Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys

Estrogen (E2) has activational effects on sexual motivation and mitigating effects on anxiety-like behaviors that can be attenuated with chronic exposure to psychosocial stress. Some studies suggest that this attenuation can be overcome by higher doses of E2, while others show that chronic psychosocial stress may alter the mechanisms of E2 function, thus reducing any positive benefit from higher doses of E2. To determine the interaction between psychosocial stress and E2 dose on behavior, we examined the scope of attenuation across a suite of socioemotional behaviors, including reproduction, affiliation, aggression, submission, and anxiety-like behaviors on 36 ovariectomized female rhesus monkeys. Females were exposed to graded psychosocial stress, established by an intrinsic female dominance hierarchy, where subordinate animals receive high amounts of harassment. Our data show that E2 dose-dependently increased sexual motivation and male-affiliation in dominant (e.g. low-stress) females, while subordinate females showed no positive effects of E2, even at higher doses. In addition, contact aggression was attenuated in dominant females, while non-contact aggression was attenuated in both dominant and middle-ranking females. These results suggest that the stress-induced attenuation of E2's activational effects on sexual behavior and affiliation with males may not be overcome with higher doses of E2. Furthermore, the observed behavioral consequences of psychosocial stress and E2 dose may be dependent on the behaviors of all the females in the social-group, and better resolution on these effects depends on isolating treatment to individuals within the group to minimize alterations in social-group interactions.     

Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys

Estrogen (E2) has activational effects on sexual motivation and mitigating effects on anxiety-like behaviors that can be attenuated with chronic exposure to psychosocial stress. Some studies suggest that this attenuation can be overcome by higher doses of E2, while others show that chronic psychosocial stress may alter the mechanisms of E2 function, thus reducing any positive benefit from higher doses of E2. To determine the interaction between psychosocial stress and E2 dose on behavior, we examined the scope of attenuation across a suite of socioemotional behaviors, including reproduction, affiliation, aggression, submission, and anxiety-like behaviors on 36 ovariectomized female rhesus monkeys. Females were exposed to graded psychosocial stress, established by an intrinsic female dominance hierarchy, where subordinate animals receive high amounts of harassment. Our data show that E2 dose-dependently increased sexual motivation and male-affiliation in dominant (e.g. low-stress) females, while subordinate females showed no positive effects of E2, even at higher doses. In addition, contact aggression was attenuated in dominant females, while non-contact aggression was attenuated in both dominant and middle-ranking females. These results suggest that the stress-induced attenuation of E2's activational effects on sexual behavior and affiliation with males may not be overcome with higher doses of E2. Furthermore, the observed behavioral consequences of psychosocial stress and E2 dose may be dependent on the behaviors of all the females in the social-group, and better resolution on these effects depends on isolating treatment to individuals within the group to minimize alterations in social-group interactions.     

Expression of adult female patterns of sexual behavior by male, female, and pseudohermaphroditic female rhesus monkeys

Gonadally intact pseudohermaphroditic female and normal female and neonatally castrated male rhesus monkeys were given estrogen treatment as adults and evaluated for attractivity, proceptivity, and receptivity during tests with a tethered stud male. Pseudohermaphrodites were produced by injecting their mothers during pregnancy with either testosterone propionate (TP) or dihydrotestosterone propionate (DHTP). Castrated males had reliably lower attractivity than normal females on all indicator responses shown by the tethered males. Additionally, castrated males showed reliably fewer proceptive responses on 4 of 5 measures than normal females. Receptivity could not be assessed in this situation for castrated males, because tethered males never contacted them unless the castrated males were displaying presentation. No reliable differences were observed between pseudohermaphrodites produced by prenatal treatments with TP or DHTP. Pseudohermaphrodites generally showed reliably less attractivity and proceptivity than normal females and reliably more of these traits than castrated males. Attractivity scores for pseudohermaphrodites were not different from those for normal females until proximity to the tethered male was established. Receptivity was not different in pseudohermaphrodites compared with normal females. Results indicate prenatal androgenization and its developmental sequelae lead to a defeminization in adulthood which, in this testing situation, was principally manifested by a deficiency in the performance of proceptive behaviors. Additionally, defeminization in rhesus monkeys, unlike that demonstrated in rodents, does not depend upon actions of an aromatizable androgen.     

Seasonal changes in reproductive behavior in two ovariectomized female rhesus monkeys treated year-round with estradiol

Two ovariectomized female rhesus monkeys treated year-round with estradiol-filled capsules were used in hour-long behavioral tests with male rhesus monkeys both in and out of the normal breeding season. The study was designed primarily to test male hormonal responses to copulatory behavior and it was expected that behavior of the females would be essentially the same under both seasonal conditions. Several behaviors of the female, however, were found to fluctuate on a seasonal basis, namely (1) proximity to the male, (2) grooming of the male, (3) sexual presentations, and (4) threatening away (a form of sexual invitation). All of these behaviors, except proximity, were found to be positively correlated with the male partner's testosterone levels before and after the behavior test in the only test condition in which most males ejaculated. The preliminary suggestion is made that these females responded to some cue, either from the environment or from the males, that caused a change in their behavior between breeding and nonbreeding seasons despite the constant hormonal environment provided by the estradiol capsules. Since the same behaviors which were sensitive to seasonal effects were positively correlated with male testosterone levels, it is possible that the male's hormonal status affects affects female behavior.     

Female sexual behavior displayed by androgenized female rhesus macaques

Adult, prenatally androgenized female rhesus macaques (female pseudohermaphrodites) that had been ovariectomized were treated with estradiol benzoate (20 micrograms/day) and paired with males at weekly intervals for 4 weeks beginning on Day 12 of injection. Their sexual behavior was compared to that of a control group of females. The sexual behavior of the males toward the two groups of genetic females (control females with normal female genitalia and hermaphrodites with well-formed male genitalia) was also observed. Females and hermaphrodites were equally receptive to male invitations to copulate. Although there were some differences in the specific components of proceptive behavior displayed by the two groups, the overall differences were negligible. Earlier studies had shown that infant and juvenile hermaphrodites resemble males in patterns of play and sexual behavior. When treated with testosterone as adults and paired with receptive females, they displayed mounting patterns typical of males--one of seven hermaphrodites achieved intromission and ejaculated. It has now been demonstrated that when treated with estrogen and paired with males, they responded as females. Hence, the capacity to behave sexually as males is not incompatible with the capacity to respond sexually as females under certain hormonal and environmental conditions.     

Effects of estradiol and aging on fine manual performance in female rhesus monkeys

Aging is characterized by a progressive deterioration of motor function related to dysfunctions of the nigrostriatal system. Because estrogen has been reported to protect dopaminergic neurons and to improve the motor deficits associated with Parkinson's disease, we hypothesized that it would partially reverse the age-related decline of motor function in normal aging. We tested the effects of estrogen treatment and withdrawal on fine motor performance in five aged (21-24 years old) and five young (6-9 years old) ovariectomized female rhesus monkeys. The tests required the monkeys to use each hand to retrieve a Life Saver candy from metal rods bent in shapes of different complexity. Monkeys were tested twice a week for 8 consecutive weeks, during treatment with placebo or ethinyl estradiol (EE(2)) in alternating 14-day blocks. Each behavioral test was videotaped and subsequently scored for the duration and the success of the first trial on each shape. Both groups of monkeys improved rapidly with practice in speed and success of retrieval. The older monkeys were slower but as successful as the young monkeys in retrieving the candy. The left hand was faster than the right hand for both the aged and young females. We failed to detect any effect of EE(2) treatment on speed or success of retrieval in either group. These results confirm the slowing of fine motor performance with aging in female rhesus monkeys. They also indicate that estradiol, at least as administered in this study, does not benefit fine manual performance.     

Periovulatory changes in female sexual behavior and patterns of ovarian steroid secretion in group-living rhesus monkeys

The behavior of nine intact group-living adult female rhesus was observed for 30 min daily with each of four adult male rhesus across a verified ovulatory menstrual cycle. Blood samples collected from females daily or on alternate days were analyzed for estradiol, testosterone, and progesterone. Female patterns of approach, follow, and initiate proximity increased several days prior to the estradiol peak, peaked on the day of the estradiol peak, then declined completely or to very low frequencies. Mounts, intromissions, and ejaculations increased significantly on the day of the estradiol peak, remained elevated for 2 more days, then declined completely by the fifth day after peak estradiol. Ejaculations never occurred outside of a 10-day period starting 4 days before the estradiol peak and ending 5 days after the estradiol peak. During this period females initiated over 90% of all approaches. Female hand slap, threaten away, and stand up increased significantly on the first day of increased copulation, remained elevated while copulation was significantly elevated, then decreased along with the decline in copulation. Ten of eleven patterns of female behavior correlated significantly with estradiol level prior to the estradiol peak. All were significantly inversely correlated with progesterone level after the estradiol peak. No pattern of female behavior correlated significantly with testosterone either before or after the estradiol peak. Similarly, male patterns of behavior correlated with female levels of estradiol and progesterone, but not testosterone. These results demonstrate a relationship between increased serum estradiol and increased female initiation of sexual behavior. The finding that some patterns of female behavior increase several days prior to copulation, whereas other behaviors increase coincident with increased copulation suggests that the behavior of group-living rhesus females serves two functions. The first is to communicate sexual interest and the second is to maintain the consort pair and increase the probability that ejaculation will occur. In addition, the strong correlation between preovulatory female behavior and estradiol level suggests that the female's behavior provides precise information about her reproductive state and could thus coordinate copulation with maximal fertility.     

Effects of androgen administration on sexual invitations by female rhesus monkeys (Macaca mulatta).

Pairs of adult rhesus monkeys of opposite sexes (12 pairs) were studied during 1-h mating tests (986 tests). Ovariectomized females received 5 microgram oestradiol intravaginally throughout to keep them attractive to males and maintain a relatively constant level of male sexual activity. Females were given subcutaneous silastic implants of testosterone to change their sexual receptivity. A threefold change in sexual invitations resulted from the implantation and removal of testosterone in the absence of any major changes in the behaviour of their male partners. These changes in invitational behaviour therefore reflected an action of the hormone upon an internal mechanism within the female subserving sexual motivation which was independent of changes in the behaviour of the male. Radioimmunoassay of plasma testosterone (109 samples) and plasma oestradiol (86 samples), and gas-liquid chromatography of vaginal secretions (306 samples), facilitated the monitoring of variables needed to interpret the results.     

Menopause in female rhesus monkeys

Fifteen female rhesus monkeys (Macaca mulatto), ranging in age from 8 to 34 years, were studied for one year to characterize the endocrine and menstrual changes associated with menopause in this species. Five monkeys were premenopausal; these younger monkeys, ages 8–11 years, menstruated and showed cyclic ovarian activity during the 12–month study period, as evidenced by menses and periodic elevations of serum estradiol (E₂) and luteinizing hormone (LH) concentrations. Four females, ages 24–26 years, were in transition to menopause. Two of these perimenopausal females menstruated and secreted E₂ and LH in a periodic fashion; the other two females showed elevated LH concentrations, consistently low E₂ levels, and no evidence of menstruation. Six females, ages 27–34 years, were clearly postmenopausal; LH concentrations were high, whereas E₂ concentrations were uniformly low. There was a significant inverse correlation between basal E₂ concentrations and age, and a significant positive correlation between age and LH concentrations across all 15 animals. Hormonal changes indicative of ovulation, when they occurred, were generally restricted to the winter and early spring months. Histological analysis of ovaries from four postmenopausal females revealed little or no evidence of active folliculogenesis. These data indicate that menopause in female rhesus monkeys does not occur until the second half of thethird decade of life. © 1995 Wiley-Liss, Inc.     

Influence of progesterone on sexual behavior in castrated male rhesus monkeys treated with testosterone

The effect of progesterone (P) on sexual behavior was tested in five long-term castrated rhesus monkeys treated simultaneously with testosterone (T) and P. A control group consisting of three long-term castrates was treated only with T. Plasma levels of T and P were measured at weekly intervals, and behavioral data were collected for each animal twice a week throughout the study. Progesterone has been reported to inhibit sexual behavior in male guinea pigs and mice, but the levels of behavior in our two groups of monkeys did not differ from each other over 8 weeks of treatment and testing.     

Proceptive behavior of female rhesus monkeys during tests with tethered males

Proceptive behavior of female rhesus monkeys during follicular and luteal phases of the ovarian cycle was examined in laboratory tests with a tethered male partner. Cyclical changes in proceptive behavior were observed. In tests during the follicular phase of their cycles, females on the average approached and solicited the male at a higher rate, spent more time sitting within proximity of him, and less time at a maximum distance away from him than during tests in the luteal phase of their cycles. Additionally, in the follicular phase of their cycles, females exhibited an increase in proceptivity following the male's ejaculation. This latter finding was discussed in light of other observations demonstrating that male rhesus monkeys are capable of multiple ejaculations. When females were paired with a tethered, ovariectomized female as a partner, rather than an adult male, none of the cyclical changes in proceptive and sexual behavior were observed.     

The sexual behavior of Japanese monkeys

The sexual behavior of four troops of wild Japanese monkeys at Jigokudani and at Takasakiyama was observed for about one month during the middle of the breeding season. Sexual behavior was classified into 46 types from the viewpoint of sign behavior, and a catalogue of this was presented. It was shown that there was high correlation between the two most common types of behavior of the male, hindquarters-display and hand-on-back, and subsequent copulation. Seven stages were noticed in the sequence from initial encounter to leave-taking of a consort pair, and these stages were observed in a fairly regular order in the copulatory sequence. There was correlation between male positive attitude toward females and dominance rank order of the male, but was not between copulation and the dominance rank order. Adult females without infant showed and received positive sexual behavior; females who had an infant neither showed nor received the behavior; juvenile females showed but did not receive the behavior. Males showed positive sexual behavior toward females of their own group, but copulation between them was the most scarce due to female refusal.     

Timing of sexual maturity in female rhesus monkeys (Macaca mulatta) housed outdoors

A comparison of the age and season at first parturition was made for spring-born female rhesus monkeys and for females born in the fall to mothers who had been laboratory-housed before being transferred outdoors. Females (N = 9) born during the fall had first parturition during the spring and summer, as did all spring-born females (N = 68), and not during the fall as would be predicted if age were the determining factor. A separate analysis of post-menarchial, spring-born females (N = 5) beginning in September at 29 months of age revealed that the ensuing 12 months were characterized by low serum levels of oestradiol (less than 50 pg/ml), progesterone (less than 1.0 ng/ml), LH (less than 7.0 ng/ml), and FSH (less than 5.50 micrograms/ml). First ovulation subsequently occurred in the fall in all subjects at a mean age of 41.9 +/- 0.1 months, and was preceded by significant elevations in basal LH and FSH, coincident in time with the transition of summer to fall (September). Female copulatory behaviour was restricted to the period surrounding first ovulation, beginning some 2 weeks before and ceasing within 3 days after the oestradiol peak. The most rapid gain in weight occurred during the summer months before first ovulation, and was associated with significant elevations in serum GH and prolactin. These data suggest that season may influence the timing of sexual maturation in rhesus monkeys kept outside in such a way that the occurrence of first ovulation is restricted to the fall and winter months.     

Impact of a privacy panel on the behavior of caged female rhesus monkeys living in pairs

Thirty paired female rhesus monkeys were tested in a control situation when companions had no privacy, and in an experimental situation when they were offered the option to move behind a panel and be alone. Paired partners spent significantly more time in close proximity (same half of the cage) when the privacy panel was provided (means with panel = 76.0%/h vs. means no panel = 60.8%/h; p less than 0.005). At the same time, they were more engaged in affiliative interactions (means with panel = 37.4%/h vs. means no panel = 26.5%/h; p less than 0.025) while the incidence of agonistic interactions tended to decrease (means with panel = 0.3/h vs. means no panel = 2.2/h; p less than 0.1). It was concluded that rhesus monkeys have a need for companionship. They prefer to stay in close proximity with a compatible partner even though this may reduce their available cage space. It was further concluded that companions have no need for prolonged periods of visual seclusion, but occasional privacy is beneficial for their relationship.     

Dihydrotestosterone propionate effects on dominance and sexual behaviors in gonadectomized male and female rhesus monkeys.

One triad of male and two triads of female gonadectomized rhesus monkeys were observed as social groups assembled for repeated hour-long sessions. Social relationships were measured in terms of aggressive behavior between the members of each group in order to determine the dominance hierarchical order. Sexual performance was assessed for each male, before and after castration, in tests with an estrogen-stimulated ovariectomized female. Similar measures were made when the same female was periodically introduced to the all-male triad. When dihydrotestosterone propionate (DHTP) was administered for a period of 6 weeks to the middle-ranking member of each group, social status changes occurred in two groups, one male and one female, resulting in the elevation of the treated monkeys to the highest rank in the dominance hierarchy. In the other female group, aggressive behavior was increased with DHTP treatment of the middle-ranking female. Somatic effects, particularly a gain in body weight, occurred in all treated animals. Yawning behavior also increased significantly in those animals receiving DHTP. The latter two effects returned toward pretreatment levels following the cessation of hormone injection; however, changes in dominance hierarchy persisted to the end of the experiment, 6 weeks following the last DHTP treatment.     

Estimation of body fat in female rhesus monkeys

Measurement of height (crown–rump length), body weight, and abdominal subcutaneous fat depth, based on skinfold thickness taken from 13 female rhesus monkeys comprising two age groups were correlated with body fat values derived from tritiated water determinations of total body water. The manner with which each measure was related to percent body fat differed as a function of age of the animal. In the young, nulliparous females, crown–rump length was the single best predictor of body fat, whereas in the older, multiparous females, skinfold thickness correlated most highly with body fat. When all measurements, including the Quetelet index [(wt/ht)² × 1,000], were combined statistically and regressed against percent body fat, a significant increase in predictive ability was obtained. When each age group was considered separately, the resulting equations again reflected the agegroup biases. In addition, as an internal check on the validity of the regression equations, an additional regression analysis was performed using morphometric data from selected animals in each age group. These equations yielded accurate estimates of body fat when compared to determinations made from total body water. These analyses indicate that the predictive accuracy of morphometric data is greatly enhanced by using these measurements in concert. Furthermore, the utility of such predictions is influenced by the specific physical characteristics of the subject population.