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

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

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

The diet of an individual is a result of the availability of dietary items and the individual's foraging skills and preferences. Behavioural differences may thus influence diet variation, but the evolvability of diet choice through behavioural evolution has not been studied. We used experimental evolution combined with a field enclosure experiment to test whether behavioural selection leads to dietary divergence. We analysed the individual dietary niche via stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) 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 δ15N 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 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 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.

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

Zoonotic diseases, caused by pathogens transmitted between other vertebrate animals and humans, pose a major risk to human health. Rodents are important reservoir hosts for many zoonotic pathogens, and rodent population dynamics affect the infection dynamics of rodent-borne diseases, such as diseases caused by hantaviruses. However, the role of rodent population dynamics in determining the infection dynamics of rodent-associated tick-borne diseases, such as Lyme borreliosis (LB), caused by Borrelia burgdorferi sensu lato bacteria, have gained limited attention in Northern Europe, despite the multiannual abundance fluctuations, the so-called vole cycles, that characterise rodent population dynamics in the region. Here, we quantify the associations between rodent abundance and LB human cases and Puumala Orthohantavirus (PUUV) infections by using two time series (25-year and 9-year) in Finland. Both bank vole (Myodes glareolus) abundance as well as LB and PUUV infection incidence in humans showed approximately 3-year cycles. Without vector transmitted PUUV infections followed the bank vole host abundance fluctuations with two-month time lag, whereas tick-transmitted LB was associated with bank vole abundance ca. 12 and 24 months earlier. However, the strength of association between LB incidence and bank vole abundance ca. 12 months before varied over the study years. This study highlights that the human risk to acquire rodent-borne pathogens, as well as rodent-associated tick-borne pathogens is associated with the vole cycles in Northern Fennoscandia, yet with complex time lags.

Population cycles and outbreaks of small rodents: ten essential questions we still need to solve.

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.

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

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

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

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

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

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.

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

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.

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.

Socio-reproductive Conflicts and the Father's Curse Dilemma.

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.

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.

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

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

Balancing selection maintains polymorphisms at neurogenetic loci in field experiments.

Most variation in behavior has a genetic basis, but the processes determining the level of diversity at behavioral loci are largely unknown for natural populations. Expression of arginine vasopressin receptor 1a (Avpr1a) and oxytocin receptor (Oxtr) in specific regions of the brain regulates diverse social and reproductive behaviors in mammals, including humans. That these genes have important fitness consequences and that natural populations contain extensive diversity at these loci implies the action of balancing selection. In Myodes glareolus, Avpr1a and Oxtr each contain a polymorphic microsatellite locus located in their 5' regulatory region (the regulatory region-associated microsatellite, RRAM) that likely regulates gene expression. To test the hypothesis that balancing selection maintains diversity at behavioral loci, we released artificially bred females and males with different RRAM allele lengths into field enclosures that differed in population density. The length of Avpr1a and Oxtr RRAMs was associated with reproductive success, but population density and the sex interacted to determine the optimal genotype. In general, longer Avpr1a RRAMs were more beneficial for males, and shorter RRAMs were more beneficial for females; the opposite was true for Oxtr RRAMs. Moreover, Avpr1a RRAM allele length is correlated with the reproductive success of the sexes during different phases of reproduction; for males, RRAM length correlated with the numbers of newborn offspring, but for females selection was evident on the number of weaned offspring. This report of density-dependence and sexual antagonism acting on loci within the arginine vasopressin-oxytocin pathway explains how genetic diversity at Avpr1a and Oxtr could be maintained in natural populations.

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

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.

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.

Predator-vole interactions in Northern Europe: the role of small mustelids revised.

The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986-2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator-prey interactions during winter. Our results support the importance of the small mustelids for the vole cycle. However, weakening specialist predation during winters, or an increase in generalist predation, was not associated with the loss of cyclicity. Strengthening of delayed density dependence coincided with strengthening small mustelid influence on the summer population growth rates of voles. In conclusion, a strong impact of small mustelids during summers appears highly influential to vole population dynamics, and deteriorating winter conditions are not a viable explanation for collapsing small mammal population cycles.

First report of Anaplasma phagocytophilum and Babesia microti in rodents in Finland.

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

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

Individuals often differ in their ability to transmit disease and identifying key individuals for transmission is a major issue in epidemiology. Male hosts are often thought to be more important than females for parasite transmission and persistence. However, the role of infectious females, particularly the transient immunity provided to offspring through maternal antibodies (MatAbs), has been neglected in discussions about sex-biased infection transmission. We examined the effect of host sex upon infection dynamics of zoonotic Puumala hantavirus (PUUV) in semi-natural, experimental populations of bank vole (Myodes glareolus). Populations were founded with either females or males that were infected with PUUV, whereas the other sex was immunized against PUUV infection. The likelihood of the next generation being infected was lower when the infected founders were females, underlying the putative importance of adult males in PUUV transmission and persistence in host populations. However, we show that this effect probably results from transient immunity that infected females provide to their offspring, rather than any sex-biased transmission efficiency per se. Our study proposes a potential contrasting nature of female and male hosts in the transmission dynamics of hantaviruses.

Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles.

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.