Female Voles Research Articles

Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

Social relationships are dynamic and evolve with shared and personal experiences. Whether the functional role of social neuromodulators also evolves with experience to shape the trajectory of relationships is unknown. We utilized pair bonding in the socially monogamous prairie vole as an example of socio-sexual experience that dramatically alters behaviors displayed toward other individuals. We investigated oxytocin-dependent modulation of excitatory synaptic transmission in the nucleus accumbens as a function of pair-bonding status. We found that an oxytocin receptor agonist decreases the amplitude of spontaneous excitatory postsynaptic currents (sEPSCs) in sexually naive virgin, but not pair-bonded, female voles, while it increases the amplitude of electrically evoked EPSCs in paired voles, but not in virgins. This oxytocin-induced potentiation of synaptic transmission relies on the de novo coupling between oxytocin receptor signaling and endocannabinoid receptor type 1 (CB1) receptor signaling in pair-bonded voles. Blocking CB1 receptors after pair-bond formation increases the occurrence of a specific form of social rejection-defensive upright response-that is displayed toward the partner, but not toward a novel individual. Altogether, our results demonstrate that oxytocin's action in the nucleus accumbens is changed through social experience in a way that regulates the trajectory of social interactions as the relationship with the partner unfolds, potentially promoting the maintenance of a pair bond by inhibiting aggressive responses. These results provide a mechanism by which social experience and context shift oxytocinergic signaling to impact neural and behavioral responses to social cues.

Sex differences in the reward value of familiar mates in prairie voles.

The rewarding properties of social interactions facilitate relationship formation and maintenance. Prairie voles are one of the few laboratory species that form selective relationships, manifested as "partner preferences" for familiar partners versus strangers. While both sexes exhibit strong partner preferences, this similarity in outward behavior likely results from sex-specific neurobiological mechanisms. We recently demonstrated that in operant trials, females worked hardest for access to familiar conspecifics of either sex, while males worked equally hard for access to any female, indicating a sex difference in social motivation. As tests were performed with one social target at a time, males might have experienced a ceiling effect, and familiar females might be more relatively rewarding in a choice scenario. Here we performed an operant social choice task in which voles lever-pressed to gain temporary access to either the chamber containing their mate or one containing a novel opposite-sex vole. Females worked hardest to access their mate, while males pressed at similar rates for either female. Individual male behavior was heterogeneous, congruent with multiple mating strategies in the wild. Voles exhibited preferences for favorable over unfavorable environments in a non-social operant task, indicating that lack of social preference does not reflect lack of discrimination. Natural variation in oxytocin receptor genotype at the intronic single nucleotide polymorphism NT213739 was associated with oxytocin receptor density, and predicted individual variation in stranger-directed aggressive behavior. These findings suggest that convergent preference behavior in male and female voles results from sex-divergent pathways, particularly in the realm of social motivation.

Are male meadow voles (Microtus pennsylvanicus) influenced by social odor context with regard to scent marking behaviors?

AbstractMeadow voles (Microtus pennsylvanicus) rely on olfactory communication, such as scent marking, to find and secure mating opportunities during the breeding season. Scent marks, and odors in general, provide information about the donors and persist in the environment for extended periods, allowing a wide audience. Whether a vole responds to another scent mark(s), or odor(s), depends on the social context and the information the odor provides about the donor(s). Therefore, we examined if male scent marking toward a social odor or female meadow voles is influenced by information present or previously encountered based on contextual differences in the social odor. We presented males with two odor associations of a male with a female with contextual differences in the age of the rival. We tested male scent marking under two conditions: one with two social odors present, current information, and a second with the females present from previously encountered social information, prior information. It was found that rival male age did not affect the scent marking behavior of males toward a social odor or female voles. Rival male age also did not affect preference as males did not show a preference for either female. The lack of an effect may lie in the properties of scent marks and the natural history of meadow voles during the breeding season. The odor of an individual rival may not represent a strong enough competitive threat to influence a signaler's decisions, but the association could still provide the signaler with valuable information about which females are considered high quality.

Meadow voles differentiate between scents of different sources

Abstract Scent marks are an important means of transmitting information between rodents, and they can be produced from several body sources. Previous studies have shown that scents from multiple sources can convey the same information; female meadow voles, for example, have three scent sources that communicate sex. However, possessing three separate sources that convey the same information is likely costly due to the metabolic energy required to produce these signals and the increased chance that eavesdropping individuals may intercept information present in these signals. In this study, we investigated if these scent sources could communicate other information, in addition to scent donor sex, by determining if male meadow voles could distinguish scent marks taken from different sources of a single female scent donor. This was accomplished with a habituation-test method, that allowed us to compare how male meadow voles differently investigate scent from a familiar and novel source of a female scent donor. Male meadow voles could distinguish between faeces and urine scent marks of a female, but could only distinguish mouth from urine and faeces scent marks when first familiarized with mouth scent marks. Our findings suggest that mouth, urine, and faeces scent marks of female meadow voles produce both redundant and distinct information. The overlap in information between scent marks produced from separate sources may be needed to provide social context, which allows receiving individuals to accurately weigh the tradeoffs associated with responding to an olfactory cue. While this overlap in information remains costly, this cost may be minimized by the different fade-out times of scent marks from distinct body sources, which may limit the amount of time information in a scent mark is available to a time period where this information is socially relevant.

Sex-dependent effects of pair bond interruption on anxiety- and depression-like behaviors in adult mandarin voles

Stable and positive social bonds are pretty vital to the development of animals. Instability and disruptions of social bonds, such as maternal separation and social isolation, always produce disastrous influence on physiology, neuroendocrine and behaviors. Pair bond is one of the most important social bonds in adulthood. But the different effects of pair bond interruption between males and females are rarely studied. In the present study, the monogamous mandarin voles (Microtus mandarinus) were used to confirm the time window of pair bond formation. After that, voles were separated from their partner for 1 or 2 weeks. Then anxiety- and depression-like behaviors were investigated by using open field test, light-dark box test, tail suspension test and forced swimming test, respectively. The results showed that: (1) cohabitation for 5 days is sufficient and necessary for mandarin voles to form pair bond; (2) loss of partner is always crucial for the effects of pair bond interruption, while social isolation works in certain behavioral tests.; (3) pair bond interruption for 2 weeks significantly increased the level of anxiety and depression in adult males, but not female mandarin voles. Overall, this research suggested that loss of partner plays a key role in pair bond interruption in male mandarin voles.

Social Experience Alters Oxytocinergic Modulation in the Nucleus Accumbens of Female Prairie Voles

Social relationships are dynamic and evolve with shared and personal experiences. Whether the functional role of social neuromodulators also evolves with experience to shape the trajectory of relationships is unknown. We utilized pair bonding in the socially monogamous prairie voles as an example of socio-sexual experience that dramatically alters behaviors displayed toward other individuals. We investigated oxytocin-dependent modulation of excitatory synaptic transmission in the nucleus accumbens as a function of pair bonding status. We found that an oxytocin receptor agonist decreases the amplitude of spontaneous Excitatory Postsynaptic Currents (EPSCs) in sexually naive virgin, but not pair-bonded, female voles, while it increases the amplitude of electrically evoked EPSCs in paired voles, but not in virgins. This oxytocin-dependent potentiation of synaptic transmission relies on the de novo coupling between oxytocin receptor signaling and endocannabinoid CB1 receptor signaling in pair bonded voles. Blocking CB1 receptors after pair bond formation increases the occurrence of a specific form of social rejection – defensive upright response – that is displayed towards the partner but not towards a novel individual. Altogether, our results demonstrate that oxytocin’s action in the nucleus accumbens is changed through social experience in a way that regulates the trajectory of social interactions as the relationship with the partner unfolds, potentially promoting the maintenance of a pair bond by inhibiting aggressive responses. These results provide a mechanism by which social experience and context shift oxytocinergic signaling to impact neural and behavioral responses to social cues.

Field study reveals morphological and neuroendocrine correlates of seasonal breeding in female water voles, Arvicola terrestris

Seasonally breeding mammals display timely physiological switches between reproductive activity and sexual rest, which ensure synchronisation of births at the most favourable time of the year. These switches correlate with seasonal changes along the hypothalamo-pituitary–gonadal axis, but they are primarily orchestrated at the hypothalamic level through environmental control of KISS1-dependent GnRH release. Our field study shows that births of fossorial water voles, Arvicola terrestris, are concentrated between March and October, which indicates the existence of an annual reproductive cycle in this species. Monthly field monitoring for over a year further reveals dramatic seasonal changes in the morphology of the ovary, uterus and lateral scent glands, which correlate with the reproductive status. Finally, we demonstrate seasonal variation in kisspeptin expression within the hypothalamic arcuate nucleus. Altogether, this study demonstrates a marked rhythm of seasonal breeding in the water vole and we speculate that this is governed by seasonal changes in photoperiod.

Sex-Dependent Effects of Chronic Social Defeat on Emotional and Social Behaviors, and Parameters of Oxytocin and Vasopressin Systems in Mandarin Voles (Microtus mandarinus).

In the regulation of emotional and social behaviors, both oxytocin (OT) and vasopressin (AVP) are sex specific. Although significant sex differences have been reported in the context of behavioral and hormonal responses to social stress, such differences in response to chronic social defeat stress (CSDS) and the underlying neural mechanisms remain largely unknown. By investigating monogamous mandarin voles (Microtus mandarinus), CSDS was found to decrease the percentages of time spent in the central area of the open field, in the open arms of the elevated plus maze, as well as in the light area of the light and dark boxes in both male and female voles. CSDS also increased the observed level of social withdrawal in both sex groups. However, CSDS exposure increased the percentages of immobile time in both the tail suspension test and the forced swim test and reduced the locomotor activity in the open field (in females only). Along with these behavioral changes, the oxytocin receptor (OTR) levels in the nucleus accumbens (NAc) were significantly lower in CSDS-exposed voles of both sexes; however, in males, the levels of OTR in the paraventricular nucleus (PVN) were reduced. CSDS-exposed males showed lower levels of V1aR in the NAc than CSDS-exposed females. Furthermore, induced by a single social defeat event, CSDS reduced c-Fos and OT double labeling in the PVN of females but increased c-Fos and AVP double-labeled neurons in the PVN of males exposed to a single social defeat event. Collectively, the present study indicates that OT and AVP systems may play important regulatory roles in the sex differences of behavioral performances in response to CSDS. These findings suggest mandarin voles as a useful animal model for studying sex-specific behavioral performance and the underlying neurobiological mechanisms of stress-related mental disorders in preclinical studies.

Effects of Tannic Acid on Antioxidant Activity and Ovarian Development in Adolescent and Adult Female Brandt's Voles.

It is well known that tannins can influence the reproduction of animals, but there is little research published to elucidate the mechanics of this phenomenon. The purpose of this study was to investigate the role of antioxidation in the influence of tannic acid on the ovarian development of Brandt's voles (Lasiopodomys brandtii), which is a species of prairie animal that feeds on plants containing tannins. Postnatal 4-week-old female Brandt's voles were treated with 0 (control), 0.3% (low dose), or 0.6% (high dose) tannic acid for 4 or 9 weeks (i.e., when they reached puberty [8 weeks] or sexual maturity [13 weeks], respectively). The results showed that in both adolescent and adult Brandt's voles, firstly, treatment with tannic acid produced a higher ovary coefficient (ratio of the weight of ovaries to body weight), a greater proportion of mature follicles, and an increased follicular diameter. Secondly, tannic acid increased the serum contents of luteinizing hormone, follicle-stimulating hormone, and serum estradiol. Thirdly, tannic acid elevated the levels of antioxidant enzymes (superoxide dismutase, glutathione peroxidase, and catalase) and reduced the level of malondialdehyde. Therefore, it is suggested that tannic acid may promote the ovarian development of female Brant's voles by enhancing their antioxidant capacity.

Molecular mechanisms of self-regulation in multiannual rodent populations: Experimental test of an updated hypothesis.

Edwards, P. D., Frenette-Ling, C., Palme, R., & Boonstra, R. (2021). Social density suppresses GnRH expression and reduces reproductivity in voles: A mechanism for population self-regulation. Journal of Animal Ecology, 90, 784-795. Intrinsic population processes are important in the regulation of populations of small rodents, including those which display multiannual cycles. By measuring reproductive parameters, faecal androgen metabolites, and gene expression and DNA methylation in the CNS of juvenile voles, this paper demonstrates that suppression of reproduction occurs in female voles at high density compared to low density in enclosures, and that this maternal, epigenetic effect is also apparent in their offspring. This suggsests that direct density dependence influences reproduction and, hence, immediate rate of population growth, while gene expression mediated by DNA methylation blocking transcription, may have a delayed density-dependent effect in juveniles. Both direct and delayed density dependence are necessary to generate multiannual population cycles. Edwards et al. (2021) break new ground in demonstrating the molecular and physiological basis of variation in population dynamics of small mammals ranging from multiannual cycles to stability that have fascinated researchers for nearly a century.

Natural variation in the oxytocin receptor gene and rearing interact to influence reproductive and nonreproductive social behavior and receptor binding

Individual variation in social behavior offers an opportunity to explore gene-by-environment interactions that could contribute to adaptative or atypical behavioral profiles (e.g., autism spectrum disorders). Outbred, socially monogamous prairie voles provide an excellent model to experimentally explore how natural variations in rearing and genetic diversity interact to shape reproductive and nonreproductive social behavior. In this study, we manipulated rearing (biparental versus dam-only), genotyped the intronic NT213739 single nucleotide polymorphism (SNP) of the oxytocin receptor gene (Oxtr), and then assessed how each factor and their interaction related to reciprocal interactions and partner preference in male and female adult prairie voles. We found that C/T subjects reared biparentally formed more robust partner preferences than T/T subjects. In general, dam-only reared animals huddled less with a conspecific in reproductive and nonreproductive contexts, but the effect of rearing was more pronounced in T/T animals. In line with previous literature, C/T animals exhibited higher densities of oxytocin receptor (OXTR) in the striatum (caudoputamen, nucleus accumbens) compared to T/T subjects. There was also a gene-by-rearing interaction in the striatum and insula of females: In the insula, T/T females expressed varying OXTR densities depending on rearing. Overall, this study demonstrates that significant differences in adult reproductive and nonreproductive social behavior and OXTR density can arise due to natural differences in Oxtr, experimental manipulations of rearing, and their interaction.

Predator odor exposure increases social contact in adolescents and parental behavior in adulthood in Brandt’s voles

Research suggests that predation risk during adolescence can program adult stress response and emotional behavior; however, little is known about the short-term and lasting residual effects of this experience on social behavior. We explored this concept in social Brandt’s voles (Lasiopodomys brandtii). Adolescent male and female voles were exposed to distilled water, rabbit urine (as a non-predator stimulus), and cat urine for 60 min daily from postnatal day (PND) 28–49. Social play tests were conducted immediately following exposure on PND 28, 35, 42, and 49. In the social play test, repeated cat odor (CO) exposure enhanced the contact behavior of voles with their cagemate. Adolescent exposure to CO did not affect behavioral responses toward unrelated pups in the alloparental behavior test or same-sex individuals in the social interaction test. However, exposure to CO significantly enhanced the licking/grooming behavior of voles towards their own pups in the home cage parental behavior test. Repeated CO exposure significantly inhibited weight gain in male voles during adolescence. This effect was transmitted to the next generation, with lower weight gain in offspring before weaning. Following repeated CO exposure, males tended to have more female offspring whereas females produced more offspring, suggesting an adaptive strategy to increase inclusive fitness under predatory risk. These findings demonstrate that adolescent exposure to predatory risk augments adolescent social contact and adult parental behavior and suggest a role for improved inclusive fitness in mediating long-term outcomes.

A mechanism for population self-regulation: Social density suppresses GnRH expression and reduces reproductivity in voles.

Nearly 100years ago, Charles Elton described lemming and vole population cycles as ecological models for understanding population regulation in nature. Yet, the mechanisms driving these cycles are still not fully understood. These rodent populations can continue to cycle in the absence of predation and with food supplementation, and represent a major unsolved problem in population ecology. It has been hypothesized that the social environment at high population density can drive selection for a low-reproduction phenotype, resulting in population self-regulation as an intrinsic mechanism driving the cycles. However, a physiological mechanism for this self-regulation has not been demonstrated. We manipulated population density in wild meadow voles Microtus pennsylvanicus using large-scale field enclosures over 3years and examined reproductive performance and physiology. Within the field enclosures, we assessed the proportion of breeding animals, mass at sexual maturation, and faecal androgen and oestrogen metabolites. We then collected brain tissue from juvenile voles born at high or low density, quantified mRNA expression of gonadotropin-releasing hormone (GnRH) and oestrogen receptor alpha (ERα) and measured DNA methylation at six CpG sites in a region that was highly conserved with the mouse GnRH promoter. At high density, there was a lower proportion of reproductive animals. Juvenile voles born at high densities had reduced expression of GnRH in the hypothalamus, accompanied by marginally lower faecal sex hormone metabolites. Female juvenile voles born at high density also had higher methylation levels at two CpG sites while males did not, aligning with prior observations that females (but not males) from high-density environments retain reduced reproduction long term. Our results support a physiological basis for population self-regulation in vole cycles, as altering population density alone induced reproductive downregulation at the hypothalamic level. Our results demonstrate that altering the early-life social environment can fundamentally impact reproductive function in the brain. This, in turn, can drive population demography changes in wild animals.

Kinase CDK2 in Mammalian Meiotic Prophase I: Screening for Hetero- and Homomorphic Sex Chromosomes.

Cyclin-dependent kinases (CDKs) are crucial regulators of the eukaryotic cell cycle. The critical role of CDK2 in the progression of meiosis was demonstrated in a single mammalian species, the mouse. We used immunocytochemistry to study the localization of CDK2 during meiosis in seven rodent species that possess hetero- and homomorphic male sex chromosomes. To compare the distribution of CDK2 in XY and XX male sex chromosomes, we performed multi-round immunostaining of a number of marker proteins in meiotic chromosomes of the rat and subterranean mole voles. Antibodies to the following proteins were used: RAD51, a member of the double-stranded DNA break repair machinery; MLH1, a component of the DNA mismatch repair system; and SUN1, which is involved in the connection between the meiotic telomeres and nuclear envelope, alongside the synaptic protein SYCP3 and kinetochore marker CREST. Using an enhanced protocol, we were able to assess the distribution of as many as four separate proteins in the same meiotic cell. We showed that during prophase I, CDK2 localizes to telomeric and interstitial regions of autosomes in all species investigated (rat, vole, hamster, subterranean mole voles, and mole rats). In sex bivalents following synaptic specificity, the CDK2 signals were distributed in three different modes. In the XY bivalent in the rat and mole rat, we detected numerous CDK2 signals in asynaptic regions and a single CDK2 focus on synaptic segments, similar to the mouse sex chromosomes. In the mole voles, which have unique XX sex chromosomes in males, CDK2 signals were nevertheless distributed similarly to the rat XY sex chromosomes. In the vole, sex chromosomes did not synapse, but demonstrated CDK2 signals of varying intensity, similar to the rat X and Y chromosomes. In female mole voles, the XX bivalent had CDK2 pattern similar to autosomes of all species. In the hamster, CDK2 signals were revealed in telomeric regions in the short synaptic segment of the sex bivalent. We found that CDK2 signals colocalize with SUN1 and MLH1 signals in meiotic chromosomes in rats and mole voles, similar to the mouse. The difference in CDK2 manifestation at the prophase I sex chromosomes can be considered an example of the rapid chromosome evolution in mammals.

Predator-prey interactions in the canopy.

Small mammal abundances are frequently limited by resource availability, but predators can exert strong lethal (mortality) and nonlethal (e.g., nest abandonment) limitations. Artificially increasing resource availability for uncommon small mammals provides a unique opportunity to examine predator–prey interactions. We used remote cameras to monitor 168 nest platforms placed in the live tree canopy (n = 23 young forest stands), primarily for arboreal red tree voles (tree voles; Arborimus longicaudus), over 3 years (n = 15,510 monitoring‐weeks). Tree voles frequently built nests and were detected 37% of monitoring‐weeks, whereas flying squirrels (Glaucomys oregonensis) built nests infrequently but were detected 45% of monitoring‐weeks. Most nest predators were detected infrequently (<1% of monitoring‐weeks) and were positively correlated with tree vole presence. Weasels (Mustela spp.) were highly effective predators of tree voles (n = 8 mortalities; 10% of detections) compared to owls (n = 1), flying squirrels (n = 2), and Steller's jays (n = 1). Tree vole activity decreased from 84.1 (95% confidence interval [CI]: 56.2, 111.9) detections/week 1‐week prior to a weasel detection to 4.7 detections/week (95% CI: 1.7, 7.8) 1‐week postdetection and remained low for at least 12 weeks. Interpretations of predator–prey interactions were highly sensitive to how we binned continuously collected data and model results from our finest bin width were biologically counter‐intuitive. Average annual survival of female tree voles was consistent with a previous study (0.14; 95% CI: −0.04 [0.01], 0.32) and high compared to many terrestrial voles. The relative infrequency of weasel detections and inefficiency of other predators did not provide strong support for the hypothesis that predation per se limited populations. Rather, predation pressure, by reducing occupancy of already scarce nest sites through mortality and nest abandonment, may contribute to long‐term local instability of tree vole populations in young forests. Additional monitoring would be needed to assess this hypothesis.

Sexual dimorphism in skeletal shape in voles (Arvicolinae): disparate selection on male bodies and female heads

AbstractSexual dimorphism evolves as a response to different selective pressures on males and females. In mammals, sexual selection on traits that improve a male’s ability to compete for access to mates is a common cause of sexual dimorphism. In addition to body mass, adaptations in specific components of the musculoskeletal system that increase strength, stability, and agility, may improve male fighting performance. Here we test the hypotheses that males, when compared to females, are more specialized for physical competition in their skeletal anatomy and that the degree of this sexual dimorphism increases with the intensity of male–male competition. In three species of voles (Cricetidae: Arvicolinae: Microtus), we found partial support for these hypotheses. Male-biased sexual dimorphism in a set of functional indices associated with improved fighting performance was identified in the postcranial anatomy. This dimorphism was greatest in the polygynous Microtus californicus, absent in the monogamous M. ochrogaster, and intermediate in the promiscuous or socially flexible M. oeconomus. However, in the skull, we found results opposite to our predictions. Females had larger skulls relative to overall skeletal size than did males. This may be associated with selection for increased food processing efficiency, which should be highly important because of the compounding effects of increased caloric requirements during gestation and lactation, and the generally low-quality diet of voles. In addition, larger heads in females may be associated with selection for greater digging ability or for defending offspring. These results suggest disparate selective pressures on the postcranial skeletons and skulls of male and female voles.

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

AbstractTerrestrial 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.

Neonatal exposure to chlordecone alters female social behaviors and central estrogen alpha receptor expression in socially monogamous mandarin voles.

Chlordecone (CD) is one of the common persistent organic pollutants in nature and has a profound impact on the environment and on public health. Accumulating evidence has demonstrated that neonatal exposure of CD influences adult physiology and behavior due to its estrogenic properties. Using socially monogamous mandarin voles as an experimental animal model, the present study aimed to evaluate the impact of neonatal exposure to CD on female social behaviors and central estrogen receptor alpha (ERα) expression in adulthood. After receiving a single subcutaneous injection with sesame seed oil (female control group), 17 beta-estradiol (E2 group), or CD group on postnatal Day 1, the social behaviors of adult animals and ERα expression in specific brain regions were assessed. The data indicated that CD or E2-treated female animals displayed increased affiliative behaviors and decreased aggressive behaviors with regard to the unfamiliar females in the social interaction test. In addition, CD or E2-treated female voles exhibited significant preferences to females over males in the sexual preference test. Moreover, CD-treated female animals exhibited higher levels of ERα expression in the bed nucleus of the stria terminalis, the central amygdala, the medial amygdala and the medial preoptic area compared with those of the control voles. The results suggested that neonatal exposure to CD may masculinize female social behaviors, possibly via CD-induced changes in the ERα expression of relevant brain regions.

How does individual variation in sociality influence fitness in prairie voles?

Comparative studies aid in our understanding of specific conditions favouring the initial evolution of different types of social behaviours, yet there is much unexplained intraspecific variation in the expression of social behaviour that comparative studies have not yet addressed. The proximate causes of this individual variation in social behaviour within a species have been examined in some species but its fitness consequences have been less frequently investigated. In this study, we quantified the fitness consequences of variation in the sociality of prairie voles, Microtus ochrogaster. We characterized sociality of voles in seminatural enclosures using an automated behavioural tracking system paired with social network analyses to quantify the degree of spatial and temporal co-occurrence of different voles. We then assessed the relationship between sociality and both mating success (number of different conspecifics with which an individual produced offspring) and reproductive success (total number of offspring surviving to first capture). We measured the number of social connections each individual had with all voles and with only opposite-sex voles (unweighted degree) through social network analyses. Both female and male voles varied in the number of social connections they had with all conspecifics and with opposite-sex conspecifics. In both analyses, females and males with an intermediate number of social connections had higher mating success overall and, for the analysis with all connections, produced more offspring. Males with many or few social connections also had the lowest average body mass. Overall, our results suggest some limit on the fitness benefits of sociality. Although there was substantial individual variation in our measure of vole social behaviour, intermediate levels of social connections may be most favourable.

Synthetic mustelid semiochemicals depress survival of long-tailed vole (Microtus longicaudus) populations and feeding damage

Microtus and Myodes continue to be major pests in agricultural and forest production in many temperate and boreal ecosystems of North America and Eurasia. However, voles may also be keystone species because of their predator-prey dynamics and feeding linkages in many networks. As an alternative to rodenticides, exploration continues for a suitable fear-based method to reduce vole damage to crops. This study tested the hypotheses (H) that a “neat” formulation of synthetic anal-gland compounds of the short-tailed weasel (Mustela erminea L.) would reduce (H1) abundance, reproduction, survival, body mass, and movement of long-tailed vole (Microtus longicaudus Merriam) populations; and (H2) feeding damage to coniferous seedlings by voles in forest plantations. Vole populations were live-trapped on replicate sites from May 2005 to June 2006 during a peak year in abundance near Golden, British Columbia, Canada. Synthetic weasel odour was continually present on treatment sites from June 2005 to June 2006. Overwinter mortality to planted coniferous seedlings from vole feeding was measured on all sites in May–June 2006.Synthetic weasel odour compounds did not reduce mean abundance of M. longicaudus but, in fact, resulted in significantly higher numbers of voles in the treatment sites owing to a major pulse of transient (single capture) animals. Mean number of successful pregnancies and total recruits were also higher in treatment than control sites, but early juvenile survival, movements, and body mass were all similar between control and weasel-odour sites. However, mean Jolly-Seber 28-day total survival rates were higher (2.9–3.9 times) on control than treatment sites for both male and female voles during the overwinter-spring 2005–06 period. Much of the reduced survival was due to transient animals which tended to have a higher proportion of adults to juveniles in treatment than control sites. Some degree of disruption presumably occurred on the treatment sites perhaps owing to increased breeding intensity by females in the face of perceived predation or the presence of various mammalian predators attracted to the weasel odour and preying upon voles. This disruption may be linked to the use of synthetic weasel odour in suitable release devices that maintain the odour even in high quality habitats for voles. Despite the difference in abundance, voles seemed to feed less on plantation trees in the treatment than control sites. If this population disruption is real, we suggest that large-scale (e.g., 10+ ha) application of synthetic weasel odour in areas requiring crop protection from voles would be a worthwhile endeavour. This prediction is particularly germane for M. longicaudus where weasel odour treatment might be able to disrupt substantially their one population fluctuation on newly clearcut sites.