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

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.

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.

Background Animal skin and gut microbiomes are important components of host fitness. However, the processes that shape the microbiomes of wildlife are poorly understood, particularly with regard to exposure to environmental contaminants. We used 16S rRNA amplicon sequencing to quantify how exposure to radionuclides impacts the skin and gut microbiota of a small mammal, the bank vole Myodes glareolus , inhabiting areas within and outside the Chernobyl Exclusion Zone (CEZ), Ukraine. Results Skin microbiomes of male bank voles were more diverse than females. However, the most pronounced differences in skin microbiomes occurred at a larger spatial scale, with higher alpha diversity in the skin microbiomes of bank voles from areas within the CEZ, whether contaminated by radionuclides or not, than in the skin microbiomes of animals from uncontaminated locations outside the CEZ, near Kyiv. Similarly, irrespective of the level of radionuclide contamination, skin microbiome communities (beta diversity) showed greater similarities within the CEZ, than to the areas near Kyiv. Hence, bank vole skin microbiome communities are structured more by geography than the level of soil radionuclides. This pattern presents a contrast with bank vole gut microbiota, where microbiomes could be strikingly similar among distant (~ 80 km of separation), uncontaminated locations, and where differences in microbiome community structure were associated with the level of radioactivity. We also found that the level of (dis)similarity between the skin and gut microbiome communities from the same individuals was contingent on the potential for exposure to radionuclides. Conclusions Bank vole skin and gut microbiomes have distinct responses to similar environmental cues and thus are structured at different spatial scales. Our study shows how exposure to environmental pollution can affect the relationship between a mammalian host’s skin and gut microbial communities, potentially homogenising the microbiomes in habitats affected by pollution.

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.

Understanding how societies resolve conflicts between individual and common interests remains one of the most fundamental issues across disciplines. The observation that humans readily incur costs to sanction uncooperative individuals without tangible individual benefits has attracted considerable attention as a proximate cause as to why cooperative behaviours might evolve. However, the proliferation of individually costly punishment has been difficult to explain. Several studies over the last decade employing experimental designs with isolated groups have found clear evidence that the costs of punishment often nullify the benefits of increased cooperation, rendering the strong human tendency to punish a thorny evolutionary puzzle. Here, we show that group competition enhances the effectiveness of punishment so that when groups are in direct competition, individuals belonging to a group with punishment opportunity prevail over individuals in a group without this opportunity. In addition to competitive superiority in between-group competition, punishment reduces within-group variation in success, creating circumstances that are highly favourable for the evolution of accompanying group-functional behaviours. We find that the individual willingness to engage in costly punishment increases with tightening competitive pressure between groups. Our results suggest the importance of intergroup conflict behind the emergence of costly punishment and human cooperation.

Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus , collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides, and from uncontaminated control sites elsewhere in Ukraine. Inhabiting the Chernobyl Exclusion Zone was associated with reduced TL in the liver and testis, and upregulation of telomerase in brain and liver. Thus upregulation of telomerase does not appear to associate with longer telomeres but may reflect protective functions other than telomere maintenance or an attempt to maintain shorter telomeres in a stressful environment. Tissue specific differences in the rate of telomere attrition and apparent radiosensitivity weaken the intra-individual correlation in telomere length among tissues in voles exposed to radionuclides. Our data show that ionizing radiation alters telomere homeostasis in wild animal populations in tissue specific ways.

Background Lyme borreliosis is the most common tick-borne disease in Europe and is often caused by Borrelia afzelii, which is transmitted by Ixodes ricinus ticks. The prevalence and abundance of infected ticks fluctuate in time and space, influencing human infection risk. Rodents are reservoir hosts for B. afzelii and important feeding hosts for larval ticks. In the study reported here, we examined how variation in rodent abundance is associated with B. afzelii infection prevalence in ticks, the density of nymphs (DON) and the density of infected nymphs (DIN) in the following year. We further analysed the relationships between the abundance of infected rodents and nymphal infection prevalence (NIP) and DIN. Methods We conducted a study that combined experimental and observational approaches on 15 islands (10 small islands and 5 large islands) in Finland. On all of the islands, ticks and rodents were monitored and sampled during the summer of 2019, with the monitoring of tick abundance and sampling continuing into the spring of 2020. On five of the 10 small islands, captured rodents were removed from the island (“removal” islands), and on the other five small islands, captured rodents were released back to the trapping site after marking and sampling (“control” islands). On the five large islands, captured rodents were released back to the trapping site after marking and sampling. The presence of B. afzelii from nymph and rodent samples was examined. Results The results of the experimental study showed that neither treatment (removal), rodent abundance index nor abundance index of infected rodents in 2019 was associated with DON, NIP or DIN in 2020. Based on data from the observational study, the NIP in 2020 decreased with increasing rodent abundance index and abundance index of infected rodents in 2019. However, the DIN in 2020 was not associated with the rodent abundance index or the abundance index of infected rodents in 2019. In addition, in the observational study, DON in 2020 increased with increasing rodent abundance index. Conclusions Our results suggest that low rodent abundance during the tick activity period is not sufficient for reducing the disease hazard and, hence, rodent removal may not be a feasible control measure in natural ecosystems. Graphical abstract

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.

A cataract is a clouding of the lens that reduces light transmission to the retina and it decreases the visual acuity of the bearer. The prevalence of cataracts in natural populations of mammals and their potential ecological significance, is poorly known. Cataracts have been reported to arise from high levels of oxidative stress and a major cause of oxidative stress is ionizing radiation. We investigated whether elevated frequencies of cataracts are found in eyes of bank voles Myodes glareolus collected from natural populations in areas with varying levels of background radiation in Chernobyl. We found high frequencies of cataracts in voles collected from different areas in Chernobyl. The frequency of cataracts was positively correlated with age and in females also with the accumulated radiation dose. Furthermore, the number of offspring in female voles was negatively correlated with cataract severity. The results suggest that cataracts primarily develop as a function of ionizing background radiation, most likely as a plastic response to high levels of oxidative stress. It is therefore possible that the elevated levels of background radiation in Chernobyl affect the ecology and fitness of local mammals both directly through, for instance, reduced fertility and indirectly, through increased cataractogenesis.