PUUV infections. In this study, the complete PUUV genome sequence of a bank vole-derived tissue sample from the 2007 outbreak was determined by a combined primer-walking and RNA ligation strategy. The S, M and L genome segments were 1,828, 3,680 and 6,550 nucleotides in length, respectively. Sliding-window analyses of the nucleotide sequences of all available complete PUUV genomes indicated a non-homogenous distribution of variability with hypervariable regions located at the 3'-ends of the S and M segments. The overall similarity of the coding genome regions to the other PUUV strains ranged between 80.1 and 84.7 % at the level of the nucleotide sequence and between 89.5 and 98.1 % for the deduced amino acid sequences. In comparison to the phylogenetic trees of the complete coding sequences, trees based on partial segments revealed a general drop in phylogenetic support and a lower resolution. The Astrup strain S and M segment sequences showed the highest similarity to sequences of strains from geographically close sites in the Osnabrück Hills region. In conclusion, a primer-walking-mediated strategy resulted in the determination of the first complete nucleotide sequence of a PUUV strain from Central Europe. Different levels of variability along the genome provide the opportunity to choose regions for analyses according to the particular research question, e.g., large-scale phylogenetics or within-host evolution.
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http://dx.doi.org/10.1007/s11262-014-1157-6DOI Listing
April 2015

Continental-scale footprint of balancing and positive selection in a small rodent (Microtus arvalis).

PLoS One 2014 10;9(11):e112332. Epub 2014 Nov 10.

Computational and Molecular Population Genetics (CMPG), Institute of Ecology and Evolution, University of Bern, Bern, Switzerland; Swiss Institute of Bioinformatics, Lausanne, Switzerland.

Genetic adaptation to different environmental conditions is expected to lead to large differences between populations at selected loci, thus providing a signature of positive selection. Whereas balancing selection can maintain polymorphisms over long evolutionary periods and even geographic scale, thus leads to low levels of divergence between populations at selected loci. However, little is known about the relative importance of these two selective forces in shaping genomic diversity, partly due to difficulties in recognizing balancing selection in species showing low levels of differentiation. Here we address this problem by studying genomic diversity in the European common vole (Microtus arvalis) presenting high levels of differentiation between populations (average F ST = 0.31). We studied 3,839 Amplified Fragment Length Polymorphism (AFLP) markers genotyped in 444 individuals from 21 populations distributed across the European continent and hence over different environmental conditions. Our statistical approach to detect markers under selection is based on a Bayesian method specifically developed for AFLP markers, which treats AFLPs as a nearly codominant marker system, and therefore has increased power to detect selection. The high number of screened populations allowed us to detect the signature of balancing selection across a large geographic area. We detected 33 markers potentially under balancing selection, hence strong evidence of stabilizing selection in 21 populations across Europe. However, our analyses identified four-times more markers (138) being under positive selection, and geographical patterns suggest that some of these markers are probably associated with alpine regions, which seem to have environmental conditions that favour adaptation. We conclude that despite favourable conditions in this study for the detection of balancing selection, this evolutionary force seems to play a relatively minor role in shaping the genomic diversity of the common vole, which is more influenced by positive selection and neutral processes like drift and demographic history.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0112332PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4226552PMC
July 2015

Hepeviridae: an expanding family of vertebrate viruses.

Infect Genet Evol 2014 Oct 19;27:212-29. Epub 2014 Jul 19.

Friedrich-Loeffler-Institut, Institute for Novel and Emerging Infectious Diseases, Greifswald-Insel Riems, Germany. Electronic address:

The hepatitis E virus (HEV) was first identified in 1990, although hepatitis E-like diseases in humans have been recorded for a long time dating back to the 18th century. The HEV genotypes 1-4 have been subsequently detected in human hepatitis E cases with different geographical distribution and different modes of transmission. Genotypes 3 and 4 have been identified in parallel in pigs, wild boars and other animal species and their zoonotic potential has been confirmed. Until 2010, these genotypes along with avian HEV strains infecting chicken were the only known representatives of the family Hepeviridae. Thereafter, additional HEV-related viruses have been detected in wild boars, distinct HEV-like viruses were identified in rats, rabbit, ferret, mink, fox, bats and moose, and a distantly related agent was described from closely related salmonid fish. This review summarizes the characteristics of the so far known HEV-like viruses, their phylogenetic relationship, host association and proposed involvement in diseases. Based on the reviewed knowledge, a suggestion for a new taxonomic grouping scheme of the viruses within the family Hepeviridae is presented.
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http://dx.doi.org/10.1016/j.meegid.2014.06.024DOI Listing
October 2014

The changing pace of insular life: 5000 years of microevolution in the Orkney vole (Microtus arvalis orcadensis).

Evolution 2014 Oct 29;68(10):2804-20. Epub 2014 Jul 29.

CNRS-Muséum National d'Histoire Naturelle, UMR 7209, Archéoozoologie, histoire des sociétés humaines et de peuplements animaux, 55 rue Buffon, 75005, Paris, France; Department of Archaeology, University of Aberdeen, St. Mary's, Elphinstone Road, Aberdeen, United Kingdom.

Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior-lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.
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http://dx.doi.org/10.1111/evo.12476DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5366975PMC
October 2014
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