Search

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 increasing levels of anthropogenic disturbance, and was thus highest in urban forest soils and lowest in the national parks. The forest soil microbial communities were structured according to the level of anthropogenic disturbance, with a clear urban signature evident in both bacteria and fungi. Despite notable differences in community composition, there was little change in the predicted functional traits of urban bacteria. By contrast, urban soils exhibited a marked loss of ectomycorrhizal fungi. Soil pH was positively correlated with the level of disturbance, and thus was the strongest predictor of variation in alpha and beta diversity of forest soil communities, indicating a role of soil alkalinity in structuring urban soil microbial communities. Hence, our study shows how the properties of urban forest soils promote an increase in microbial diversity and a change in forest soil microbiota composition. peerReviewed

Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.

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 15 N values than control voles, supporting our hypothesis that predatory voles would consume a higher trophic level diet (more animal versus plant foods). This difference was significant in the early but not the late summer season. The δ 13 C values also indicated a seasonal change in the consumed plant matter and a difference in food sources among selection lines in the early summer. These results imply that environmental factors interact with evolved behavioural tendencies to determine dietary niche heterogeneity. Behavioural selection thus has potential to contribute to the evolution of diet choice and ultimately the species' ecological niche breadth.

The 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 control voles, supporting our hypothesis that predatory voles would consume a higher trophic level diet (more animal vs. plant foods). This difference was significant in the early but not the late summer season. The δ13C values also indicated a seasonal change in the consumed plant matter and a difference in food sources among selection lines in the early summer. These results imply that environmental factors interact with evolved behavioral tendencies to determine dietary niche heterogeneity. Behavioral selection thus has potential to contribute to the evolution of diet choice and ultimately the species’ ecological niche breadth.

The 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 was positively associated with open water coverage and human population density around the study sites. Borrelia burgdorferi s. l.-infected rodents were found only in sites where I. ricinus was abundant, whereas the occurrence of other TBP was independent of I. ricinus presence. These results suggest that I. trianguliceps is not sufficient, at least alone, in maintaining the circulation of B. burgdorferi s. l. in wild hosts. In addition, anthropogenic factors might affect the distribution of I. ricinus ticks and, hence, their pathogens, thus shaping the landscape of tick-borne disease risk for humans.

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) antagonistically affected basal metabolic rate (BMR) and fitness of females under wild conditions. Our results showed elevated BMR in females, but not in males, from the dominant breeding line. However, phenotypically dominant males from the subordinate breeding line had the highest BMR. Males from the dominant line with low BMR sired the most litters and offspring in the field. Similarly, females from the dominant selection line tended to have more offspring if they had lower BMR, while the opposite trend was found in females from the subordinate selection line. Females with high and low BMR reproduced most often, as indicated by a significant quadratic selection gradient. The increased female BMR resulting from selection for male dominance suggests genetic incompatibility between sexes in metabolism inheritance. Elevated BMR in behaviourally dominant males, but not in males from the dominant breeding line, suggests physiological costs in males not genetically suited for dominance. Fitness costs of elevated maintenance costs (measured as BMR) shown here support the energetic compensation hypothesis where high BMR is selected against as it would trade off energy required for other important life‐history attributes. A plain language summary is available for this article.

Evolutionary conflicts between males and females can manifest over sexually antagonistic interactions at loci or over sexually antagonistic interests within a locus. The latter form of conflict, intralocus sexual conflict, arises from sexually antagonistic selection and constrains the fitness of individuals through a phenotypic compromise. These conflicts, and socio-reproductive interactions in general, are commonly mediated by hormones, and thus predictive insights can be gained from studying their mediating effects. Here, we integrate several lines of evidence to describe a novel, hormonally mediated reproductive dilemma that we call the father’s curse, which results from an intralocus conflict between mating and parental efforts. Essentially, a genetic locus exerts pleiotropic and antagonistic effects on the mating effort of one individual and the parental effort of a related individual who is the primary provider of parental care. We outline the criteria for operation of the father’s curse dilemma, provide evidence of the phenomenon, and discuss the predictions and outcomes arising from its dynamics. By integrating the effects of hormones into socio-reproductive conflicts and socio-reproductive effort, clearer links between genotypes, phenotypes, and fitness can be established. peerReviewed

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 test the hypothesis that a high population density environment in the early life of fathers can affect traits associated with offspring fitness. We show that the protein content in the diet and/or social environment experienced during the father's early life (prenatal and weaning) influence the phenotype and survival of his offspring and may indicate adaptation to density-dependent costs. Furthermore, we show that experiencing multiple environmental factors during the paternal early life can lead to a different outcome on the offspring phenotype than stimulated by experience of a single environmental factor, highlighting the need to study developmental experiences in tandem rather than independent of each other.

The 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 polymorphism influences variation in the susceptibility to infection with B. afzelii, we challenged pathogen-free, lab-born individuals of known TLR2 genotype with B. afzelii-infected ticks. We measured the spirochete load in tissues of the bank voles. The susceptibility to infection with B. afzelii following an infected tick bite was very high (95%) and did not differ between TLR2 genotypes. The TLR2 polymorphism also had no effect on the spirochete abundance in the tissues of the bank voles. Under the laboratory conditions of our study, we did not find that the TLR2 polymorphism in bank voles influenced variation in the susceptibility to B. afzelii infection.

Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.

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 multiple lines of evidence from the bank vole (Myodes glareolus) system to outline how T impacts traits associated with reproduction and survival, resulting in a sexually antagonistic genetic trade-off in fitness. A major prediction arising from this work is that lower T is favored in females, whereas the optimal T level in males fluctuates in relation to social and ecological factors. We additionally discuss future directions to further integrate endocrinology into the study of sexual and parent–offspring conflicts.

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 stimuli (variation in food and social environment) in a controlled environment. To assess possible intra-generational effects, the reproductive success of female individuals was investigated by placing them in large outdoor enclosures in two different, ecologically relevant environments (population densities). Resulting offspring were raised in the same population densities where they were conceived and their growth was recorded. When adult, half of the offspring were transferred to opposite population densities to evaluate their winter survival, a crucial fitness trait for bank voles. Our setup allowed us to assess: (a) do early life population density cues elicit an intra-generational adaptive response, that is a higher reproductive success when the density matches the early life cues and (b) can early life stimuli of one generation elicit an intergenerational adaptive response in their offspring, that is a higher growth and winter survival when the density matches the early life cues of their mother. Our results show that the early life environment directly affects the phenotype and reproductive success of the focal generation, but adaptive responses are only evident in the offspring. Growth of the offspring is maintained only when the environment matches their mother's early life environment. Furthermore, winter survival of offspring also tended to be higher in high population densities if their mothers experienced an competitive early life. These results show that the early life environment can contribute to maintain high fitness in challenging environments, but not necessarily in the generation experiencing the early life cues.

Interaction between mitochondrial and nuclear genomes is expected to affect energetic phenotypes of traits linked to mitochondrial physiology, further influencing the fitness. A rodent, the bank vole (Myodes glareolus), has a population structure completely or partially introgressed with mitochondria from its relative, the red vole (M. r utilus). Females that carried either bank vole mitochondria or mitochondria from the introgressed species were repeatedly mated with males of both mtDNA types. We found that in males, but not in females, morpho-physiological phenotypes are affected by sire type, causing decreases in body mass (BM) and basal metabolic rate (BMR; including BM corrected, rBMR) in individuals sired by fathers carrying introgressed mitochondria. Higher effect sizes for the proportion of additive genetic variation (and 5.6, 1.9 and 3.6 times higher narrow sense heritability for BM, BMR and rBMR, respectively), and lower for proportion of environmental variation were detected in progeny of non-introgressed males. Our data indicate that co-adapted and possibly co-introgressed nuclear genes related to energetic physiology have an important role in adaptation to the northern conditions in bank voles, and that sex linked nuclear genes are a potential source for variation in basal metabolic rate.

To estimate the optimality of brood size, it is essential to study the effects of brood size manipulation on offspring survival and reproductive success. Moreover, testing the generality of the hypothesis of reproductive costs requires experimental data from a diversity of organisms. Here I present data on the growth, survival and reproductive success of bank vole Clethrionomys glareolus individuals from manipulated litters. Furthermore, the survival of mothers whose litter size was manipulated was studied. At weaning, the mean weight of pups from enlarged litters was lower and from reduced litters higher compared to control litters. After winter, at the start of the breeding season, individuals from enlarged litters, especially males, were still lighter than individuals from the other two treatments. Litter enlargements did not increase the number of reproducing female offspring per mother, nor did the litter sizes of female offspring differ between treatments. There were no differences between treatments in winter survival of offspring after weaning, but among female offspring, weaning weight explained the survival probabilities over winter. A higher weight of females at winter determined the probability of starting to reproduce in spring. The survival of mothers did not seem to be influenced by litter manipulation performed the previous year. According to the results, mothers nursing enlarged or reduced litters do not gain any fitness benefits in terms of number of offspring surviving to breeding. The results are consistent with the majority of experiments conducted in birds, which have found costs of enlarged brood appearing as offspring trade-offs rather than parent trade-offs.

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 small mustelids have been suggested to be important mammalian predators of voles. As in most of the earlier laboratory studies, predation risk was simulated using fresh mustelid faeces and urine. This made it possible to compare the results from experiments at different spatial scales. We did not find any effect of increased predation risk on spacing behaviour (mean and/or maximum distance moved and home range size) or trappability in either vole species. Simulated predation risk did not affect the breeding of females in gray-tailed voles, as has previously been shown in bank voles. The results disagree with most of the studies conducted in laboratory conditions with small mammals. We discuss whether this discrepancy could be caused by differences in the scale of the experiments.

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 species in the study area, the bank vole Myodes glareolus. Results Ixodes ricinus nymphs and adult females, the life stages responsible for the most of tick bites in humans, peaked in May-June and August-September. Larvae and nymphs were simultaneously active in June and abundance of questing larvae and nymphs in the vegetation showed a positive association with bank vole abundance. Moreover, infesting larvae and nymphs were aggregated on bank voles, and the infestation of bank voles with I. ricinus larvae and nymphs was positively associated with bank vole abundance. Conclusion Our results indicate early summer and early autumn as periods of increased risk for humans to encounter I. ricinus ticks in boreal urban forests and suggest a 2 years life-cycle for I. ricinus with two cohorts of ticks during the same year. Moreover, we identified a simultaneous activity of larvae and nymphs which allows co-feeding on the rodent host, which in turn supports the transmission of several important zoonotic tick-borne pathogens. Finally, we showed that a high density of the rodent host may enhance the risk that ticks and, potentially, tick-borne pathogens pose to human health. Electronic supplementary material The online version of this article (doi:10.1186/s13071-017-2112-x) contains supplementary material, which is available to authorized users.

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.

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 protein structures of the mtDNA marker (cytochrome b) and estimated the environmental envelopes of mitotypes. We found that massive mtDNA introgression occurred without any trace of introgression in the analysed nuclear genes. The results show that the native glareolus mtDNA evolved under past positive selection, suggesting that mtDNA in this system has selective relevance. The environmental models indicate that the rutilus mitotype inhabits colder and drier habitats than the glareolus one that can result from local adaptation or from the geographic context of introgression. Finally, homology models of the cytochrome b protein revealed a substitution in rutilus mtDNA in the vicinity of the catalytic fraction, suggesting that differences between mitotypes may result in functional changes. These results suggest that the evolution of mtDNA in Myodes may have functional, ecological and adaptive significance. This work opens perspective onto future experimental tests of the role of natural selection in mtDNA introgression in this system.

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 respirometer. A significant relationship was found between individuals' consistent (repeatable) personality trait (principal component analysis score reflecting individual differences in proactivity) and their consistent (repeatable) residual BMR (body mass corrected); however, this association depended on mtDNA type and sex. Particularly, the males with original mtDNA showed a positive relationship between proactive behaviour and BMR, which supports the increased-intake model, stating that BMR is positively related to the capacity to engage in costly behaviours. However, this relationship was disrupted in introgressed males, and showed a negative trend in females, suggesting the alternative compensation model. According to our findings, it is likely that consistent differences in behavioural patterns and mtDNA types promote variation between individuals in energy metabolism.

Small rodents are key species in many ecosystems. In boreal and subarctic environments, their importance is heightened by pronounced multiannual population cycles. Alarmingly, the previously regular rodent cycles appear to be collapsing simultaneously in many areas. Climate change, particularly decreasing snow quality or quantity in winter, is hypothesized as a causal factor, but the evidence is contradictory. Reliable analysis of population dynamics and the influence of climate thereon necessitate spatially and temporally extensive data. We combined data on vole abundances and climate, collected at 33 locations throughout Finland from 1970 to 2011, to test the hypothesis that warming winters are causing a disappearance of multiannual vole cycles. We predicted that vole population dynamics exhibit geographic and temporal variation associated with variation in climate; reduced cyclicity should be observed when and where winter weather has become milder. We found that the temporal patterns in cyclicity varied between climatically different regions: a transient reduction in cycle amplitude in the coldest region, low-amplitude cycles or irregular dynamics in the climatically intermediate regions, and strengthening cyclicity in the warmest region. Our results did not support the hypothesis that mild winters are uniformly leading to irregular dynamics in boreal vole populations. Long and cold winters were neither a prerequisite for high-amplitude multiannual cycles, nor were mild winters with reduced snow cover associated with reduced winter growth rates. Population dynamics correlated more strongly with growing season than with winter conditions. Cyclicity was weakened by increasing growing season temperatures in the cold, but strengthened in the warm regions. High-amplitude multiannual vole cycles emerge in two climatic regimes: a winter-driven cycle in cold, and a summer-driven cycle in warm climates. Finally, we show that geographic climatic gradients alone may not reliably predict biological responses to climate change.

The physiological requirements of reproduction are predicted to generate a link between energy, physiology and life history traits. Simultaneously, low maintenance costs, measured by energy consumption, are expected to be advantageous. Here we investigated fitness relatedness of traits by estimating genetic correlations between, and inbreeding depression for, body mass, basal metabolic rate (BMR) and other life history characters in a wild rodent, Myodes glareolus. The narrow-sense heritability of absolute and mass corrected BMRs were high for females (h 2 = 0.48 and 0.42) but low and non-significant for males (0.32 and 0.09). A significant positive genetic correlation between BMR and litter size suggests that traits connected to female fecundity might favour higher metab- olism (i.e. support increased intake hypothesis). However, the estimates of inbreeding depression indicate that, while higher values of body mass and female litter size could be positively associated with overall fitness, the association between BMR and overall fitness in bank voles would be negative (i.e. support compensation hypothesis). This result sug- gests that the advantages of larger litters and larger body mass might be evolutionary constrained by high costs of maintenance of those traits, as reflected by the level of basal metabolism.

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 relatively high even during the crash phases. We further evaluated potential mechanisms contributing to the genetic diversity of the population and found that the peak phases are characterized by both a change in spatial pattern of individuals and a rapid accession of new alleles probably due to migration. We propose that these events act together in maintaining the high genetic diversity within cyclical populations.

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-density enclosures and vice versa. Our results show that the effect of summer (past) density was strong especially on survival and body mass. The response of body mass to summer density was negative in both winter (present) density groups, whereas the response of survival probability was nonlinear and differed between the winter density groups. In particular, our data show a trend for higher overwintering success of individuals originating from the lowest summer densities in low winter density and vice versa. We therefore conclude that the capacity of individuals to respond to a change in density was constrained by the delayed density-dependent effects of environment experienced in the past. These effects have the potential to contribute to vole population dynamics. Possible mechanisms mediating the effects of past environment into present performance include both intrinsic and environmental factors.

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 changed to either a similar or opposite resource environment to overwinter. 3. Adult environment had an overriding effect on reproductive success of females so that females overwintering in food-supplemented enclosures had a higher probability of breeding and advanced the initiation of breeding. However, the characteristics of their litters were determined by juvenile environment: females initially grown in food-supplemented conditions subsequently produced larger litters with bigger pups and a male-biased sex ratio. 4. In males, individuals growing in un-supplemented conditions had the highest survival irrespective of adult environment during winter, whereas in females, neither the juvenile nor adult environments affected their survival significantly. The physiological condition of voles in spring, as determined by haematological parameters, was also differentially affected by juvenile (plasma proteins and male testosterone) and adult (haematocrit) environments. 5. Our results suggest that (i) life-history trajectories of voles are not strictly specialized to a certain environment and (ii) the plastic life-history responses to present conditions can actually be caused by delayed effects of the juvenile environment. More generally, the results are important for understanding the mechanisms of delayed life-history effects as well as recognizing their population dynamic consequences.

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 negative correlation in fitness between full siblings. Our results demonstrate the presence of intralocus sexual conflict for fitness in this small mammal and that sexually antagonistic selection is acting on T. We also found a negative correlation in fitness between parents and their opposite-sex progeny (e.g. father–daughter), highlighting a dilemma for females, as the indirect genetic benefits of selecting reproductively successful males (high T) are lost with daughters. We discuss mechanisms that may mitigate this disparity between progeny quality.

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-related trait under selection and is known to affect mating behaviour. We conducted mating trials in which females derived from family-based selection of testosterone were sequentially paired with four males of different testosterone profiles. 3. We show that artificial selection for high testosterone increased the mating rate of males, but clearly decreased the number of partners that females mated with (and vice versa). Because multiple mating was beneficial for the reproductive success of both sexes, as evidenced by the positive Bateman gradients, the divergent evolutionary interests of testosterone between the sexes can maintain this polygynandrous mating system. 4. Our results highlight how mating rate is concordantly selected in both sexes; however, it is largely influenced by testosterone, which is under sexually antagonistic selection. 5. This study is the first one to emphasise the direct and indirect effects of the endocrine system not only on reproductive physiology and behaviour but also for the evolution of genetic mating strategies in mammals.

Significant inter-individual variation in the rate of animal metabolism is a widespread phenomenon that has started to accumulate general interest. Here we follow recent calls to focus on linkage between the variation in energy metabolism and animal personality. By using wild caught root voles as a study species, we examined the relationship between the behavioral patterns (assessed in open field test) and resting metabolic rate (RMR), both of which are known to show large individual differences and intra-individual consistency in voles. Our results showed only a weak relationship between personality traits and metabolism, since the most parsimonious model (according to AICc) explaining RMR included only body mass and season as factors (explaining 84.8% of variation in RMR). However, the next two alternative models (within ΔAICc=2) also included the personality trait reflecting proactive behaviors (PC1) in addition to body mass, sex and season (85.2 and 85.8% of RMR variance explained, respectively). In all, our study does not provide compelling support for recent ideas of close linkage between behavior and metabolism. Still, our study highlights that even in the case of wild caught individuals, when behavior and metabolism often carry effects of both intrinsic and extrinsic conditions, the potential metabolic effects of varying energetically costly behaviors cannot be neglected.

One of the most striking behavioural adaptations for reducing nest predation is nesting near a top predator. However, in spite of increasing number of studies in forested landscapes reporting reproductive success benefits when nesting near protective associates, studies examining whether protective effects vary with food availability for the top predator are lacking. We asked whether the nest predation on ground nests of birds in Ural Owl (Strix uralensis) territories is dependent on varying food conditions for the owl. This was studied using dummy nests placed at different distances from the Ural Owl nests and repeating the study in different food conditions for the owls (low, increase and peak phases of the vole cycle). The proportion of predated dummy nests differed between different food conditions for Ural Owls being lowest in a low vole year. The distance from the owl nest affected the predation of dummy nests, but only in intermediate food conditions. Due to the lack of control nests located outside the owl territories, we are not able to draw conclusions about the background variation in the nest predation in different food conditions. We hypothesise that fluctuating prey availability for the top predator species under concern may have significant effects on the outcome of species interactions. This currently unexplored idea should be tested further, e.g. by including multiple breeding seasons in the future studies on protective nesting associations.

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 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 thatB. afzeliiinfection 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.

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 the linear selection gradient and selection differential for BMR were positive in females, whereas survival did not correlate with male characteristics. Our findings emphasize the relative importance of individual physiology over ecological factors (e.g. intra-specific competition). Most current models of the origin of endothermy underline the importance of metabolic optima in females, whose physiology evolved to fulfil demands of parental provisioning in mammals. Our novel findings of sex-specific selection could be related to these life history differences between sexes.

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) operating in Finland, and vole abundance data from 15 long-term monitoring projects across the country. Voles were confirmed to have destroyed ca. 4.7 million tree seedlings, covering a total effective damage area of ca. 2600 ha. The directors of the FMAs estimated that the actual level of damage was likely to exceed 8.5 million seedlings, or 5400 ha. Roughly 80% of all damage was inflicted on Norway spruce (Picea abies), ca. 10% on Scots pine (Pinus sylvestris) and ca. 10% on birch (Betula sp.) and other species. Considering costs of replanting alone, a most likely very conservative estimate of the financial impact of vole damage during the winter 2005/06 lies between 2.2 and 4.0 million s. The occurrence of damage during the winter was positively related to vole abundance in the previous autumn. This validates vole population monitoring as an effective tool for forecasting near-future damage to silviculture. Our results suggest that if vole populations continue to fluctuate as they currently do, levels of damage to Finnish forests will be great also in the future, far exceeding damage levels recorded in earlier decades.

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 rather than male offspring regardless of their own body condition. Male pups had a significantly lower growth rate than female pups, so that at weaning, males from enlarged litters were the smallest. Mothers produced more milk for female litters and also defended them more intensively than male offspring. 4. The results agree with the predictions based on the bank vole life history: there will be selection for greater investment in daughters rather than sons, as a larger size seems to be more influencial for female reproductive success in this species. Our finding could be a general rule in highly polygynous, but weakly dimorphic small mammals where females are territorial. 5. The results disagree with the narrow sense Trivers & Willard hypothesis, which states that in polygynous mammals that show higher variation in male than in female reproductive success, high-quality mothers are expected to invest more in sons than in daughters.

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.

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-density populations living on large islands had the highest survival. The results were similar at the population level as the spring population size and density were negatively correlated with PUUV prevalence in the autumn. Our results provide the first evidence for a significant effect of PUUV on host survival suggesting that hantaviruses, and endemic pathogens in general, deserve even more attention in studies of host population dynamics.

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 changing rearing environments from father to son. The bank vole is naturally exposed to considerable sources of spatial and temporal environmental variation and male reproductive success is determined by both intra- (male-male competition) and inter- (females prefer to mate with dominant males) sexual selection. Significant G x E for male dominance was found with crossing reaction norms. Plasma testosterone level (T), rather than condition, determined a male's dominance and T also showed a significant G x E. Dominance showed a considerable plasticity across environments, but was only heritable under stable conditions. We document a negative between-environments correlation of male dominance, suggesting that when the environment changes between father and son, the dominance signal is unreliable to females and sexual selection may be compromised. We discuss how G x E and environmental variation interacting with other mechanisms may preserve the reliability of signals and thus the mechanism of sexual selection itself.

Lack of food resources has been suggested as a factor which limits the growth of cyclic vole populations. During peak phases of the cycle, vole population growth typically ceases during late autumn or early winter, and is followed by a decrease in density over the winter. To investigate whether this decrease is due to increased mortality induced by a depletion of food resources, we studied overwinter food consumption and physiological condition of field voles (Microtus agrestis) in western Finland in both an increase and a decrease phase of a three-year population cycle. The growth rate of vole populations was negatively related both to prevailing vole densities and to densities six months earlier. The condition index of voles, as well as their blood levels of haematocrit, proteins, free fatty acids and immunoglobulin G, were positively related to population growth rate when populations were declining. When populations were increasing, these parameters tended to be negatively related to population growth rate. The overall physiological condition of voles was lower in the winter of the decrease phase as compared to the increase phase. The return rate of voles, a proxy of survival, was also lower in the decrease than in the increase phase of the cycle and positively related to haematocrit levels. Almost 90% of all green vegetation shoots were consumed by voles during the winter of the decrease phase while only two thirds were eaten in the increase phase. Our results suggest that the winter decrease phase of cyclic vole populations is associated with both a deterioration in the physiological condition of voles and a significant depletion of winter food resources. This implies that malnutrition induces poor physiological condition in voles, which in turn may increase mortality either directly through starvation or indirectly through increased susceptibility to predators and pathogens.

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 load (blood parasite Trypanosoma), to non-supplemented mothers. Food supplements affected neither the litter size, the reproductive effort of mothers, nor the litter sex ratios at birth. However, food supplementation significantly increased the birth size of male offspring and improved their condition, as indicated by reduced parasite loads (intestinal Eimeria). Interestingly, mothers in good body condition produced larger male offspring only when environmental conditions were improved by food supplements. Although the adaptiveness of variation in mammalian sex ratios is still questionable, our study indicates that mothers in good condition bias their investment towards male offspring, but only when environmental conditions are favourable.

Predatory birds were formerly suggested to have only negative effects on the breeding success of other birds that breed in the vicinity of their nests. However, the predator may also protect these breeding birds by chasing away other nest predators whilst either defending its own nest or by eating other predators in its territory. Ural owl Strix uralensis is known to be an aggressive nest defender. Although its diet mainly consists of voles, it also preys upon bird species (e.g. Corvidae) and even weasels Mustela nivalis, particularly when the vole densities are low. We carried out a dummy nest experiment on six Ural owl territories in central Finland to study whether Ural owls affect the nest predation rates of ground nesting birds. We found that although dummy nest predation differed between Ural owl territories, in every territory the predation risk was lowest in close proximity to Ural owl nests. The protecting effect of the predator continued for a distance of up to several hundred metres from its nest; a much further distance than could be expected if the effect was due solely to the defence of its own nest. Consequently, as suggested for other predatory birds, it may be that breeding Ural owls influence the bird community both directly by predating upon some species and/or indirectly by providing protection for other species. However, natural evidence on breeding habitat selection and predation risk of ground nesting birds should be obtained before detailed inferences on the effects of Ural owl nests on bird community levels are made.

It is a long held assumption that women have concealed ovulation, which means that men do not know when women's menstrual cycles are in their most fertile phase. Recent empirical results have provided evidence that ovulation may not be totally concealed from pair-bonded males, but the generality and the mechanisms of the finding demand further study. To examine the possible adaptive value of the phenomenon, it is necessary to study whether the ability to detect ovulation is confined to males. We studied these questions in an experiment in which male and female raters rated the sexual attractiveness and intensity of T-shirts' odors worn by 42 women using oral contraceptives (pill users) and by 39 women without oral contraceptives (nonusers). Males rated the sexual attractiveness of nonusers highest at midcycle. However, female raters showed only a nonsignificant trend for this relationship. Neither sex rated attractiveness of the odors of pill users according to their menstrual cycle. The results indicate that men can use olfactory cues to distinguish between ovulating and nonovulating women. Furthermore, the contrasting results between pill users and nonusers may indicate that oral contraceptives demolish the cyclic attractiveness of odors. Together, these findings give more basis for the study of the role of odors in human sexual behavior. Copyright 2004.

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 mean offspring body size at birth by replacing the original litter with heavier pups from smaller litters. Offspring quality was estimated from body size measurements, parasitic infection with Eimeria spp. and the level of immune response to a novel antigen. 3 The analyses revealed that large body size at birth was an advantage in ‘normal’ rearing environments, but a disadvantage in poor ones. The initially normal sized offspring grown in enlarged litters had a relatively good capacity for growth and high immune function confirming that a poor rearing environment alone does not reduce their quality. 4 Our findings that the benefits of large body size depend on the rearing environment suggest that offspring body size is adjusted in relation to litter size, and thus the evolution of these two traits is combined.

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 been considered typical income breeders, in which potential reproductive costs may be masked due to their ability to compensate for increased energetic demands of reproduction. Our results provide evidence that, in the wild, females may be incapable of escaping the costs of reproduction.

Spacing behaviour of female mammals is suggested to depend on the distribution and abundance of food. In addition, food limitation has been found to constrain the reproductive success of females. However, whether females maximize their reproductive success by adjusting space use in relation to current food availability and reproductive effort (e.g. litter size) has not been experimentally studied. We examined these questions by manipulating simultaneously food resources (control vs. food supplementation) and litter sizes (control vs. plus two pups) of territorial female bank voles (Clethrionomys glareolus) in large outdoor enclosures. Females with supplementary food had smaller home ranges (foraging area) and home range overlaps than control females, whereas litter size manipulation had no effect on space use. In contrast, the size of territory (exclusive area) was not affected by food supplementation or litter size manipulation. As we have previously shown elsewhere, extra food increases the reproductive success of bank vole females in terms of size and proportion of weaned offspring. According to the present data, greater overlap of female home ranges had a negative effect on reproductive success of females, particularly on survival of offspring. We conclude that higher food availability increases the reproductive success of bank vole females, and this effect may be mediated through lower vulnerability of offspring to direct killing and/or detrimental effects from other females in the population. Moreover, it seems that when density of conspecifics is controlled for, home range sizes of females, but not territoriality, is related to food resources in Clethrionomys voles.

Reproductive success of territorial female mammals depends partly on their capability to defend their young from conspecific intruders. However, how this is related to the characteristics of females and their litter sizes is largely unknown. The defence activity of 25 female bank voles (Clethrionomys glareolus) in relation to the number of offspring was studied in a behavioural arena by manipulating litter sizes (–2 pups or +2 pups). Infanticidal male bank voles were used as intruders–predators. Moreover, the weaning success (weaned at least one offspring or none) of 15 pairs of neighbouring females was investigated in a large indoor runway system. In each pair of females, the litter size of one female was reduced (–2 pups) and the litter size of the other enlarged (+2 pups). Defence activity of females increased with the number of offspring and the mother's size. However, weaning success of neighbours was related only to their body mass, and litter-size manipulation did not affect weaning success. Present results indicate that, although bank vole females increase their defence intensity with an increase in the number of pups, the weaning success of neighbouring females may be primarily determined by their size and dominance rank.

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, which is considered to be nonzoonotic. The A. phagocytophilum strain (based on a fragment of the msp4 gene) was identical to one found earlier in rodents in the United Kingdom that is transmitted by the tick Ixodes trianguliceps, all the life stages of which feed on small mammals. The infection probability of B. microti in the bank voles was the greater the older the individual was, and males were more often infected than females. A. phagocytophilum infection probability first increased and then decreased with the age of individual without any difference between sexes. While these pathogens presumably pose a limited zoonotic risk to humans in Finland, they might have important interactions with other rodent pathogens and therefore affect infection dynamics of, for example, zoonotic pathogens.