Male Voles Research Articles

Chronic metals ingestion by prairie voles produces sex-specific deficits in social behavior: An animal model of autism

We examined the effects of chronic metals ingestion on social behavior in the normally highly social prairie vole to test the hypothesis that metals may interact with central dopamine systems to produce the social withdrawal characteristic of autism. Relative to water-treated controls, 10 weeks of chronic ingestion of either Hg ++ or Cd ++ via drinking water significantly reduced social contact by male voles when they were given a choice between isolation or contact with an unfamiliar same-sex conspecific. The effects of metals ingestion were specific to males: no effects of metals exposure were seen in females. Metals ingestion did not alter behavior of males allowed to choose between isolation or their familiar cage-mates, rather than strangers. We also examined the possibility that metals ingestion affects central dopamine functioning by testing the voles’ locomotor responses to peripheral administration of amphetamine. As with the social behavior, we found a sex-specific effect of metals on amphetamine responses. Males that consumed Hg ++ did not increase their locomotor activity in response to amphetamine, whereas similarly treated females and males that ingested only water significantly increased their locomotor activities. Thus, an ecologically relevant stimulus, metals ingestion, produced two of the hallmark characteristics of autism – social avoidance and a male-oriented bias. These results suggest that metals exposure may contribute to the development of autism, possibly by interacting with central dopamine function, and support the use of prairie voles as a model organism in which to study autism.

Parental care, aggressiveness, and testosterone secretion in male common voles (Microtus arvalis) and steppe lemmings (Lagurus lagurus)

Parental care, aggressiveness, and testosterone secretion in male common voles (Microtus arvalis) and steppe lemmings (Lagurus lagurus)

Androgenic and Oestrogenic Influences on Tyrosine Hydroxylase‐Immunoreactive Cells of the Prairie Vole Medial Amygdala and Bed Nucleus of the Stria Terminalis

The posterodorsal medial amygdala (MeApd) and principal nucleus of the bed nucleus of the stria terminalis (pBST) are densely interconnected sites integrating steroid hormone and olfactory information necessary for sociosexual behaviours in many rodents. Our laboratory recently reported sexually dimorphic populations of cells containing tyrosine hydroxylase (TH) located in the MeApd and pBST of prairie voles (Microtus ochrogaster), with males having many more TH-immunoreactive (-ir) cells in these sites than do females. Gonadal hormones circulating during adulthood were showm to regulate this sex difference because it was eliminated by castrating adult males or implanting females with testosterone-filled capsules. In the present study, we demonstrate that many (25-65%) TH-ir cells in the MeApd and pBST of adult virgin male and female prairie voles also contain immunoreactivity for either the androgen receptor or oestrogen receptor alpha. Subcutaneous implants of oestradiol benzoate mimicked the effects of testosterone and maintained high numbers of TH-ir cells in these sites in castrated males. However, implants of dihydrotestosterone (DHT) did not, and these males had low numbers of TH-ir cells similar to castrated males given empty capsules. A similar effect was found in females, where testosterone or oestradiol benzoate greatly increased the number of TH-ir cells in these sites compared to intact or ovariectomised controls, but DHT did not. DHT implants did, however, maintain high seminal vesicle weights in males. Thus, many of the TH-ir cells in the prairie vole MeApd and pBST are potentially sensitive to androgens and oestrogens, although maintaining immunocytochemically detectable levels of TH in these cells may depend more on an oestrogen-mediated mechanism in both sexes. These data have implications for understanding how gonadal hormone release across the reproductive cycle modulates these species-specific groups of catecholaminergic cells and socially monogamous behaviours in prairie voles.

Effects of photoperiod and temperature on the body mass and the mass of reproductive organs in male Brandt's voles (Lasiopodomys brandtii)

Abstract Using a laboratory colony we demonstrated that the body mass (BM) and reproductive organ mass (ROM) of Brandt's voles vary in response to photoperiod and temperature. Male Brandt's voles from 25 days of age were housed under long (14L) or short (10L) photoperiod, which corresponds to seasonal changes in their natural environment. Under 10L, animals housed for the first 7 weeks at 10°C were significantly lighter than those housed at 20°C. This effect was not observed under 14L. However, a change from an initial 10L photoperiod to the 14L photoperiod for the following 9 weeks could compensate the effects of low temperature on BM. Changes in BM in response to photoperiod and/or temperature exposure appeared to be primarily as a result of the deposition or loss of fat-free dry mass and water. For Brandt's voles, ROM was regulated significantly by photoperiod but not by temperature. Taken together, the results suggest that BM and ROM for male Brandt's voles respond selectively to photoperiodic information and temperature. We propose that a compensatory relationship between photoperiod and temperature should be considered in animal physiology research.

Self-grooming induced by sexual chemical signals in male root voles (Microtus oeconomus Pallas)

Sniffing is one-way animals collect chemical signals, and many males self-groom when they encounter the odor of opposite-sex conspecifics. We tested the hypothesis that sexual chemical signals from females can induce self-grooming behavior in male root voles (Microtus oeconomus Pallas). Specifically, we investigated the sniffing pattern of male root voles in response to odors from the head, trunk, and tail areas of lactating and non-lactating females. The self-grooming behavior of males in response to female individual odorant stimuli was documented, and the relationship between self-grooming and sniffing of odors from the head, trunk, and tails areas were analyzed. Sniffing pattern results showed that males are most interested in odors from the head area, and more interested in odors from the tail as compared to the trunk area. Males displayed different sniffing and self-grooming behaviors when they were exposed to odors from lactating females as compared to non-lactating females. Males also spent more time sniffing and engaged in more sniffing behaviors in response to odors from the lactating females' tail area as compared to the same odors from non-lactating females. Similarly, males spent more time self-grooming and engaged in more self-grooming behaviors in the presence of individual odors from lactating females as compared to individual odors from non-lactating females. Partial correlation analyses revealed that the frequency of self-grooming was significantly correlated with the frequency of tail area sniffs. Results from this experiment suggest that sexual attractiveness of lactating females is stronger than that of non-lactating females. Furthermore, the partial correlation analysis demonstrated that self-grooming in males is induced by odors from the tail area of females. Collectively, these results support the hypothesis that sexual chemical signals from females can induce self-grooming behavior in male root voles. Self-grooming may also reflect the groomer's sexual motivation and facilitate sexual interactions.

Parent–offspring recognition in Brandt's voles, Lasiopodomys brandti

We investigated social interaction behaviour (amicable versus agonistic) to evaluate parent–offspring recognition in male and female Brandt's voles. We first examined whether the parents were able to distinguish their own familiar related offspring at the age of weaning from unfamiliar unrelated offspring. Both male and female parents, when encountering unfamiliar unrelated juveniles in a neutral arena, showed significantly more agonistic behaviour than when encountering their own familiar offspring, which suggested that adult Brandt's voles might be able to discriminate their own familiar descendants from unfamiliar unrelated ones. Second, we used cross-fostering to investigate the underlying parent–offspring recognition mechanism. Both males and females showed more amicable behaviour and less agonistic behaviour to familiar related offspring than to unfamiliar related offspring. Males showed significantly more amicable behaviour to familiar related offspring than to unfamiliar related offspring, and significantly less agonistic behaviour to familiar unrelated offspring than to unfamiliar unrelated offspring. Remarkably, females showed less agonistic behaviour to familiar related offspring than to unfamiliar related offspring. Furthermore, males and females did not show a significant difference in amicable or agonistic behaviour between familiar related and familiar unrelated offspring or between unfamiliar related and unfamiliar unrelated offspring. Our results suggest that the mechanism of parent–offspring discrimination in Brandt's voles could be familiarity.

Self-grooming by male meadow voles differs across copulation but is not affected by the risk and intensity of sperm competition

AbstractMeadow voles, Microtus pennsylvanicus, self-groom before, during and after copulation, which may convey olfactory information to nearby conspecifics. Since males who self-groom at high rates were found to be attractive to females, it is possible that the copulating male may attempt to increase his attractiveness over that of other males who are present or nearby. In that the presence of other males affects sperm investment and can be used by males as an indicator of sperm competition, we tested the hypothesis that the presence of scent marks of other males near a sexually receptive female affects the self-grooming behaviour of males that encounter them. We did so by pairing a male and a female vole in the presence of the odours of one male conspecific, five male conspecifics, or no male conspecifics. The amount of time male voles self-groomed was not affected by the risk or intensity of sperm competition. We also tested the hypothesis that self-grooming behaviour of males differed depending on whether it was performed before, during, or after copulation. Male voles differed in the amount of time and the location on their body that they self-groomed before, during, and after copulation.

Density dependence of infanticide and recognition of pup sex in male bank voles

[Infanticide — the killing of conspecific young — is a common phenomenon in many invertebrate and vertebrate species, particularly common in rodents. It can increase juvenile mortality and, thus, affect population growth. Male infanticide is explained by adaptive hypotheses based on sexual selection. Removing future competitors for mating opportunities would require recognition of pup sex and directing infanticide against male pups. We studied whether the sex of a pup and population density affect male bank voles' ( Myodes glareolus ) aggressive behaviour towards conspecific pups. Population density increased aggressiveness. Against our predictions, male bank voles from high density populations reacted more aggressively towards female than male pups. No sex bias in aggressive behaviour was found among males from low density populations. Our study is the first one to show that males are able to recognize pup sex and act accordingly. We suggest resource competition as an explanation for male infanticide. Our results suggest that females are the critical sex in species where female territoriality and saturation of reproductive space determine the social structure and individual reproductive success. Thus, selective infanticide of female pups in high density populations may act to reduce future female–female competition and enhance the perpetrator male's inclusive fitness., Infanticide — the killing of conspecific young — is a common phenomenon in many invertebrate and vertebrate species, particularly common in rodents. It can increase juvenile mortality and, thus, affect population growth. Male infanticide is explained by adaptive hypotheses based on sexual selection. Removing future competitors for mating opportunities would require recognition of pup sex and directing infanticide against male pups. We studied whether the sex of a pup and population density affect male bank voles' ( Myodes glareolus ) aggressive behaviour towards conspecific pups. Population density increased aggressiveness. Against our predictions, male bank voles from high density populations reacted more aggressively towards female than male pups. No sex bias in aggressive behaviour was found among males from low density populations. Our study is the first one to show that males are able to recognize pup sex and act accordingly. We suggest resource competition as an explanation for male infanticide. Our results suggest that females are the critical sex in species where female territoriality and saturation of reproductive space determine the social structure and individual reproductive success. Thus, selective infanticide of female pups in high density populations may act to reduce future female–female competition and enhance the perpetrator male's inclusive fitness.]

How Owls Select Their Prey: A Study of Barn OwlsTyto albaand Their Small Mammal Prey

Male Barn Owls Tyto alba delivered significantly more male than female Field Voles Microtus agrestis to their mates and nestlings in spring. The male bias was evident both in the prey stored at the nest and in the skeletal remains of prey in pellets taken from the nest. The sex ratio in voles caught by trapping showed a slight female bias. Analysis of pellets produced by the male barn owls at their roosts at the same time, showed the same biased sex ratio of voles, demonstrating that selection of male voles occurred at capture and was not a result of differences between prey delivered to the nest and those consumed by the males. The mean weights of trapped male and female voles in spring were 23.4 g (SE 0.5) and 18.5 g (SE 0.4) respectively. During winter when voles were not breeding the sex ratio in pellets of male and female owls was close to unity. This suggests that the increased aggressiveness and/or activity levels of male voles associated with territorial behaviour and breeding in spring led to an increase in their detection rate by owls hunting by use of auditory cues. Thus the selection for male voles was the result of an increased encounter rate rather than optimal foraging based on the greater body mass of male voles. In spring the owls caught significantly more Field Voles than Wood Mice Apodemus sylvaticus than predicted from the relative abundances of the two species in the field. It is suggested this was the result of the greater ability of Wood Mice to detect the owls and their greater agility in evading capture.

Age Affects Over-Marking of Opposite-Sex Scent Marks in Meadow Voles, Microtus pennsylvanicus

Models of age-related effects on behavior predict that among short-lived species younger adults are more attractive and attracted to opposite-sex conspecifics than are older adults, whereas the converse is predicted for long-lived species. Although most studies of age-related effects on behavior support these predictions, they are not supported by many studies of scent marking, a behavior used in mate attraction. Over-marking, a form of scent marking, is a tactic used by many terrestrial mammals to convey information about themselves to opposite-sex conspecifics. The present study tested the hypothesis that the age of meadow voles, Microtus pennsylvanicus; a microtine rodent, affects their over- and scent marking behaviors when they encounter the marks of opposite-sex conspecifics. Sex differences existed in the over-marking behavior of adult voles among the three different age groups that were tested. Male voles that were 5-7 mo-old and 10-12 mo-old over-marked a higher proportion of the marks of females than did 2-3 mo-old male voles. Female voles that were 2-3 mo-old, 5-7 mo-old, and 10-12 mo-old over-marked a similar number of marks deposited by male voles. Overall, the data were not consistent with models predicting the behavior of short-lived animals such as rodents when they encounter the opposite sex. The differences in over-marking displayed by older and younger adult male voles may be associated with life history tradeoffs, the likelihood that they will encounter sexually receptive females, and being selected as mates.

Role of hypoleptinemia during cold adaptation in Brandt's voles (Lasiopodomys brandtii)

Brandt's voles Lasiopodomys brandtii exhibit large increases in nonshivering thermogenesis to cope with chronic cold exposure, resulting in compensatory hyperphagia and fat mobilization. These physiological events are accompanied by a remarkable reduction in serum leptin levels. However, the role of hypoleptinemia in cold adaptation in this species is still unknown. In the present study, we tested the hypothesis that hypoleptinemia contributes to increases in food intake and brown adipose tissue (BAT) thermogenesis by modifying hypothalamic neuropeptides in cold-exposed Brandt's voles. Adult male voles were transferred to 5 degrees C for 28 days. Accompanied by a decrease in serum leptin levels, hypothalamic agouti-related protein (AgRP) mRNA levels were significantly increased, but there were no changes in the long form of leptin receptor (Ob-Rb), suppressor of cytokine signaling 3 (SOCS3), neuropeptide Y (NPY) mRNA, proopiomelanocortin (POMC), and cocaine- and amphetamine-regulated peptide (CART) mRNA levels in the hypothalamus. When cold-exposed voles were returned to warm (23 degrees C) for 28 days, body mass, food intake, serum leptin, and AgRP mRNA were restored to control levels. Leptin administration in cold-exposed voles decreased food intake as well as hypothalamic AgRP mRNA levels. There were no significant effects of leptin administration on hypothalamic Ob-Rb, SOCS3, NPY, POMC, CART mRNA, and uncoupling protein 1 levels under cold conditions. These results suggest that hypoleptinemia partially contributes to cold-induced hyperphagia, which might involve the elevation of hypothalamic AgRP gene expression.

Flea infestation reduces the life span of the common vole

Parasitism is often a source of variation in host's fitness components. Understanding and estimating its relative importance for fitness components of hosts is fundamental from physiological, ecological and evolutionary perspectives. Host-parasite studies have often reported parasite-induced reduction of host fecundity, whereas the effect of parasitism on host survival has been largely neglected. Here, we experimentally investigated the effect of infestation by rat fleas (Nosopsyllus fasciatus) on the life span of wild-derived male common voles (Microtus arvalis) bred in captivity. We found that the mean life span of parasitized voles was reduced by 36% compared to control voles. Parasitized voles had a smaller body size, but a relatively larger heart and spleen than control voles. These results indicate an effect of flea infestation on host life span and our findings strongly suggest that ectoparasites should be taken into account in the studies of host population dynamics.

Paternal care, aggressiveness, and testosterone secretion in male mandarin voles (Lasiopodomys mandarinus)

Paternal care, aggressiveness, and testosterone secretion in male mandarin voles (Lasiopodomys mandarinus)

Comparison of social interaction and neural activation in the main olfactory bulb and the accessory olfactory bulb between Microtus mandarinus and Microtus fortis

Abstract To gain insight into the function of AOB and MOB during different social interaction and in different vole species, the behaviors and neural activation of the olfactory bulbs in social interactions of mandarin voles Microtus mandarinus and reed voles Microtus fortis were compared in the present research. Mandarin voles spent significantly more time attacking and sniffing their opponents and sniffing sawdust than reed voles. During same sex encounters, mandarin voles attacked their opponents for a significantly longer time and sniffed its opponent for shorter time compared with male-female interactions. However, no significant behavioral differences were found during encounters of two individual reed voles, regardless of gender composition of the pair. Using c-Fos as an indicator of neural activation, we observed that neural activation was significantly higher in almost all sub-regions of the main olfactory bulb (MOB) and the accessory olfactory bulb (AOB) of mandarin voles compared with reed voles. Numbers of c-Fos-ir neurons in almost all sub-regions of the AOB and the MOB during male-female interactions were also higher than those in interactions of the same sex. Anterior-posterior ratios of Fos-ir neurons in the AOBM (AOBMR) and the AOBG (AOBGR) in male-female interaction were significantly higher than those in interaction of the same sex. The AOBMR of male mandarin voles and reed voles were larger than those of females in male-female interactions. Behavioral patterns are consistent with cellular activity patterns. Consistent level of neural activation in MOB and AOB suggests important roles of both the main olfactory bulb and the accessory olfactory bulb in social interaction in two species.

Semen quantity and quality correlate with bank vole males’ social status

Laboratory studies reveal that in several rodent species the females prefer dominant males as mating partners. Here we investigate the correlation between bank vole males' social rank and their sperm quality and quantity. We used agonistic encounters to determine males' social status. Sperm quality was assessed by its motility, viability, maturity, morphology and sperm tail membrane integrity. Relatively more dominant males were heavier than males of lower social status. The males' social position affected the testes, seminal vesicles and coagulation gland development. The weights of these reproductive organs were significantly higher in more dominant males than in more subordinate males. Sperm counts and the values of the other parameters describing sperm quality were higher in high-ranking males than in subordinates. Our results suggest that bank vole females benefit from choosing and mating with high-ranking males by obtaining more and better-quality sperm.

The effect of testicular macrophages, macrophage-conditioned medium and interleukin-1alpha on the cytoskeleton of bank vole Leydig cells.

Recently, morphological and functional interactions between cytoskeletal elements and their involvement in cell movements, shape changes and/or translocation of organelles have been intensively studied. Thus, the aim of our work was to determine whether testicular macrophages and/or their products have an influence on Leydig cell cytoskeleton. The source of Leydig cells and macrophages were male bank voles from spring and autumn generations, reared in different regime of light for 7-8 weeks. The Leydig cells were growing in monocultures or in co-cultures with testicular macrophages. All cell cultures were divided to controls or human chorionic gonadotropin-stimulated ones. To some of the cultures testicular macrophage-conditioned medium or interleukin-1alpha were added. The cells were analysed immunocytochemically and radioimmunologically. In Leydig cells obtained from animals kept in a long day, grown in co-cultures with macrophages as well as in those stimulated by testicular macrophage-conditioned medium, distinct rearrangements of microtubules and microfilaments were observed. This phenomenon was strengthened in the presence of hCG in culture media. Concomitantly, basal and hCG-stimulated level of testosterone was enhanced, which indicates the possible involvement of the cytoskeleton in the process of androgen biosynthesis. The influence of IL-1alpha on reorganization of cytoskeletal structures was not observed, suggesting that in the modulation of steroidogenesis by this cytokine cytoskeletal elements do not play an important role.

The effect of testicular macrophages, macrophage-conditioned medium and interleukin-1alpha on bank vole Leydig cell steroidogenesis.

It has already been accepted that the function and activity of the testis is regulated not only by gonadotrophins, but also by many locally produced factors and by cell-cell interactions. That is why the aim of our work was to determine whether macrophages and/or their products have an influence on Leydig cell steroidogenic activity. The source of Leydig cells and macrophages were male bank voles of spring and autumn generations, reared in 18 light:6 dark or 6 light:18 dark (18L:6D or 6L:18D) conditions for 7-8 weeks. The Leydig cells were growing in monocultures or in co-cultures with macrophages (testicular or peritoneal), either as control or hCG-stimulated ones. To some of the cultures 6 IU/ml of interleukin 1alpha (IL-1alpha) was added. After then the cells were analysed morphologically, histochemically, and radioimmunologically. In the present study we found many differences in morphology and steroidogenic activity of Leydig cells obtained from different photoperiods. Leydig cells from a long day formed monolayer contrary to the cells from a short one growing as single cells or in clusters. Moreover, Leydig cells from a long photoperiod produced more testosterone and were sensitive to the stimulatory effect of both testicular macrophages and testicular macrophage-conditioned medium. They were also more sensitive to the inhibitory influence of IL-1alpha.

Parental care in captive red-backed vole (Clethrionomys rutilus)

Parental behavior in ten pairs of male and female red-backed voles, Clethrionomus rutilus, was studied under laboratory conditions. Significant sex differences were found in total time spent in the nest, time spent by adults alone in the nest, grooming time, and nest-building activity; in half of the males under study, the level of paternal care was extremely low. These findings indicate different paternal contributions of female and male red-backed voles into the rearing of young, in agreement with the spatial-ethological structure of populations of this species. Parental behavior of C. rutilus is discussed in comparison with that of other species of the subfamily Microtinae.

Patterns of Orthopox Virus Wild Rodent Hosts in South Germany

Although cowpox virus (CPXV) infections in a variety of dead-end hosts have been investigated in Germany for more than 50 years, data on species and geographical distribution of CPXV in reservoir hosts are sparse. Here we present the first comprehensive study of 825 rodents that have been collected in Bavaria, Southern Germany. In summary, six different rodent species (Apodemus flavicollis, Myodes glareolus, Microtus arvalis, Apodemus sylvaticus, Microtus agrestis, and Arvicola amphibius) were trapped at three main trapping sites and investigated using a serum neutralization test (SNT). Prevalence of orthopox virus (OPV)-neutralizing antibodies was (with exception of one trapping site) highest in bank voles, ranging from 24.5% to 42.4%; often with SNT titers > or =96. Two up to 25% of yellow-necked mice were OPV sero-positive, but wood mice only at one site with 5.5%. Up to 7.7% of common voles were found to be OPV seroreactive, while M. agrestis and A. amphibius only sporadically showed seroreactivity. Further analyses of a subset of 450 bank voles and yellow-necked mice trapped at one site over a 18-month period revealed that male yellow-necked mice and female gravid yellow-necked mice had significantly more OPV-neutralizing antibodies. Mean body weight and OPV-seroreactivity were significantly negatively associated in male A. flavicollis. This was not due to shorter body length or smaller body mass index, but previously OPV-infected male A. flavicollis had dramatically reduced mean kidney weights. Seroreactivity in female bank voles was positively related to lung weights. We also found that both male yellow-necked mice and male bank voles with positive SNT titers had higher infestation rates with ectoparasites. We here show for the first time that A. flavicollis beside M. glareolus is a hypothetic host for CPXV, and that there are big geographical and spatial variations concerning the seroprevalence in rodent populations in South Germany.

Longevity differs among sexes but is not affected by repeated immune activation in voles (Microtus arvalis)

Investment of resources in immune defences, despite obvious short-term benefits, may be detrimental to long-term maintenance and thus decrease longevity in absence of parasites. In addition, females and males may differ in immune investment and intrinsic longevity because they are subjected to different degrees of sexual competition and extrinsic mortality. In order to test if sex-specific investment in mounting an immune response reduced longevity, we compared the longevity of captive male and female common voles Microtus arvalis regularly challenged with keyhole limpet haemocyanin, an antigen which elicits the production of antibodies, to the longevity of voles injected with the corresponding antigen-free buffer (phosphate-buffered saline). Injections were repeated every 28 days to mimic a chronic infection. The magnitude of immune response did not vary between males and females and did not affect longevity. Overall, females lived longer than males, independently of the immune challenge. Thus, the long-term costs of immunity seem small in voles. The longevity pattern is consistent with the prediction that male-biased predation or parasitism in the wild causes reduced intrinsic lifespan, but this reduction is not mediated by a decrease in male immunity. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 328–333.