Female Bank Voles Research Articles

The role of male scent in female attraction in the bank vole, Myodes glareolus.

Chemical signals are frequently utilised by male mammals for intersexual communication and females are often attracted to male scent. However, the mechanism underlying female attraction has only been identified in a small number of mammalian species. Mammalian scents contain airborne volatiles, that are detected by receivers at a distance from the scent source, as well as non-volatile molecules, such as proteins, that require physical contact for detection. Lipocalin proteins, produced within the scent secretions of many terrestrial mammals, are thought to be particularly important in chemical signalling. Here, we explore if the male-specific protein, glareosin, expressed by adult male bank voles, Myodes glareolus, stimulates female attraction to male scent. We show that female bank voles are more attracted to male compared to female scent, supporting the results of previous studies. Increased investigation and attraction to male scent occurred to both airborne volatiles and non-volatile proteins when they were presented separately. However, we found no evidence that attraction to male scent was driven by glareosin. Our results differ from those previously described in house mice, where a single protein induces female attraction to male scent, suggesting the mechanism underlying female attraction to male scent differs between species.

Maternal Antibodies Provide Bank Voles with Strain-Specific Protection against Infection by the Lyme Disease Pathogen.

Multistrain microbial pathogens often induce strain-specific antibody responses in their vertebrate hosts. Mothers can transmit antibodies to their offspring, which can provide short-term, strain-specific protection against infection. Few experimental studies have investigated this phenomenon for multiple strains of zoonotic pathogens occurring in wildlife reservoir hosts. The tick-borne bacterium Borrelia afzelii causes Lyme disease in Europe and consists of multiple strains that cycle between the tick vector (Ixodes ricinus) and vertebrate hosts, such as the bank vole (Myodes glareolus). We used a controlled experiment to show that female bank voles infected with B. afzelii via tick bite transmit protective antibodies to their offspring. To test the specificity of protection, the offspring were challenged using a natural tick bite challenge with either the maternal strain to which the mothers had been exposed or a different strain. The maternal antibodies protected the offspring against a homologous infectious challenge but not against a heterologous infectious challenge. The offspring from the uninfected control mothers were equally susceptible to both strains. Borrelia outer surface protein C (OspC) is an antigen that is known to induce strain-specific immunity. Maternal antibodies in the offspring reacted more strongly with homologous than with heterologous recombinant OspC, but other antigens may also mediate strain-specific immunity. Our study shows that maternal antibodies provide strain-specific protection against B. afzelii in an ecologically important rodent reservoir host. The transmission of maternal antibodies may have important consequences for the epidemiology of multistrain pathogens in nature.IMPORTANCE Many microbial pathogen populations consist of multiple strains that induce strain-specific antibody responses in their vertebrate hosts. Females can transmit these antibodies to their offspring, thereby providing them with short-term strain-specific protection against microbial pathogens. We investigated this phenomenon using multiple strains of the tick-borne microbial pathogen Borrelia afzelii and its natural rodent reservoir host, the bank vole, as a model system. We found that female bank voles infected with B. afzelii transmitted to their offspring maternal antibodies that provided highly efficient but strain-specific protection against a natural tick bite challenge. The transgenerational transfer of antibodies could be a mechanism that maintains the high strain diversity of this tick-borne pathogen in nature.

Borrelia afzelii alters 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 of Borrelia 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 that B. afzelii can 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 without alteration of the offspring size at birth. At low density, infected males produced fewer offspring, fertilized fewer females and had lower mobility than uninfected individuals. Meanwhile, the infection did not affect the proportion of offspring produced or the proportion of mating partner in female bank voles. Our study is the first to show that B. afzelii infection alters the reproductive success of the natural host. The effects observed could reflect the sickness behaviour due to the infection or they could be a consequence of a manipulation of the host behaviour by the bacteria.

Oxidative damage and antioxidant defense are assay and tissue-dependent both in captive and wild-caught bank voles (Myodes glareolus) before and after reproduction.

Reproduction is costly and life‐history theory predicts that current parental investment will result in lower survival or decreased future reproduction. The physiological mechanisms mediating the link between reproduction and survival are still under debate and elevated oxidative damage during reproduction has been proposed as a plausible candidate. Previous studies of oxidative stress during reproduction in animals under natural conditions have been restricted to analyses of blood. Herein, we measured the level of oxidative damage to lipids (tiobarbituric‐acid‐reactive substances) and proteins (carbonyls) in the liver, kidneys, heart and skeletal muscles in free‐living bank vole females from spring and autumn generations, before and after reproduction. Antioxidant defense in the liver and kidneys was also determined. We expected oxidative damage to tissues and hypothesized that the damage would be more uniform between tissues in wild animals compared to those breeding under laboratory conditions. Considering all combinations of markers/tissues/generations, oxidative damage in females did not differ before and after reproduction in 12 comparisons, was lower after reproduction in three comparisons, and was higher after breeding in one comparison. The total glutathione was significantly increased after reproduction only in the liver of the autumn generation and there was no change in catalase activity. Our results confirm—for the first time in the field—previous observations from laboratory studies that there is no simple link between oxidative stress and reproduction and that patterns depend on the tissue and marker being studied. Overall, however, our study does not support the hypothesis that the cost of reproduction in bank voles is mediated by oxidative stress in these tissues.

Tissue Trace Elements and Lipid Peroxidation in Breeding Female Bank Voles Myodes glareolus

Recent studies have demonstrated that reproduction reduces oxidative damage in various tissues of small mammal females. The present work was designed to determine whether the reduction of oxidative stress in reproductive bank vole females was associated with changes in tissue trace elements (iron, copper, zinc) that play an essential role in the production of reactive oxygen species. Lipid peroxidation (a marker of oxidative stress) and iron concentration in liver, kidneys, and skeletal muscles of reproducing bank vole females that weaned one litter were significantly lower than in non-reproducing females; linear regression analysis confirmed a positive relation between the tissue iron and lipid peroxidation. The concentrations of copper were significantly lower only in skeletal muscles of reproductive females and correlated positively with lipid peroxidation. No changes in tissue zinc were found in breeding females when compared with non-breeding animals. These data indicate that decreases in tissue iron and copper concentrations may be responsible for the reduction of oxidative stress in reproductive bank vole females.

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 background radioactivity, and also from control areas outside the CEZ (i.e. sites with no detectable environmental radionuclides) in Ukraine. Expression of these DDR genes did not significantly differ between male and female bank voles, nor among sites within the CEZ. We found a near two-fold upregulation in the DDR initiators Mre11 and Atm in animals collected from the CEZ compared with samples from control sites. As Atm is an important regulator of oxidative stress, our data suggest that antioxidant activity may be a key component of the defense against exposure to environmental radioactivity.

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 breeding. Moreover, there was a significant interaction between male and female oxtr genotypes, where potential breeding pairs with dissimilar length alleles had reduced probability of breeding. These data show how genetic variation at microsatellite loci associated with avpr1a and oxtr is associated with fitness, and highlight complex patterns of selection at these loci. More widely, these data show how stabilizing selection might act on allele length frequency distributions at gene-associated microsatellite loci.

Ultrasonic Reaction of Bank Vole Males to the Presence of Females Varying in Hormonal Activity

AbstractRodents are known to emit ultrasounds during social interactions. Despite the evidence that ultrasonic vocalizations are emitted during sexual encounters and may play a certain role in sexual selection, only a few studies have investigated this phenomenon, mainly in laboratory rodents. We analysed the ultrasonic calls of bank vole (Myodes glareolus) males from an outbred colony in the presence of females differing in hormonal activity. Sexually experienced males were tested during interactions with naive, ovariectomized, pregnant and post‐partum oestrous females. We found that the males’ ultrasound vocalizations depend on the phase of the bank vole females’ reproductive cycle. During encounters with post‐partum oestrous females the males emitted significantly more ultrasounds, and the total duration of ultrasound vocalization was longer. The presence of post‐partum oestrous females also influenced the type of ultrasounds: the most typical constant‐frequency sounds were significantly shorter, and two additional types of ultrasounds were presented during interactions with females ready to mate: U‐shaped frequency‐modulated sounds and frequency‐modulated upsweep sounds. To our knowledge this is the first evidence that male voles of the subfamily Arvicolinae emit different types of ultrasounds in the presence of females depending on their reproductive stage. We suggest that these ultrasounds may be employed as an attractant during reproductive behaviour and that they are potentially an element of sexual selection.

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 characteristics of PUUV-infected and uninfected female bank voles. 3. Young infected females had a significantly higher, and old individuals lower, likelihood of reproducing than uninfected animals during the middle of the breeding season. The implication is that PUUV infection may have long-term deleterious effects that are observed at old age, while in young individuals, the infection may enhance breeding probability by directing resources towards current breeding. 4. Moreover, PUUV infection was related with the mother's body condition. Infected mothers were in poorer condition than uninfected mothers in the early breeding season, but were in better condition than uninfected mothers during the middle of the breeding season. Offspring body condition was positively associated with mother's body condition, which, in turn, was related to the PUUV infection status of the mother. 5. Our findings indicate that chronic infection may affect the reproduction of female hosts, but the effect is dependent on the host age. The effect of chronic hantavirus infection was small and density-independent and hence unlikely to contribute to the cyclic population dynamics of the host. However, the effects on a female's reproductive output might affect the abundance of young susceptible individuals in the population and hence influence the transmission and persistence of the pathogen. Although experimental and long-term capture-mark-recapture studies are required to further clarify the fitness effects of hantavirus infection and their consequences for pathogen dynamics, this study shows that the infection may have complex effects that are dependent on the age of the individual and the time of the breeding season.

Female host sex-biased parasitism with the rodent stomach nematode Mastophorus muris in wild bank voles (Myodes glareolus).

Abundance and prevalence of helminth infections often differ between host sexes, and are usually biased in favor of males. Relatively few cases of female-biased parasitism have been reported. We sampled bank voles in three woodland sites in N.E. Poland over 11 years at 3-4-year intervals, and assessed their parasite burdens. Prevalence and abundance of the stomach nematode Mastophorus muris were consistently higher among females. Among adult female bank voles from the two sites that showed the highest prevalence with M. muris, both prevalence and abundance were significantly higher in lactating bank voles, but not pregnant animals, and the effect of lactation was evident in both sites, in all four surveys, and in both age classes. Although the magnitude of the effect of lactation varied between years, it was not confounded by any significant interactions with other factors. We hypothesize that mature and reproductively active female bank voles are subject to higher exposure compared with males of similar age, as a consequence of the increased content of invertebrates in their diet, including the intermediate hosts of M. muris, required to meet the higher increased energy and protein demands of nursing litters throughout the summer months.

Puumala hantavirus infection alters the odour attractiveness of its reservoir host.

The random-mixing assumptions of many parasite-transmission models are challenged if healthy individuals can alter their behaviour to reduce their risk of infection. Some pathogens reduce the attractiveness of their hosts' excretions, for example, potentially altering contact rates and thus the predicted force of infection for pathogens transmissible by contact with excretions. For bank voles (Myodes glareolus), contact with contaminated urine is an important route of transmission for Puumala hantavirus (PUUV); however, it is not known whether PUUV infection changes the voles' urinary odours or their attractiveness. Here, we use a Y-maze to test whether PUUV infection alters the attractiveness of male bank voles' urine. We presented wild-caught PUUV-free male and female bank voles with PUUV-infected conspecific urine, uninfected urine and a water control, and measured the relative and absolute latency to first visit, number of visits, and total time bank voles spent investigating each treatment over 30 min. PUUV infection significantly altered the bank voles' initial response to conspecific urine, with fewer visits and less time spent close to infected urine relative to uninfected urine, and less total time spent near the infected urine than the uninfected urine or control. These strong preferences weakened over the 30-min trial, however, partly due to a general decline in male activity, and there were no absolute differences between the treatments overall. This suggests that PUUV infection does change the attractiveness of bank vole urine to conspecifics, and we discuss the implications of these results for random-mixing assumptions.

Polyandrous females produce sons that are successful at post‐copulatory competition

Some of the genetic benefit hypotheses put forward to explain multiple male mating (polyandry) predict that sons of polyandrous females will have an increased competitive ability under precopulatory or post-copulatory competition via paternally inherited traits, such as attractiveness or fertilization efficiency. Here, we tested these predictions by comparing the competitive ability of sons of experimentally monandrous and polyandrous female bank voles (Myodes glareolus), while controlling for potential material and maternal effects. In female choice experiments, we found no clear preference for sons of either monandrous or polyandrous mothers. Moreover, neither male type was dominant over the other, indicating no advantage in precopulatory male contest competition. However, in competitive matings, sons of polyandrous mothers significantly increased their mating efforts (mating duration, intromission number). In line with this, paternity success was biased towards sons of polyandrous mothers. Because there was no evidence for maternal effects, our results suggest that female bank voles gain genetic benefits from polyandry.

Concurrent effects of age class and food distribution on immigration success and population dynamics in a small mammal

During the settlement stage of dispersal, the outcome of conflicts between residents and immigrants should depend on the social organization of resident populations as well as on individual traits of immigrants, such as their age class, body mass and/or behaviour. We have previously shown that spatial distribution of food influences the social organization of female bank voles (Myodes glareolus). Here, we aimed to determine the relative impact of food distribution and immigrant age class on the success and demographic consequences of female bank vole immigration. We manipulated the spatial distribution of food within populations having either clumped or dispersed food. After a pre-experimental period, we released either adult immigrants or juvenile immigrants, for which we scored sociability and aggressiveness prior to introduction. We found that immigrant females survived less well and moved more between populations than resident females, which suggest settlement costs. However, settled juvenile immigrants had a higher probability to reproduce than field-born juveniles. Food distribution had little effects on the settlement success of immigrant females. Survival and settlement probabilities of immigrants were influenced by adult female density in opposite ways for adult and juvenile immigrants, suggesting a strong adult-adult competition. Moreover, females of higher body mass at release had a lower probability to survive, and the breeding probability of settled immigrants increased with their aggressiveness and decreased with their sociability. Prior to the introduction of immigrants, resident females were more aggregated in the clumped food treatment than in the dispersed food treatment, but immigration reversed this relationship. In addition, differences in growth trajectories were seen during the breeding season, with populations reaching higher densities when adult immigrants were introduced in a plot with dispersed food, or when juvenile immigrants were introduced in a plot with clumped food. These results indicate the relative importance of intrinsic and extrinsic factors on immigration success and demographic consequences of dispersal and are of relevance to conservation actions, such as reinforcement of small populations.

Seasonal modulation of sex-related differences in hippocampus size and spatial behavior in bank voles, Clethrionomys glareolus (Rodentia, Cricetidae)

Male and female bank voles (Clethrionomys glareolus) were compared with respect to seasonal variation in hippocampus size and dynamics of spatial behavior during the annual population cycle. The winter decrease in the size of the hippocampus (the brain region involved in the processing of spatial information about the environment) in young autumn-born voles coincided in time with reduction of their home ranges and did not differ significantly between males and females. The growth of the hippocampus in spring, after winter regression, was higher in males (19–28% in different populations) than in females (8–20%) and coincided with an increase in spatial activity, which was also more distinct in males. A significantly greater hippocampus size in males during the breeding period correlated with their higher mobility (reflected in capture rate) and greater size of home ranges. Thus, parallel seasonal modulation of sex-related differences in hippocampus size and spatial behavior was revealed: sexual dimorphism in these characters was insignificant among young voles in autumn; disappeared in winter; manifested itself again, synchronously in both characters, in early spring (with the onset of puberty); and reached a peak in summer.

Expression of androgen receptor in adult female bank voles after prenatal exposition to flutamide

Expression of androgen receptor in adult female bank voles after prenatal exposition to flutamide

Effect of dietary cadmium and/or lead on histopathological changes in the kidneys and liver of bank voles Myodes glareolus kept in different group densities

Bank voles free living in a contaminated environment are known to be more sensitive to cadmium (Cd) toxicity than the rodents exposed to Cd under laboratory conditions, but the reasons for this difference are poorly defined. The present work was designed to determine whether dietary lead (Pb), a common environmental co-contaminant, and/or animal density that affects various physiological processes, would influence susceptibility to Cd toxicity in the kidneys and liver of these animals. For 6 weeks, the female bank voles were kept individually or in a group of six and provided with diet containing environmentally relevant concentrations of Cd [<0.1 μg/g (control) and 60 μg/g dry wt] and Pb [<0.2 μg/g (control) and 300 μg/g dry wt] alone or in combination. At the end of exposure period, histopathology and analyses of metallothionein, glutathione and zinc that are linked to a protective effect against Cd toxicity, as well as Cd, Pb, copper, iron and lipid peroxidation were carried out. Histopathological changes in the kidneys (a focal glomerular swelling and proximal tubule degeneration) and liver (a focal hepatocyte swelling, vacuolation and inflammation) occurred exclusively in some bank voles kept in a group and exposed to Cd alone (2/6) or Cd + Pb (4/6). The observed toxicity in grouped bank voles appeared not to be based on altered (1) tissue disposition of Cd and/or Pb, (2) metallothionein, glutathione and zinc concentrations, or (3) tissue copper, iron and lipid peroxidation. The data indicate that high population density in combination with environmental Pb may be responsible for an increased susceptibility to Cd toxicity observed in bank voles free living in a contaminated environment; the mechanism by which animal density affects Cd toxicity deserves further study.

Is reproduction costly? No increase of oxidative damage in breeding bank voles

According to life-history theory, investment in reproduction is associated with costs, which should appear as decreased survival to the next reproduction or lower future reproductive success. It has been suggested that oxidative stress may be the proximate mechanism of these trade-offs. Despite numerous studies of the defense against reactive oxygen species (ROS) during reproduction, very little is known about the damage caused by ROS to the tissues of wild breeding animals. We measured oxidative damage to lipids and proteins in breeding bank vole (Myodes glareolus) females after rearing one and two litters, and in non-breeding females. We used bank voles from lines selected for high maximum aerobic metabolic rates (which also had high resting metabolic rates and food intake) and non-selected control lines. The oxidative damage was determined in heart, kidneys and skeletal muscles by measuring the concentration of thiobarbituric acid-reactive substances, as markers of lipid peroxidation, and carbonyl groups in proteins, as markers of protein oxidation. Surprisingly, we found that the oxidative damage to lipids in kidneys and muscles was actually lower in breeding than in non-breeding voles, and it did not differ between animals from the selected and control lines. Thus, contrary to our predictions, females that bred suffered lower levels of oxidative stress than those that did not reproduce. Elevated production of antioxidant enzymes and the protective role of sex hormones may explain the results. The results of the present study do not support the hypothesis that oxidative damage to tissues is the proximate mechanism of reproduction costs.

Gene conversion in the mitochondrial genome on interspecific hybridization in voles of the Clethrionomys genus

The phenomenon of interspecific hybridization accompanied by transfer of the mitochondrial genome from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (Cl. glareolus) in northeastern Europe is well known already for 25 years. However, the possibility of recombination between homologous segments of maternal and paternal mtDNAs of the voles during fertilization was not previously studied. Analysis of data on variability of nucleotide sequences of the mitochondrial gene for cytochrome b in populations of red-backed and bank voles in the area of their sympatry has shown that as a result of interspecific hybridization, the mitochondrial gene pool of bank voles contains not only mtDNA haplotypes of red-backed vole females, but also mtDNA haplotypes of bank voles bearing short nucleotide tracts of red-backed vole mtDNA. This finding supports the hypothesis that an incomplete elimination of red-backed vole paternal mtDNA during the interspecific hybridization between bank vole females and red-backed vole males leads to the gene conversion of bank vole maternal mtDNA tracts by homologous ones of mtDNA of red-backed vole males.

Combined Effect of Dietary Cadmium and Benzo(a)pyrene on Metallothionein Induction and Apoptosis in the Liver and Kidneys of Bank Voles

Bank voles free living in a contaminated environment have been shown to be more sensitive to cadmium (Cd) toxicity than the rodents exposed to Cd under laboratory conditions. The objective of this study was to find out whether benzo(a)pyrene (BaP), a common environmental co-contaminant, increases Cd toxicity through inhibition of metallothionein (MT) synthesis—a low molecular weight protein that is considered to be primary intracellular component of the protective mechanism. For 6 weeks, the female bank voles were provided with diet containing Cd [less than 0.1 μg/g (control) and 60 μg/g dry wt.] and BaP (0, 5, and 10 μg/g dry wt.) alone or in combination. At the end of exposure period, apoptosis and analyses of MT, Cd, and zinc (Zn) in the liver and kidneys were carried out. Dietary BaP 5 μg/g did not affect but BaP 10 μg/g potentiated rather than inhibited induction of hepatic and renal MT by Cd, and diminished Cd-induced apoptosis in both organs. The hepatic and renal Zn followed a pattern similar to that of MT, attaining the highest level in the Cd + BaP 10-μg/g group. These data indicate that dietary BaP attenuates rather than exacerbates Cd toxicity in bank voles, probably by potentiating MT synthesis and increasing Zn concentration in the liver and kidneys.

Variable mode of estrus affects female decision for multiple mating

Investigating patterns of variation in mating strategies may shed light on their evolutionary importance as well as their impact on the strength and shape of sexual selection. Multimale mating (polyandry) and mate choice are intensely studied subjects in the area of sexual selection, but little is known about intraspecific patterns of variation that may respond to dynamic cost-benefit balances. In a laboratory study, we investigated the mating behavior of female bank voles (Myodes glareolus) with distinctly different time and energy budgets: They were either in cycling estrus (CE) or postpartum estrus (PPE) shortly after delivery. Postpartum mating is highly constrained by time and energy due to maternal commitments to the newborn litter. All females had a free and simultaneous choice among 4 males that differed in scent-marking frequency (indicator of dominance) and body mass. We show that females in CE engaged significantly more often in multimale mating than females in PPE. Additionally, PPE females mated with males that scent marked more, whereas CE females seemingly mated indiscriminately. We discuss our findings in light of time and energy budgets of females and also consider alternative explanations such as pup protection against infanticidal males or physiological constraints to estrus modes.