Acceleration and delay of puberty in female mice via urinary chemosignals: age of the urine stimulus

Five experiments were conducted to test the effects of the age of urine on the acceleration and delay of puberty in female mice resulting from treatment with urinary chemosignals. The chemosignal in the urine of male mice that accelerates female puberty was not affected by remaining exposed to the air at room conditions for up to 7 days, or when dried in air and reconstituted with water. The chemosignal in the urine of grouped female mice that delays puberty in females and the chemosignal present in the urine of pregnant and lactating female mice that accelerates female puberty were affected to varying degrees by exposure to room conditions; at 5-to-7 days of exposure the urine samples lost their capacity to delay or accelerate sexual maturation. These results are in agreement with earlier work indicating that the male chemosignal is not volatile, whereas the substances in urine from grouped females and pregnant or lactating females are more volatile. The results also have implications for interpretations of how the urinary chemosignals may affect the population biology of house mice under natural conditions.     

Delay and acceleration of puberty in female mice by urinary chemosignals from other females

A sequence of 7 experiments tested various aspects of the acceleration and delay of sexual maturation in young female mice as affected by cues from other females: Singly caged females produce the maturation-delaying chemosignal when exposed to urine from grouped females. Urine from females housed 3 or more/cage produces delays in puberty for young females. Urine from females in estrus accelerates puberty in young females relative to untreated controls or urine from nonestrous females. The delay-of-maturation phenomenon in female mice is not affected by reproductive history, cross-fostering of pups, or varying the cagemates according to whether they are sibs or nonsibs. Taken together these and previous findings suggest that female mice excrete, in their urine, a series of chemicals which act as signals regarding the adequacy of reproductive conditions.     

Preweaning stimulation with urinary chemosignals and age of puberty in female mice

Six experiments were conducted to assess the effects of preweaning stimulation with urinary chemosignals from four different sources on the age of sexual maturation in young female mice. The urinary chemosignals tested were those in male urine, urine from females in estrus, urine from pregnant or lactating females, and urine from females housed in groups. The split-litter technique was used for assigning mice to particular treatments. When treatments were applied during the period from 2 to 11 days postpartum, none of the chemosignals exerted any detectable influence on the age of first vaginal estrus. All 4 chemosignal treatments were effective in altering the age of puberty when treatment was applied daily from Days 12 to 21 postpartum. For urine from males and urine from estrous females, 3 days of treatment during the last 10 days prior to weaning at 21 days of age were sufficient to produce an acceleration of puberty. For urine from pregnant or lactating females, 5 days of treatment just prior to weaning were necessary to produce an acceleration of sexual development. For urine from grouped females, delays in puberty were produced only when the treatment lasted for 7 of the last 10 days prior to weaning. These findings suggest that the preweaning stimulus environment of young female mice may be important for their later sexual development. Further, use of the split-litter technique permitted the determination that variation in the age of puberty was smaller within than between litters; inheritance and/or maternal influences are clearly important factors affecting the age of sexual maturation.     

Urinary chemosignals and puberty in female house mice: effects of photoperiod and food deprivation

Urinary chemosignals from male and female house mice alter the age of puberty in females and thus influence the onset of reproductive behavior. These chemosignal phenomena have been examined with respect to a variety of factors pertaining to the social and reproductive biology of the mice. The pair of experiments reported here tested whether two non-social, environmental factors might affect the presence of the chemosignals. Alteration in the photoperiod from the normal 12 hr light/day to 6 hr light/day and restricting food intake every other day significantly altered some of the chemosignal effects on puberty for urine from singly-caged adult male and female mice, but did not change the delay of puberty produced by treatment with urine from grouped females. The results conform with a general hypothesis that the urinary chemosignals in house mice that influence puberty in young females are effective in communicating the adequacy of conditions for reproduction to conspecifics.     

Mouse vomeronasal organ: effects on chemosignal production and maternal behavior

Adult male mice excrete a urinary chemosignal that accelerates puberty in females, whereas group-housed female mice excrete a urinary chemosignal that delays puberty in young females. We found that: (1) the excretion of the puberty-acceleration chemosignal by males persisted in the absence of the vomeronasal organs and (2) the puberty-delay chemosignal was not present in the urine of group-housed females whose vomeronasal organs had been surgically removed (VNX), but was present in the urine of group-housed females subjected to sham surgery (SHAM). These results suggest that in males, vomeronasal chemoreception does not affect the excretion of the puberty-acceleration chemosignal, but that in females, the vomeronasal organ receives chemosignals that influence the excretion of the puberty-delay chemosignal. Additionally, we found no difference between SHAM and VNX females in rates of conception, litter size, pup growth, pup recognition, or maternal behavior, indicating that normal maternal processes are expressed in the absence of an intact accessory olfactory system.     

Pre- and postweaning excretion of puberty-influencing chemosignals in house mice.

Pre- and postweaning excretion of urinary chemosignals that influence puberty in female house mice were tested. The dependent variable used to assess the effectiveness of urine samples collected from donor mice was the age of first vaginal estrus in young female mice. Preweaning excretion of the puberty-delaying chemosignal by females was affected by litter sex composition; this effect interacted with the age of the young donor females. In litters of all females, the substance occurred from about the age of 9 days and in litters with 6 females and 2 males the delay substance was released from about the age of 17 days. Grouping dams during gestation but not prior to conception resulted in excretion of the puberty-delaying substance in the female progeny from the age of 17 days or possibly earlier. Young male mice do not excrete the puberty-accelerating chemosignal prior to the age of puberty. However, giving young males injections of testosterone resulted in an earlier first excretion of the acceleratory signal, suggesting that the machinery for chemosignal production is operative prior to the time of sexual maturity. Caging young males with an adult female prior to puberty resulted in earlier excretion of the puberty-accelerating substance, while caging young males with adult males retarded excretion of the substance. The findings are discussed in terms of early hormone effects on behavior and with regard to consequences for the chemosignal systems in house mice.     

Peripheral anosmia affects puberty-influencing chemosignals in mice: donors and recipients

A series of five experiments tested the effects of peripheral anosmia on both donors and recipients of urinary chemosignals that accelerate and delay puberty in female mice. Control tests determined that the manipulations, in and of themselves, did not bring about any changes in release or reception of the chemosignals. Rendering mice peripherally anosmic using a solution of zinc sulfate did result in effects on both donors and recipients. For donors, release of the substances in male urine, urine from females in estrus, or urine from pregnant or lactating females, all of which accelerate female puberty, were not influenced by peripheral anosmia. Peripheral anosmia did, however, bring about the cessation of release of the substance in the urine of grouped adult females that delays sexual maturation in conspecific females. Peripherally anosmic young female recipients of the chemosignals were accelerated in their sexual development when the treatment applied involved urine from pregnant or lactating females. However, the acceleratory effects normally produced by male urine or urine from females in estrus did not occur in peripherally anosmic young females. The substance in the urine of grouped adult females did not produce delays in puberty when the recipient females were rendered peripherally anosmic prior to urine treatment.     

Chemosignal effects on puberty in young female mice: Urine from pregnant and lactating females

A series of 8 experiments tested the effects of urine from pregnant and lactating female mice on sexual maturation of young females. Urine collected from females at various intervals during pregnancy and lactation and painted on the nares of young test females produced different effects on the age of puberty depending upon the collection interval. The urinary substance which accelerates puberty is found in the bladder urine of both pregnant and lactating females as well as in the excreted urine of females that are both lactating and also simultaneously pregnant. Four separate experiments demonstrated that grouping pregnant or lactating females at various densities, either with other females in the same stage of reproduction, or with nonreproductive females, resulted in excretion of urine which did not accelerate or delay puberty in young test mice. These results conform with a general hypothesis regarding the release of urinary chemosignals in female house mice as indicators of the adequacy of social and environmental conditions for successful reproduction.     

Acceleration of puberty in female mice by a urinary chemosignal from pregnant or lactating females: timing and duration of stimulation

Six experiments were designed to test the acceleration of puberty in young female mice treated with urine from pregnant or lactating females. Manipulations involved varying the age of onset for and duration of treatment with urine. For both urine sources the findings were similar: 1 day of treatment was insufficient to accelerate puberty, but a minimum of about 3 consecutive days of urine exposure begun before the mice were 30 days of age did hasten the onset of first vaginal estrus.     

Behavioral selection of odor cues by young female mice affects age of puberty.

Female house mice were reared from weaning at 21 days of age until first vaginal estrus in 40 1 aquaria in which they were given a choice of exposing themselves to bedding placed on opposite halves of the aquarium floor and sprayed with water or urine containing puberty-influencing chemosignals. In Experimental 1, mice housed with only male urine cues sprayed on the bedding matured significantly earlier and mice housed with only grouped female urine sprayed on the bedding matured significantly later than control mice where water was sprayed on the bedding for both halves of the aquarium. In Experiment 2, there were no significant differences in mean ages at vaginal introitus or first estrus for females reared with choices between (a) bedding sprayed with male urine versus bedding sprayed with water, (b) bedding sprayed with urine from grouped females versus bedding sprayed with water, (c) bedding sprayed with male urine versus bedding sprayed with urine from grouped females, or (d) the control condition where both sides of the aquarium contained bedding sprayed with water. Analysis of continuous video tapes of the locations of the females for Experiment 2 revealed that females chose initially to spend more time on the half of the floor with bedding that delayed puberty relative to the other side, but shifted their preference toward a more puberty-enhancing signal at about the time of first estrus. Female house mice appear to be able to exert some behavioral control over their own sexual maturation.     

Infanticide in rats: male strategy and female counter-strategy

The present series of experiments addresses the question of whether mating governs infanticide in the male rat and, in addition, asks whether the female rat has available an effective counter-strategy to male infanticide. With regard to the first question, we found that mating provides a safeguard against the killing of own young. That is, mating induces a general inhibition of infanticide coincident with the birth of the male's young and a recrudescence of infanticide synchronized with their weaning. The particular gain realized in killing alien young depends on the age of young and consequently on whether the mother had reached postpartum estrus. We also found that the pregnant female has an effective strategy to counter male infanticide which she employs before the young are born. The data show that this counter-strategy involves the synthesis of a chemosignal of low volatility emitted during pregnancy. The possible role of the male's vomeronasal system in the reception of this chemosignal is discussed.     

Acceleration of reproductive development in female Djungarian hamsters by adult males

Housing young female Djungarian hamsters (Phodopus campbelli) with an adult male accelerates uterine and ovarian development and there is a strong relationship between uterine weight and ovarian measures (e.g., follicular size). Uterine weights of females housed with an adult male for 10 days following weaning are comparable to values from females housed alone for 25 days. Removal of endogenous androgens by castration eliminated the capacity of adult males to accelerate reproductive development in young females and treatment of castrated males with exogenous androgens maintained the production of the acceleratory chemosignal. When adult male urine and ventral gland sebum were examined as possible sources for the acceleratory chemosignal, only male urine had an acceleratory effect on reproductive development. Thus, female Djungarian hamsters respond with accelerated reproductive development to androgen-dependent chemosignals in the urine of adult males. These mechanisms are similar to those found in several other rodents but contrast with the lack of such effects in the golden hamster (Mesocricetus auratus).     

Facilitation of the lordosis response of the female hamster (Mesocricetus auratus)

A series of experiments investigated the facilitative effects of stimulation from the male hamster on the lordosis response of the female. Experiments 1 and 2 demonstrated that repeated exposure to copulatory stimulation increased lordosis duration of both females in natural estrus and females in induced estrus. Experiment 3 compared the facilitative effects of mounts and intromissions. Both mounts and intromissions increased lordosis duration. Experiment 4 compared the effects on lordosis duration of (1) noncoital contact with a male (2) the sight of a male, and (3) exposure to an empty cage. Noncoital contact with a male increased the lordosis duration; the other conditions had no effect.     

Conspecific urine marking in male-female pairs of laboratory rats

Male-female pairs of rats were observed during social interactions for conspecific markings where an animal deposits urine on the body of a second animal. Injections of sodium fluorescein were used to change urinary color and provide a visible mark on the back of a conspecific. The general hypothesis tested in the three experiments was that a female would mark males differently dependent upon her hormonal status and upon the relative hormonal integrity of the males. Results of Experiment 1 were that males marked females more frequently than vice versa and female marking decreased during her estrus. Moreover, a diestrous female marked an aggressive male more than she marked a non-aggressive male (Experiment 2), and a diestrous female marked a castrated male receiving 800 micrograms testosterone propionate (TP) injections more copiously than she marked a castrated male receiving 200 micrograms TP injections (Experiment 3). Finally, aggressive and non-aggressive males marked females similarly, though the 800 micrograms TP males marked females more than the 200 micrograms TP males. These data were compared with findings from research on environmental marking in rodents, and an hypothesis was suggested that female rats use conspecific marking to identify and select males with preferred behavioral and endocrine characteristics.     

An accessory sex gland aggression-promoting chemosignal in male mice

The present study investigated male murine accessory sex glands as potential sources of a urinary aggression-promoting chemosignal. Experiments 1-4 were designed to determine whether the removal of the following glands would eliminate voided urine chemosignal activity: vesicular and coagulating glands, Cowper's gland, prostate gland, or preputial gland. The findings indicate that only preputialectomy eliminated the aggression-promoting properties of voided urine, which provides evidence that this gland is a necessary condition for chemo-activity. The efficacy of the preputial gland as sufficient for chemosignal production was examined in Experiment 5. Urine from males that had an intact preputial but removed vesicular, coagulating, Cowper's, and prostate glands was assessed and shown to possess the chemocue. It was concluded that the presence of a functional preputial gland is a necessary and sufficient condition for providing an accessory sex gland aggression-promoting chemosignal.     

Puberty-affecting synthetic analogs of urinary chemosignals in the house mouse, Mus domesticus

Endocrinologically- and socially-dependent volatile constituents of female mouse urine, identified in a previous study, were tested for their capability to accelerate puberty and extend the estrous period in young females. Several volatile ketones advanced puberty by approximately three days and extended the period of vaginal cornification in 55-75% of exposed females. High High concentrations of these substances were capable of overriding the known puberty-delaying chemosignals. Volatile cyclic enol ethers were also effective in extending estrus, but not puberty acceleration.     

Environmental factors and age of puberty in female house mice

Genetics, urinary chemosignals and related social influences, and ambient conditions affect reproduction in female mice. Five experiments tested the effects of environmental stressors on age at first vaginal estrus in female house mice. Environmental disruption in the form of changing the cage bedding and/or nesting material at various prescribed intervals resulted in different degrees of puberty delay relative to non-disrupted control mice. Disruption in the form of a male chasing the female for one to three 15-min intervals each day or the female being trapped and held in a live-trap for one to three 15-min intervals each day resulted in delays in puberty for treatments involving multiple daily disruptions. Food deprivation, but not water deprivation, influenced the onset of puberty. Variations in temperature and humidity resulted in differences in the age of puberty; low but not high temperatures and extremely low humidity levels delayed sexual maturation.     

Effects of urine from pregnant and lactating female house mice on sexual maturation of juvenile females

The effects of urine from pregnant and lactating female/mice on puberty in young females were examined. In Experiment I urine from pregnant or lactating females painted daily on the external nares of young females led to earlier sexual maturation than treatment with water or urine from singly-caged, nonlactating, multiparous adult females. In Experiment II urine from either pregnant or lactating females, injected daily into perforated plastic capsules containing cotton, effected earlier maturation in female mice caged with these capsules than did the urine of singly-caged females or water. In Experiment III the effectiveness of these treatments on reproduction per se was confirmed: young females reaching maturity earlier as the result of urine treatments were in fact ovulating and were capable of conceiving and bearing young. One explanation for the presence of the urinary pheromone(s) involves changes in hormone levels during pregnancy and/or lactation and urinary excretion levels of hormones, hormone metabolites, or chemical compounds which are hormone dependent. The pheromone excretion, triggered by external factors, may be a general signal to other females that environmental and/or social conditions are favorable for reproductive activities.     

Male odors that influence the preference of female mice: roles of urinary and preputial factors

Female mice preferred to investigate the odor of normal male urine to that of either castrated or preputialectomized male urine. Females showed no particular preferences in two-choice tests among castrated, castrated-preputialectomized and preputialectomized male urine. These results suggest that both urinary and preputial factors of males are involved in female attraction. In an experiment with urine mixtures, females preferred a mixture of urine from preputialectomized males and castrated males to a mixture of urine from preputialectomized males and castrated-preputialectomized males. This strongly suggests that the urinary factor is androgen-dependent, while the preputial factor is possibly androgen-independent. Further experiments demonstrated the possibility that the preputial odorous factor involved in female attraction is increased or newly formed after excretion of the secretion.     

Conspecific odor investigation by gray short-tailed opossums (Monodelphis domestica)

Gray short-tailed opossums (Monodelphis domestica) are small marsupials, which have recently become the subjects of numerous laboratory investigations. While these opossums have well-developed olfactory systems and complex scent-marking behaviors, the significance of their use of odors in conspecific communication is still poorly understood. Investigation of body odors by male and female opossums was examined in the present study. Males investigated flank and urine odors of nonestrous adult females significantly more than controls, but not urine from sexually inexperienced juvenile females or urine of females at cytological estrus. Since in this species females have an induced estrus, it would be advantageous for males to investigate and follow the odors of urine of diestrous females, which become receptive in proximity to males. Female opossums investigated odors of male mandibles and suprasternal glands significantly more than controls but not odors of male urine. We suggest that the use of glandular secretions is more common and more effective than urine for intraspecific communication between gray short-tailed opossums: In the semiarid conditions inhabited by the opossums, glandular secretions are less volatile and are effective for longer periods than urine and would be of greater value in intraspecific communication if, as suggested in the literature, these opossums are nomadic and meet one another infrequently.