Additional file 4: of Fibroblasts from bank voles inhabiting Chernobyl have increased resistance against oxidative and DNA stresses

The trapping locations of the bank voles used in this study for fibroblast isolation. The green circles present the location at Kiev control area (average site radiation 0.2 μSv/h) where the control voles were trapped and the red circle denotes the site where Chernobyl voles were caught (average site radiation 21 μSv/h). Black dashed line indicates the 30 km Chernobyl exclusion zone. CNPP with a red triangle shows the location of the Chernobyl nuclear power plants. A map of Ukraine as an inset show by a red square the location of Chernobyl area. Map was created with ESRI ArcGIS 10.0. Satellite imagery © CNES/Airbus DS, Earthstar Geographics. Source: Esri, DigitalGlobe, GeoEye, i-cubed, Eart…

Evolutionary constraints of warning signals: A genetic trade-off between the efficacy of larval and adult warning coloration can maintain variation in signal expression

To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11,000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic cor…

Manipulation of offspring number and size: benefits of large body size at birth depend upon the rearing environment

Summary 1. Allocation of reproductive effort between the number and size of offspring determines the immediate rearing environment for the growing young. As the number of offspring increases, the amount of parental investment per individual offspring decreases, and the quality of the rearing environment is expected to decrease. This may result in a lower quality of offspring reared in such conditions. 2. We studied the effects of the rearing environment on the quality of juvenile bank voles, Clethrionomys glareolus , with different initial body sizes at birth in a 2 〈 2 factorial experiment. The rearing environment was manipulated by enlarging both the litter size by two extra pups, and mea…

Island selection on mammalian life-histories: genetic differentiation in offspring size

Abstract Background Since Darwin's pioneering work, evolutionary changes in isolated island populations of vertebrates have continued to provide the strongest evidence for the theory of natural selection. Besides macro-evolutionary changes, micro-evolutionary changes and the relative importance of natural selection vs. genetic drift are under intense investigation. Our study focuses on the genetic differentiation in morphological and life-history traits in insular populations of a small mammal the bank vole Myodes glareolus. Results Our results do not support the earlier findings for larger adult size or lower reproductive effort in insular populations of small mammals. However, the individ…

Rodent host population dynamics drive zoonotic Lyme Borreliosis and Orthohantavirus infections in humans in Northern Europe

Zoonotic diseases, caused by pathogens transmitted between other vertebrate animals and humans, pose a major risk to human health. Rodents are important reservoir hosts for many zoonotic pathogens, and rodent population dynamics affect the infection dynamics of rodent-borne diseases, such as diseases caused by hantaviruses. However, the role of rodent population dynamics in determining the infection dynamics of rodent-associated tick-borne diseases, such as Lyme borreliosis (LB), caused by Borrelia burgdorferi sensu lato bacteria, have gained limited attention in Northern Europe, despite the multiannual abundance fluctuations, the so-called vole cycles, that characterise rodent population d…

Sex-specific selection on energy metabolism - selection coefficients for winter survival

Selection for different fitness optima between sexes is supposed to operate on several traits. As fitness-related traits are often energetically costly, selection should also act directly on the energetics of individuals. However, efforts to examine the relationship between fitness and components of the energy budget are surprisingly scarce. We investigated the effects of basal metabolic rate (BMR, the minimum energy required for basic life functions) and body condition on long-term survival (8 winter months) with manipulated densities in enclosed populations of bank voles (Myodes glareolus). Here, we show that survival selection on BMR was clearly sex-specific but density-independent. Both…

Maintenance of genetic diversity in cyclic populations - a longitudinal analysis in Myodes glareolus

Conspicuous cyclic changes in population density characterize many populations of small northern rodents. The extreme crashes in individual number are expected to reduce the amount of genetic variation within a population during the crash phases of the population cycle. By long-term monitoring of a bank vole (Myodes glareolus) population we show that despite the substantial and repetitive crashes in the population size, high heterozygosity is maintained throughout the population cycle. The striking population density fluctuation in fact only slightly reduced the allelic richness of the population during the crash phases. Effective population sizes of vole populations remained also relativel…

Borrelia afzeliialters reproductive success in a rodent host

The impact of a pathogen on the fitness and behaviour of its natural host depends upon the host–parasite relationship in a given set of environmental conditions. Here, we experimentally investigated the effects ofBorrelia afzelii,one of the aetiological agents of Lyme disease in humans, on the fitness of its natural rodent host, the bank vole (Myodes glareolus), in semi-natural conditions with two contrasting host population densities. Our results show thatB. afzeliican modify the reproductive success and spacing behaviour of its rodent host, whereas host survival was not affected. Infection impaired the breeding probability of large bank voles. Reproduction was hastened in infected females…

Fitness costs of increased cataract frequency and cumulative radiation dose in natural mammalian populations from Chernobyl

AbstractA cataract is a clouding of the lens that reduces light transmission to the retina and it decreases the visual acuity of the bearer. The prevalence of cataracts in natural populations of mammals and their potential ecological significance, is poorly known. Cataracts have been reported to arise from high levels of oxidative stress and a major cause of oxidative stress is ionizing radiation. We investigated whether elevated frequencies of cataracts are found in eyes of bank voles Myodes glareolus collected from natural populations in areas with varying levels of background radiation in Chernobyl. We found high frequencies of cataracts in voles collected from different areas in Chernob…

Genotype-by-Environment Interactions and Reliable Signaling of Male Quality in Bank Voles

Urban forest soils harbour distinct and more diverse communities of bacteria and fungi compared to less disturbed forest soils.

Anthropogenic changes to land use drive concomitant changes in biodiversity, including that of the soil microbiota. However, it is not clear how increasing intensity of human disturbance is reflected in the soil microbial communities. To address this issue, we used amplicon sequencing to quantify the microbiota (bacteria and fungi) in the soil of forests (n=312) experiencing four different land uses, national parks (set aside for nature conservation), managed (for forestry purposes), suburban (on the border of an urban area) and urban (fully within a town or city), which broadly represent a gradient of anthropogenic disturbance. Alpha diversity of bacteria and fungi increased with increasin…

The effect of chronic low-dose environmental radiation on organ mass of bank voles in the Chernobyl Exclusion Zone

Purpose: Animals are exposed to environmental ionizing radiation (IR) externally through proximity to contaminated soil and internally through ingestion and inhalation of radionuclides. Internal organs can respond to radioactive contamination through physiological stress. Chronic stress can compromise the size of physiologically active organs, but studies on wild mammal populations are scarce. The effects of environmental IR contamination on organ masses was studied by using a wild rodent inhabiting the Chernobyl Exclusion Zone (CEZ). Material and Methods: The masses of brain, heart, kidney, spleen, liver and lung were assessed from bank voles (Myodes glareolus) captured from areas across r…

Additional file 7: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Measures of alpha diversity for the skin microbiota of bank voles inhabiting areas that differ in levels of environmental radiation. Box-and-whisker plots represent the median and interquartile range of alpha diversity estimates (i.e. number of observed OTUs, Shannon index). Each box plot represent alpha diversity of the skin microbiome of bank vole females and males from contaminated (CH) and uncontaminated (CL) with radionuclides areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL), Ukraine. (PDF 8â kb)

Sympatric Ixodes-tick species: pattern of distribution and pathogen transmission within wild rodent populations

AbstractThe generalist tick Ixodes ricinus is the most important vector for tick-borne pathogens (TBP), including Borrelia burgdorferi sensu lato, in Europe. However, the involvement of other sympatric Ixodes ticks, such as the specialist vole tick I. trianguliceps, in the enzootic circulations of TBP remains unclear. We studied the distribution of I. ricinus and I. trianguliceps in Central Finland and estimated the TBP infection likelihood in the most common rodent host in relation with the abundance of the two tick species. Ixodes trianguliceps was encountered in all 16 study sites whereas I. ricinus was frequently observed only at a quarter of the study sites. The abundance of I. ricinus…

ENDEMIC HANTAVIRUS INFECTION IMPAIRS THE WINTER SURVIVAL OF ITS RODENT HOST

The influence of pathogens on host fitness is one of the key questions in infection ecology. Hantaviruses have coevolved with their hosts and are generally thought to have little or no effect on host survival or reproduction. We examined the effect of Puumala virus (PUUV) infection on the winter survival of bank voles (Myodes glareolus), the host of this virus. The data were collected by monitoring 22 islands over three consecutive winters (a total of 55 island populations) in an endemic area of central Finland. We show that PUUV infected bank voles had a significantly lower overwinter survival probability than antibody negative bank voles. Antibody negative female bank voles from low-densi…

Artificial selection for predatory behavior results in dietary niche differentiation in an omnivorous mammal

AbstractThe diet of an individual is a result of the availability of dietary items and the individual’s foraging skills and preferences. Behavioral differences may thus influence diet variation, but the evolvability of diet choice through behavioral evolution has not been studied. We used experimental evolution combined with a field enclosure experiment to test whether behavioral selection leads to dietary divergence. We analysed the individual dietary niche via stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) in the hair of an omnivorous mammal, bank vole, from 4 lines selected for predatory behavior and 4 unselected control lines. Predatory voles had higher hair δ15N values than…

Hantavirus infections in fluctuating host populations: the role of maternal antibodies.

Infected females may transfer maternal antibodies (MatAbs) to their offspring, which may then be transiently protected against infections the mother has encountered. However, the role of maternal protection in infectious disease dynamics in wildlife has largely been neglected. Here, we investigate the effects of Puumala hantavirus (PUUV)-specific MatAbs on PUUV dynamics, using 7 years' data from a cyclic bank vole population in Finland. For the first time to our knowledge, we partition seropositivity data from a natural population into separate dynamic patterns for MatAbs and infection. The likelihood of young of the year carrying PUUV-specific MatAbs during the breeding season correlated p…

Additional file 2: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Individual dosimetry supplementary information: measurements of the 137Cs activity and external radiation dose estimates for sampled bank voles. (DOCX 15â kb)

Molecular and ecological signs of mitochondrial adaptation: consequences for introgression?

The evolution of the mitochondrial genome and its potential adaptive impact still generates vital debates. Even if mitochondria have a crucial functional role, as they are the main cellular energy suppliers, mitochondrial DNA (mtDNA) introgression is common in nature, introducing variation in populations upon which selection may act. Here we evaluated whether the evolution of mtDNA in a rodent species affected by mtDNA introgression is explained by neutral expectations alone. Variation in one mitochondrial and six nuclear markers in Myodes glareolus voles was examined, including populations that show mtDNA introgression from its close relative, Myodes rutilus. In addition, we modelled prote…

High population density in bank voles stimulates food hoarding after breeding.

The effects of conspecific density (i.e. risk of intraspecific competition) on hoarding behaviour were studied in breeding pairs of bank voles, Clethrionomys glareolus. I simulated high population density by using odours of conspecifics, to exclude the direct effects of exploitation or interference competition for food. The pairs of bank voles hoarded only at the end of their breeding season. Hoarding was not correlated with whether the voles had a litter during the experiment or their litter size, but was more likely at the high population density and for pairs with small females. This may indicate that smaller females especially make caches in the autumn, possibly to ensure better winter …

COST OF REPRODUCTION IN THE WILD: MANIPULATION OF REPRODUCTIVE EFFORT IN THE BANK VOLE

For three years, we manipulated litter size by adding or subtracting pups in eight wild populations of the bank vole, Clethrionomys glareolus, to examine reproductive costs and allocation of reproductive effort between offspring number and size. In general, litter enlargements did not increase the number of weanlings per mother and significantly decreased the size of weanlings. Reproductive effort and the breeding success of individuals varied within breeding seasons, but time of breeding and litter manipulation did not interact to affect reproductive trade-offs. Our 3-yr field experiment revealed that litter enlargements also reduced survival and fecundity of mothers. Small mammals have be…

Evolutionary Conflict Between Maternal and Paternal Interests: Integration with Evolutionary Endocrinology

International audience; Conflict between mates, as well as conflict between parents and offspring are due to divergent evolutionary interests of the interacting individuals. Hormone systems provide genetically based proximate mechanisms for mediating phenotypic adaptation and maladaptation characteristic of evolutionary conflict between individuals. Testosterone (T) is among the most commonly studied hormones in evolutionary biology, and as such, its role in shaping sexually dimorphic behaviors and physiology is relatively well understood, but its role in evolutionary conflict is not as clear. In this review, we outline the genomic conflicts arising within the family unit, and incorporate m…

The joint emergence of group competition and within-group cooperation

Abstract Between-group conflict and within-group cooperation can be seen as two sides of the same coin, coevolving in a group-structured population. There is strong support for between-group competition facilitating the evolution of human cooperative tendencies, yet our understanding of how competition arises is less clear. We show that groups of randomly assembled individuals spontaneously engage in costly group competition, and that decisions promoting between-group conflict are associated with high levels of within-group cooperation. Remarkably, when groups were given the possibility to compete against other groups, net earnings for individuals were higher than when groups were not allow…

Additional file 12: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Measures of alpha diversity for the skin and gut microbiome of bank voles inhabiting areas that differ in levels of environmental radiation. Box-and-whisker plots represent the median and interquartile range of alpha diversity estimates (i.e. number of observed OTUs, Shannon index). Each point represent a single sample from contaminated (CH) and uncontaminated (CL) with radionuclides areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL), Ukraine. (PDF 39â kb)

HORMONAL MANIPULATION OF OFFSPRING NUMBER: MATERNAL EFFORT AND REPRODUCTIVE COSTS

We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade-off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body s…

Infanticide in the evolution of reproductive synchrony: effects on reproductive success.

Synchronous breeding in animals and plants has stimulated both a theoretical and empirical examination of the possible benefits of active synchronization. The selective pressures of predation and infanticide are the strongest candidates proposed to explain the evolution of reproductive synchrony. Alternatively, breeding asynchronously with conspecifics may ensure a greater availability of resources per breeder. However, the possible fitness benefits resulting from active asynchronization have not yet received attention in evolutionary ecology. Here we present a hypothesis, based on a graphical model, illustrating the costs and benefits of the two modes of reproduction. We tested the hypothe…

Maintenance costs of male dominance and sexually antagonistic selection in the wild

Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the corresponding effects of male energetics on his sisters recognized. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) antagonis…

Evolutionary constraints of warning signals : a genetic trade-off between the efficacy of larval and adult warning coloration can maintain variation in signal expression

To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11,000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic cor…

Intergenerational fitness effects of the early life environment in a wild rodent.

The early life environment can have profound, long-lasting effects on an individual's fitness. For example, early life quality might (a) positively associate with fitness (a silver spoon effect), (b) stimulate a predictive adaptive response (by adjusting the phenotype to the quality of the environment to maximize fitness) or (c) be obscured by subsequent plasticity. Potentially, the effects of the early life environment can persist beyond one generation, though the intergenerational plasticity on fitness traits of a subsequent generation is unclear. To study both intra- and intergenerational effects of the early life environment, we exposed a first generation of bank voles to two early life…

Balancing selection maintains polymorphisms at neurogenetic loci in field experiments

Most variation in behavior has a genetic basis, but the processes determining the level of diversity at behavioral loci are largely unknown for natural populations. Expression of arginine vasopressin receptor 1a (Avpr1a) and oxytocin receptor (Oxtr) in specific regions of the brain regulates diverse social and reproductive behaviors in mammals, including humans. That these genes have important fitness consequences and that natural populations contain extensive diversity at these loci implies the action of balancing selection. In Myodes glareolus, Avpr1a and Oxtr each contain a polymorphic microsatellite locus located in their 5′ regulatory region (the regulatory region-associated microsatel…

Sex–biased maternal investment in voles: importance of environmental conditions

Adaptive bias in sex allocation is traditionally proposed to be related to the condition of mothers as well as to the unequal fitness values of produced sexes. A positive relationship between mother condition and investment into male offspring is often predicted. This relationship was also recently found to depend on environmental conditions. We studied these causalities experimentally using a design where winter food supply was manipulated in eight outdoor-enclosed populations of field voles Microtus agrestis. At the beginning of the breeding season in spring, food-supplemented mothers seemed to be in a similar condition, measured as body mass, head width, body condition index and parasite…

A large panel of novel microsatellite markers for the bank vole (Myodes glareolus)

We describe a set of 66 highly polymorphic microsatellite loci isolated from the bank vole, Myodes (Clethrionomys) glareolus. These microsatellites were characterized for a long-term study on periodically fluctuating density of the bank vole population in Central Finland. We detected six to 38 alleles per locus in the population sampled at two different density phases, and the levels of observed and expected heterozygosities varied between 0.17 and 1.00, and between 0.72 and 0.95, respectively. This microsatellite panel serves as an informative tool for population and molecular genetic studies.

Maintenance of genetic diversity in cyclic populations-a longitudinal analysis inMyodes glareolus

Conspicuous cyclic changes in population density characterize many populations of small northern rodents. The extreme crashes in individual number are expected to reduce the amount of genetic variation within a population during the crash phases of the population cycle. By long-term monitoring of a bank vole (Myodes glareolus) population, we show that despite the substantial and repetitive crashes in the population size, high heterozygosity is maintained throughout the population cycle. The striking population density fluctuation in fact only slightly reduced the allelic richness of the population during the crash phases. Effective population sizes of vole populations remained also relative…

Skin and gut microbiomes of a wild mammal respond to different environmental cues

Background Animal skin and gut microbiomes are important components of host fitness. However, the processes that shape the microbiomes of wildlife are poorly understood, particularly with regard to exposure to environmental contaminants. We used 16S rRNA amplicon sequencing to quantify how exposure to radionuclides impacts the skin and gut microbiota of a small mammal, the bank vole Myodes glareolus, inhabiting areas within and outside the Chernobyl Exclusion Zone (CEZ), Ukraine. Results Skin microbiomes of male bank voles were more diverse than females. However, the most pronounced differences in skin microbiomes occurred at a larger spatial scale, with higher alpha diversity in the skin m…

Stabilizing selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

The loci arginine vasopressin receptor 1a ( avpr1a ) and oxytocin receptor ( oxtr ) have evolutionarily conserved roles in vertebrate social and sexual behaviour. Allelic variation at a microsatellite locus in the 5′ regulatory region of these genes is associated with fitness in the bank vole Myodes glareolus . Given the low frequency of long and short alleles at these microsatellite loci in wild bank voles, we used breeding trials to determine whether selection acts against long and short alleles. Female bank voles with intermediate length avpr1a alleles had the highest probability of breeding, while male voles whose avpr1a alleles were very different in length had reduced probability of …

Maintenance of genetic diversity in cyclic populations—a longitudinal analysis in Myodes glareolus

Conspicuous cyclic changes in population density characterize many populations of small northern rodents. The extreme crashes in individual number are expected to reduce the amount of genetic variation within a population during the crash phases of the population cycle. By long-term monitoring of a bank vole (Myodes glareolus) population, we show that despite the substantial and repetitive crashes in the population size, high heterozygosity is maintained throughout the population cycle. The striking population density fluctuation in fact only slightly reduced the allelic richness of the population during the crash phases. Effective population sizes of vole populations remained also relative…

Comparable response of wild rodent gut microbiome to anthropogenic habitat contamination

Abstract Species identity is thought to dominate over environment in shaping wild rodent gut microbiota, but it remains unknown whether the responses of host gut microbiota to shared anthropogenic habitat impacts are species-specific or if the general gut microbiota response is similar across host species. Here, we compare the influence of exposure to radionuclide contamination on the gut microbiota of four wild mouse species: Apodemus flavicollis, A. sylvaticus, A. speciosus and A. argenteus. Building on the evidence that radiation impacts bank vole (Myodes glareolus) gut microbiota, we hypothesized that radiation exposure has a general impact on rodent gut microbiota. Because we sampled (…

Sexual antagonism for testosterone maintains multiple mating behaviour

Summary 1. The persistence of multiple mating remains one of the fundamental questions in evolutionary biology. In theory, multiple mating is predicted to improve female fitness cumulatively through direct and ⁄ or genetic benefits. However, intra-locus sexual conflicts may potentially constrain or even eliminate these benefits owing to the gender load imposed by sexually antagonistic selection. 2. Here, we tested whether sexually antagonistic selection can maintain the variance in multiple mating behaviour of bank voles (Myodes glareolus) by manipulating the hormone testosterone through artificial selection in the laboratory. Among mammals, testosterone is a sexually dimorphic fitness-rela…

Addressing ecological effects of radiation on populations and ecosystems to improve protection of the environment against radiation: Agreed statements from a Consensus Symposium

AbstractThis paper reports the output of a consensus symposium organized by the International Union of Radioecology in November 2015. The symposium gathered an academically diverse group of 30 scientists to consider the still debated ecological impact of radiation on populations and ecosystems. Stimulated by the Chernobyl and Fukushima disasters' accidental contamination of the environment, there is increasing interest in developing environmental radiation protection frameworks. Scientific research conducted in a variety of laboratory and field settings has improved our knowledge of the effects of ionizing radiation on the environment. However, the results from such studies sometimes appear…

Cyclic hantavirus epidemics in humans--predicted by rodent host dynamics.

Wildlife-originated zoonotic diseases are a major contributor to emerging infectious diseases. Hantaviruses cause thousands of human disease cases annually worldwide, and understanding and predicting human hantavirus epidemics still poses unsolved challenges. Here we studied the three-level relationships between the human disease nephropathia epidemica (NE), its etiological agent Puumala hantavirus (PUUV) and the rodent host of the virus, the bank vole (Myodes glareolus). A large and long-term data set (14 years, 2583 human NE cases and 4751 trapped bank voles) indicates that the number of human infections shows both seasonal and multi-annual fluctuations, is influenced by the phase of vole…

A trade-off between current and future sex allocation revealed by maternal energy budget in a small mammal.

Sex-allocation theories generally assume differential fitness costs of raising sons and daughters. Yet, experimental confirmation of such costs is scarce and potential mechanisms are rarely addressed. While the most universal measure of physiological costs is energy expenditure, only one study has related the maternal energy budget to experimentally controlled offspring sex. Here, we experimentally test this in the bank vole (Myodes glareolus) by simultaneously manipulating the litter's size and sex ratio immediately after birth. Two weeks after manipulation, when mothers were at the peak of lactation and were pregnant with concurrent litters, we assessed their energy budget. We found that …

Addressing ecological effects of radiation on populations and ecosystems to improve protection of the environment against radiation : agreed statements from a Consensus Symposium

This paper reports the output of a consensus symposium organized by the International Union of Radioecology in November 2015. The symposium gathered an academically diverse group of 30 scientists to consider the still debated ecological impact of radiation on populations and ecosystems. Stimulated by the Chernobyl and Fukushima disasters' accidental contamination of the environment, there is increasing interest in developing environmental radiation protection frameworks. Scientific research conducted in a variety of laboratory and field settings has improved our knowledge of the effects of ionizing radiation on the environment. However, the results from such studies sometimes appear contrad…

Susceptibility to infection with Borrelia afzelii and TLR2 polymorphism in a wild reservoir host

AbstractThe study of polymorphic immune genes in host populations is critical for understanding genetic variation in susceptibility to pathogens. Controlled infection experiments are necessary to separate variation in the probability of exposure from genetic variation in susceptibility to infection, but such experiments are rare for wild vertebrate reservoir hosts and their zoonotic pathogens. The bank vole (Myodes glareolus) is an important reservoir host of Borrelia afzelii, a tick-borne spirochete that causes Lyme disease. Bank vole populations are polymorphic for Toll-like receptor 2 (TLR2), an innate immune receptor that recognizes bacterial lipoproteins. To test whether the TLR2 polym…

Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus.

Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show …

Introgression of mitochondrial DNA among Myodes voles: consequences for energetics?

Abstract Background Introgression of mitochondrial DNA (mtDNA) is among the most frequently described cases of reticulate evolution. The tendency of mtDNA to cross interspecific barriers is somewhat counter-intuitive considering the key function of enzymes that it encodes in the oxidative-phosphorylation process, which could give rise to hybrid dysfunction. How mtDNA reticulation affects the evolution of metabolic functions is, however, uncertain. Here we investigated how morpho-physiological traits vary in natural populations of a common rodent (the bank vole, Myodes glareolus) and whether this variation could be associated with mtDNA introgression. First, we confirmed that M. glareolus ha…

The origin of two cryptic species of African desert jerboas (Dipodidae: Jaculus)

The desert biota is exposed to extreme and variable conditions that shape its evolution and diversification processes. In this respect, the Jaculus jerboas have gained the attention of researchers as a result of their broad Saharan–Arabian distribution and their high and unexplained, morphological, anatomical, and molecular variation. In the present study, mitochondrial and nuclear genealogies where used to confirm monophyly of two cryptic species: Jaculus jaculus and Jaculus deserti. The reconstructed demography showed that the evolutionary histories of the species are markedly different and that the expansion into North-West Africa by J. deserti was more recent than that of J. jaculus. Th…

Ectoparasites, nest site choice and breeding success in the pied flycatcher

It has recently been suggested that nest box studies might bias the measurement of behavioural and life-history traits, because the removal of old nests may reduce the load of ectoparasites. This experimental artefact may have notable effects on nest site choice and breeding success in cavity-breeding birds. We tested (i) if pied flycatchers Ficedula hypoleuca prefer clean nest boxes and (ii) if old nest material affects the number of parasites and the breeding success of pied flycatchers. In the first experiment we offered birds one cleaned nest box and one nest box with old nest material from the previous year. The two nest boxes were placed in very similar sites near each other. In this …

Exposure to environmental radionuclides associates with tissue-specific impacts on telomerase expression and telomere length

International audience; Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus, collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides,…

Reproductive costs and litter size in the bank vole.

The potential reproductive costs for free-ranging bank vole (Clethrionomys glareolus) offspring and mothers were assessed by manipulating litter size and by determining the effects of nursing varied numbers of offspring. Litter enlargement did not increase the number of weanlings per mother. The mass of juveniles was significantly lower in the enlarged litters and higher in the reduced litters, compared to the control group. However, the survival of juveniles from weaning aged three months did not depend on their mass at weaning. Data from a previous study (Mappes et al. 1995) indicated that a higher mass at weaning may increase juveniles' abilities to maturate and breed during their summer…

Chronic Background Radiation Correlates With Sperm Swimming Endurance in Bank Voles From Chernobyl

Sperm quantity and quality are key features explaining intra- and interspecific variation in male reproductive success. Spermatogenesis is sensitive to ionizing radiation and laboratory studies investigating acute effects of ionizing radiation have indeed found negative effects of radiation on sperm quantity and quality. In nature, levels of natural background radiation vary dramatically, and chronic effects of low-level background radiation exposure on spermatogenesis are poorly understood. The Chernobyl region offers a unique research opportunity for investigating effects of chronic low-level ionizing radiation on reproductive properties of wild organisms. We captured male bank voles (Myo…

Optimal allocation of reproductive effort: manipulation of offspring number and size in the bank vole

The number of offspring attaining reproductive age is an important measure of an individual's fitness. However, reproductive success is generally constrained by a trade-off between offspring number and quality. We conducted a factorial experiment in order to study the effects of an artificial enlargement of offspring number and size on the reproductive success of female bank voles (Clethrionomys glareolus). We also studied the effects of the manipulations on growth, survival and reproductive success of the offspring. Potentially confounding effects of varying maternal quality were avoided by cross-fostering. Our results showed that the number of offspring alive in the next breeding season w…

The effects of Borrelia infection on its wintering rodent host

AbstractIn seasonal environments, appropriate adaptations are crucial for organisms to maximize their fitness. For instance, in many species, the immune function has been noticed to decrease during winter, which is assumed to be an adaptation to the season’s limited food availability. Consequences of an infection on the health and survival of the host organism could thus be more severe in winter than in summer. Here, we experimentally investigated the effect of a zoonotic, endemic pathogen, Borrelia afzelii infection on the survival and body condition in its host, the bank vole (Myodes glareolus), during late autumn–early winter under semi-natural field conditions in 11 large outdoor enclos…

Fibroblasts from bank voles inhabiting Chernobyl have increased resistance against oxidative and DNA stresses

Background Elevated levels of environmental ionizing radiation can be a selective pressure for wildlife by producing reactive oxygen species and DNA damage. However, the underlying molecular mechanisms that are affected are not known. Results We isolated skin fibroblasts from bank voles (Myodes glareolus) inhabiting the Chernobyl nuclear power plant accident site where background radiation levels are about 100 times greater than in uncontaminated areas. After a 10 Gy dose of gamma radiation fibroblasts from Chernobyl animals recovered faster than fibroblasts isolated from bank voles living in uncontaminated control area. The Chernobyl fibroblasts were able to sustain significantly higher do…

Exposure to environmental radionuclides alters mitochondrial DNA maintenance in a wild rodent

AbstractMitochondria are sensitive to oxidative stress, including that derived from ionizing radiation. To quantify the effects of exposure to environmental radionuclides on mitochondrial DNA (mtDNA) dynamics in wildlife, bank voles (Myodes glareolus) were collected from the chernobyl exclusion zone (CEZ), where animals are exposed to elevated levels of radionuclides, and from uncontaminated areas within the CEZ and elsewhere in Ukraine. Brains of bank voles from outside the CEZ were characterized by low mtDNA copy number and low mtDNA damage; by contrast, bank voles within the CEZ had high mtDNA copy number and high mtDNA damage, consistent with putative damaging effects of elevated radiat…

Two hundred and fifty-four metagenome-assembled bacterial genomes from the bank vole gut microbiota.

Abstract Vertebrate gut microbiota provide many essential services to their host. To better understand the diversity of such services provided by gut microbiota in wild rodents, we assembled metagenome shotgun sequence data from a small mammal, the bank vole Myodes glareolus (Rodentia, Cricetidae). We were able to identify 254 metagenome assembled genomes (MAGs) that were at least 50% ( n  = 133 MAGs), 80% ( n  = 77 MAGs) or 95% ( n  = 44 MAGs) complete. As typical for a rodent gut microbiota, these MAGs are dominated by taxa assigned to the phyla Bacteroidetes ( n  = 132 MAGs) and Firmicutes ( n  = 80), with some Spirochaetes ( n  = 15) and Proteobacteria ( n  = 11). Based on coverage over…

Maternal investment in relation to sex ratio and offspring number in a small mammal - a case for Trivers and Willard theory?

Summary 1. Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment. 2. We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus, by manipulating both the postnatal sex ratio (all-male ⁄ all-female litters) and the quality of rearing environment (through manipulation of litter size by )2 ⁄ +2 pups) of their offspring in a laboratory setting. 3. We found that mothers clearly biased their allocation to female ra…

Temporal dynamics of the tick Ixodes ricinus in northern Europe : epidemiological implications

Background Tick-borne pathogens pose an increasing threat to human and veterinary health across the northern hemisphere. While the seasonal activity of ticks is largely determined by climatic conditions, host-population dynamics are also likely to affect tick abundance. Consequently, abundance fluctuations of rodents in northern Europe are expected to be translated into tick dynamics, and can hence potentially affect the circulation of tick-borne pathogens. We quantified and explained the temporal dynamics of the tick Ixodes ricinus in the northernmost part of its European geographical range, by estimating (i) abundance in vegetation and (ii) infestation load in the most common rodent speci…

Additional file 1 of Evolutionary history of two cryptic species of northern African jerboas

Additional file 1: Microsatellite optimization. Supplementary Tables and Figures.

THE COST OF REPRODUCTION INDUCED BY BODY SIZE AT BIRTH AND BREEDING DENSITY

Body size at birth has implications for the quality of individuals throughout their life. Although large body size is generally considered an advantage, the relationship between body size at birth and long-term fitness is often complicated. Under spatial or temporal variation in environmental conditions, such as the seasonally changing densities of Fennoscandian vole populations, selection should favor variation in offspring phenotypes, as different qualities may be beneficial in different conditions. We performed an experiment in which a novel hormonal manipulation method was used to increase phenotypic variance in body size at birth in the bank vole (Myodes glareolus). The effects of body…

Intralocus sexual conflict for fitness: sexually antagonistic alleles for testosterone

Intralocus sexual conflict occurs when a trait encoded by the same genetic locus in the two sexes has different optima in males and females. Such conflict is widespread across taxa, however, the shared phenotypic traits that mediate the conflict are largely unknown. We examined whether the sex hormone, testosterone (T), that controls sexual differentiation, contributes to sexually antagonistic fitness variation in the bank vole, Myodes glareolus . We compared (opposite-sex) sibling reproductive fitness in the bank vole after creating divergent selection lines for T. This study shows that selection for T was differentially associated with son versus daughter reproductive success, causing a …

Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent

Wildlife inhabiting environments contaminated by radionuclides face putative detrimental effects of exposure to ionizing radiation, with biomarkers such as an increase in DNA damage and/or oxidative stress commonly associated with radiation exposure. To examine the effects of exposure to radiation on gene expression in wildlife, we conducted a de novo RNA sequencing study of liver and spleen tissues from a rodent, the bank vole Myodes glareolus. Bank voles were collected from the Chernobyl Exclusion Zone (CEZ), where animals were exposed to elevated levels of radionuclides, and from uncontaminated areas near Kyiv, Ukraine. Counter to expectations, we did not observe a strong DNA damage resp…

Applying the Anna Karenina principle for wild animal gut microbiota : temporal stability of the bank vole gut microbiota in a disturbed environment

Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (i) temporally stable and (ii) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mar…

Chronic Background Radiation Correlates With Sperm Swimming Endurance in Bank Voles From Chernobyl

Sperm quantity and quality are key features explaining intra- and interspecific variation in male reproductive success. Spermatogenesis is sensitive to ionizing radiation and laboratory studies investigating acute effects of ionizing radiation have indeed found negative effects of radiation on sperm quantity and quality. In nature, levels of natural background radiation vary dramatically, and chronic effects of low-level background radiation exposure on spermatogenesis are poorly understood. The Chernobyl region offers a unique research opportunity for investigating effects of chronic low-level ionizing radiation on reproductive properties of wild organisms. We captured male bank voles (Myo…

On the evolutionary stability of female infanticide

Territoriality among female rodents may have evolved as an adaptation to intraspecific competition for resources or, alternatively, to defend pups against infanticide. In order to evaluate the latter, we analyse the conditions that allow an infanticidal strategy to invade a population of non-infanticidal females, and the circumstances under which infanticide may become an evolutionarily stable strategy (ESS). Our game theoretical analyses indicate that infanticide has to be associated with some direct (cannibalism) or indirect (reduced competition) resource benefits in order to invade a non-infanticidal population. We also expect that females will primarily kill litters of nearby neighbors,…

Density-dependent vole damage in silviculture and associated economic losses at a nationwide scale

Voles inflict damage to silviculture by debarking or severing tree seedlings. The large-scale impacts of vole damage to silviculture, both in terms of severity and financial losses are, however, poorly known. In autumn 2005, cyclically fluctuating vole populations were at their highest in Finland for over 15 years, which led to extensive damage to silviculture during the winter 2005/06. We carried out a nationwide assessment of the incidence, spatial extent and economic value of damage and its relation to vole abundance in privately owned forests during this winter. Damage data were obtained with a questionnaire addressed to the directors of all Forest Management Associations (FMAs) operati…

Additional file 2: of Fibroblasts from bank voles inhabiting Chernobyl have increased resistance against oxidative and DNA stresses

The repair efficiency of nicked, oxidized, or linear plasmids is similar in control and Chernobyl bank vole fibroblasts. For host-cell reactivation assay, 5000 cells were plated on 96 well plate, treated next day with 20 μM etoposide for 8 hours, and then transfected with pGL3 (Promega) plasmid treated either with Nb.BsmI that nicked the plasmid coding sequence three times, with HindIII that linearized the plasmid after promoter sequence, or with 50 μM FeSO4 and 1 mM H2O2, which created oxidative damage on the plasmid. To control transfection efficiency cells were transfected also with pNL1.1 nano-luc vector. Luciferase expression was analysed 24 h after transfection with Nano-Glo Dual-Luci…

Different demography of friends and strangers: an experiment on the impact of kinship and familiarity in Clethrionomys glareolus.

We examined demographic effects of familiarity and relatedness in the bank vole Clethrionomys glareolus (Schreber) in four 0.5-ha enclosures in Central Finland. In two enclosures were mature voles which had overwintered together and some of their mature off-spring (hereafter referred to as “Friends”), and in the other two individuals of the same species captured from different localities near the study area (“Strangers”). The experiment lasted from June to September. The populations of Friends reached densities twice as high as those of Strangers with a significantly higher rate of recruitment and survival of the young. This may have been due to mutual familiarity decreasing antagonism towa…

Intracerebral Borna Disease Virus Infection of Bank Voles Leading to Peripheral Spread and Reverse Transcription of Viral RNA

Bornaviruses, which chronically infect many species, can cause severe neurological diseases in some animal species; their association with human neuropsychiatric disorders is, however, debatable. The epidemiology of Borna disease virus (BDV), as for other members of the family Bornaviridae, is largely unknown, although evidence exists for a reservoir in small mammals, for example bank voles (Myodes glareolus). In addition to the current exogenous infections and despite the fact that bornaviruses have an RNA genome, bornavirus sequences integrated into the genomes of several vertebrates millions of years ago. Our hypothesis is that the bank vole, a common wild rodent species in traditional B…

ESM for Watts et al. Stabilising selection on microsatellite allele length from Stabilizing selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

Details of model selection procedure (Supplementary Tables 1, 2) and analyses of effect of microsatellite allele length on litter size (Supplementary Methods, Results, Supplementary Table 3).

Eimeria-parasites are associated with a lowered mother's and offspring's body condition in island and mainland populations of the bank vole.

This study, based on correlative data, tests the hypothesis that infections withEimeriaspp. parasites exert a significant loss of fitness of bank voles (Clethrionomys glareolus) reflected in lower reproductive success and survival, declining host population densities and are associated positively with population size. The study was conducted in 20 mainland and 27 island populations in central Finland during May–September in 1999. Faecal samples showed that 28% of 767 individuals were infected withEimeriaspp. The presence ofEimeriaparasites was higher in dense mainland populations than in sparsely populated islands. Eimerian infections increased during the course of the breeding season, prob…

Food provisioning alters infection dynamics in populations of a wild rodent

While pathogens are often assumed to limit the growth of wildlife populations, experimental evidence for their effects is rare. A lack of food resources has been suggested to enhance the negative effects of pathogen infection on host populations, but this theory has received little investigation. We conducted a replicated two-factor enclosure experiment, with introduction of the bacteriumBordetella bronchisepticaand food supplementation, to evaluate the individual and interactive effects of pathogen infection and food availability on vole populations during a boreal winter. We show that prior to bacteria introduction, vole populations were limited by food availability.Bordetella bronchisept…

Description of research methods and results tables from Food limitation constrains host immune responses to nematode infections

Trade-offs in the allocation of finite-energy resources among immunological defences and other physiological processes are believed to influence infection risk and disease severity in food-limited wildlife populations. However, this prediction has received little experimental investigation. Here we test the hypothesis that food limitation impairs the ability of wild field voles (Microtus agrestis) to mount an immune response against parasite infections. We conducted a replicated experiment on vole populations maintained in large outdoor enclosures during boreal winter, using food supplementation and anthelmintic treatment of intestinal nematodes. Innate immune responses against intestinal p…

Interpretation of gut microbiota data in the ‘eye of the beholder’: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’

1.Evidence that exposure to environmental pollutants can alter the gut microbiota composition of wildlife includes studies of rodents exposed to radionuclides. 2.Antwis et al. (2021) used amplicon sequencing to characterise the gut microbiota of four species of rodent (Myodes glareolus, Apodemus agrarius, A. flavicollis and A. sylvaticus) inhabiting the Chernobyl Exclusion Zone (CEZ) to examine possible changes in gut bacteria (microbiota) and gut fungi (mycobiota) associated with exposure to radionuclides and whether the sample type (from caecum or faeces) affected the analysis. 3.The conclusions derived from the analyses of gut mycobiota are based on data that represent a mixture of inges…

Environmental radiation alters the gut microbiome of the bank vole Myodes glareolus.

International audience; Gut microbiota composition depends on many factors, although the impact of environmental pollution is largely unknown. We used amplicon sequencing of bacterial 16S rRNA genes to quantify whether anthropogenic radionuclides at Chernobyl (Ukraine) impact the gut microbiome of the bank vole Myodes glareolus. Exposure to elevated levels of environmental radionuclides had no detectable effect on the gut community richness but was associated with an almost twofold increase in the Firmicutes:Bacteroidetes ratio. Animals inhabiting uncontaminated areas had remarkably similar gut communities irrespective of their proximity to the nuclear power plant. Hence, samples could be c…

Additional file 13: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Community dissimilarity between gut and skin microbiomes within each replicate site. Box-and-whisker plots represent the median and interquartile range of Bray-Curtis distance between samples. Each box plot represent contaminated (CH1-3) and uncontaminated (CL1-2) with radionuclides study areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL1-2), Ukraine. (PDF 43â kb)

Experimental manipulation of breeding density and litter size: effects on reproductive success in the bank vole

1. Reproductive success of individual females may be determined by density-dependent effects, especially in species where territory provides the resources for a reproducing female and territory size is inversely density-dependent. 2. We manipulated simultaneously the reproductive effort (litter size manipulation: ± 0 and + 2 pups) and breeding density (low and high) of nursing female bank voles Clethrionomys glareolus in outdoor enclosures. We studied whether the reproductive success (number and quality of offspring) of individual females is density-dependent, and whether females can compensate for increased reproductive effort when not limited by saturated breeding density. 3. The females …

Food resources and intestinal parasites as limiting factors for boreal vole populations during winter

Processes limiting the growth of cyclic vole populations have stimulated considerable research and debate over several decades. In Fennoscandia, the peak density of cyclic vole populations occurs in fall, and is followed by a severe winter decline. Food availability and intestinal parasites have been demonstrated to independently and synergistically limit wildlife populations. The purpose of this study was to directly compare competing food and parasite hypotheses on the limitation of overwintering high-density vole populations. Moreover, we evaluated the ability of food limitation and nematode infection to interact and thereby intensify population declines. A two-factor experiment with foo…

Maternal investment in relation to sex ratio and offspring number in a small mammal – a case for Trivers and Willard theory?

1. Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment. 2. We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus, by manipulating both the postnatal sex ratio (all-male/all-female litters) and the quality of rearing environment (through manipulation of litter size by -2/+2 pups) of their offspring in a laboratory setting. 3. We found that mothers clearly biased their allocation to female rather than ma…

Testosterone-Mediated Effects on Fitness-Related Phenotypic Traits and Fitness

International audience; The physiological and behavioral mechanisms underlying life-history trade-offs are a continued source of debate. Testosterone (T) is one physiological factor proposed to mediate the trade-off between reproduction and survival. We use phenotypic engineering and multiple laboratory and field fitness-related phenotypic traits to test the effects of elevated T between two bank vole Myodes glareolus groups: dominant and subordinate males. Males with naturally high T levels showed higher social status (laboratory dominance) and mobility (distance between capture sites) than low-T males, and the effect of T on immune response was also T group specific, suggesting that behav…

Early life of fathers affects offspring fitness in a wild rodent

Intergenerational fitness effects on offspring due to the early life of the parent are well studied from the standpoint of the maternal environment, but intergenerational effects owing to the paternal early life environment are often overlooked. Nonetheless, recent laboratory studies in mammals and ecologically relevant studies in invertebrates predict that paternal effects can have a major impact on the offspring's phenotype. These non‐genetic, environment‐dependent paternal effects provide a mechanism for fathers to transmit environmental information to their offspring, and could allow rapid adaptation. We used the bank vole Myodes glareolus, a wild rodent species with no paternal care, t…

cayol_texte_tables_figures_ESM from Borrelia afzelii alters reproductive success in a rodent host

Supplementary material from "Borrelia afzelii alters reproductive success in a rodent host". Detailed material and methods, supplementary tables, figures and results.

GENETIC BASIS OF THE TRADE-OFF BETWEEN OFFSPRING NUMBER AND QUALITY IN THE BANK VOLE

One of the main tenets of modern life-history theory is the negative relationship (trade-off) between the number and quality of offspring produced. Theory predicts a negative genetic correlation between these traits since both are closely related to fitness of individuals. However, the genetic basis of the trade-off has only been tested to a limited extent in natural populations. We examined whether size and quality of offspring are negatively related to litter size in the bank vole Clethrionomys glareolus. First, we found a significant negative phenotypic correlation between the number and size of offspring at birth in both laboratory and field populations of the bank vole. Second, a large…

Interactive effects of past and present environments on overwintering success-a reciprocal transplant experiment

Life-history traits are influenced by environmental factors throughout the lifespan of an individual. The relative importance of past versus present environment on individual fitness, therefore, is a relevant question in populations that face the challenge of temporally varying environment. We studied the interacting effects of past and present density on body mass, condition, and survival in enclosure populations of the bank vole (Myodes glareolus) using a reciprocal transplant design. In connection with the cyclic dynamics of natural vole populations, our hypothesis was that individuals born in low-density enclosures would do better overwintering in low-density enclosures than in high-den…

First Report of Anaplasma phagocytophilum and Babesia microti in Rodents in Finland

Tick-borne diseases pose an increasingly important public health problem in Europe. Rodents are the reservoir host for many tick-transmitted pathogens, including Anaplasma phagocytophilum and Babesia microti, which can cause human granulocytic anaplasmosis and babesiosis, respectively. To estimate the presence of these pathogens in rodents in Finland, we examined blood samples from 151 bank voles (Myodes glareolus) and demonstrate, for the first time, that A. phagocytophilum and B. microti commonly infect bank voles (in 22% and 40% of animals, respectively) in Finland. Sequence analysis of a fragment of 18S rRNA showed that the B. microti strain isolated was identical to the Munich strain, …

Ecological mechanisms can modify radiation effects in a key forest mammal of Chernobyl

International audience; Nuclear accidents underpin the need to quantify the ecological mechanisms which determine injury to ecosystems from chronic low-dose radiation. Here, we tested the hypothesis that ecological mechanisms interact with ionizing radiation to affect natural populations in unexpected ways. We used large-scale replicated experiments and food manipulations in wild populations of the rodent, Myodes glareolus, inhabiting the region near the site of the Chernobyl disaster of 1986. We show linear decreases in breeding success with increasing ambient radiation levels with no evidence of any threshold below which effects are not seen. Food supplementation of experimental populatio…

Distinct bhaplotype structure at the innate immune receptor Toll-like receptor 2 across bank vole populations and lineages in Europe

Abstract: Parasite-mediated selection may contribute to the maintenance of genetic variation at host immune genes over long time scales. To date, the best evidence for the long-term maintenance of immunogenetic variation in natural populations comes from studies on the major histocompatibility complex (MHC) genes, whereas evidence for such processes from other immune genes remains scarce. In the present study, we show that, despite pronounced population differentiation and the occurrence of numerous private alleles within populations, the innate immune gene Toll-like receptor 2 (TLR2) displays a distinct haplotype structure in 21 bank vole (Myodes glareolus) populations across Europe. Haplo…

Infection Load and Prevalence of Novel Viruses Identified from the Bank Vole Do Not Associate with Exposure to Environmental Radioactivity

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-asso…

Can number and size of offspring increase simultaneously?--a central life-history trade-off reconsidered.

Abstract Background To maximize their fitness, parents are assumed to allocate their resources optimally between number and size of offspring. Although this fundamental life-history trade-off has been subject to long standing interest, its genetic basis, especially in wild mammals, still remains unresolved. One important reason for this problem is that a large multigenerational pedigree is required to conduct a reliable analysis of this trade-off. Results We used the REML-animal model to estimate genetic parameters for litter size and individual birth size for a common Palearctic small mammal, the bank vole (Myodes glareolus). Even though a phenotypic trade-off between offspring number and …

Intergenerational fitness effects of the early life environment in a wild rodent

The early life environment can have profound, long‐lasting effects on an individual's fitness. For example, early life quality might (a) positively associate with fitness (a silver spoon effect), (b) stimulate a predictive adaptive response (by adjusting the phenotype to the quality of the environment to maximize fitness) or (c) be obscured by subsequent plasticity. Potentially, the effects of the early life environment can persist beyond one generation, though the intergenerational plasticity on fitness traits of a subsequent generation is unclear. To study both intra‐ and intergenerational effects of the early life environment, we exposed a first generation of bank voles to two early life…

Younger bank voles are more vulnerable to avian predation

The importance of predation on prey populations is mainly determined by the number of eaten prey. However, the total impact of predation might also be determined by the selection of certain prey individuals, e.g., different sexes or age categories. Here we tested selective predation by an avian predator, the pygmy owl ( Glaucidium passerinum (L., 1758)), on bank voles ( Myodes ( Clethrionomys ) glareolus (Schreber, 1780)). We compared the sex, age, and mass of hoarded prey with the animals snap-trapped from the field. There were no differences in the sex ratio between hoarded bank voles and those available in the field. However, hoarded voles were significantly younger than ones in the fie…

Advantage of rare infanticide strategies in an invasion experiment of behavioural polymorphism

Killing conspecific infants (infanticide) is among the most puzzling phenomena in nature. Stable polymorphism in such behaviour could be maintained by negative frequency-dependent selection (benefit of rare types). However, it is currently unknown whether there is genetic polymorphism in infanticidal behaviour or whether infanticide may have any fitness advantages when rare. Here we show genetic polymorphism in non-parental infanticide. Our novel invasion experiment confirms negative frequency-dependent selection in wild bank vole populations, where resource benefits allow an infanticidal strategy to invade a population of non-infanticidal individuals. The results show that infanticidal beh…

Age-related effects of chronic hantavirus infection on female host fecundity.

1. Pathogens often cause detrimental effects to their hosts and, consequently, may influence host population dynamics that may, in turn, feed back to pathogen transmission dynamics. Understanding fitness effects of pathogens upon animal host populations can help to predict the risks that zoonotic pathogens pose to humans. 2. Here we determine whether chronic infection by Puumala hantavirus (PUUV) affects important fitness-related traits, namely the probability of breeding, reproductive effort and mother and offspring condition, in the bank vole (Myodes glareolus). Using 9 years empirical data in a PUUV endemic area in Central Finland, we found differences between reproductive characteristic…

Low-level environmental metal pollution is associated with altered gut microbiota of a wild rodent, the bank vole (Myodes glareolus)

Mining and related industries are a major source of metal pollution. In contrast to the well-studied effects of ex-posure to metals on animal physiology and health, the impacts of environmental metal pollution on the gut mi-crobiota of wild animals are virtually unknown. As the gut microbiota is a key component of host health, it is important to understand whether metal pollution can alter wild animal gut microbiota composition. Using a combination of 16S rRNA amplicon sequencing and quantification of metal levels in kidneys, we assessed whether multi-metal exposure (the sum of normalized levels of fifteen metals) was associated with changes in gut microbiota of wild bank voles (Myodes glar…

Additional file 1: Figure S1. of Temporal dynamics of the tick Ixodes ricinus in northern Europe: epidemiological implications

Average monthly saturation deficit and temperature during the monitoring years. Figure S2. Observed mean abundance of ticks in vegetation per session, from May 2012 to October 2015. Figure S3. Mean number of vole captured per trap-night at each session and in each site, from May 2012 to October 2015. Table S1. Selection table for models explaining the abundance of ticks questing in the vegetation. Figure S4. Predicted number of larvae, nymphs and pooled nymphs and females per 100Â m2 of vegetation explained by bank vole abundance. Table S2. Selection table for models explaining the abundance of ticks questing in the vegetation. Table S3. Total number of ticks (per species and stage) collect…

Applying the Anna Karenina principle for wild animal gut microbiota: Temporal stability of the bank vole gut microbiota in a disturbed environment.

Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (a) temporally stable and (b) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mark…

Early life of fathers affects offspring fitness in a wild rodent.

Intergenerational fitness effects on offspring due to the early life of the parent are well studied from the standpoint of the maternal environment, but intergenerational effects owing to the paternal early life environment are often overlooked. Nonetheless, recent laboratory studies in mammals and ecologically relevant studies in invertebrates predict that paternal effects can have a major impact on the offspring's phenotype. These nongenetic, environment-dependent paternal effects provide a mechanism for fathers to transmit environmental information to their offspring and could allow rapid adaptation. We used the bank vole Myodes glareolus, a wild rodent species with no paternal care, to …

Evolved high aerobic capacity has context-specific effects on gut microbiota

Publisher Copyright: Copyright © 2022 Hanhimäki, Watts, Koskela, Koteja, Mappes and Hämäläinen. Gut microbiota is expected to coevolve with the host's physiology and may play a role in adjusting the host's energy metabolism to suit the host's environment. To evaluate the effects of both evolved host metabolism and the environmental context in shaping the gut microbiota, we used a unique combination of (1) experimental evolution to create selection lines for a fast metabolism and (2) a laboratory-to-field translocation study. Mature bank voles Myodes glareolus from lines selected for high aerobic capacity (A lines) and from unselected control (C lines) were released into large (0.2 ha) outdo…

SIGNAL RELIABILITY COMPROMISED BY GENOTYPE-BY-ENVIRONMENT INTERACTION AND POTENTIAL MECHANISMS FOR ITS PRESERVATION

Sexual selection based on signaling requires that signals used by females in mate choice are reliable indicators of a male's heritable total fitness. A signal and the preference for it are expected to be heritable, resulting in the maintenance of genetic covariance between these two traits. However, a recent article has proposed that signals may quickly become unreliable in the presence of both environmental variation and genotype-by-environment interaction (G x E) with crossing reaction norms, potentially compromising the mechanisms of sexual selection. Here we examine the heritability and plasticity of a male dominance advertisement in the bank vole, Clethrionomys glareolus, in stable and…

Low-level environmental metal pollution is associated with altered gut microbiota of a wild rodent, the bank vole (Myodes glareolus)

Mining and related industries are a major source of metal pollution. In contrast to the well-studied effects of exposure to metals on animal physiology and health, the impacts of environmental metal pollution on the gut microbiota of wild animals are virtually unknown. As the gut microbiota is a key component of host health, it is important to understand whether metal pollution can alter wild animal gut microbiota composition. Using a combination of 16S rRNA amplicon sequencing and quantification of metal levels in kidneys, we assessed whether multi-metal exposure (the sum of normalized levels of fifteen metals) was associated with changes in gut microbiota of wild bank voles (Myodes glareo…

Intra‐ and Intersexual Trade‐Offs between Testosterone and Immune System: Implications for Sexual and Sexually Antagonistic Selection

International audience; Parasites indirectly affect life-history evolution of most species. Combating parasites requires costly immune defenses that are assumed to trade off with other life-history traits. In vertebrate males, immune defense is thought to trade off with reproductive success, as androgens enhancing sexual signaling can suppress immunity. The phenotypic relationship between male androgen levels and immune function has been addressed in many experimental studies. However, these do not provide information on either intra- or intersex genetic correlations, necessary for understanding sexual and sexually antagonistic selection theories. We measured male and female humoral antibod…

Additional file 9: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Differences in bank vole skin microbiome beta diversity associated with environmental radiation exposure. PCoA on unweighted UniFrac distances between bank vole skin microbiome profiles among the three study areas that differ in levels of environmental radioactivity are shown along the first two PC axes. Each point represents a single sample, shape indicate host sex, coloured according to study area: CH, red (n = 64); CL, blue (n = 44); KL, green (n = 43). Ellipses represent a 95% CI around the cluster centroid. (PDF 12 kb)

FITNESS TRADE-OFFS MEDIATED BY IMMUNOSUPPRESSION COSTS IN A SMALL MAMMAL

International audience; Trade-offs are widespread between life-history traits, such as reproduction and survival. However, their underlying physiological and behavioral mechanisms are less clear. One proposed physiological factor involves the trade-off between investment in male reproductive effort and immunity. Based on this hypothesis, we investigated differences in fitness between artificially selected immune response bank vole groups, Myodes glareolus. Significant heritability of immune response was found and a correlated response in testosterone levels to selection on immune function. Male reproductive effort, reproductive success, and survival of first generation offspring were assess…

Maintenance costs of male dominance and sexually antagonistic selection in the wild

Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the corresponding effects of male energetics on his sisters recognized. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) antagonis…

Food limitation constrains host immune responses to nematode infections.

Trade-offs in the allocation of finite-energy resources among immunological defences and other physiological processes are believed to influence infection risk and disease severity in food-limited wildlife populations. However, this prediction has received little experimental investigation. Here we test the hypothesis that food limitation impairs the ability of wild field voles ( Microtus agrestis ) to mount an immune response against parasite infections. We conducted a replicated experiment on vole populations maintained in large outdoor enclosures during boreal winter, using food supplementation and anthelmintic treatment of intestinal nematodes. Innate immune responses against intestina…

Artificial selection for predatory behaviour results in dietary niche differentiation in an omnivorous mammal

The diet of an individual is a result of the availability of dietary items and the individual's foraging skills and preferences. Behavioural differences may thus influence diet variation, but the evolvability of diet choice through behavioural evolution has not been studied. We used experimental evolution combined with a field enclosure experiment to test whether behavioural selection leads to dietary divergence. We analysed the individual dietary niche via stable isotope ratios of nitrogen ( δ 15 N) and carbon ( δ 13 C) in the hair of an omnivorous mammal, the bank vole, from four lines selected for predatory behaviour and four unselected control lines. Predatory voles had higher hair δ 1…

On personality, energy metabolism and mtDNA introgression in bank voles

Consistent interindividual differences in behaviour, or animal personality, are emerging as an important determinant of a wide range of life history traits and fitness. Individual behaviour, however, may be constrained by between-individual variability in energy metabolism and may become unstable owing to intrinsic and extrinsic stressors. Here we tested the relationship between personality and physiology using wild-caught bank voles, Myodes glareolus, that varied according to mtDNA type (original or introgressed from Myodes rutilus). Personality traits and their within-individual consistency were assessed using an open field test and basal metabolic rate (BMR) was measured in an open-flow …

Between-group competition and human cooperation.

A distinctive feature of human behaviour is the widespread occurrence of cooperation among unrelated individuals. Explaining the maintenance of costly within-group cooperation is a challenge because the incentive to free ride on the efforts of other group members is expected to lead to decay of cooperation. However, the costs of cooperation can be diminished or overcome when there is competition at a higher level of organizational hierarchy. Here we show that competition between groups resolves the paradigmatic ‘public goods’ social dilemma and increases within-group cooperation and overall productivity. Further, group competition intensifies the moral emotions of anger and guilt associated…

Additional file 13: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Community dissimilarity between gut and skin microbiomes within each replicate site. Box-and-whisker plots represent the median and interquartile range of Bray-Curtis distance between samples. Each box plot represent contaminated (CH1-3) and uncontaminated (CL1-2) with radionuclides study areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL1-2), Ukraine. (PDF 43â kb)

Does risk of predation by mammalian predators affect the spacing behaviour of rodents? Two large-scale experiments.

Predator-prey interactions between small mammals and their avian and mammalian predators have attracted much attention. However, large-scale field experiments examining small-mammal antipredatory responses under the risk of predation by mammals are rare. As recently pointed out, the scale of experiments may cause misleading results in studies of decision-making under predation risk. We studied the effect of small mustelid predators on the spacing behaviour of the gray-tailed vole (Microtus canicaudus) and the bank vole (Clethrionomys glareolus) in two separate field enclosure experiments. The experiments were conducted during the breeding season in North America and northern Europe, where s…

Ionizing radiation from Chernobyl affects development of wild carrot plants.

AbstractRadioactivity released from disasters like Chernobyl and Fukushima is a global hazard and a threat to exposed biota. To minimize the deleterious effects of stressors organisms adopt various strategies. Plants, for example, may delay germination or stay dormant during stressful periods. However, an intense stress may halt germination or heavily affect various developmental stages and select for life history changes. Here, we test for the consequence of exposure to ionizing radiation on plant development. We conducted a common garden experiment in an uncontaminated greenhouse using 660 seeds originating from 33 wild carrots (Daucus carota) collected near the Chernobyl nuclear power pl…

Large Spatial Scale of the Phenotype-Environment Color Matching in Two Cryptic Species of African Desert Jerboas (Dipodidae: Jaculus)

We tested the camouflage hypothesis, or the linkage between animal (Saharan rodent) and habitat coloration, on the largest geographical scale yet conducted. We aimed to determine whether phenotypic variation is explained by micro-habitat variation and/or genetic polymorphism to determine 1) the strength of linkage between fur color and local substrate color, and 2) the divergence in fur coloration between two genetic clades, representing cryptic species, throughout the complete range of the African desert jerboas (Jaculus jaculus). We used a combination of museum and field-collected specimens, remote sensing tools, satellite and digital photography and molecular genetic and phylogenetic met…

Analysis of heteroplasmy in bank voles inhabiting the Chernobyl exclusion zone : A commentary on Baker et al. (2017) "Elevated mitochondrial genome variation after 50 generations of radiation exposure in a wild rodent."

Evolutionary history of two cryptic species of northern African jerboas

Abstract Background: Climatic variation and geologic change both play significant roles in shaping species distributions, thus affecting their evolutionary history. In Sahara-Sahel, climatic oscillations shifted the desert extent during the Pliocene-Pleistocene interval, triggering the diversification of several species. Here, we investigated how these biogeographical and ecological events have shaped patterns of genetic diversity and divergence in African Jerboas, desert specialist rodents. We focused on two sister and cryptic species, Jaculus jaculus and J. hirtipes, where we (1) evaluated their genetic differentiation, (2) reconstructed their evolutionary and demographic history; (3) tes…

Quantitative measure of sexual selection with respect to the operational sex ratio: a comparison of selection indices

Despite numerous indices proposed to predict the evolution of mating systems, a unified measure of sexual selection has remained elusive. Three previous studies have compared indices of sexual selection under laboratory conditions. Here, we use a genetic study to compare the most widely used measures of sexual selection in natural populations. We explored the mating and reproductive successes of male and female bank voles,Clethrionomys glareolus, across manipulated operational sex ratios (OSRs) by genotyping all adult and pup bank voles on 13 islands using six microsatellite loci. We used Bateman's principles (IsandIand Bateman gradients) and selection coefficients (s′ andβ′) to evaluate, f…

Maternal effort and male quality in the bank vole, Clethrionomys glareolus.

Parental investment in reproduction is adjusted according to potential benefits in terms of offspring survival and/or mating success. If male quality affects the reproductive success of a female, then females mating with high-quality males should invest more in reproduction. Although the subject has been of general interest, further experimental verification of the hypothesis is needed. We studied whether female bank voles (Clethrionomys glareolus) adjusted their maternal effort according to male quality, measured as mating success. To enable the measurement of maternal effort during nursing separately from male genetic effects the litters were cross-fostered. Further, the genetic backgroun…

Predation on artificial ground nests in relation to forest fragmentation, agricultural land and habitat structure

The impacts of forest fragmentation, agricultural land and habitat structure on depredation of artificial ground nests were studied in the cultivated area in central Finland and in the forest dominated area in Finnish Lapland. The overall predation rate did not differ between the regions. The overall predation rate was also independent of landscape characteristics forest patch size and the distance to patch edge. However, nest predation was clearly affected by the agricultural land since the robbing rate in forest edges was higher near farmlands than further away. This effect was caused by avian predators which proportional importance in predation was higher in the agricultural landscape th…

Life in varying environments: experimental evidence for delayed effects of juvenile environment on adult life history

Summary 1. The effects of environment experienced during early development on phenotype as an adult has started to gain vast amounts of interest in various taxa. Some evidence on long-term effects of juvenile environment is available, but replicated experimental studies in wild animals are still lacking. 2. Here we report the first replicated experiment in wild mammals which examines the long-term effects of juvenile and adult environments on individual fitness (reproduction, survival and health). The early development of bank vole (Myodes glareolus) individuals took place in either foodsupplemented or un-supplemented outdoor enclosures. After the summer, adult individuals were reciprocally…

A test of male mating and hunting success in the kestrel: the advantages of smallness?

We tested female choice for male wing and tarsus length and body mass in the kestrel (Falco tinnunculus), a species in which males average about 10% smaller than females. We also studied how male characters are related to their hunting success. In the laboratory, females preferred lighter males with shorter tarsi as mates, if the difference in those characters between competing males was larger than average. Lighter and shorter-winged males seemed to be better hunters than heavier and longer-winged males. Field observations in a year in which voles were scarce suggested that shorter-winged males were also better food providers in courtship feeding than longer-winged males,although in good v…

Supplementary methods and results from Artificial selection for predatory behaviour results in dietary niche differentiation in an omnivorous mammal

The diet of an individual is a result of the availability of dietary items and the individual's foraging skills and preferences. Behavioural differences may thus influence diet variation, but the evolvability of diet choice through behavioural evolution has not been studied. We used experimental evolution combined with a field enclosure experiment to test whether behavioural selection leads to dietary divergence. We analysed the individual dietary niche via stable isotope ratios of nitrogen (��15N) and carbon (��13C) in the hair of an omnivorous mammal, bank vole, from four lines selected for predatory behaviour and four unselected control lines. Predatory voles had higher hair ��15N values…

Frequency and density-dependent selection on life-history strategies--a field experiment.

Negative frequency-dependence, which favors rare genotypes, promotes the maintenance of genetic variability and is of interest as a potential explanation for genetic differentiation. Density-dependent selection may also promote cyclic changes in frequencies of genotypes. Here we show evidence for both density-dependent and negative frequency-dependent selection on opposite life-history tactics (low or high reproductive effort, RE) in the bank vole (Myodes glareolus). Density-dependent selection was evident among the females with low RE, which were especially favored in low densities. Instead, both negative frequency-dependent and density-dependent selection were shown in females with high R…

Gonadotropin Hormone Modulation of Testosterone, Immune Function, Performance, and Behavioral Trade‐Offs among Male Morphs of the Lizard Uta stansburiana

Sexual selection predicts that trade-offs maintain trait variation in alternative reproductive strategies. Experiments often focus on testosterone (T), but the gonadotropins follicle-stimulating hormone and luteinizing hormone may provide a clearer understanding of the pleiotropic relationships among traits. We assess the activational role of gonadotropins on T and corticosterone regulation in traits expressed by polymorphic male side-blotched lizards Uta stansburiana. Gonadotropins are found to enhance and suppress multiple physiological, morphological, and behavioral traits independently, as well as indirectly via T, and we demonstrate selective trade-offs between reproduction and surviva…

Maternal antibodies contribute to sex-based difference in hantavirus transmission dynamics

Individuals often differ in their ability to transmit disease and identifying key individuals for transmission is a major issue in epidemiology. Male hosts are often thought to be more important than females for parasite transmission and persistence. However, the role of infectious females, particularly the transient immunity provided to offspring through maternal antibodies (MatAbs), has been neglected in discussions about sex-biased infection transmission. We examined the effect of host sex upon infection dynamics of zoonotic Puumala hantavirus (PUUV) in semi-natural, experimental populations of bank vole ( Myodes glareolus ). Populations were founded with either females or males that we…

Advantage of rare infanticide strategies in an invasion experiment of behavioural polymorphism

Killing conspecific infants (infanticide) is among the most puzzling phenomena in nature. Stable polymorphism in such behaviour could be maintained by negative frequency-dependent selection (benefit of rare types). However, it is currently unknown whether there is genetic polymorphism in infanticidal behaviour or whether infanticide may have any fitness advantages when rare. Here we show genetic polymorphism in non-parental infanticide. Our novel invasion experiment confirms negative frequency-dependent selection in wild bank vole populations, where resource benefits allow an infanticidal strategy to invade a population of non-infanticidal individuals. The results show that infanticidal beh…

Does risk of small mustelid predation affect the oestrous cycle in the bank vole,Clethrionomys glareolus?

Female bank voles suppress their reproduction when the risk of small mustelid predation is high. The mechanism for this reproductive suppression is unknown. Because rodents are known to alter their oestrous cycle in response to changing environmental conditions, the eVect of predation risk on the oestrous cycle of bank vole females was studied. The oestrous cycles of 24 females divided into two treatments (predation risk and control) were observed for 20 days using female receptivity as an indication of oestrus. Voles exposed for 2-3 h a day for 20 days to the close presence of a least weasel, Mustela nivalis nivalis, had fewer oestrous cycles than control females exposed to a domestic rabb…

Additional file 3: of Fibroblasts from bank voles inhabiting Chernobyl have increased resistance against oxidative and DNA stresses

Etoposide induces apoptosis in bank vole fibroblasts. We treated the cells with DMSO or 20 μM of etoposide for 24 h, replaced the media, and collected samples 72 h post-treatment for propidium iodide and Annexin V flow cytometry with eBioscience Annexin V apoptosis Detection kit FITC as recommended by the manufacturer. The figure shows one control and one Chernobyl cell line. The percentage of healthy cells are shown in the lower-left corner, necrotic cells in the upper-left corner, and apoptotic cells at right. (PDF 66 kb)

Increased radiation from Chernobyl decreases the expression of red colouration in natural populations of bank voles (Myodes glareolus)

AbstractPheomelanin is a pink to red version of melanin pigment deposited in skin and hair. Due to its bright colour, pheomelanin plays a crucial function in signalling, in particular sexual signalling. However, production of pheomelanin, as opposed to its dark alternative, eumelanin, bears costs in terms of consumption of antioxidants important for protection of DNA against naturally produced reactive oxidative species. Therefore, decreased expression of pheomelanin is expected in organisms exposed to severe oxidative stress such as that caused by exposure to chronic ionizing radiation. We tested if variable exposure to radiation among natural populations of bank voles Myodes glareolus in …

Additional file 1: of Fibroblasts from bank voles inhabiting Chernobyl have increased resistance against oxidative and DNA stresses

Chernobyl and control fibroblasts are able to adjust to constant exposure to small concentrations of oxidant. The oxidant was added every other day for four times before scoring the wells that were 100% confluent a day after the last exposure. The results are from three separate experiments using the eight Chernobyl (N = 24) and eight control cell lines (N = 24). Variation is shown by standard deviation. (PDF 28 kb)

Additional file 7: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Measures of alpha diversity for the skin microbiota of bank voles inhabiting areas that differ in levels of environmental radiation. Box-and-whisker plots represent the median and interquartile range of alpha diversity estimates (i.e. number of observed OTUs, Shannon index). Each box plot represent alpha diversity of the skin microbiome of bank vole females and males from contaminated (CH) and uncontaminated (CL) with radionuclides areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL), Ukraine. (PDF 8â kb)

Additional file 5: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Correlations (Spearman’s correlation analysis) between the SK microbiome alpha diversity estimates (Number of observed OTUs and Shannon index) and (a, b) the whole-body 137Cs radionuclide burden, and (c, d) the external radiation doses of sampled bank voles. All correlations were not significant. (PDF 287 kb)

Repeated evolution of camouflage in speciose desert rodents

AbstractThere are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in t…

Diet Quality Limits Summer Growth of Field Vole Populations

Marked variation occurs in both seasonal and multiannual population density peaks of northern European small mammal species, including voles. The availability of dietary proteins is a key factor limiting the population growth of herbivore species. The objective of this study is to investigate the degree to which protein availability influences the growth of increasing vole populations. We hypothesise that the summer growth of folivorous vole populations is positively associated with dietary protein availability. A field experiment was conducted over a summer reproductive period in 18 vegetated enclosures. Populations of field voles (Microtus agrestis) were randomised amongst three treatment…

Costly punishment prevails in intergroup conflict.

Understanding how societies resolve conflicts between individual and common interests remains one of the most fundamental issues across disciplines. The observation that humans readily incur costs to sanction uncooperative individuals without tangible individual benefits has attracted considerable attention as a proximate cause as to why cooperative behaviours might evolve. However, the proliferation of individually costly punishment has been difficult to explain. Several studies over the last decade employing experimental designs with isolated groups have found clear evidence that the costs of punishment often nullify the benefits of increased cooperation, rendering the strong human tenden…

Transcriptional Upregulation of DNA Damage Response Genes in Bank Voles (Myodes glareolus) Inhabiting the Chernobyl Exclusion Zone

Exposure to ionizing radiation (IR) from radionuclides released into the environment can damage DNA. An expected response to exposure to environmental radionuclides, therefore, is initiation of DNA damage response (DDR) pathways. Increased DNA damage is a characteristic of many organisms exposed to radionuclides but expression of DDR genes of wildlife inhabiting an area contaminated by radionuclides is poorly understood. We quantified expression of five central DDR genes Atm, Mre11, p53, Brca1, and p21 in the livers of the bank vole Myodes glareolus that inhabited areas within the Chernobyl Exclusion Zone (CEZ) that differed in levels of ambient radioactivity, and also from control areas ou…

Data from: Age-related effects of chronic hantavirus infection on female host fecundity

1. Pathogens often cause detrimental effects to their hosts and, consequently, may influence host population dynamics that may, in turn, feed back to pathogen transmission dynamics. Understanding fitness effects of pathogens upon animal host populations can help to predict the risks that zoonotic pathogens pose to humans. 2. Here we determine whether chronic infection by Puumala hantavirus (PUUV) affects important fitness-related traits, namely the probability of breeding, reproductive effort and mother and offspring condition, in the bank vole (Myodes glareolus). Using 9 years empirical data in a PUUV endemic area in Central Finland, we found differences between reproductive characteristic…

Additional file 10: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Permutational MANOVA (PERMANOVA) statistical tests on unweighted UniFrac (unwUniFrac) distances and Bray-Curtis dissimilarity for skin microbial communities of bank voles inhabiting areas that differ in environmental radiation levels. (XLSX 11â kb)

Data from: Food limitation constrains host immune responses to nematode infections

Trade-offs in the allocation of finite-energy resources among immunological defences and other physiological processes are believed to influence infection risk and disease severity in food-limited wildlife populations. However, this prediction has received little experimental investigation. Here we test the hypothesis that food limitation impairs the ability of wild field voles (Microtus agrestis) to mount an immune response against parasite infections. We conducted a replicated experiment on vole populations maintained in large outdoor enclosures during boreal winter, using food supplementation and anthelmintic treatment of intestinal nematodes. Innate immune responses against intestinal p…

Data from: Stabilising selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

The loci arginine vasopressin receptor 1a (avpr1a) and oxytocin receptor (oxtr) have evolutionarily conserved roles in vertebrate social and sexual behavior. Allelic variation at a microsatellite locus in the 5’ regulatory region of these genes is associated with fitness in the bank vole Myodes glareolus. Given the low frequency of long and short alleles at these microsatellite loci in wild bank voles, we used breeding trials to determine whether selection acts against long and short alleles. Female bank voles with intermediate length avpr1a alleles had the highest probability of breeding, while male voles whose avpr1a alleles were very different in length had reduced probability of breedin…

Appendix A. Structure of missing data (see data analysis of Methods section).

Structure of missing data (see data analysis of Methods section).

Additional file 4: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Summary of skin microbiota of the Phyla, Classes, Orders, Families and Genera for wild-caught bank voles (Myodes glareolus), with significantly different relative abundances (Kruskal–Wallis tests using Dunn’s post hoc test and followed by a Benjamini-Hochberg False Discovery Rate (FDR) correction) among the study areas (e.g. CL, KL and CH). (XLSX 97 kb)

Additional file 1: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

16S rRNA gene sequencing metadata. (XLSX 35â kb)

Additional file 11: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Summary of predictive accuracy of Random Forest modelling for skin and gut microbial communities of bank voles inhabiting areas that differ in environmental radiation levels. (XLSX 10â kb)

Data from: Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus

Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show …

Data from: Maintenance costs of male dominance and sexually antagonistic selection in the wild

1. Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the correlational effects of male energetics on his sisters recognized. 2. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) ant…

Data from: Maternal antibodies contribute to sex based difference in hantavirus transmission dynamics

Individuals often differ in their ability to transmit disease and identifying key individuals for transmission is a major issue in epidemiology. Male hosts are often thought to be more important than females for parasite transmission and persistence. However, the role of infectious females, particularly the transient immunity provided to offspring through maternal antibodies (MatAbs), has been neglected in discussions about sex-biased infection transmission. We examined the effect of host sex upon infection dynamics of zoonotic Puumala hantavirus (PUUV) in semi-natural, experimental populations of bank vole (Myodes glareolus). Populations were founded with either females or males that were …

Additional file 8: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Final GLMs that show significant predictors of alpha diversity estimates within the skin microbiota of bank voles inhabiting the area within the Chernobyl Exclusion Zone (CEZ) and areas near Kyiv, Ukraine. Only significant models are shown, with significant P-values shown in bold. AIC fit criterion is given for each full model. (XLSX 12â kb)

Additional file 6: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Statistical comparison of alpha diversity estimates by Kruskal–Wallis tests using Dunn’s post hoc test and followed by a Benjamini-Hochberg False Discovery Rate (FDR) correction. (XLSX 14 kb)

Additional file 3: of Skin and gut microbiomes of a wild mammal respond to different environmental cues

Relative abundance (average of taxonomic groups abundance within each sample) of Phyla, Classes, Orders, Families or Genera for skin microbiome of wild-caught bank voles (Myodes glareolus) from contaminated (CH) and uncontaminated (CL) areas with radionuclides within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL), Ukraine. (XLSX 91â kb)

Data from: Food provisioning alters infection dynamics in populations of a wild rodent

While pathogens are often assumed to limit the growth of wildlife populations, experimental evidence for their effects is rare. A lack of food resources has been suggested to enhance the negative effects of pathogen infection on host populations, but this theory has received little investigation. We conducted a replicated two-factor enclosure experiment, with introduction of the bacterium Bordetella bronchiseptica and food supplementation, to evaluate the individual and interactive effects of pathogen infection and food availability on vole populations during a boreal winter. We show that prior to bacteria introduction, vole populations were limited by food availability. Bordetella bronchis…

Can number and size of offspring increase simultaneously? – A central life-history trade-off reconsidered

Background: To maximize their fitness, parents are assumed to allocate their resources optimally between number and size of offspring. Although this fundamental life-history trade-off has been subject to long standing interest, its genetic basis, especially in wild mammals, still remains unresolved. One important reason for this problem is that a large multigenerational pedigree is required to conduct a reliable analysis of this trade-off. Results: We used the REML-animal model to estimate genetic parameters for litter size and individual birth size for a common Palearctic small mammal, the bank vole (Myodes glareolus). Even though a phenotypic trade-off between offspring number and size wa…

Intracerebral Borna disease virus infection of bank voles leading to peripheral spread and reverse transcription of viral RNA

Bornaviruses, which chronically infect many species, can cause severe neurological diseases in some animal species; their association with human neuropsychiatric disorders is, however, debatable. The epidemiology of Borna disease virus (BDV), as for other members of the family Bornaviridae, is largely unknown, although evidence exists for a reservoir in small mammals, for example bank voles (Myodes glareolus). In addition to the current exogenous infections and despite the fact that bornaviruses have an RNA genome, bornavirus sequences integrated into the genomes of several vertebrates millions of years ago. Our hypothesis is that the bank vole, a common wild rodent species in traditional B…

Research data of article: "Borrelia afzelii alters reproductive success in a rodent host"

Research data of article: "Sympatric Ixodes-tick species: pattern of distribution and pathogen transmission within wild rodent populations"

Longitudinal monitoring of bank voles as well as their ticks and tick-borne pathogens in Central Finland, carried out in 2012.

Lisämateriaali artikkeliin "Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent".

Electronic material for Kesäniemi J, Jernfors T, Lavrinienko A, Kivisaari K, Kiljunen M, Mappes T & Watts PC. 2019. Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent. Molecular Ecology 28: 4620–4635. Contains transcriptome annotation data and output of differential expression and gene ontology enrichment analyses. Parts of the dataset originally published in DRYAD (https://doi.org/10.5061/dryad.j3c6r69).

Interactive effects of past and present environments on overwintering success - A reciprocal transplant experiment

Life-history traits are influenced by environmental factors throughout the lifespan of an individual. The relative importance of past versus present environment on individual fitness, therefore, is a relevant question in populations that face the challenge of temporally varying environment. We studied the interacting effects of past and present density on body mass, condition, and survival in enclosure populations of the bank vole (Myodes glareolus) using a reciprocal transplant design. In connection with the cyclic dynamics of natural vole populations, our hypothesis was that individuals born in low-density enclosures would do better overwintering in low-density enclosures than in high-den…

Frequency and Density-Dependent Selection on Life-History Strategies - A Field Experiment

Negative frequency-dependence, which favors rare genotypes, promotes the maintenance of genetic variability and is of interest as a potential explanation for genetic differentiation. Density-dependent selection may also promote cyclic changes in frequencies of genotypes. Here we show evidence for both density-dependent and negative frequency-dependent selection on opposite life-history tactics (low or high reproductive effort, RE) in the bank vole (Myodes glareolus). Densitydependent selection was evident among the females with low RE, which were especially favored in low densities. Instead, both negative frequency-dependent and density-dependent selection were shown in females with high RE…

Island selection on mammalian life-histories: genetic differentiation in offspring size

BACKGROUND: Since Darwin's pioneering work, evolutionary changes in isolated island populations of vertebrates have continued to provide the strongest evidence for the theory of natural selection. Besides macro-evolutionary changes, micro-evolutionary changes and the relative importance of natural selection vs. genetic drift are under intense investigation. Our study focuses on the genetic differentiation in morphological and life-history traits in insular populations of a small mammal the bank vole Myodes glareolus. RESULTS: Our results do not support the earlier findings for larger adult size or lower reproductive effort in insular populations of small mammals. However, the individuals li…