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Several short-duration tests have demonstrated that the surgical removal of the vomeronasal organ (VNX) from sexually-inexperienced male rodents results in a reduction in copulatory behavior, compared to the effects of sham surgery (SHAM). We extended these studies to adult male prairie voles, Microtus ochrogaster, and substantially increased the duration of the tests. During the initial interactions with females, VNX males spent significantly less time with their noses in close proximity to the females than did SHAM males. Moreover, only two of nine VNX males sired offspring after having been paired with females for 8 weeks, whereas nine of 12 SHAM males sired offspring in that interval. We also found that VNX and SHAM males were equivalently non-aggressive to an anesthetized stimulus-male prior to being paired with females. However, after spending 2 weeks paired with a female, the VNX males were significantly less aggressive than were the SHAM males, possibly as a result of having copulated less often. In a later test, nearly all of the VNX and SHAM males that sired offspring were vigorously aggressive to a stimulus male. We conclude that the stimulation of the vomeronasal system in sexually-inexperienced male prairie voles is important for maximal reproductive performance and that the VNX-induced impairment in reproduction is associated with a decrease in inter-male aggression. The possible sensory effects of the vomeronasal system on the neural and endocrine control of reproduction and behavior are discussed.

Chemical cues from male voles activate reproduction in female prairie voles (Microtus ochrogaster). Twelve hours of contact with a male, followed by exposure to his soiled bedding for 2 days, is sufficient to initiate follicular maturation and induce uterine hypertrophy. Our recent work indicates that the chemosensory vomeronasal organ (VNO) can mediate this response. Here, we examined whether other sensory systems can acquire the ability to activate female reproduction as a result of learning or experience. To explore this issue, the VNO was removed (VNX) from nulliparous and primiparous females who were then exposed to cues from males. In Experiment 1, we found that nulliparous VNX females had lower uterine and ovarian weights than did sham-operated females. In Experiment 2, we determined that sexual experience did not ameliorate the reproductive deficits normally induced by VNX. The present results contrast with those of previous studies suggesting that males of some rodent species, when allowed reproductive experience prior to VNX, can utilize other sensory systems to mediate subsequent reproductive responses. We conclude that the role of the VNO in transducing chemosensory information is crucial for coordinating the reproductive efforts of male and female prairie voles.

We investigated the reproductive biology of an induced ovulator, the pine vole (Microtus pinetorum). Male puberty, measured as age at first impregnation, was found to occur as early as 44 days of age. Female puberty measured as age at first conception, was found to occur as early as 32 days of age, considerably earlier than previously reported. Females paired with stud males exhibited a doubling of uterine weight within 12 h, and vaginal sperm were present after 48 h. This indicates that although behavioral responses to males--including mating--require prolonged contact, physiological responses to males occur rapidly. Chemosignals from males slightly increased uterine and ovarian weights of females, but chemosignals from other females did not. Young females paired with stud males for 48 h in the presence of soiled bedding from the female's family had significantly smaller increases in ovarian and uterine weights than similar females paired on clean bedding. Suppression of reproduction in female offspring while they remain with the extended family unit is discussed as a life-history tactic and as a possible mechanism for inbreeding avoidance.

We investigated the vocalizations produced by adult pine voles during various social interactions by presenting an experimental animal with either an anesthetized or awake (unanesthetized) conspecific. Ultrasonic vocalizations (USVs) occurred frequently during tests in which an awake male was present, but were rarely detected in tests involving only awake females, or when a female was presented with an anesthetized conspecific. Higher rates of USVs were produced when males were tested with a familiar female than when tested with an unfamiliar male or female. Equivalent rates were produced when males were presented with either anesthetized or awake animals, but female-soiled bedding failed to elicit USVs from males. Sonic vocalizations (SVs) were produced by both sexes and were associated with aggressive behavior, but occurred only in tests between awake, unfamiliar animals. Castration greatly reduced and testosterone therapy restored USVs emitted by males in response to anesthetized conspecifics. Our results suggest that (i) USVs are emitted predominantly by males; (ii) familiarity enhances USV response; (iii) SVs are produced during aggressive interactions; and (iv) androgens regulate the production of USVs by males. Possible roles for pine vole vocalizations are discussed.

The reproductive system of female prairie voles remains quiescent in the absence of stimulation from males; however, chemosignals from males are capable of at least partially activating female reproduction. In other species, the vomeronasal system mediates some of the reproductive responses of females to males. We found that surgical removal of the vomeronasal organ (VNX) from adult female prairie voles impeded reproductive activation in response to pairing with stud males: ovarian and uterine weights of VNX females paired with stud males for 24 or 60 hours were significantly less than those of normal (NORMAL) or sham-operated (SHAM) females. Furthermore, 8 of 9 NORMAL, 10 of 13 SHAM, but only 4 of 9 VNX females paired with stud males for 60 hours mated. VNX females, however, were still able to use chemosensory cues to locate food. Behavioral observations of females encountering stud males were similar for VNX, SHAM and NORMAL females. We conclude that vomeronasal chemoreception may be a primary component of reproductive activation in female prairie voles, presumably by mediating neuroendocrine responses to chemosignals.

Male and female Microtus ochrogaster were presented with anesthetized and awake conspecifics while ultrasonic vocalizations (USVs) were monitored. Males produced significantly more USVs than females during 5-min testing sessions. Males tended to produce more USVs to unfamiliar females than to familiar female siblings. Sexual experience led to increased USV scores by males. These results suggest that USVs by male prairie voles communicate to females the male's gender and his availability for reproductive behavior.