Continued copulation of ovariectomized adrenal-suppressed stumptail macaques (Macaca arctoides).

Female stumptail macaques continue to copulate at moderate to high levels for years after gonadectomy. This study examined the extent to which sexual behavior of ovariectomized stumptail females was maintained by steroids of adrenal origin, and second, considered the possibility that ovarian fragments might have been left in situ following surgery. Daily injections of 0.1 mg of dexamethasone sodium phosphate suppressed serum cortisol, estradiol, and testosterone by at least 85% in three of four ovariectomized females, but dihydrotestosterone was suppressed by only 50 to 70%. The fourth female showed maximal suppression of cortisol but maintained much higher levels of the other steroids, in particular estradiol, and therefore it was strongly suspected that this animal had an ovarian fragment.Within the limits to which sex steroids were depressed with dexamethasone, no correlation was found between steroid levels and sexual performance. Ejaculatory frequencies and measures of attractivity, proceptivity, and receptivity collected during heterosexual pair tests remained unaffected in all four females during 4 weeks of dexamethasone treatment. Thus it was concluded that the maintenance of copulatory activity after ovariectomy in this species was largely due to nonsteroidal mechanisms.     

Heterosexual interactions of pairs of laboratory-housed stumptail macaques (Macaca arctoides) under continuous observation with closed-circuit video recording

Female-male interaction of heterosexual pairs of stumptail macaques, housed together continuously, was studied 24 hr per day using closed-circuit video recording. Two pairs were studied for approximately 2 months each. Although no generalizations can be made from such a small sample, no aspect of behavioral interaction varied significantly with the stage of the menstrual cycle of the female partner. Copulation occurred regularly but only during the daylight hours. Both pairs showed several peak ejaculation days (5–21 ejaculations/day), which were distributed throughout the entire menstrual cycle. In general, the highest number of ejaculations was observed to occur when the animals were put together either for the first time or following a separation of a few days. In one pair the female became pregnant, and from the fifth week of pregnancy onward there was a gradual increase in male aggression, coinciding with a decrease in male sexual and grooming behavior. In a second study eight different pairs were observed during the first day together and male copulatory behavior was studied. Two patterns of copulatory behavior could be discerned: pairs displaying a high number of ejaculations (19–38) and pairs displaying a low number of ejaculations (4–8). With regard to the interejaculatory interval (IEI), the male stumptail appeared to be unique. In contrast to what has been reported for other mammals, i.e., a steady increase in IEI with subsequent ejaculations, the stumptail showed increasing IEIs only during the first three to four, as well as between the last, ejaculations; in between, the IEI remained relatively constant. The maximum number of consecutive ejaculations observed was 38, displayed during a 10-hr time period (mean (± SEM)IEI, 12.9 ± 3.5 min).     

Persistence of sexual behavior in ovariectomized stumptail macaques following dexamethasone treatment or adrenalectomy

Daily administration over a period of 6 weeks of increasing doses of dexamethasone sodium phosphate (DEX) to seven long-term ovariectomized female stumptail monkeys significantly lowered circulating levels of testosterone without reducing any aspect of the females' sexual behavior or that of their male partners. Since treatment with DEX failed to suppress serum testosterone levels completely an additional experiment was performed in which the sexual behavior of five ovariectomized stumptails was compared before and after bilateral adrenalectomy, combined with chronic administration of both gluco- and mineralocorticoids. Serum levels of both testosterone and estradiol were reduced to very low levels in females after ovariectomy and adrenalectomy, yet no significant depression of females' sexual performance or that of their male partners occurred. Subsequent sc administration of estradiol or estradiol + testosterone in Silastic capsules to ovariectomized, adrenalectomized stumptails had little effect on sexual interaction. In a third experiment five ovariectomized stumptails which initially were relatively unreceptive and unattractive to males were given first testosterone and then testosterone + estradiol sc in Silastic capsules. One of the three indexes of females' receptivity increased significantly after testosterone; however, no other essential aspect of sexual interaction was affected. These findings suggest that sex steroids are normally not required in the female stumptail macaque for activation of preceptive and receptive sexual behaviors or for maintenance of sexual attractivity.     

Natural or hormone-induced sexual and social behaviors in the female brown lemming (Lemmus trimucronatus)

The behaviors of intact or ovariectomized, estradiol benzoate-treated or estradiol benzoate followed by progesterone-treated female brown lemmings were compared. Intact, diestrous females engaged in more social interactions with a male than did ovariectomized females (Experiment 1). In the first 5 min of a 1-hr mating exposure (Experiment 2, Test A) intact females in natural estrus engaged in more social and sexual behaviors than did ovariectomized females in estrogen-induced estrus. However, during the last 5 min of the 1-hr exposure (Test B) ovariectomized females receiving estrogen alone continued to show high levels of sexual activity with a male partner, while intact estrous females or females receiving estrogen followed by progesterone showed an apparent drop in sexual receptivity and an increase in aggressivity. Aggressive behaviors, as indexed by threat-leap behaviors on the part of the female may increase in the presence of progesterone. Declines in sexual activity, occurring within 1 hr of progesterone injection, were apparently dependent on the interaction of progesterone and copulatory events which may affect both the male and female.     

The Role of Gonadal Steroid Receptor Activation in the Restoration of Sociosexual Behavior in Adult Male Rats

This work tested the hypothesis that gonadal steroid receptor activation was necessary for the restoration of several sociosexual behaviors (such as copulatory behavior, partner preference, 50-kHz vocalizations, and scent marking) in testosterone-treated gonadectomized male rats. Gonadal steroid receptors were blocked by systemic administration of the antiandrogen hydroxyflutamide, the antiestrogen RU 58668, or both antagonists simultaneously in a restoration paradigm. Inhibiting androgen receptors with hydroxyflutamide blocked the restoration of male copulatory behavior, partner preference (time spent with a sexually receptive female over a nonreceptive female), 50-kHz ultrasonic vocalizations, and scent marking. On the other hand, we did not find that blocking estrogen receptors with RU 58668 inhibited the restoration of copulatory behavior or partner preference in testosterone-treated gonadectomized male rats, even though the level of brain nuclear estrogen receptor occupation was significantly reduced to the level found in gonadectomized males. However, the restoration of scent marking and 50-kHz vocalizations were impaired by RU 58668. Blocking both nuclear androgen and estrogen receptors with the two antagonists simultaneously did not have a greater inhibitory effect than treatment with each antagonist alone. Therefore, the activation of nuclear estrogen receptors is necessary for the restoration of some, but not all, sociosexual behaviors, which are also androgen receptor-dependent. Besides nuclear estrogen receptors, there are additional, but unknown, targets of estradiol that play a role in mediating copulatory behavior in adult male rats. Moreover, the signals from multiple gonadal steroid signaling pathways converge in the regulation of some sociosexual behaviors in adult male rats.     

Inhibition of sexual behaviour among subordinate stumptail macaques,Macaca arctoides

A series of four experiments was conducted to examine rank-related differences in copulatory behaviour among male stumptail macaques, and to investigate the proximal mechanisms responsible for the reduced sexual activity among subordinate males. In the first experiment observations were made for 34 months on a group of 97 individuals. Lower-ranking males usually copulated surreptitiously and copulations attempted in view of higher-ranking males were more likely to be interrupted. Lower-ranking males also copulated more frequently when higher-ranking males were removed from their view; however, even the presence of a restrained higher-ranking male was sufficient to inhibit their copulatory behaviour. Three experiments were performed on a second social group of 30 stumptails to replicate and extend the findings of experiment 1. Increases in sexual activity in the absence of higher-ranking males were specific to sexual behaviour, and were not caused by general excitement due to removal or handling of animals. Female proceptive behaviour also increased in the absence of high-ranking males suggesting that the suppression of copulatory activity may not be solely due to behavioural changes in the males. These findings provide the first experimental support for the hypothesis that the copulatory behaviour of subordinate male stumptail macaques is suppressed by the presence of dominant males and that the absence of these males removes the suppression.     

On the correlation between sexual behavior and ovarian hormone level during the menstrual cycle in captive Japanese monkeys

The amount of estradiol and progesterone in the systemic blood plasma of six adult female Japanese monkeys was measured by radioimmunoassay. Data on heterosexual pairing tests was also collected and examined for correlation with these hormones. The relationship between ovarian hormones and frequency of ejaculation varied with each female. In nine normal menstrual cycles, the frequencies of invitation and approach by the female reached peaks on the day of the estradiol surge, after which they rapidly decreased. Frequencies of male behaviors including approach, leaving, invitation, and yawning significantly decreased during the luteal phase, as compared with those at the midcycle. Grooming by both sexes of the partner reached low points during the late follicular phase. The number of ejaculations per test increased significantly at the midcycle and reached a maximum a few days after the estradiol surge. The present results suggest that female proceptivity is highly correlated with the amount of estradiol, but her attractiveness is little correlated with estradiol and is lowered by progesterone.     

根田鼠的熟悉性及其自然动情下的配偶选择

报道了在室内雌鼠自然动情条件下根田鼠两性个体配偶选择的3种熟悉性效应的5组实验结果,包括雌性对熟悉和陌生雄鼠、配偶和陌生雄鼠、配偶和熟悉雄鼠的择偶行为实验 , 雄性对熟悉和陌生雌鼠、配偶和陌生雌鼠的择偶行为实验。在实验前, 将1对性成熟的雌雄鼠 (非亲缘关系) 每天关养8 h 共8 d 建立熟悉性; 配对雌雄鼠至少生育1胎则为配偶关系。在 Y 形迷宫内的30 min 实验中, 两个被选择鼠分别以项链拴在横跨选择箱顶端中央的一根铁丝上, 限制它们在各自箱内活动; 而允许异性选择鼠从中立箱自由进入两个选择箱。记录选择鼠对异性被选择鼠的访问、社会探究、攻击、交配和友好行为的频次和时间。经Wilcoxon 关联样本 T 检验发现, 除交配行为不显著外, 雌性根田鼠均选择熟悉性较高的雄鼠; 而雄鼠不具这种选择性。该结果提示雌雄根田鼠的不同择偶行为也许就是反映该种婚配制度特征的直接行为过程。因此, 在择偶行为中, 雌性根田鼠表现的单配性倾向和雄鼠的多配性倾向, 只能以其婚配制度为一雄多雌制的假设来解释。我们的实验还说明在多配制田鼠中, 一雄多雌制与混交制在雌鼠择偶行为上是不同的, 而与单配制的相似或相近, 故简单地比较多配制与单配制则不能反映田鼠亚科动物婚配制度的多样性。     

Hormonal and monoaminergic influences on masculine copulatory behavior in the female rat.

Ovariectomized female rats receiving estradiol benzoate (EB), testosterone propionate, or no hormone treatment were administered parachlorophenylalanine (PCPA), alone, or in combination with pargyline. Sixteen days of EB-treatment resulted in hypertrophied pituitaries and concomitant pressure damage to ventral portions of the brain. Irrespective of hormonal condition females receiving PCPA treatment displayed more masculine copulatory behavior than females receiving PCPA + pargyline or saline treatment. In a second study PCPA also potentiated masculine copulatory behavior in ovariectomized and adrenalectomized females receiving no hormone treatment. The ejaculatory pattern was observed in one of eight females receiving EB + PCPA treatment and in two of seven ovariectomized-adrenalectomized females receiving PCPA treatment. The possible role of the hypothalamic-pituitary-adrenal system in the expression of the ejaculatory pattern in male and female rats is discussed.     

Determinants of behavioral rhythmicity during artificial menstrual cycles in rhesus monkeys (Macaca mulatta)

Reproductive success in many mammals depends on synchrony between copulation and ovulation, which is insured by the phenomenon of heat in the female. Certain anthropoid primates including rhesus monkeys do not show heat but may copulate throughout the menstrual cycle, especially when pairs are isolated from conspecifics. In social groups, however, mating mostly occurs around midcycle. We wished to test the hypothesis that copulations are more closely linked to ovulation when males have simultaneous access to several females in different cycle phases. Artificial menstrual cycles were therefore induced by giving hormones to ovariectomized female rhesus monkeys observed in small social groups that each consisted of four females and one male. The cycles of two hormone-treated femlab in each group were either made to synchronize or be offset by 7-day increments so that the estradiol peak of one female occurred 7 days before, and 7 and 14 days after, the estradiol peak of the other. Radioimmunoassay of plasma samples (N = 224) confirmed the timing of the estradiol peaks. Results from eight unique male-female groups (4 males, 8 females, 16 male-female pairs, 718 tests) fully supported the hypothesis. Compared with synchronized cycles, the amplitudes of rhythmic changes in offset cycles were reduced for ejaculations made by males but greatly enhanced for ejaculations received by females. We propose that this socio-hormonal integration of behavior in the group is highly adaptive and enhances the reproductive success of both males and females.     

Female-infant interactions among free-ranging stumptail macaques (Macaca arctoides)

The friendly and aggressive behaviors directed by females other than the mother to the troop's infants were recorded during a six-month long study of stumptail macaques living on an island. A great deal of friendly contacts were directed by the females toward the troop's infants. Juvenile females interacted with infants mainly through social play while adult females directed passive contacts (e.g., touch-hand) to them. While the adult females displayed more care contacts toward male infants the juvenile females preferred the female infants. The social position of the infant's mother in the troop and the attention it received from the males regulated the caring behavior an infant received from the females.     

Variation and consistency in the social behavior of two groups of stumptail macaques (Macaca arctoides)

Social interactions of two five-member groups of stumptail macaques were observed. Behavior of all but one of these animals has been reported in two previous studies. In the third study, high-ranking females maintained their positions in the dominance order when the alpha male with whom they were previously associated was either removed from the group or displaced by a male added to the group. The results of all three studies indicated a tendency for interaction among animals holding adjacent hierarchical ranks. The data suggested that one function of selective grooming was pacifying the grooming partner, and that one function of selective adult play was behavior testing under conditions of moderate arousal.     

Influence of androgen on the development of sexual behavior in the rat. II. Time and dosage of androgen administration during the neonatal period and masculine and feminine copulatory behavior in females

The objective of the present study was to delineate the period of sensitivity to a single androgen exposure during the initial neonatal hours on the development of masculine and feminine copulatory behavior in female rats. Female rats were injected once with either 500, 50, or 5 micrograms testosterone propionate (TP) at either 1 or 24 hr after birth. Following castration in adulthood and TP replacement, the females were tested four times at weekly intervals in prolonged sessions for masculine copulatory behavior. One month following the masculine copulatory tests the females were tested for 3 weeks for feminine copulatory behavior with weekly increasing levels of estradiol benzoate (2.5, 10, and 25 micrograms) and progesterone (200 micrograms). The results demonstrate that a single injection of TP administered at either 1 or 24 hr after birth can significantly increase the capacity of female rats to exhibit ejaculation patterns and that the amount of androgen that is administered is critical in determining the levels of ejaculatory responding. Similarly, the females given high doses (50 and 500 micrograms) of TP at either 1 or 24 hr neonatally were almost completely defeminized. In contrast, however, the females treated with 5 micrograms TP at 1 and 24 hr showed different levels of lordotic performance indicating a greater sensitivity to androgen immediately after birth than at 24 hr in female rats as has been shown in male rats.     

Copulatory behavior in a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico

This paper presents copulatory data gathered on a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico. The study found evidence for seasonal clumping of matings, with the peak in the month of February, and that matings are more common in the afternoon, when measuring diurnal changes. It also found that males require an average of one and a half mounts before ejaculating, and mating among females is distributed unequally, when the measurement is between those females that mated. Furthermore, male dominance rank and male-female affiliation are both positively correlated with mating frequency. Variations between this study and captive studies are minimal. The variances that do occur may be explained by differences in the research settings or the individual differences in the subjects' behavior across studies.     

Steroid hormone influences on the mating behavior of vervet monkeys (Cercopithecus aethiops)

Eight ovariectomized female vervet monkeys (Cercopithecus aethiops) were tested in heterosexual and isosexual pairs, under estradiol and testosterone treatments. Pairs were tested under two different experimental situations in which the male was either restrained or left free. There were only small behavioral changes across the treatments, involving mainly male responses. Erection time, frequency of intromission, ejaculation, and olfactory investigation increased during estradiol treatment whereas during administration of testosterone erection time, the number of approaches, contacts, and olfactory investigations decreased. Female behaviors were relatively independent of hormone treatment showing only the disappearance of negative responses with estradiol and an increase of yawns with testosterone. Female behaviors were performed at a higher level with male partners than with other females, and the frequencies of spontaneous presents varied with the sex of partner. It is suggested that in vervet monkeys both estradiol and testosterone affect female attractivity, estradiol further influences receptivity, whereas proceptivity appears to be less directly involved in sexual interactions and more related to social context.     

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.     

Sustained influence of previous estradiol or testosterone treatments on sexual behaviors of female pigs

Two studies were conducted to determine the consequences of extended treatment with estradiol or testosterone on sexual behavior in postpubertal, female pigs. After ovariectomy, either steroid was administered for 6 weeks at dosages sufficient to maintain serum concentrations similar to those observed in mature male pigs. Behavioral evaluations were initiated 2 months after the last steroid treatment. These treatments reduced receptivity (immobile stance when placed with a mature male) and proceptivity (preference to remain near a mature male) in association with an increase in aggressive behavior. In females treated previously with both estradiol and progesterone, sexual behaviors 2 months later were similar to those of control females. When evaluations were repeated 5 months after extended estradiol treatment had ceased, receptivity and proceptivity had returned to that of control pigs and aggressive behavior had diminished greatly. Interpretation of these changes in behavior is that extended periods of estradiol or testosterone treatment sustain activational influences for a considerable amount of time after treatments cease and progesterone antagonizes estradiol's effect on these behaviors. In a companion study, pubertal and post-pubertal females were similar for receptivity but pubertal females spent less time near a mature male. This difference in proceptivity likely reflects a maturational change associated with sexual development in female pigs. Collectively, these observations in postpubertal, female pigs document that prolonged estrogen treatment will activate aggressive behaviors in association with reduced proceptivity and receptivity. Because these behavioral changes are reversible by 5 months after cessation of treatment, they are not the result of sexual differentiation.     

Rhesus macaque copulation calls: Re-evaluating the “honest signal” hypothesis

Male rhesus macaques sometimes give loud calls while thrusting or dismounting during multi-mount copulations.Hauser (1993) has proposed that these calls (1) impose a cost (increased risk of aggression) on calling males, and (2) increase callers' copulation frequencies, supporting the hypothesis that calls function as honest signals (handicaps) that females use to evaluate male quality during mate choice. This hypothesis was re-examined using data collected at Cayo Santiago, Puerto Rico on 40 focal females and their 56 observed copulatory partners. Although attacks by males against copulating pairs were frequent, they were usually directed only against the female of the pair. Males that called were no more likely than silent males to suffer male escalated attack during or immediately following mount series. Male-female dyads in which the male called during copulation were significantly more likely than non-calling dyads to complete the most copulations observed for any given female. Males that called at least once were significantly more likely than non-calling males to complete at least one copulation with a peri-ovulatory female. A log-linear model revealed that male rank and calling were both associated with likelihood of experiencing at least one peri-ovulatory copulation. However, calling was not associated with reception of demonstrated female mate choice behaviors. Controlling for dominance rank, callers did not experience more female proximity maintenance than non-callers. Nor were callers' hip-grasps refused less frequently than non-callers' hip-grasps. These results cast doubt on the hypothesis that rhesus macaque copulation calls are costly, honest indicators of intrinsic male quality. A contrasting alternative hypothesis, that a male's copulatory calls advertise relative immunity from attacks against his copulatory partners, was not supported either. Thus, the function of rhesus macaque copulatory calls remains unknown. The unusually high rate of copulations amongHauser's (1993) subjects may explain the discrepancy in results, but it is unclear how high copulation rates would increase the cost of copulatory calling to males.     

Sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles

Copulatory behaviors in most rodents are highly sexually dimorphic, even when circulating hormones are equated between the sexes. Prairie voles (Microtus ochrogaster) are monomorphic in their display of some social behaviors, including partner preferences and parenting, but differences between the sexes in their masculine and feminine copulatory behavior potentials have not been studied in detail. Furthermore, the role of neonatal aromatization of testosterone to estradiol on the development of prairie vole sexual behavior potentials or their brain is unknown. To address these issues, prairie vole pups were injected daily for the first week after birth with 0.5 mg of the aromatase inhibitor 1,4,6-androstatriene-3,17-dione (ATD) or oil. Masculine and feminine copulatory behaviors in response to testosterone or estradiol were later examined in both sexes. Males and females showed high mounting and thrusting in response to testosterone, but only males reliably showed ejaculatory behavior. Conversely, males never showed feminine copulatory behaviors in response to estradiol. Sex differences in these behaviors were not affected by neonatal ATD, but ATD-treated females received fewer mounts and thrusts than controls, possibly indicating reduced attractiveness to males. In other groups of subjects, neonatal ATD demasculinized males' tyrosine hydroxylase expression in the anteroventral periventricular preoptic area, and estrogen receptor alpha expression in the medial preoptic area. Thus, although sexual behavior in both sexes of prairie voles is highly masculinized, aromatase during neonatal life is necessary only for females' femininity. Furthermore, copulatory behavior potentials and at least some aspects of brain development in male prairie voles are dissociable by their requirement for neonatal aromatase.     

Sexual preferences during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

Eight groups of rhesus monkeys each consisting of one male and four ovariectomized females were observed while two of the females were treated with hormones to produce artificial menstrual cycles. These were either synchronized or offset by 7-day increments. Sexually preferred females, defined by the numbers of ejaculations per test, received almost twice as many ejaculations as did non-preferred females during all synchronized and offset cycles and during all cycle phases. However, short-term changes in partner preference occurred when the midcycle phase of non-preferred females coincided with the middle or late progesterone phase of preferred females, suggesting a negative effect of progesterone on behavior during the menstrual cycle. There were highly significant differences between preferred and non-preferred partners for almost all of their sexual and social interactions, and preferred partners showed longer proximity and grooming times as well as higher levels of sexual activity. Partner preferences accounted for more of the behavioral variance between pairs than did female dominance, although males sought the proximity of dominant females independently of their partner preferences. Thus, in a setting uncomplicated by male mate competition, sexual preference by male rhesus monkeys is a robust phenomenon depending on complex interactions between dominance, hormonal status, and the individual behavior of female partners.