Maternal antibodies postpone hantavirus infection and enhance individual breeding success

The transfer of maternal antibodies from mother to progeny is a well-known phenomenon in avian and mammalian species. Optimally, they protect the newborn against the pathogens in the environment. The effect of maternal antibodies on microparasite transmission dynamics may have important consequences for both the fitness of the host and the epizootic processes of the pathogens. However, there is a scarcity of studies examining these effects in free-living wild species. We studied the influence of maternal antibodies against the zoonotic Puumala hantavirus (PUUV) on the fitness of bank voles (Clethrionomys glareolus) and on PUUV transmission by exposing young maternal antibody-positive (MatAb+) and negative (MatAb-) bank voles (n=160) to PUUV in experimental populations. PUUV-specific maternal antibodies delayed the timing of infection. Females were more susceptible to PUUV infection than males. Interestingly, both the females and the males with maternal antibodies matured earlier than the other individuals in the population. Our results highlight the significance of maternal antibodies in the transmission of a pathogen and in the breeding success of the carriers.     

Landscape features and helminth co-infection shape bank vole immunoheterogeneity,with consequences for Puumala virus epidemiology

Heterogeneity in environmental conditions helps to maintain genetic and phenotypic diversity in ecosystems. As such, it may explain why the capacity of animals to mount immune responses is highly variable. The quality of habitat patches, in terms of resources, parasitism, predation and habitat fragmentation may, for example, trigger trade-offs ultimately affecting the investment of individuals in various immunological pathways. We described spatial immunoheterogeneity in bank vole populations with respect to landscape features and co-infection. We focused on the consequences of this heterogeneity for the risk of Puumala hantavirus (PUUV) infection. We assessed the expression of the Tnf-α and Mx2 genes and demonstrated a negative correlation between PUUV load and the expression of these immune genes in bank voles. Habitat heterogeneity was partly associated with differences in the expression of these genes. Levels of Mx2 were lower in large forests than in fragmented forests, possibly due to differences in parasite communities. We previously highlighted the positive association between infection with Heligmosomum mixtum and infection with PUUV. We found that Tnf-α was more strongly expressed in voles infected with PUUV than in uninfected voles or in voles co-infected with the nematode H. mixtum and PUUV. H. mixtum may limit the capacity of the vole to develop proinflammatory responses. This effect may increase the risk of PUUV infection and replication in host cells. Overall, our results suggest that close interactions between landscape features, co-infection and immune gene expression may shape PUUV epidemiology.     

Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis

Many zoonotic diseases are caused by rodent-borne viruses. Major fluctuations in the transmission of these viruses have been related to large changes in reservoir host population numbers due to external factors. However, the impact of the pathogen itself on the demography of its reservoir host is often overlooked. We investigated the impact of Puumala virus (PUUV) on survival and reproductive maturation probability of its reservoir host, the bank vole (Myodes glareolus). Three years (2004-06) of data from nine independent sites in southern Belgium were collected and analyzed with a capture-mark-recapture (CMR) method that includes statistical correction for the variation in capture probability of voles. A multistate model based on four states of reproductive activity and PUUV immunoglobulin G (IgG) antibody status was used to estimate survival and probability of transition from one reproductive or infection state to another. Although survival estimates for reproductively active voles were similar between infected and noninfected individuals, PUUV infection in reproductively inactive voles decreased mean monthly survival by 14%. PUUV infection was associated with a threefold increase in the probability of reproductive maturation in bank voles. Moreover, the probability of PUUV IgG seroconversion was three times higher for reproductively active voles compared to reproductively inactive voles. Our model indicates that PUUV infection may alter bank vole population dynamics by affecting both survival and maturation in its host. Additional studies, using CMR methodology with shorter time intervals between trapping sessions and possibly a longer duration, are needed to confirm these findings.     

Environmental change and disease dynamics: effects of intensive forest management on Puumala hantavirus infection in boreal bank vole populations

Intensive management of Fennoscandian forests has led to a mosaic of woodlands in different stages of maturity. The main rodent host of the zoonotic Puumala hantavirus (PUUV) is the bank vole (Myodes glareolus), a species that can be found in all woodlands and especially mature forests. We investigated the influence of forest age structure on PUUV infection dynamics in bank voles. Over four years, we trapped small mammals twice a year in a forest network of different succession stages in Northern Finland. Our study sites represented four forest age classes from young (4 to 30 years) to mature (over 100 years) forests. We show that PUUV-infected bank voles occurred commonly in all forest age classes, but peaked in mature forests. The probability of an individual bank vole to be PUUV infected was positively related to concurrent host population density. However, when population density was controlled for, a relatively higher infection rate was observed in voles trapped in younger forests. Furthermore, we found evidence of a "dilution effect" in that the infection probability was negatively associated with the simultaneous density of other small mammals during the breeding season. Our results suggest that younger forests created by intensive management can reduce hantaviral load in the environment, but PUUV is common in woodlands of all ages. As such, the Fennoscandian forest landscape represents a significant reservoir and source of hantaviral infection in humans.     

Influenza Infection Neutralizes the Attractiveness of Male Odour to Female Mice (Mus musculus)

This study aimed to determine if female house mice, Mus musculus domesticus, are able to assess a male's infection status from odour cues. We collected urine from male mice before, during, and after they were experimentally infected with influenza, a respiratory virus. Females spent more time investigating urine collected from males while they were uninfected than when they were infected. Also 70 % of females released into a large enclosure preferred to nest in boxes containing urine collected from uninfected rather than infected males. This is the first evidence that mice can discriminate virally infected individuals through chemical signals and the first evidence that infection causes odour changes in the urine. To determine if the odour of infected males is repulsive, we presented females with urine samples and neutral water blanks. Normal urine collected from uninfected males was more attractive, whereas urine collected during infection was as attractive as water. This indicates that rather than being aversive, influenza infection abolishes the attractiveness of a male's odour. A similar effect also occurs when male mice are infected with coccidian gut parasites (Kavaliers & Colwell 1995, Proc. R. Soc. Lond. 261B, 31–35). One proximate reason for the neutralization of the attractiveness of a male's odour may be a decrease in serum androgen concentrations during infection.     

Olfactory Experience Affects the Response of Meadow Voles to the Opposite‐Sex Scent Donor of Mixed‐Sex Over‐Marks

Scent marking and over‐marking are important forms of communication between the sexes for many terrestrial mammals. Over the course of three experiments, we determined whether the amount of time individuals investigate the scent marks of opposite‐sex conspecifics is affected by 4 d of olfactory experience with those conspecifics. In Experiment 1, female meadow voles, Microtus pennsylvanicus, spent more time investigating the scent mark of the novel male conspecific than that of the familiar male donor, whereas male voles spent similar amounts of time investigating the scent mark of the familiar female and a novel female conspecific. In Experiment 2, voles were exposed to a mixed‐sex over‐mark in which subjects did not have 4 d of olfactory experience with either the top‐scent donor or the bottom‐scent donor. During the test phase, male and female voles spent more time investigating the scent mark of the opposite‐sex conspecific that provided the top‐scent mark than that of a novel, opposite‐sex conspecific. Male and female voles spent similar amounts of time investigating the scent mark of the bottom‐scent donor and that of a novel opposite‐sex conspecific. In Experiment 3, voles were exposed to a mixed‐sex over‐mark that contained the scent mark of an opposite‐sex conspecific with which they had 4 d of olfactory experience. During the test phase, male voles spent more time investigating the mark of the familiar, top‐scent female than the scent mark of a novel female donor but spent similar amounts of time investigating the mark of the familiar, bottom‐scent female and that of a novel female donor. In contrast, female voles spent more time investigating the mark of a novel male donor than that of either the familiar, top‐scent male or that of the familiar, bottom‐scent male. The sex differences in the responses of voles to scent marks and mixed‐sex over‐marks are discussed in relation to the natural history and non‐monogamous mating system of meadow voles.     

A model system for in vitro studies of bank vole borne viruses

The bank vole (Myodes glareolus) is a common small mammal in Europe and a natural host for several important emerging zoonotic viruses, e.g. Puumala hantavirus (PUUV) that causes hemorrhagic fever with renal syndrome (HFRS). Hantaviruses are known to interfere with several signaling pathways in infected human cells, and HFRS is considered an immune-mediated disease. There is no in vitro-model available for infectious experiments in bank vole cells, nor tools for analyses of bank vole immune activation and responses. Consequently, it is not known if there are any differences in the regulation of virus induced responses in humans compared to natural hosts during infection. We here present an in vitro-model for studies of bank vole borne viruses and their interactions with natural host cell innate immune responses. Bank vole embryonic fibroblasts (VEFs) were isolated and shown to be susceptible for PUUV-infection, including a wild-type PUUV strain (only passaged in bank voles). The significance of VEFs as a model system for bank vole associated viruses was further established by infection studies showing that these cells are also susceptible to tick borne encephalitis, cowpox and Ljungan virus. The genes encoding bank vole IFN-β and Mx2 were partially sequenced and protocols for semi-quantitative RT-PCR were developed. Interestingly, PUUV did not induce an increased IFN-β or Mx2 mRNA expression. Corresponding infections with CPXV and LV induced IFN-β but not Mx2, while TBEV induced both IFN-β and Mx2. In conclusion, VEFs together with protocols developed for detection of bank vole innate immune activation provide valuable tools for future studies of how PUUV and other zoonotic viruses affect cells derived from bank voles compared to human cells. Notably, wild-type PUUV which has been difficult to cultivate in vitro readily infected VEFs, suggesting that embryonic fibroblasts from natural hosts might be valuable for isolation of wild-type hantaviruses.     

Differential foraging in presence of predator and conspecific odors in bank voles: a field enclosure study

Bank voles detect and discriminate other organisms, e.g., predators versus conspecifics, based on olfactory clues like urine, feces, or scent marks. The present field enclosure experiment was set up to determine whether scented food is sufficient for inducing such differentiated reactions in bank voles. Fourteen different odors were tested, divided into four categories: (1) terrestrial predators, (2) avian predators, (3) conspecifics, and (4) neutral origin (human, dog, solvent-treated, and unscented). The odors were extracted with methanol from pellets or feces, or were an artificial substitute. To test the influence of odors on the foraging behavior of voles, artificial food patches containing scented feeders were used. The feeders were cleaned and refilled daily with a calibrated amount of food sprayed with 1 ml of a different odor randomly chosen. The patches were also equipped with monochromatic cameras to monitor the occurrences of voles around the feeders. Both the visits at scented feeders and food consumption were analyzed for each odor. The results show that relative to their foraging activity on unscented food, bank voles significantly reduce it on food scented with odors of terrestrial predators, and increase it in the presence of conspecific odors. Their foraging activity was not affected by neutral scent, nor by scents from avian predators. These results prove that bank voles react to scented food in a way that varies according to the source of odor, even in the semi-natural conditions of an outdoor enclosure.     

Sex differences in olfactory social recognition memory in meadow voles,Microtus pennsylvanicus

Terrestrial mammals, like rodents, use odors, and scent marks to indicate their presence in an area to conspecifics. These odors convey information about the scent donor's genotype, sex, condition, and age. The ability to discriminate among the scent marks of conspecifics and later recollect the identity of the donor is essential for choosing between familiar and unfamiliar mates. We tested the hypothesis that the promiscuous meadow vole (Microtus pennsylvanicus) can recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific. We also hypothesized that because reproductive success is highly skewed among male meadow voles and competition for mates is intense, males will be more likely than females to recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific, for a longer period of time. Using a habituation task, we first exposed the voles, 4 times successively, to the anogenital area scent of an opposite-sex conspecific. Then, 1 hr, 24 hrs, 72 hrs, or 96 hrs after the fourth exposure, voles were presented with the odor of the donor from the exposure phase (familiar donor) and that of an unfamiliar, opposite-sex conspecific. Female meadow voles spent similar amounts of time investigating the scent of the familiar male donor and that of an unfamiliar male donor after the 1-hr and 24-hr intervals. Male meadow voles, however, spent more time with the scent of an unfamiliar female donor than that of the familiar female donor after the 1-hr, 24-hr, and 72-hr intervals, suggesting that male voles could recollect the scent mark of a familiar female for at least three days. The implications of these sex differences in social memory may reflect the different strategies male and female meadow voles use in the recognition of previous and potential mates. Recognition of an individual's scents may enhance fitness by allowing animals to direct appropriate behaviors toward those individuals.     

Dampening of population cycles in voles affects small mammal community structure,decreases diversity,and increases prevalence of a zoonotic disease

Long‐term decline and depression of density in cyclic small rodents is a recent widespread phenomenon. These observed changes at the population level might have cascading effects at the ecosystem level. Here, we assessed relationships between changing boreal landscapes and biodiversity changes of small mammal communities. We also inferred potential effects of observed community changes for increased transmission risk of Puumala virus (PUUV) spread, causing the zoonotic disease nephropatica epidemica in humans. Analyses were based on long‐term (1971–2013) monitoring data of shrews and voles representing 58 time series in northern Sweden. We calculated richness, diversity, and evenness at alpha, beta, and gamma level, partitioned beta diversity into turnover (species replacement) and nestedness (species addition/removal), used similarity percentages (SIMPER) analysis to assess community structure, and calculated the cumulated number of PUUV‐infected bank voles and average PUUV prevalence (percentage of infected bank voles) per vole cycle. Alpha, beta, and gamma richness and diversity of voles, but not shrews, showed long‐term trends that varied spatially. The observed patterns were associated with an increase in community contribution of bank vole (Myodes glareolus), a decrease of gray‐sided vole (M. rufocanus) and field vole (Microtus agrestis) and a hump‐shaped variation in contribution of common shrew (Sorex araneus). Long‐term biodiversity changes were largely related to changes in forest landscape structure. Number of PUUV‐infected bank voles in spring was negatively related to beta and gamma diversity, and positively related to turnover of shrews (replaced by voles) and to community contribution of bank voles. The latter was also positively related to average PUUV prevalence in spring. We showed that long‐term changes in the boreal landscape contributed to explain the decrease in biodiversity and the change in structure of small mammal communities. In addition, our results suggest decrease in small mammal diversity to have knock‐on effects on dynamics of infectious diseases among small mammals with potential implications for disease transmission to humans.     

Bearded reedlings adjust their pair-bond behaviour in relation to the sex and attractiveness of unpaired conspecifics

An individual's investment in mating or keeping a pair bond intact may be influenced not only by the attractiveness of its current mate, but also by that of other potential mates. In this study, we investigated the effect of relative attractiveness on pair-bond behaviour in bearded reedlings, Panurus biarmicus. We showed that mate attractiveness, in terms of beard length in males and tail length in females, influenced courtship behaviour when the pair was kept isolated. In the presence of a conspecific, contact initiations within a pair increased. This increment was mainly related to the sex of the unpaired conspecific, however, and less to differences in attractiveness between the current partner and the unpaired conspecific. Female contact initiations towards potential extra mates were independent of male attractiveness, whereas male contact behaviour was significantly influenced by female attractiveness. However, females displayed more contact initiations to their current mate when they were less attractive than the unpaired females. Males decreased their overtures towards other females with increasing attractiveness of their current mates. Overall, our results suggested that, when there was a risk of losing their mate, bearded reedlings adjust their pair-bond investment mainly in response to the presence or absence of a competitor, and fine-tune investment to a lesser extent in response to the attractiveness of that potential competitor.     

Behavioural development of conspecific odour preferences in bank voles,Clethrionomys glareolus

Biological odours of conspecifics are known to have strong influences on behavioural interaction in bank voles Clethrionomys glareolus. This experiment tested two hypotheses. (1) Olfactory cues from familiar and unfamiliar mature opposite-sex conspecifics differ in their attractiveness to males and females, and their behavioural reactions change with age. (2) A genetically based mechanism is involved in female recognition of kin.In a two-choice preference test, prepubertal males and females were more attracted to familiar than to unfamiliar odours of opposite-sex conspecifics, as manifested by more time spent sniffing familiar voles. As the young reached sexual maturity they shifted their odour preferences. Mature males and females preferred the novel odour of unrelated opposite-sex conspecifics to that of relatives. The results of experiments testing the second hypothesis indicate that females use a genetically based mechanism to recognise their kin. Young and mature females were able to recognise the odour of their biological but socially unknown fathers, and showed the same pattern of behaviour as females in previous experiments.The possible biological functions of kin recognition in bank voles are discussed.     

Brain mast cells are influenced by chemosensory cues associated with estrus induction in female prairie voles (Microtus ochrogaster)

Historically, the brain has been viewed as protected from the infiltration of peripheral hematopoietic cells by the blood-brain barrier. However, numerous immune cell types have been found in the central nervous system (CNS). Mast cells, granulocytic immune cells, are found in the CNS of birds and mammals and their numbers and location are influenced by both extrinsic and intrinsic factors, including reproductive behavior and endocrine status. The present study used female prairie voles (Microtus ochrogaster) to investigate the interactions between brain mast cells and stimuli associated with estrus induction. Unlike spontaneous ovulators such as rats and mice, female prairie voles are induced into estrus by chemosensory stimuli present in conspecific male urine. Prior to estrus induction, female voles have undetectable concentrations of estrogen that rise rapidly following exposure to a male or male urine. In the first experiment, we examined whether mast cells may be influenced by estrus induction. Female voles exposed to conspecific male urine had increased numbers of mast cells in the main olfactory bulbs and epithalamus (medial habenula), but not the thalamus or median eminence, relative to control groups. Next, to determine if this mast cell increase was the result of elevated estrogen concentrations, female voles were injected with estradiol or vehicle and brain mast cell numbers analyzed. No differences in brain mast cell numbers were observed between estradiol-injected and control females in any brain area investigated. Together, these results lend further support to the contention that mast cell numbers and/or distribution can be influenced by reproductively relevant stimuli and underscore the utility of this vole model for delineating the function of brain mast cells.     

Meadow Voles (Microtus pennsylvanicus, Arvicolidae) Over-mark and Adjacent-mark the Scent Marks of Same-sex Conspecifics

Scent over-marking occurs when an animal deposits its scent mark on top of the scent mark of a conspecific; adjacent-marking occurs when an animal deposits its scent mark next to the scent mark of a conspecific. Given that male rodents usually scent mark more than females and that animals spend more time investigating the odor of the top-scent donor of an over-mark, I tested the following three hypotheses. First, male meadow voles deposit more scent marks than female meadow voles. Second, male meadow voles will deposit more over-marks and adjacent-marks in response to the scent marks of a same-sex conspecific than females would. Third, meadow voles spend more time investigating the odor of the second vole placed in the arena than that of the first vole placed in the arena. To test these hypotheses, two age-matched, like-sex conspecifics (first vole and second vole) were placed successively into an arena in which they were allowed to freely explore and scent mark for 15 min. The first hypothesis was not supported. The first and second vole, independently of sex, deposited a similar number of scent marks. The second hypothesis was also not supported by the data: more conspecific scent marks were over-marked by the second female than by the second male. The third hypothesis was supported by the data. After investigating a scented arena, males and females spent more time investigating the odor of the second vole than that of the first vole. Sex differences in scent-marking behaviors of meadow voles are unlike those reported for other species of rodents.     

Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents

Sublethal effects of parasitic infection, such as reductions in reproductive rate, can significantly affect host population dynamics. Here we show that in wild populations of both Clethrionomys glareolus (bank vole) and Apodemus sylvaticus (wood mouse), females infected with cowpox virus are likely to delay maturation and therefore reproduction – in most cases until the following breeding season. Some infected bank voles do mature in their year of birth but still take longer than uninfected females. Together with our previous demonstration that individuals infected with cowpox virus in the summer survive better than uninfected individuals, these results support the prediction that hosts that develop an acute infection may best optimise their fitness by decreasing current reproduction to maximise the probability of surviving infection. Moreover, as the proportion of individuals infected increases with density, the reduction in host fecundity may have significant consequences for host dynamics.     

The degree of leukocytosis and urine GATA-3 mRNA levels are risk factors for severe acute kidney injury in Puumala virus nephropathia epidemica

Puumala hantavirus (PUUV) infection, also known as nephropathia epidemica, is the most common cause of hemorrhagic fever with renal syndrome (HFRS) in Europe. The pathogenesis of PUUV nephropathia epidemica is complex and multifactorial, and the risk factors for severe acute kidney injury (AKI) during acute PUUV infection are not well defined. We conducted a prospective study of hospitalized patients with PUUV infection in Tampere, Finland to identify acute illness risk factors for HFRS severity. Serial daily blood and urine samples were collected throughout acute illness and at 2 week and 6 month convalescent visits. By univariate analyses, the maximum white blood cell count during acute illness was a risk factor for severe AKI. There were no significant associations between PUUV-induced AKI severity and platelet counts, C-reactive protein, or alanine aminotransferase levels. Maximum plasma interleukin (IL)-6, urine IL-6, and urine IL-8 concentrations were positively associated with PUUV-induced AKI. Finally, the maximum urinary sediment GATA-3 mRNA level was positively correlated with the peak fold-change in serum creatinine, regardless of AKI severity classification. By multivariate analyses, we found that the maximum levels of leukocytes and urinary sediment GATA-3 mRNA during acute illness were independent risk factors for severe PUUV-induced AKI. We have identified novel acute illness risk factors for severe PUUV-induced AKI.     

Landscape genetics highlights the role of bank vole metapopulation dynamics in the epidemiology of Puumala hantavirus

Rodent host dynamics and dispersal are thought to be critical for hantavirus epidemiology as they determine pathogen persistence and transmission within and between host populations. We used landscape genetics to investigate how the population dynamics of the bank vole Myodes glareolus, the host of Puumala hantavirus (PUUV), vary with forest fragmentation and influence PUUV epidemiology. We sampled vole populations within the Ardennes, a French PUUV endemic area. We inferred demographic features such as population size, isolation and migration with regard to landscape configuration. We next analysed the influence of M. glareolus population dynamics on PUUV spatial distribution. Our results revealed that the global metapopulation dynamics of bank voles were strongly shaped by landscape features, including suitable patch size and connectivity. Large effective size in forest might therefore contribute to the higher observed levels of PUUV prevalence. By contrast, populations from hedge networks highly suffered from genetic drift and appeared strongly isolated from all other populations. This might result in high probabilities of local extinction for both M. glareolus and PUUV. Besides, we detected signatures of asymmetric bank vole migration from forests to hedges. These movements were likely to sustain PUUV in fragmented landscapes. In conclusion, our study provided arguments in favour of source‐sink dynamics shaping PUUV persistence and spread in heterogeneous, Western European temperate landscapes. It illustrated the potential contribution of landscape genetics to the understanding of the epidemiological processes occurring at this local scale.     

布氏田鼠在不同光周期下对陌生个体尿液和粪便的气味辨别

研究了成年布氏田鼠在10min内,对不同光照周期下（长光照：LD;短光照：SD）陌生雌／雄个体尿液和粪便两种单一个体气味源的气味行为反应,实验发现：所有雌雄被试鼠对LD气味源比SD气味源表现出更多的嗅闻行为。LD和SD被试鼠对同性／异性尿液气味的嗅闻行为没有表现出明显的差别,但LD被试雄鼠对陌生雌鼠粪便的嗅闻频次显多于SD被试雄鼠,从嗅闻行为特征量（嗅闻行为占所有行为的百分比）来看,所有LD和SD被试雌,雄鼠对尿液的嗅 明显多于粪便,除SD粪便气味外,被试鼠对异性气味源的嗅闻明显多于同性,实验结果表明：作为两种个体气味源,尿液和粪便都带有季节性信息,而且是具有性别特性的。异性的个体气味源比同性的个体气味源更具吸引力;长光照动物的个体气味比短光照动物的气味更具吸引力。     

Is Mating Alone Enough to Inhibit Infanticide in Male Bank Voles?

Infanticide, the killing of conspecific young, is commonly recognized as an adaptive behavioural strategy enhancing the fitness of the perpetrator. Infanticide is supposed to be inhibited in several male rodent species after mating with a time lag to the time when perpetrators own offspring would be born. This is because males with no parental care do not recognize their own offspring. It has been suggested that copulation alone is enough to inhibit infanticidal behaviour in male rodents. Infanticidal behaviour occurs in more than 50% of male bank voles (Myodes glareolus), and offspring loss because of infanticide may have a great effect on breeding success and population recruitment. In a laboratory experiment, we studied whether infanticidal male bank voles after successful mating stop the killing of pups. Infanticidal males were paired with a female until successful copulation. After the young were born, the males’ infanticidal behaviour was studied from the time of expected birth of own pups until their post‐weaning age. We predicted that mated infanticidal males are inhibited from committing infanticide especially during the time period when pups are less than 10 d old. Against our prediction, 67% of the infanticidal males continued the killing of pups in the age of 3 d. Infanticidal behaviour remained stable, and half of the males were infanticidal still at the age of weaning of pups. Our results are contradictory to previous studies, as we observed no inhibition of infanticide during early life of pups nor increase in infanticide again when their own offspring would have reached the ‘safe’ age and size after weaning. We suggest that mating alone is not sufficient to inhibit infanticide. Thus, we suggest that other cues of the female with whom the male mated with or on her territory are needed for inhibition to occur.     

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

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