The effects of mate removal on pregnancy success in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus).

The effects of removing the stud male have not been controlled in many studies relating pregnancy block to the presence of an unfamiliar male. We examined the effects of removing the male on pregnancy success in prairie voles and meadow voles, two species that differ in degree of paternal investment. Whereas prairie vole males provide extensive care to offspring and accelerate pup development, meadow vole males display little or no care and delay development of pups. We predicted that removal of the stud male would decrease pregnancy success in prairie voles and either have no effect or increase success in meadow voles. In experiment 1, females were in male-induced estrus, and their mates were either left with them or were removed 4 h, 1 day, 2 days, or 8 days after mating. In experiment 2, females were in postpartum estrus, and their mates were either left with them or were removed 1 day, 2 days, or 8 days after birth of their first litter. Removal of the male soon after mating in postpartum estrus decreased pregnancy success in prairie voles and increased success in meadow voles. Thus, although removal of the stud male influenced litter production, the direction of the effect varied with species.     

Pre-implantation Pregnancy Disruption in Female Meadow Voles Microtus pennsylvanicus (Rodentia: Muridae): Male Competition or Female Mate Choice?

I investigated alternative hypotheses concerning the functions of pre-implantation male-induced pregnancy disruption in meadow voles. Disruptions may be viewed as: 1. Postcopulatory male competition; 2. A mechanism for postcopulatory mate choice by females; and 3. A means of benefitting females by terminating investment in litters that may be harmed by new males. Female voles were paired with a second male 3 d after mating with their first mate. Behavioural interactions between the female and each male were compared for females that disrupted or retained the pregnancy sired by the first male. Whether they were the females' first or second mates, males siring litters showed similar high levels of approach and moderately high aggression, behaviour that differed from the females' other mates. Disrupted females huddled sooner with their second mates than females that retained their original pregnancies, and females tended to approach males that approached them. These results suggest that females influence whether a disruption occurs by the amount of contact they initiate with the second male, and thus pregnancy disruption may facilitate postcopulatory mate choice by females. This pre-implantation disruption did not enhance female reproductive success: pup survival was the same whether or not a disruption occurred, and males living with pups they had sired (after a disruption) spent as much time with them as males with unrelated pups (females did not disrupt).     

Social Dominance among Male Meadow Voles is Inversely Related to Reproductive Success

Intrasexual selection can occur through direct aggressive interactions between males for access to females. We tested the relationship between social dominance and male reproductive success among meadow voles, Microtus pennsylvanicus. Dominance ranks of wild‐caught males were determined using neutral arena trials, with the winner of two of three trials considered dominant. These males were then released into field enclosures and allowed to visit females housed in nestboxes for 8 wk, and males’ home range sizes were determined using weekly grid trapping. Male reproductive success was determined using molecular paternity analysis (six microsatellite primers) for all pups born during the field experiment. Males with higher dominance ranks had larger home ranges. However, male dominance rank was not predictive of the number of total visits to females’ nestboxes or the number of visits to each male's most frequently visited nestbox. Males that made more visits to nestboxes sired more litters. Males that had higher dominance ranks sired fewer litters. These results suggest that there is a reproductive disadvantage to having higher dominance rank among male meadow voles.     

Effects of repeated pup exposure on behavioral,neural, and adrenocortical responses to pups in male California mice (Peromyscus californicus)

In biparental mammals, the factors facilitating the onset of male parental behavior are not well understood. While hormonal changes in fathers may play a role, prior experience with pups has also been implicated. We evaluated effects of prior exposure to pups on paternal responsiveness in the biparental California mouse (Peromyscus californicus). We analyzed behavioral, neural, and corticosterone responses to pups in adult virgin males that were interacting with a pup for the first time, adult virgin males that had been exposed to pups 3 times for 20 min each in the previous week, and new fathers. Control groups of virgins were similarly tested with a novel object (marble). Previous exposure to pups decreased virgins' latency to approach pups and initiate paternal care, and increased time spent in paternal care. Responses to pups did not differ between virgins with repeated exposure to pups and new fathers. In contrast, repeated exposure to a marble had no effects. Neither basal corticosterone levels nor corticosterone levels following acute pup or marble exposure differed among groups. Finally, Fos expression in the medial preoptic area, ventral and dorsal bed nucleus of the stria terminalis was higher following exposure to a pup than to a marble. Fos expression was not, however, affected by previous exposure to these stimuli. These results suggest that previous experience with pups can facilitate the onset of parental behavior in male California mice, similar to findings in female rodents, and that this effect is not associated with a general reduction in neophobia.     

Adaptive immune responses are linked to the mating system of arvicoline rodents

ABSTRACT Males generally exhibit reduced immune responses and greater susceptibility to disease than females. The suppressive effect of testosterone on immune function is hypothesized to be one reason why males have lower immune responses than females. Presumably, this effect of testosterone should be more pronounced among polygynous than monogamous species because circulating testosterone is higher among polygynous than monogamous males. The present study examined the extent to which sex differences in specific humoral immunity are related to the endocrine status and mating system of two arvicoline rodents. Humoral immunity was evaluated among polygynous meadow voles (Microtus pennsylvanicus) and monogamous prairie voles (Microtus ochrogaster) by challenging them with the novel antigen keyhole limpet hemocyanin (KLH) and assessing specific immune responses 5, 10, and 15 d following immunization. Overall, meadow voles mounted higher anti-KLH IgM and IgG responses than prairie voles did. Sex differences were also apparent for anti-KLH IgM responses; male meadow voles mounted higher antibody responses than conspecific females, whereas female prairie voles mounted greater responses to KLH than did conspecific males. Male meadow voles had significantly higher testosterone concentrations and reproductive organ mass than male prairie voles did but had elevated immune responses, suggesting that testosterone may not be the primary factor involved in the observed sex and species differences in immune responses. Species and sex differences in corticosterone concentrations were also evident and may contribute to the observed differences in immune function. The influence of extrinsic factors on immune function is also discussed. Taken together, these data provide evidence that the mating system may influence endocrine-immune interactions.     

Androgens exert opposite effects on body mass of heavy and light meadow voles

The influence of gonadal hormones on body mass of adult male meadow voles varied systematically as a function of the animals' baseline body weight; heavier voles decreased and lighter voles increased their body mass after castration. Testosterone replacement reversed the effects of castration; changes in body mass during hormone treatment were negatively correlated with changes observed after castration. Body mass of intact males was not correlated with plasma testosterone titers. Individual differences in body mass of male voles appear to reflect variations among animals in substrate responsiveness to hormones rather than differences in circulating hormone levels.     

Parental care and testosterone in males of the bank vole (Myodes glareolus): Sensitization and androgenic stimulation of paternal behavior

The relationship between parental responsiveness of bank vole males and their body weight, testes mass, and plasma and gonadal testosterone levels were examined. Two groups of voles were studied: Group I consisted of 14 breeding pairs where females gave birth to young within a month after formation of pairs, and Group II represented 13 pairs without offspring and signs of pregnancy in females. Males in Group I, unlike those in Group II, had contact with pups before the tests on parental responsiveness. In Group I, males were found to have larger testes and to exhibit a higher level of care-giving activity (pup retrieval) as compared to males in Group II. Both the plasma and gonadal testosterone levels in males exhibiting pup retrieval were revealed to be significantly higher than those for males exhibiting infanticide. Thus, promiscuity, competition for receptive females, and a higher level of testosterone secretion, which are characteristic of bank vole males during the breeding season, are not out of the realm of possibility of the males to care of young. Our findings suggest that factors promoting parental responsiveness in bank vole males are sensitization due to contact with pups and an increase in testosterone secretion. Obviously, there is a need to reexamine the role that testoster-one plays in regulating rodent paternal behavior.     

The effect of familiarity on social interactions in meadow voles,Microtus pennsylvanicus: a laboratory and field study

The role of familiarity in affecting the outcome of social interactions among meadow voles was investigated in both a laboratory and a field experiment. In the laboratory, captive meadow voles, Microtus pennsylvanicus, were exposed to a conspecific's odour. The voles were then placed into two groups: familiar and unfamiliar. Familiar voles were individuals who underwent staged dyadic encounters with the conspecific to whose odours they had been exposed. Unfamiliar voles were individuals who underwent paired encounters with conspecifics to whose odours they had not been exposed. In the field experiment, familiar voles were neighbours that were trapped within each other's home ranges over two consecutive bi-weekly trapping sessions. Unfamiliar voles were individuals that were trapped on different trapping grids. The results of the laboratory and field studies were similar. Encounters between familiar females resulted in less agonistic behaviour and more amicable acts than encounters between unfamiliar females. In contrast, encounters between familiar males resulted in more agonistic behaviour than encounters between unfamiliar males. Familiarity did not affect the outcome of male-female interactions. These results are discussed in the framework of the social system of the meadow vole.     

Changes in Paternal Responsiveness of Prairie Voles (Microtus ochrogaster) in Response to Olfactory Cues and Continuous Physical Contact with a Female

In mammals, paternal care is rarely displayed, and we know little about the mechanisms regulating this behavior. Prairie voles (Microtus ochrogaster) are ideal mammals for the study of paternal behavior because they are a monogamous, bi‐parental species that is easily raised in the laboratory. Paternal responsiveness occurs at moderate levels in sexually‐naive voles and is heightened following a short cohabitation period of 72 h with a female. To determine how increased levels of paternal care are maintained after the initial cohabitation period, we tested the paternal behavior of males that were housed in isolation, were in physical contact with a female, or were exposed to various olfactory cues. The results indicate that the absence of odor cues from a female did not diminish the male’s motivation to care for infants following the initial cohabitation period. In contrast, odor cues from a male appeared to negatively influence the male’s paternal tendencies. The data also show that males that had continuous physical contact with a female spent more time responding paternally and more time hovering over the young compared to males that were housed alone. Together, these results suggest that although paternal behavior is maximized in response to continuous physical contact with females, olfactory cues may not be necessary for the maintenance of heightened paternal behavior.     

Male copulatory behavior and the induction of ovulation in female voles: a quest for species specificity.

Two experiments were conducted to investigate species specificity in the neuroendocrine responsiveness of female prairie voles to the copulatory patterns of males. In Experiment 1, prairie vole males mated for one ejaculatory series were not significantly more effective in inducing ovulation in prairie vole females than montane voles mated with prairie vole females for one series, two series, or to satiety. Mating with conspecific males did result in significantly more implanted embryos than did heterospecific matings. In Experiment 2, it was found that, when the amount of vaginal stimulation was both low and equated across groups, prairie vole males were significantly more effective in triggering ovulation in female prairie voles than were either meadow voles or montane voles. Although there appears to be some species specificity to the “vaginal codes” of these congeneric species, its biological significance is unclear.     

Sexual motivation suppresses paternal behaviour of male gerbils during their mates' postpartum oestrus

Adult male Mongolian gerbils, Meriones unguiculatus, avoid contact with their young on the day that the young are born. However, on succeeding days, fathers spend nearly as much time in contact with their offspring as do mothers. We undertook a series of studies to investigate the causes of the day-to-day change in male parental behaviour. In experiment 1, we tested males' response to pups before, after and on the day of their mates' parturition, and found that males were more parental both before and after the day of birth of their young than on that day. In experiment 2, we compared the parental behaviour of males paired either with intact or with ovariectomized dams (which do not come into postpartum oestrus) and found that males that were mated to intact females were less attentive to pups on the day of their birth than were the males mated to ovariectomized females. In experiment 3, we compared the parental responses of castrated and intact males to newborn pups and found that castrated males were more parental than intact males. In experiment 4, we compared the parental responses of males that were exposed to postpartum oestrous females but prevented from mating for 24 h. Extending the period of male sexual arousal to 24 h inhibited paternal responsiveness to neonates for 24 h. We interpret these results as being consistent with the hypothesis that on the day of birth of a litter, a male's parental behaviour is inhibited by the motivation to mate during his partner's postpartum oestrus.     

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

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

Female meadow voles,Microtus pennsylvanicus,do not alter their over-marking in response to female conspecifics that were food deprived

Many terrestrial mammals will deposit scent marks and over-marks, the latter being the overlapping scent marks of two conspecifics. Studies have shown that male rodents that are exposed to the overlapping scent marks of two female conspecifics later spend more time investigating the mark of the top-scent female than that of the bottom-scent female. This suggests that over-marking is a form of competition and that the top-scent female is more likely than the bottom-scent female to be chosen as a potential mate. Thus, females should over-mark the scents of neighboring females at a rate that will maximize their chances of attracting males. However, meadow voles live in areas that may contain patchy food availability and residents may differ in their nutritional status. Females in a better nutritional state may be more likely than those in poorer nutritional states to indicate their presence in an area, signal possession of a territory, and to attract mates. Thus, we tested the prediction that female meadow voles, Microtus pennsylvanicus, that were not food deprived would deposit more over-marks than female voles that were food deprived for 6 h. Food-deprived female voles and female voles that had continuous access to food deposited a similar number of scent marks and used a similar proportion of those marks as over-marks when they encountered the scent marks of female conspecifics. These findings suggest that the nutritional status of female voles does not affect their ability to signal their presence in an area marked by a female conspecific.     

Central Vasopressin Administration Regulates the Onset of Facultative Paternal Behavior in Microtus pennsylvanicus (Meadow Voles)

Pharmacological experiments have implicated a role for central arginine vasopressin (AVP) in regulating paternal behavior in monogamous prairie voles. Although nonmonogamous meadow voles exhibit appreciable paternal care when housed under winter, short day lengths (SD), no research has examined whether the same neurobiological systems are involved in regulating paternal behavior in a nonmonogamous species when it behaves paternally. The goal of these experiments was to determine whether central administration of AVP, but not cerebrospinal fluid (CSF), affected the suppression of pup-directed aggression and/or the onset of paternal behavior in meadow voles. Data from experiment 1 implicated a role for AVP in facilitating changes in male behavior: central administration of 1 ng of AVP (but not 3 ng or CSF) inhibited pup-directed aggression in previously pup-aggressive males, and 3 ng of AVP (but not 1 ng or CSF) induced paternal behavior in previously nonpaternal males. In contrast, AVP (1 and 3 ng) did not enhance paternal behavior in already paternal males. Experiment 2 tested the specificity of AVP. Previous research indicated that 24 h of unmated cohabitation with a female reliably induced paternal behavior in SD males. Hence, experiment 2 examined whether administration of a V_1a AVP antagonist (AVPA), but not CSF, prior to 24 h of unmated cohabitation would block the onset of paternal behavior. Males that received CSF displayed paternal behavior faster and engaged in more investigatory and paternal behaviors than males that received AVPA. Thus, pharmacological experiments support the hypothesis that AVP likely regulates paternal behavior in both facultatively and consistently paternal vole species.     

Persistence of the Attractiveness of Two Sex-specific Scents in Meadow Voles,Microtus pennsylvanicus

The function of an odour may be reflected in its fade-out time in the environment. In this study, we investigated fade-out times of two specific odours, the anogenital area scent and that of the posterolateral region. These two odours support opposite-sex preferences in male and female meadow voles, Microtus pennsylvanicus, but convey nonidentical information to conspecifics during the breeding season. The first experiment tested whether meadow voles respond preferentially to scents that were aged for 15 min (fresh) to 30 d. Males preferred female anogenital area scent to male anogenital area scent if both scents were ≤ 10 d old. By comparison, females preferred male anogenital area scent to female anogenital area scent if the scents were ≤ 25 d old. However, male and female voles preferred the posterolateral scent of males to that of females if the scents were ≤ 1 d old. Thus, fade-out times for these two scents differ for males and females, suggesting different functions. In the second experiment, male and female voles preferred fresh anogenital area scent and fresh posterolateral region scent compared with those same scents that were older. This result suggests that older scents may have lost information over time about the sex of the donor. Overall, data from both experiments indicate that voles may use specific scents for communication in different social contexts.     

Natural variation in paternal behavior is associated with central estrogen receptor alpha and oxytocin levels

In monogamous mammals paternal care plays an important role in the neural and behavioral development of offspring. However, the neuroendocrine mechanisms underlying paternal behavior remain poorly understood. Here, we investigate the association between natural variation in paternal responsiveness and central levels of oxytocin (OT) and estrogen receptor alpha (ERα). We used the frequency of licking and grooming behavior to distinguish low paternal responsiveness and high paternal responsiveness in virgin mandarin voles (Microtus mandarinus). Males that engaged in high paternal behavior had elevated levels of OT immunoreactive neurons in the paraventricular nuclei of the hypothalamus and supraoptic nuclei of the hypothalamus compared with males that displayed low paternal behavior. Likewise, males of high paternal responsiveness had more ERα immunoreactive neurons in the medial preoptic area, bed nucleus of the stria terminalis, arcuate nucleus of the hypothalamus and medial amygdaloid nucleus compared to low responsive males. The level of ERα immunoreactive neurons in the ventromedial hypothalamic nucleus was lower in highly paternal males compared to less paternal males. These results suggest that natural variation in paternal responsiveness may be directly related to variation in central OT and ERα.     

Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor α mRNA expression in the MeA and NAcc,and serum oxytocin in mandarin voles

Paternal care is necessary for the healthy development of social behavior in monogamous rodents and social recognition underpins social behavior in these animals. The effects of paternal care on the development of social recognition and underlying neuroendocrine mechanisms, especially the involvement of oxytocin and estrogen pathways, remain poorly understood. We investigated the effects of paternal deprivation (PD: father was removed from neonatal pups and mother alone raised the offspring) on social recognition in mandarin voles (Microtus mandarinus), a socially monogamous rodent. Paternal deprivation was found to inhibit the development of social recognition in female and male offspring according to a habituation–dishabituation paradigm. Paternal deprivation resulted in increased inactivity and reduced investigation during new encounters with other animals. Paternal deprivation reduced oxytocin receptor (OTR) and estrogen receptor α (ERα) mRNA expression in the medial amygdala and nucleus accumbens. Paternal deprivation reduced serum oxytocin (OT) concentration in females, but had no effect on males. Our results provide substantial evidence that paternal deprivation inhibits the development of social recognition in female and male mandarin voles and alters social behavior later in life. This is possibly the result of altered expression of central OTR and ERα and serum OT levels caused by paternal deprivation.     

Social interactions unmask sex differences in humoral immunity in voles

Sex differences in immune function are well established among laboratory rodents, with males typically having lower immunity than females. This sex difference may reflect the suppressive effects of testosterone on immune function. Because polygynous males generally have higher circulating testosterone concentrations than monogamous males, sex differences in immune function are hypothesized to be more pronounced among polygynous as compared to monogamous species. Sex differences in immune function have not been consistently observed among individually housed Microtus in the laboratory; thus, social interactions are hypothesized to be necessary for the expression of sex differences in immune function. We assessed the effect of differential housing conditions on humoral immunity and steroid hormone concentrations in polygynous meadow voles Microtus pennsylvanicus, and monogamous prairie voles M. ochrogaster. We examined humoral immunity by immunizing voles with keyhole limpet haemocyanin (KLH) and measuring antibody production 5, 10, 15 and 30 days postimmunization. Overall, meadow voles mounted higher anti-KLH immunoglobulin (Ig)M and IgG responses than prairie voles, regardless of the housing condition. Sex differences in antibody production were only observed among meadow voles housed in pairs, in which females had higher anti-KLH IgM and IgG responses than males. Sex differences in antibody production were not observed among prairie voles or meadow voles housed individually. Sex and species differences in circulating oestradiol, testosterone, and corticosterone concentrations were not related to differences in humoral immunity. These data suggest that sex differences in immune function are more pronounced among polygynous species than monogamous species, but may be context dependent. Copyright 1999 The Association for the Study of Animal Behaviour.     

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

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

Central vasopressin administration regulates the onset of facultative paternal behavior in microtus pennsylvanicus (meadow voles)

Pharmacological experiments have implicated a role for central arginine vasopressin (AVP) in regulating paternal behavior in monogamous prairie voles. Although nonmonogamous meadow voles exhibit appreciable paternal care when housed under winter, short day lengths (SD), no research has examined whether the same neurobiological systems are involved in regulating paternal behavior in a nonmonogamous species when it behaves paternally. The goal of these experiments was to determine whether central administration of AVP, but not cerebrospinal fluid (CSF), affected the suppression of pup-directed aggression and/or the onset of paternal behavior in meadow voles. Data from experiment 1 implicated a role for AVP in facilitating changes in male behavior: central administration of 1 ng of AVP (but not 3 ng or CSF) inhibited pup-directed aggression in previously pup-aggressive males, and 3 ng of AVP (but not 1 ng or CSF) induced paternal behavior in previously nonpaternal males. In contrast, AVP (1 and 3 ng) did not enhance paternal behavior in already paternal males. Experiment 2 tested the specificity of AVP. Previous research indicated that 24 h of unmated cohabitation with a female reliably induced paternal behavior in SD males. Hence, experiment 2 examined whether administration of a V(1a) AVP antagonist (AVPA), but not CSF, prior to 24 h of unmated cohabitation would block the onset of paternal behavior. Males that received CSF displayed paternal behavior faster and engaged in more investigatory and paternal behaviors than males that received AVPA. Thus, pharmacological experiments support the hypothesis that AVP likely regulates paternal behavior in both facultatively and consistently paternal vole species.