Female Voles Research Articles

Sex-Specific Impacts of Early Life Sleep Disruption: Ethanol Seeking, Social Interaction, and Anxiety Are Differentially Altered in Adolescent Prairie Voles.

Early life sleep is important for neuronal development. Using the highly social prairie vole rodent model, we have previously reported that early life sleep disruption (ELSD) during the preweaning period results in interference with social bonding and increases ethanol consumption following a stressor in adulthood. Furthermore, ELSD increases parvalbumin expression and reduces glutamatergic neurotransmission in cortical regions in adult prairie voles. To understand the impact of ELSD on the lifespan, an examination of an earlier time in life is necessary. The aim of the present study was to examine behavioral outcomes of ELSD on adolescent prairie voles. Given the known effects of ELSD on development of neuronal systems involved in mood and social motivation, we hypothesized that anxiety, risk, and reward-related behaviors would be impacted by ELSD in adolescent prairie voles. We report that both male and female adolescent prairie voles that experienced ELSD showed heightened anxiety-like behavior compared to age-matched controls (CONs) as measured by a light-dark box. Additionally, both male and female ELSD voles showed reductions in both ethanol preference and consumption, and affiliative behavior compared to CONs. These results suggest that adolescent prairie voles of both sexes experience heightened anxiety-like behavior and reduced reward-seeking behaviors after ELSD. These results further suggest that early life sleep is critically important for neurotypical behaviors in adolescence.

PVN-mPFC OT projections modulate pup-directed pup care or attacking in virgin mandarin voles

Many species of animals exhibit caregiving or aggression toward conspecific offspring. The neural mechanisms underlying the infanticide and pup care remain poorly understood. Here, using monogamous mandarin voles (Microtus mandarinus), we found that more oxytocin (OT) neurons in the paraventricular nucleus (PVN) were activated during pup caring than infanticide. Optogenetic activation of OT neurons in the PVN facilitated pup caring in male and female mandarin voles. In infanticide voles, optogenetic activation of PVN OT cells or PVN-medial prefrontal cortex (mPFC) OT projection fibers prolonged latency to approach and attack pups, whereas inhibition of these OT neurons or projections facilitated approach and infanticide. Optogenetic activation of PVN OT neuron projections to the mPFC in males shortened the latency to approach and retrieve pups and facilitated the initiation of pup care, but produced no effects on pup-care females. In addition, OT release in the mPFC increased upon approaching and retrieving pups, and decreased upon attacking pups. Intraperitoneal injection of OT promoted pup care and inhibited infanticide behavior. It is suggested that the OT system, especially PVN OT neurons projecting to mPFC, modulates pup-directed behaviors and OT can be used to treat abnormal behavioral responses associated with some psychological diseases such as depression and psychosis.

Limbic oxytocin receptor expression alters molecular signaling and social avoidance behavior in female prairie voles (Microtus ochrogaster).

The social defeat paradigm is the most representative animal model to study social anxiety disorder (SAD) and its underlying neuronal mechanisms. We have previously reported that defeat progressively reduces oxytocin receptors (OXTR) in limbic regions of the brain over an eight-week period in female prairie voles (Microtus ochrogaster). Oxytocin receptors activate the mitogen-activated protein kinase (MAPK) pathway, which has been previously associated with the anxiolytic effects of oxytocin. Here, we assessed the functional significance of OXTR in stress-induced social avoidance and the response of the MAPK signaling pathway in the nucleus accumbens (NAc), anterior cingulate cortex (ACC), and basolateral amygdala (BLA) of female prairie voles. In experiment 1, Sexually naïve adult female prairie voles were defeated for three consecutive days and tested a week after for social preference/avoidance (SPA) test. Control subjects were similarly handled without defeat conditioning. In experiment 2, sexually and stress naïve adult female prairie voles were bilaterally injected into the NAc, ACC, or the BLA with a CRISPR/Cas9 virus targeting the Oxtr coding sequence to induce OXTR knockdown. Two weeks post-surgery, subjects were tested for SPA behavior. Viral control groups were similarly handled but injected with a control virus. A subgroup of animals from each condition in both experiments were similarly treated and euthanized without being tested for SPA behavior. Brains were harvested for OXTR autoradiography, western blot analysis of MAPK proteins and quantification of local oxytocin content in the NAc, BLA, ACC, and PVN through ELISA. Social defeat reduced OXTR binding in the NAc and affected MAPK pathway activity and oxytocin availability. These results were region-specific and sensitive to exposure to the SPA test. Additionally, OXTR knockdown in the NAc, ACC, and BLA induced social avoidance and decreased basal MAPK activity in the NAc. Finally, we found that OXTR knockdown in these regions was associated with less availability of oxytocin in the PVN. Dysregulation of the oxytocin system and MAPK signaling pathway in the NAc, ACC, and BLA are important in social behavior disruptions in female voles. This dysregulation could, therefore, play an important role in the etiology of SAD in women.

Pilfering personalities: Effects of small mammal personality on cache pilferage.

Small mammals such as mice and voles play a fundamental role in the ecosystem service of seed dispersal by caching seeds in small hoards that germinate under beneficial conditions. Pilferage is a critical step in this process in which animals steal seeds from other individuals' caches. Pilferers often recache stolen seeds, which are often pilfered by new individuals, who may recache again, and so on, potentially leading to compounded increased dispersal distance. However, little research has investigated intraspecific differences in pilfering frequency, despite its importance in better understanding the role of behavioural diversity in the valuable ecosystem service of seed dispersal. We conducted a field experiment in Maine (USA) investigating how intraspecific variation, including personality, influences pilferage effectiveness. Within the context of a long-term capture-mark-recapture study, we measured the unique personality of 3311 individual small mammals of 10 species over a 7-year period. For this experiment, we created artificial caches using eastern white pine (Pinus strobus) seeds monitored with trail cameras and buried antennas for individual identification. Of the 436 caches created, 83.5% were pilfered by 10 species, including deer mice ((Peromyscus maniculatus) and southern red-backed voles (Myodes gapperi). We show how individuals differ in their ability to pilfer seeds and that these differences are driven by personality, body condition and sex. More exploratory deer mice and those with lower body condition were more likely to locate a cache, and female southern red-backed voles were more likely than males to locate caches. Also, caches were more likely to be pilfered in areas of higher small mammal abundance. Because the risk of pilferage drives decisions concerning where an animal chooses to store seeds, pilferage pressure is thought to drive the evolution of food-hoarding behaviour. Our study shows that pilferage ability varies between individuals, meaning that some individuals have a disproportionately strong influence on others' caching decisions and disproportionately contribute to compounded longer-distance seed dispersal facilitated by pilferage. Our results add to a growing body of knowledge showing that the unique personalities of individual small mammals play a critical role in forest regeneration by impacting seed dispersal.

The role of male scent in female attraction in the bank vole, Myodes glareolus.

Chemical signals are frequently utilised by male mammals for intersexual communication and females are often attracted to male scent. However, the mechanism underlying female attraction has only been identified in a small number of mammalian species. Mammalian scents contain airborne volatiles, that are detected by receivers at a distance from the scent source, as well as non-volatile molecules, such as proteins, that require physical contact for detection. Lipocalin proteins, produced within the scent secretions of many terrestrial mammals, are thought to be particularly important in chemical signalling. Here, we explore if the male-specific protein, glareosin, expressed by adult male bank voles, Myodes glareolus, stimulates female attraction to male scent. We show that female bank voles are more attracted to male compared to female scent, supporting the results of previous studies. Increased investigation and attraction to male scent occurred to both airborne volatiles and non-volatile proteins when they were presented separately. However, we found no evidence that attraction to male scent was driven by glareosin. Our results differ from those previously described in house mice, where a single protein induces female attraction to male scent, suggesting the mechanism underlying female attraction to male scent differs between species.

Melanocortin agonism in a social context selectively activates nucleus accumbens in an oxytocin-dependent manner

Social deficits are debilitating features of many psychiatric disorders, including autism. While time-intensive behavioral therapy is moderately effective, there are no pharmacological interventions for social deficits in autism. Many studies have attempted to treat social deficits using the neuropeptide oxytocin for its powerful neuromodulatory abilities and influence on social behaviors and cognition. However, clinical trials utilizing supplementation paradigms in which exogenous oxytocin is chronically administered independent of context have failed. An alternative treatment paradigm suggests pharmacologically activating the endogenous oxytocin system during behavioral therapy to enhance the efficacy of therapy by facilitating social learning. To this end, melanocortin receptor agonists like Melanotan II (MTII), which induces central oxytocin release and accelerates formation of partner preference, a form of social learning, in prairie voles, are promising pharmacological tools. To model pharmacological activation of the endogenous oxytocin system during behavioral therapy, we administered MTII prior to social interactions between male and female voles. We assessed its effect on oxytocin-dependent activity in brain regions subserving social learning using Fos expression as a proxy for neuronal activation. In non-social contexts, MTII only activated hypothalamic paraventricular nucleus, a primary site of oxytocin synthesis. However, during social interactions, MTII selectively increased oxytocin-dependent activation of nucleus accumbens, a site critical for social learning. These results suggest a mechanism for the MTII-induced acceleration of partner preference formation observed in previous studies. Moreover, they are consistent with the hypothesis that pharmacologically activating the endogenous oxytocin system with a melanocortin agonist during behavioral therapy has potential to facilitate social learning.

Hearing ability of prairie voles (Microtus ochrogaster).

The hearing abilities of mammals are impacted by factors such as social cues, habitat, and physical characteristics. Despite being used commonly to study social behaviors, hearing of the monogamous prairie vole (Microtus ochrogaster) has never been characterized. In this study, anatomical features are measured and auditory brainstem responses (ABRs) are used to measure auditory capabilities of prairie voles, characterizing monaural and binaural hearing and hearing range. Sexually naive male and female voles were measured to characterize differences due to sex. It was found that prairie voles show a hearing range with greatest sensitivity between 8 and 32 kHz, binaural hearing across interaural time difference ranges appropriate for their head sizes. No differences are shown between the sexes in binaural hearing or hearing range (except at 1 kHz), however, female voles have increased amplitude of peripheral ABR waves I and II and longer latency of waves III and IV compared to males. The results confirm that prairie voles have a broad hearing range, binaural hearing consistent with rodents of similar size, and differences in amplitudes and thresholds of monaural physiological measures between the sexes. These data further highlight the necessity to understand sex-specific differences in neural processing that may underly variability in responses between sexes.

Increased proliferation and neuronal fate in prairie vole brain progenitor cells cultured in vitro: effects by social exposure and sexual dimorphism

BackgroundThe prairie vole (Microtus ochrogaster) is a socially monogamous rodent that establishes an enduring pair bond after cohabitation, with (6 h) or without (24 h) mating. Previously, we reported that social interaction and mating increased cell proliferation and differentiation to neuronal fate in neurogenic niches in male voles. We hypothesized that neurogenesis may be a neural plasticity mechanism involved in mating-induced pair bond formation. Here, we evaluated the differentiation potential of neural progenitor cells (NPCs) isolated from the subventricular zone (SVZ) of both female and male adult voles as a function of sociosexual experience. Animals were assigned to one of the following groups: (1) control (Co), sexually naive female and male voles that had no contact with another vole of the opposite sex; (2) social exposure (SE), males and females exposed to olfactory, auditory, and visual stimuli from a vole of the opposite sex, but without physical contact; and (3) social cohabitation with mating (SCM), male and female voles copulating to induce pair bonding formation. Subsequently, the NPCs were isolated from the SVZ, maintained, and supplemented with growth factors to form neurospheres in vitro.ResultsNotably, we detected in SE and SCM voles, a higher proliferation of neurosphere-derived Nestin + cells, as well as an increase in mature neurons (MAP2 +) and a decrease in glial (GFAP +) differentiated cells with some sex differences. These data suggest that when voles are exposed to sociosexual experiences that induce pair bonding, undifferentiated cells of the SVZ acquire a commitment to a neuronal lineage, and the determined potential of the neurosphere is conserved despite adaptations under in vitro conditions. Finally, we repeated the culture to obtain neurospheres under treatments with different hormones and factors (brain-derived neurotrophic factor, estradiol, prolactin, oxytocin, and progesterone); the ability of SVZ-isolated cells to generate neurospheres and differentiate in vitro into neurons or glial lineages in response to hormones or factors is also dependent on sex and sociosexual context.ConclusionSocial interactions that promote pair bonding in voles change the properties of cells isolated from the SVZ. Thus, SE or SCM induces a bias in the differentiation potential in both sexes, while SE is sufficient to promote proliferation in SVZ-isolated cells from male brains. In females, proliferation increases when mating is performed. The next question is whether the rise in proliferation and neurogenesis of cells from the SVZ are plastic processes essential for establishing, enhancing, maintaining, or accelerating pair bond formation.HighlightsSociosexual experiences that promote pair bonding (social exposure and social cohabitation with mating) induce changes in the properties of neural stem/progenitor cells isolated from the SVZ in adult prairie voles.Social interactions lead to increased proliferation and induce a bias in the differentiation potential of SVZ-isolated cells in both male and female voles.The differentiation potential of SVZ-isolated cells is conserved under in vitro conditions, suggesting a commitment to a neuronal lineage under a sociosexual context.Hormonal and growth factors treatments (brain-derived neurotrophic factor, estradiol, prolactin, oxytocin, and progesterone) affect the generation and differentiation of neurospheres, with dependencies on sex and sociosexual context.Proliferation and neurogenesis in the SVZ may play a crucial role in establishing, enhancing, maintaining, or accelerating pair bond formation.

Sexual discrimination and attraction through scents in the water vole, Arvicola terrestris.

In mammals, especially rodents, social behaviours, such as parenting, territoriality or mate attraction, are largely based on olfactory communication through chemosignals. These behaviours are mediated by species-specific chemosignals, including small organic molecules and proteins that are secreted in the urine or in various fluids from exocrine glands. Chemosignal detection is mainly ensured by olfactory neurons in two specific sensory organs, the vomeronasal organ (VNO) and the main olfactory epithelium (MOE). This study aimed to characterise the olfactory communication in the fossorial ecotype of the water voles, Arvicola terrestris. We first measured the olfactory investigation of urine and lateral scent gland secretions from conspecifics. Our results showed that water voles can discriminate the sex of conspecifics based on the smell of urine, and that urinary male odour is attractive for female voles. Then, we demonstrated the ability of the VNO and MOE to detect volatile organic compounds (VOCs) found in water vole secretions using live-cell calcium imaging in dissociated cells. Finally, we evaluated the attractiveness of two mixtures of VOCs from urine or lateral scent glands in the field during a cyclical outbreak of vole populations.

Male and female Brandt’s voles have higher reproductive success when they have more mating partners regardless of population density

Abstract Although population density and body mass are known to alter the mating strategies of individuals, their impacts on reproductive success have not been fully investigated. We examined genetic mating system variation (estimated number of mating partners), reproductive success (offspring number), and sperm competition intensity (sires per litter) in semi-natural populations of Brandt’s voles (Lasiopodomys brandtii) under low-, medium- and high-densities. We used 12 microsatellite genetic markers and parentage assignment of 3516 voles, with the aim of identifying the estimated number of mating partners and offspring produced by founder individuals. We provided strong evidence that individuals with more mating partners experienced increased reproductive success in all density groups, as measured by the production of more offspring, compared with individuals that had fewer mating partners. Further, we found that large males had more mating partners (especially in high-population density enclosures) and also produced more offspring relative to smaller males. In high-density (HD) enclosures, the average reproductive success per female vole was lower (a negative density-dependent effect), but voles had more mating partners, more sires per litter, but lower paternity skew compared to low-density enclosures. Our results suggests that Brandt’s voles increased reproductive success through increasing mating partners under HD stress which may have significant implications in offsetting the negative density-dependency effect on population growth.

To the Stady of a Water Vole (<i>Arvicola anphibius</i>) at the North-Western Area

We have conducted the long-term expeditionary and stationary studies in the taiga Northwest of Russia (1958–2018) to characterize the population, biotopic distribution, nutrition, reproduction, spatial and ecological structure of the population, and the dynamics of the number of water voles, including those associated with its habitat in northern range boundaries: timing, reproductive cycles, course and intensity of reproduction, participation in the reproduction of individual age groups, variations in brood size, etc. The breeding season from the first pregnant females are caught in spring to the last newly born females in autumn lasts 4–6 months. It depends on the state of the population and weather and phenological conditions of the year. The average brood in wintering and arrived female voles in our region was close to the species norm and amounted to 6.5 ± 0.37 and 5.7 ± 0.41. The main reasons for the long-term dynamics of the species abundance are changes in the hydrological regime of water bodies.

Peer Social Environment Impacts Behavior and Dopamine D1 Receptor Density in Prairie Voles (Microtus ochrogaster)

Prairie voles (Microtus ochrogaster) are socially monogamous rodents that form selective, long-lasting relationships with mates and with same-sex peers. It is unknown to what extent mechanisms supporting ‘peer relationships’ are similar to those involved in mate relationships. The formation of pair bonds is dependent on dopamine neurotransmission, whereas the formation of peer relationships is not, providing evidence of relationship type-specificity. The current study assessed endogenous structural changes in dopamine D1 receptor density in male and female voles across different social environments, including long-term same-sex partnerships, new same-sex partnerships, social isolation, and group housing. We also related dopamine D1 receptor density and social environment to behavior in social interaction and partner preference tests. Unlike prior findings in mate pairs, voles paired with new same-sex partners did not exhibit upregulated D1 binding in the nucleus accumbens (NAcc) relative to controls paired from weaning. This is consistent with differences in relationship type: D1 upregulation in pair bonds aids in maintaining exclusive relationships through selective aggression, and we found that formation of new peer relationships did not enhance aggression. Isolation led to increases in NAcc D1 binding, and even across socially housed voles, individuals with higher D1 binding exhibited increased social avoidance. These findings suggest that elevated D1 binding may be both a cause and a consequence of reduced prosociality. These results highlight the neural and behavioral consequences of different non-reproductive social environments and contribute to growing evidence that the mechanisms underlying reproductive and non-reproductive relationship formation are distinct. Elucidation of the latter is necessary to understand mechanisms underlying social behavior beyond a mating context.

Effects of Group Size on Behavior, Reproduction, and mRNA Expression in Brains of Brandt’s Voles

For social animals, a moderate group size is greatly important to maintain their reproductive success. However, the underlying neurobiological mechanism of group size on behavior and reproduction has rarely been investigated. In this study, we examined the effects of group size (1, 2, 4 pairs of adult male and female voles raised per cage) on behavior and reproduction. Meanwhile, the mRNA expression of stress and reproduction response-related genes in male brains was detected. We found that Brandt's voles (Lasiopodomys brandtii) in the large-sized group fight more severely than those in the small-sized group. Meanwhile, male voles were more anxious than females. The average number of embryos and litters per female in the medium-sized group was significantly higher than that of large-sized group. In male voles, stress- or reproduction-response mRNA expressions were more related to final group size or final density due to death caused by fighting. Our results indicated that a moderate group size was beneficial to the reproductive output of Brandt's voles. Our study highlights the combined effects of stress- or reproduction-related gene expression or behavior in regulating the fitness of voles with different group sizes.

Early life sleep disruption has long lasting, sex specific effects on later development of sleep in prairie voles

In mammals, sleep duration is highest in the early postnatal period of life and is critical for shaping neural circuits that control the development of complex behaviors. The prairie vole is a wild, highly social rodent that serves as a unique model for the study of complex, species-typical social behaviors. Previous work in our laboratory has found that early life sleep disruption (ELSD) in prairie voles during a sensitive window of postnatal development leads to long lasting changes in social and cognitive behaviors as well as structural changes in excitatory and inhibitory neural circuits in the brain. However, it is currently unknown how later sleep is impacted by ELSD, both shortly after ELSD and over the long term. Therefore, the aim of this study was to describe the effects of ELSD on later life sleep, compared to sleep in normally developing prairie voles. First, we conducted tethered electroencephalogram/electromyogram (EEG/EMG) recordings in juvenile prairie voles undergoing ELSD, compared to Control conditions. Second, we conducted 24 h of home cage tethered EEG/EMG recordings in either adolescent or adult male and female prairie voles that had previously undergone ELSD or Control conditions as juveniles. We found that, as adults, male ELSD prairie voles showed persistently lower REM sleep duration and female ELSD prairie voles showed persistently higher NREM sleep duration compared to Controls, but no other sleep parameters differed. We concluded that 1) persistent effects of ELSD on sleep into adulthood may contribute to the social and cognitive deficits observed in adult voles, and 2) sleep disruption early in life can influence later sleep patterns in adulthood.

Adolescence Predatory Risk Alters Social Behaviors and Cognitive Ability and Central Oxytocin and Vasopressin Expression in Adult Brandt’s Voles

Introduction: Stress during adolescence causes long-term behavioral changes in adulthood. We previously found that adolescent exposure to predatory risk augments adolescent social contact and adult parental behavior in Brandt’s voles (Lasiopodomys brandtii). Methods: Here, we determined whether this experience alters sexual behavior, pair-bond formation, and recognition ability as well as basal HPA axis activity, central oxytocin (OT), and arginine-vasopressin (AVP) expression in adulthood. Results: In the social interaction test, repeated cat odor (CO) exposure enhanced the frequency of lordosis by female voles toward an unfamiliar opposite-sex conspecific. CO voles preferred to engage with their partners after 48-h cohabitation whereas the control groups did not, which may reflect stable pair bonds in the CO treatment group. Furthermore, adolescent exposure to CO inhibited novel object recognition and place recognition ability, while it influenced social recognition only among adult males. No effect of adolescent CO exposure was observed for basal HPA axis activity, showing a habituation effect. Finally, we found that CO exposure increased OT and decreased AVP expression in the hypothalamus, including the paraventricular nucleus and anterior hypothalamus. The levels of OT in the medial amygdala were lower, and AVP in the lateral septum was higher in CO voles compared with the control. Conclusion: These findings demonstrate that adolescent exposure to predator risk promotes adult reproductive behavior of Brandt’s voles. Deficits in recognition ability may necessitate alterations in reproductive strategies to enhance inclusive fitness. OT and AVP systems may play a modulatory role in the alteration of social behaviors elicited by adolescent predatory risk.

A Kit Mutation Associated with Black-Eyed White Phenotype in the Grey Red-Backed Vole, Myodes rufocanus

Mutations in genes causing leucism are often accompanied by serious disease limiting individual fitness in laboratory animals. Mammalian species with all-white fur exist in the wild; however, the causative genes have not yet been identified, because of the difficulty of the forward genetic approach—comparisons between individuals with different phenotypes. In this study, we conducted linkage analyses using six candidate gene markers on a wild leucistic female grey red-backed vole (Myodes rufocanus) and inbreeding F1 and F2 offspring displaying variations in coat colors, agouti, and leucism. We found that the white-furred variant was associated with a specific Kit allele characterized by a nonsynonymous substitution at amino acid position 604, leading to the replacement of glycine with arginine. In addition, the leucistic phenotype was accompanied by a small portion of black hairs, which increased with growth. Our results showed a candidate gene causing leucism in viable wild animals and provided an opportunity to consider the necessity to study growth-associated traits for coat color analyses.

Pair-bonding and social experience modulate new neurons survival in adult male and female prairie voles (Microtus ochrogaster).

Prairie voles are a socially monogamous species that, after cohabitation with mating, form enduring pair bonds. The plastic mechanisms involved in this social behavior are not well-understood. Neurogenesis in adult rodents is a plastic neural process induced in specific brain areas like the olfactory bulbs (OB) and dentate gyrus (DG) of the hippocampus. However, it is unknown how cell survival is modulated by social or sexual experience in prairie voles. This study aimed to evaluate if cohabitation with mating and/or social exposure to a vole of the opposite sex increased the survival of the new cells in the main and accessory OB and DG. To identify the new cells and evaluate their survival, voles were injected with the DNA synthesis marker 5-bromo-2’-deoxyuridine (BrdU) and were randomly distributed into one of the following groups: (A) Control (C), voles that did not receive any sexual stimulation and were placed alone during the behavioral test. (B) Social exposure (SE), voles were individually placed in a cage equally divided into two compartments by an acrylic screen with small holes. One male and one female were placed in opposite compartments. (C) Social cohabitation with mating (SCM), animals mated freely. Our findings demonstrated that SCM females had increases in the number of new cells (BrdU-positive cells) in the main olfactory bulb and new mature neurons (BrdU/NeuN-positive cells) in the glomerular layer (GlL). In contrast, these new cells decrease in males in the SE and SCM conditions. In the granular cell layer (GrL), SCM females had more new cells and neurons than the SE group. In the accessory olfactory bulb, in the anterior GlL, SCM decreased the number of new cells and neurons in females. On the other hand, in the DG, SCM and SE increase the number of new cells in the suprapyramidal blade in female voles. Males from SCM express more new cells and neurons in the infrapyramidal blade compared with SE group. Comparison between male and females showed that new cells/neurons survival was sex dependent. These results suggest that social interaction and sexual behavior modulate cell survival and influence the neuronal fate in a sex-dependent manner, in the OB and DG. This study will contribute to understand neural mechanisms of complex social and pair bond behaviors in the prairie voles; supporting adult neurogenesis as a plastic mechanism potentially involved in social monogamous strategy.

Density‐dependent changes of mating system and family structure in Brandt's voles (Lasiopodomys brandtii)

AbstractA mating system is an important life history for animals dealing with changing environments. Population density affects the plasticity of a mating system and subsequently the family structure of animals, but its impacts on mating systems and social structures are rarely investigated by using molecular markers in field conditions. In this study, using microsatellite genetic markers, we examined the changes in the social and genetic mating system and family structure of Brandt's voles in the grassland of Inner Mongolia, China, under low‐, medium‐, and high‐density enclosures (each enclosure 0.48‐ha with 4 replicates.) We found, with the increase in population density of the founder voles introduced into the enclosure in early spring, both sexes increased their number of genetic mating partners, while males increased their social partners, resulting in a more promiscuous mating system. The number of genetic fathers and mothers per family, the number of social offspring per founder male or female, and the proportion of extra‐group offspring increased with increased density, indicating that the response of the family structure to density change, which is consistent with the change in mating system observed in our study. Both male and female voles had multiple mates, but males had a larger number of social and genetic mates, the number of social and genetic offspring, and the number of social and genetic families. Our study highlights the significance of density‐dependent plasticity of a mating system and family structure in affecting the population change of small mammals.

Differential temperature effects on photoperiodism in female voles: A possible explanation for declines in vole populations.

Many mammalian species use photoperiod as a predictive cue to time seasonal reproduction. In addition, metabolic effects on the reproductive axis may also influence seasonal timing, especially in female small, short‐lived mammals. To get a better understanding of how annual cycling environmental cues impact reproductive function and plasticity in small, short‐lived herbivores with different geographic origins, we investigated the mechanisms underlying integration of temperature in the photoperiodic‐axis regulating female reproduction in a Northern vole species (tundra vole, Microtus oeconomus) and in a Southern vole species (common vole, Microtus arvalis). We show that photoperiod and temperature interact to determine appropriate physiological responses; there is species‐dependent annual variation in the sensitivity to temperature for reproductive organ development. In common voles, temperature can overrule photoperiodical spring‐programmed responses, with reproductive organ mass being higher at 10°C than at 21°C, whereas in autumn they are less sensitive to temperature. These findings are in line with our census data, showing an earlier onset of spring reproduction in cold springs, while reproductive offset in autumn is synchronized to photoperiod. The reproductive organs of tundra voles were relatively insensitive to temperature, whereas hypothalamic gene expression was generally upregulated at 10°C. Thus, both vole species use photoperiod, whereas only common voles use temperature as a cue to control spring reproduction, which indicates species‐specific reproductive strategies. Due to global warming, spring reproduction in common voles will be delayed, perhaps resulting in shorter breeding seasons and thus declining populations, as observed throughout Europe.

Helping behavior in prairie voles: A model of empathy and the importance of oxytocin

SummarySeveral studies suggest that rodents show empathic responses and helping behavior toward others. We examined whether prairie voles would help conspecifics who were soaked in water by opening a door to a safe area. Door-opening latency decreased as task sessions progressed. Female and male voles stayed close to the soaked voles' side at equal rates and opened the door with similar latencies. When the conspecific was not soaked in water, the door-opening latency did not decrease. This suggests that the distress of the conspecific is necessary for learning to open the door and that the door-opening performed by prairie voles corresponds to helping behavior. Additionally, we examined the helping behavior in prairie voles in which oxytocin receptors were genetically knocked out. Oxytocin receptor knockout voles demonstrated less learning of the door-opening behavior and less interest in soaked conspecifics. This suggests that oxytocin is important for the emergence of helping behavior.