Female Pine Voles Research Articles

Perinatal exposure to endocrine disrupting compounds alters behavior and brain in the female pine vole

Endocrine-disrupting chemicals (EDCs) are synthetic chemicals that arise from sources such as pesticides and have the ability to mimic or inhibit gonadal steroid hormones. The objective of this research was to examine the effects of EDCs on the behaviors associated with monogamy and the expression of related neuropeptide receptors. Pine voles, a novel experimental mammal, were chosen because they display strong monogamous pair bonding. Female pine voles were orally administered estrogenic diethylstilbestrol (DES) and methoxychlor (MXC) or oil control throughout gestation and lactation of pups. Exposed pups were tested as adults. Preference for the mate and maternal behaviors were assessed. While the ability to form partner preferences was intact, DES-exposed females showed increased aggression toward a stranger, while MXC exposed females showed a strong trend toward spending more time alone. Oxytocin (OT) receptor binding in the brain was assessed for possible effects on this behaviorally important neuropeptide signaling system. The cingulate cortex showed a reduction in OT binding in the MXC group. These findings demonstrate that exposure to EDCs during pre- and neonatal development can alter female adult neural phenotype and behavior related to monogamous behavior traits.

Reproductive activation of pine voles ( Microtus pinetorum): examination of physiological markers

We tested the hypothesis that the presence of an opposite-sex conspecific will result in time-related changes in measures of reproductive activation. We housed male–female pairs of pine voles together for 0, 2, 6, 12, or 24 h before collecting blood, reproductive organs and brains for immunocytochemical analysis of LHRH and c-fos. Control animals were never exposed to an opposite-sex conspecific. Following exposure to a male, there was a significant increase in uterine weight but not in LH levels. In males, there were no changes in peripheral indices of activation, i.e. LH levels, testes and seminal vesicle weights were not altered. Consistent with no change in circulating levels of LH, there was no change in LHRH immunoreactivity at any time. However, c-fos immunoreactivity was significantly greater in both males and females in the cingulate cortex and rostral bed nucleus of the stria terminalis (BNST) at 2 h, and in the caudal BNST at 2, 6 and 12 h. Similarly, c-fos immunoreactivity was increased in the rostral MPOA in both males and females at 2 and 6 h. However, in the caudal MPOA, there was a significant interaction between sex and time due to increased c-fos immunoreactivity in females only at 6 h. These results indicate that, in both male and female pine voles, exposure to an opposite-sex conspecific is sufficient to produce rapid, neural activation in brain areas known to be involved in reproductive activation and sexual behavior. This early activation did not occur in LHRH neurons. It is not known if this activation, particularly at early times, is due to reproductive activation or to the formation of pair bonds.

Mechanisms of reproductive suppression in female pine voles (Microtus pinetorum).

In co-operatively breeding birds and mammals, philopatric females are often reproductively suppressed. Many studies have focused on the functional significance of reproductive suppression, but further investigation of the mechanisms involved is required for a complete understanding of this process. This study investigated whether reproductive suppression in non-reproductive female pine voles (Microtus pinetorum) occurs as a result of lack of gamete maturation or lack of increase in LH. The behaviour of male pine voles was also examined to determine whether they show a preference for the mother versus her daughter, as lack of male stimulation may inhibit an increase of LH in daughter pine voles. Ovarian development and circulating LH concentrations were investigated in females housed with a prospective mate in the presence or absence of a parent. Maturation of gametes was not affected by the presence of a parent. In the presence of the mother, there was no increase in LH, as was observed in females housed with or exposed to a novel male. Males spent more time with mothers and possibly showed a preference for mating with the mother. These results are consistent with the contention that ovulation does not occur in female pine voles housed in the presence of their mother; however, it is not clear whether the lack of ovulation is caused by lack of stimulation from the male or suppression by the mother.

Behavioural suppression of female pine voles after replacement of the breeding male

Examination of the mechanism of reproductive suppression includes determining which cues are involved and the context in which they occur. We studied groups of pine voles,Microtus pinetorum, that were disrupted by the replacement of the breeding male and compared them with intact family groups. If reproductive suppression is mediated by chemical cues, then soiled bedding should be sufficient to prevent production of litters by daughters. If reproductive suppression involves a behavioural component, we should observe aggressive behaviours or those indicative of dominance interactions directed from the mother towards the daughter or the replacement male. If replacement of the breeding male leads to conflict between the breeding female and her daughter, then more aggression or dominance interactions would be expected in disrupted than in intact families. The presence of the mother decreased reproduction by daughters, but chemical cues alone were not sufficient to prevent the daughter from mating with the replacement male. Rather, this decrease in reproduction seemed to be mediated by behavioural interactions. We propose that the mother's tugging on the daughter may lead to subordination of the daughter. The mother's presence may also alter the behaviour patterns of the male and daughter, which could delay reproductive activation of the daughter, prevent the formation of pair bonds or inhibit sexual behaviour. These behavioural interactions appear to depend on the presence of an unfamiliar male, because tugging, for example, was less frequent in intact family groups.

Odor Preferences of Weanling and Mature Male and Female Pine Voles

Olfactory cues from conspecifics have strong influences on behavior. Both female and male juveniles are attracted to familiar odors while adults show preferences for odors of opposite-sex conspecifics. Females show an increased preference for male odors as they mature, but no study has examined whether change with age is seen in males. In this experiment, responses of weanling and mature male and female pine voles (Microtus pinetorum) to familiar odor cues from their family versus those of an unfamiliar, opposite-sex conspecific were examined. Voles were tested in a three-chambered cage with end chambers containing the stimuli. There was a significant difference in odor preference between weanling and mature females. Weanling females preferred odor cues from their families, and mature females preferred the odors of unfamiliar mature males. The pattern was similar in males but the effect was not as strong. The results support the hypothesis that responses to odor cues change with age in pine voles. At least for females, the change in response to odor cues may be involved in the timing of reproduction and thus dispersal.

Androgen Exposure and Reproductive Behavior of an Induced Ovulator, the Pine Vole (Microtus pinetorum)

The actions of steroid hormones on brain and behavior are classically divided into organizational effects that are permanent and occur early in development and activational effects that are temporary and occur throughout life. Here, we test the hypothesis that in an induced ovulator, testosterone defeminizes only those neural tissues that rely on synergistic interactions of estrogen and progesterone for normal function in adulthood. Female voles,Microtus pinetorum,injected with testosterone (T) or oil neonatally were paired with males for an 8-week period. During the pairing, androgenized and oil-treated females spent a similar amount of time investigating the caudal and rostral regions of the males. Males spent significantly less time investigating the caudal and rostral regions of androgenized females. Androgenized females mounted males, did not exhibit lordosis, and were less likely to be mounted by males. Moreover, none of the 10 androgenized females gave birth, whereas 8 of 9 control females gave birth. Androgenized females were also not capable of being stimulated into reproductive condition by males. Injection of 0.5 μg of estradiol benzoate for 4 consecutive days resulted in reduced uterine hypertrophy in androgenized females. These results support the original organizational–activational hypothesis by showing that neonatal androgenization defeminizes and masculinizes female pine voles.

Chemical Cues are Necessary but Insufficient for Reproductive Activation of Female Pine Voles (Microtus pinetorum)1

Among various arvicoline rodents, reproduction is influenced to varying degrees by social factors, including behavioral or chemical cues. Since previous research suggested that chemosignals from adult males reproductively activate female pine voles (Microtus pine-torum), we sought to determine specifically what types of stimuli promote the activation response. In these experiments, female were exposed to unfamiliar adult males, or to some combination of cues from males, or were housed alone. Using uterine mass as a measure of reproductive activation, we found that females were not activated by exposure either to male urine by itself or to male-soiled bedding by itself, but full contact with a male clearly resulted in heavier uteri. Females whose vomeronasal organs were surgically excised failed to undergo reproductive activation when housed with males. Finally, females allowed physical contact by being housed directly underneath males had heavier uteri than did females whose housing allowed contact only with the chemical cues from males. Among female arvicoline rodents, it appears that there exists a physiological continuum between absolute dependence on both contact and chemical cues from males vs. absolute independence for reproductive activation. The present results place female pine voles closer to the former extreme than to the latter.

Male siblings inhibit reproductive activity in female pine voles, Microtus pinetorum.

Pine vole females paired in breeding cages with male siblings remain unreproductive beyond the age of puberty onset. In this study only 10% of females caged with their brothers reproduced, whereas 85% of females placed with strange males had litters. Mating between a female and a strange male was also suppressed by the presence of a male sibling sequestered behind a wire mesh barrier in the breeding cage. When the sibling male was removed from the cage after 1 day, 78% of the females produced litters. When the sibling remained behind the barrier in the breeding cage, only 42% gave birth to young conceived in his presence. Conception of second litters during the postpartum estrus occurred in over 80% of females caged with strange males alone and only 10% of females caged with sibling males. Female pine voles are induced to become reproductively active by strange males but this activity is depressed by the presence of a brother, and once initiated it does not continue if the female is caged with her brother.

Copulatory behavior of pine voles (Microtus pinetorum).

7 male and 6 female pine voles, Microtus pinetorum, were observed in a total of 26 tests of copulatory behavior. They displayed a pattern with no lock intravaginal thrusting, ejaculation possible on a single insertion, and multiple ejaculations. The first ejaculatory series required approximately 5 min, with a mean of five intromissions and 36 thrusts. Post-ejaculatory intervals following the first series averaged 16 min. and increased in successive series.