Female-typical sexual behavior of rhesus and defeminization by androgens given prenatally

Adult rhesus monkeys were observed in standardized tests for female-typical sexual and related social responses. In the first experiment reported, 7 castrated males and 5 spayed females were paired with each of 4 intact males on two occasions following intramuscular injection with estradiol benzoate (EB) (6 micrograms/kg X 14 days) and on two other occasions without such treatment. In tests without EB, males and females did not behave differently toward the intact male partners, and all responses were displayed at low frequencies. In tests with EB, females showed reliably higher frequencies than males of approaching, sitting close to, grooming, and soliciting, and they presented to a higher proportion of the male partner's sexual contacts. EB reliably increased the frequency of display of all of these same five responses in females but not in castrated males. The intact male partners displayed reliably fewer approaches, sexual contacts, mounts, intromissions, and ejaculations to castrated males than to spayed females regardless of estrogenization. In a second experiment 10 intact adult pseudohermaphroditic females and 6 intact control females were tested following EB injections with each of the same 4 intact males. Pseudohermaphrodites were experimentally produced by injecting pregnant females with either testosterone propionate (TP) or dihydrotestosterone propionate (DHTP). Pseudohermaphrodites, regardless of type of androgen used in their production, showed reliably fewer solicits than controls to male partners. Moreover, they displayed most of the other responses at lower average frequencies than controls. Frequencies of intromission and ejaculation by intact male partners were reliably lower with pseudohermaphrodites than with control females, but frequencies of approach, sexual contact, and mount were not reliably different. We conclude that in this testing and measurement situation male and female rhesus monkeys differ markedly in the degree of expression of female-typical sexual behaviors, and genotypic males are behaviorally less responsive to estrogens than females. Exposing genotypic females to androgens during fetal life decreases the expression of female-typical, estrogen-influenced responses, and the effect is most pronounced on those soliciting responses that subserve proceptivity.     

Seasonal variation in sexual behavior of all-male rhesus troops

Free roaming groups of Rhesus monkeys show a clear annual cycle in the incidence of sexual behavior. One hypothesis explaining the control of this cycle is that seasonal variables act directly on females, altering their endocrine status. Aroused females then communicate their sexual receptivity to male group members. The sexual behavior of 35 male Rhesus was observed during the non-mating and the mating season. All animals were maintained in large outdoor enclosures. One group of males (N = 7) were housed with females and juveniles as part of a breeding group. A second group of males (N = 8) had visual contact with the members of the breeding group, and a third group of males (N = 20) had no contact with either of these groups. During the non-mating season no sexual behavior was observed. At the onset of the mating season, the males with females displayed evidence of hormonal arousal and became sexually active. The males with visual contact with the breeding group also evidenced hormonal arousal and began engaging in male-to-male sexual activity. The males in the third group showed no sign of sexual arousal. These findings support the hypothesis that seasonal influences act only on females; and demonstrate that females can communicate their endocrine status to males, even without direct physical contact.     

Influence of photoperiod on the secretion of testosterone as a response to sexual stimulus in male goats

Monthly sexual behavior tests were carried out for 1 yr in a group of 19 male goats (10 Verata breed and 9 Malague?a breed) 12 mo of age. Simultaneously with the tests, 5 blood samples were collected, 2 before and 3 after contact with females, to determine the influence of sexual stimulus on the secretion of testosterone. By means of radioimmunoassay, it was determined that both breeds showed a significant increase in testosterone secretion as a result of the sexual stimulus during increasing daylength (Verata: P<0.01; Malague?a: P<0.05), when testosterone secretion levels prior to the stimulus were the lowest of the year. Moreover, the level of testosterone secretion was higher in the Verata than in the Malague?a breed (P<0.01). A significant though low correlation (P<0.05) between the rise of testosterone levels as a response to sexual stimulus and the degree of sexual behavior in the males was observed in the Verata breed. However, there was no correlation between these factors in Malague?a male goats.     

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park,Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission–fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60–90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male–male SGR networks were wider than were either male–female or female–female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.     

Testosterone propionate treatment of an XY gonadal dysgenetic chacma baboon

Behavioral studies of an XY gonadal dysgenetic chacma baboon prior to and during testosterone propionate treatment were carried out. The orchidectomized dysgenetic individual, two intact males, a castrate male, and two ovariectomized females were pair-tested with a group of eight ovariectomized stimulus females prior to and during their treatment with estradiol benzoate. Three test series were carried out. One series occurred prior to any treatment of the agonadal focal subject animals. During this series it was only the intact males who showed behavior change during their testing with the estrogen treated females. A second test series occurred after a month of daily testosterone propionate injections (1 mg/kg/day) had been given to the four agonadal subjects. During this test series the castrate male ejaculated once with one of the estrogen-treated females. All of the treated subjects showed increases in their frequency of yawning. Upon completion of this test series the androgen dosage was increased (2 mg/kg/day) and 2 weeks later a third test series was carried out. During this series the castrate male ejaculated with five of his eight estrogen-treated partners. The yawning of all the treated subjects continued. As had been the case in the second series the XY gonadal dysgenetic individual continued to behave as did the ovariectomized females. None of these animals showed any increase in any measure of male sexual behavior. This study establishes the fact that a genetic male primate deprived of in utero exposure to testicular hormones will go on to develop as a normal genetic female and will fail to exhibit increased levels of male sexual behavior during androgen treatment.     

Heterosexual interactions in laboratory-housed stumptail macaques (Macaca arctoides): observations during the menstrual cycle and after ovariectomy.

Heterosexual interactions of pairs of stumptail macaques (Macaca arctoides) were studied in relation to the female menstrual cycle and after ovariectomy. Five intact male and 10 tubal-ligated female macaques were observed in laboratory pair tests of 20-mins duration, and data were obtained on various male and female behaviors. Each male was tested with the same two females during four 40-day observation periods. Males were tested daily and females were tested every other day. After two 40-day testing periods, one female partner of each male was ovariectomized and the other was sham-operated. Blood was collected regularly from the females during the course of observation and serum levels of estradiol and progesterone were determined by radioimmunoassay. The midcycle peak of estradiol was observed to occur approximately 18 days prior to menses. A distinct secondary peak in estradiol was observed to occur during the luteal phase of all cycles examined. Of 28 different male and female behaviors studied only female presentation to male sexual contact showed a significant midcycle peak related to the endogenous estradiol surge. After ovariectomy a significant decrease in the frequency of several male copulatory behaviors was observed, but most males continued to copulate regularly with their spayed partners throughout the period of this study. Thus, the pattern of copulatory behavior observed in stumptail macaques over the cycle of the female partner and subsequent to ovariectomy differs from that observed in other macaque species studied in the laboratory. It is concluded that cyclical fluctuations in the level of ovarian hormones are not significantly related to measures of sexual interactions in laboratory tests of this species, although the maintenance of copulation and associated behaviors at high levels depends to some degree upon the ovary.     

Estradiol benzoate treatment of an XY gonadal dysgenetic chacma baboon

Behavioral studies of an XY gonadal dysgenetic chacma baboon under estradiol benzoate treatment were carried out. The dysgenetic individual and two ovariectomized conspecific control females were given a total of three testing series. The dysgenetic individual showed progressive success in her sexual interactions with her male partners and during her third testing series she was copulated with to ejaculation by five of the eight male partners. This study provides the first supportive evidence from a nonhuman primate for the predicted development of female sexual behavior in a genetic male deprived of testes prior to the sensitive period for sexual differentiation.     

Sexual deprivation and its influence on testosterone levels and sexual behavior of old and middle-aged rhesus males

After approximately 6 mo without access to a receptive female, eight old (19 to 25 yr) and eight middle-aged (9 to 15 yr) males were given nine daily 10-min tests of sexual behavior with receptive females. Three ovariectomized, estrogen-primed females served as partners. Blood samples were taken from the males at 0900 and 2100 h on 2 consecutive days before and after the series of nine behavioral tests. Serum levels of testosterone (T) were measured by means of radioimmunoassay. There were no significant differences between serum T levels after 6 mo of sexual deprivation and after the nine tests of sexual behavior, nor did serum T levels differ between middle-aged and old males. Serum T levels were significantly higher in the 2100-h samples than in the 0900-h samples for both groups. The nocturnal increases in serum T, both absolute amounts and percentages of increase, did not differ between middle-aged and old males. Repeated daily testing had little effect on the major components of male sexual behavior. Middle-aged males outperformed old males; middle-aged males had higher rates of contracting the female, mounting and intromitting. They ejaculated earlier and had a greater percentage of tests with ejaculations than did old males.     

Castration, sex steroids, and heterosexual behavior in adult male laboratory-housed stumptailed macaques (Macaca arctoides)

The sociosexual behaviors of six stable male-female pairs of stumptailed monkeys were studied in half-hour pair tests. Their performance before and after castration of the males was compared. The effects of replacement therapy with sex steroids on male-female interaction were studied. Also the effects of new females as sexual partners were investigated. Castration caused a significant decrease in sexual behavior. Individual males could display ejaculatory behavior up to about 1 year postcastration. Dihydrotestosterone propionate (75 mg/week/male) alone or in combination with estradiol benzoate (0.9 or 3 mg/week/male) was not effective in restoring sexual behavior to precastration levels in the three castrated males tested. Replacement therapy with testosterone propionate (75 or 10 mg/week/male) was effective in restoring copulatory behavior in half of the castrated males. In some males the introduction of a new female caused an increase in sexual activity, usually when sexual activity with their familiar partner was low. This occurred both in the castration condition and in the steroid treatment period, suggesting, that low activity was caused by low "motivation" and not by the inability to perform.     

Female assessment of male functional fertility during mate choice in a promiscuous fish

Sexual selection should favour females that can assess the functional fertility of available sexual partners and avoid mating with recently mated, sperm‐depleted males. Our current understanding of the sensory mechanism(s) underlying female assessment of males based on their functional fertility and avoidance of sperm‐depleted males is incomplete. Female Trinidadian guppies (Poecilia reticulata) are known to avoid mating with males that they had previously observed mating with other females. Here, we investigated experimentally the proximate sensory cues that they use to distinguish between paired size‐ and colour‐matched mated and unmated males in the absence of visual public information on their prior mating histories. When only water‐borne chemical cues from the males were available, females avoided the previously mated male and preferred the unmated one, but they chose randomly when only male visual cues (and no chemical cues) were available. They also preferred unmated over mated males when freely swimming with them in a more sensorially complex environment with multiple male cues (i.e., visual, chemical and mechanical cues) concurrently available. Females exhibited no preference for either stimulus males when both were unmated, irrespectively of the sensory environment. These novel results suggest that, in the absence of prior visual public information on the recent mating histories of males, female guppies use olfactory cues putatively emitted by mated males to avoid mating with them. The source and nature of the implicated olfactory cues and the fitness benefits gained by female guppies in sexually preferring males that have not recently mated remain unknown and warrant further research.     

Sexual Selection in the Water Spider: Female Choice and Male–Male Competition

The water spider Argyroneta aquatica is the only spider spending its whole life under water, and one of the few spider species in which males are larger than females. Previous studies indicated that males can cannibalize females, which is uncommon among spiders. Here we aimed to further test for a potential influence of sexual selection on male body size. We examined the importance of female choice by testing whether females prefer the larger of two simultaneously presented males as mating partners. Further, we examined the influence of male–male competition by comparing the fighting behaviour between large and small males when alone or when together with a female, and we determined the outcome of fights. We found that females approach and choose large males as mating partners, despite the risk of male cannibalism. Additionally, males intensively compete for females, and large males clearly win against smaller ones. Hence sexual selection seems to be important for the evolution of the peculiar sexual size dimorphism of water spiders, as large size is beneficial for males in both the intra‐ and intersexual context. Previous studies have suggested an important role of natural selection in the sex‐specific body size of water spiders, but natural and sexual selection mechanisms apparently work in the same direction, favouring large male size.     

The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni

Color and pigmentation patterns of animals are often targets of sexual selection because of their role in communication. Although conspicuous male traits are typically implicated with intersexual selection, there are examples where sex-specific displays play a role in an intrasexual context, e.g. when they serve as signals for aggression level and/or status. Here, we focus on the function of a conspicuous male ornament in the most species-rich tribe of cichlid fishes, the haplochromines. A characteristic feature of these ca. 1500 species are so-called egg-spots in form of ovoid markings on the anal fins of males, which are made up of carotenoid based pigment cells. It has long been assumed that these yellow, orange or reddish egg-spots play an important role in the courtship and spawning behavior of these maternal mouth-brooding fishes by mimicking the eggs of a conspecific female. The exact function of egg-spots remains unknown, however, and there are several hypotheses about their mode of action. To uncover the function of this cichlid-specific male ornament, we used female mate choice experiments and a male aggression test in the haplochromine species Astatotilapia burtoni. We manipulated the number and arrangement of egg-spots on the anal fins of males, or removed them entirely, and tested (1) female preference with visual contact only using egg-traps, (2) female preference with free contact using paternity testing with microsatellites and (3) male aggression. We found that females did not prefer males with many egg-spots over males with fewer egg-spots and that females tended to prefer males without egg-spots over males with egg-spots. Importantly, males without egg-spots sired clutches with the same fertilization rate as males with egg-spots. In male aggression trials, however, males with fewer egg-spots received significantly more attacks, suggesting that egg-spots are an important signal in intrasexual communication.     

The effects of sexual experience and female receptivity on courtship-rape decisions in male guppies, Poecilia reticulata (Pisces: Poeciliidae)

This paper examines the effects of prior sexual experience and of female receptivity on the probability that male guppies will court females with high or low intensity displays or attempt rape. There were no differences in behaviour between males with a history of high copulation success and those with low copulation success. Males with receptive females exhibited higher levels of high intensity displays and fewer rape attempts than males with unreceptive females, regardless of prior experience. The results are discussed in terms of sexual selection and the selective advantage of behavioural plasticity in which different sexual behaviour patterns are chosen with respect to the probability of a successful mating at a given time.     

Determinants of Affiliative Interactions between Adult Males and Lactating Females in Pigtail Macaques (Macaca nemestrina nemestrina)

In some species of Cercopithecine primates, unrelated adult males and females maintain affiliative relationships ('friendships') that are apparently unrelated to mating or parental care. This study investigated the occurrence of friendships in a captive group of pigtail macaques, and some of their possible determinants. Study subjects were six adult males and 15 adult females with their newborn infants. Females were focally observed for 2 h every week during the first 12 wk of lactation. With the exception of the fourth-ranking male, adult males showed little interest in initiating affiliative interactions with lactating females and their infants. Most episodes of contact and grooming were initiated by high-ranking females and directed to the alpha male. Because female grooming was not generally reciprocated by the alpha male, it is likely that females benefited from associating with him in terms of agonistic support or protection. Genetic data on paternity determination indicated that the fourth-ranking male, who displayed high levels of affiliation towards mother-infant dyads, sired most of the infants born in the group in the year prior to this study. Thus, whereas females may be interested in associating with males to obtain their support, some males may affiliate with females as a consequence of their previous mating relationships with them or to increase the chances of future mating success. Taken together, however, the findings of this study provide little evidence that adult males and lactating females maintain strong reciprocal bonds that may qualify as friendships.     

Hormonal regulation of male reproductive behavior in the lizard Anolis sagrei: a test of the aromatization hypothesis

This study examined the hypothesis that aromatization of testosterone (T) to estradiol (E) is required to activate reproductive behavior in castrated male lizards (Anolis sagrei). Adult, reproductively active males were assigned to an intact control group or to one of four treatment groups. Treatment males were castrated and 1 week later three of the four castrated groups were implanted with subcutaneous pellets containing either 0.05 mg of E, 0.5 mg of T, or 0.5 mg of dihydrotestosterone (DHT). Two weeks after pellet implantation, males were tested with stimulus males, and 2 days later were tested with stimulus females. Behavioral tests were of 15-min duration and were videotaped. Significantly fewer E-treated castrates erected a crest in tests with stimulus males than did intact males. In tests with stimulus females, significantly fewer E-treated castrates displayed, neck-gripped, and intromitted than did intact males. Estradiol-treated castrates also showed significantly less display behavior than did intact males. However, aggressive and sexual behavior of DHT-treated castrates was not significantly different from that of intact males. The same was true for T-treated castrates with the exception that display behavior in tests with stimulus females was reduced compared to that of intact males. The results suggest that aromatization of T to E is not required for induction of androgen-dependent reproductive behavior in this lizard.     

Relation between the dominance rank of female rhesus monkeys and their access to males

Systematic observations were made on 12 measures of the sexual, aggressive, and social interactions of 24 male–female pairs of rhesus monkeys in six social groups, each consisting of one male and four ovariectomized females tested in a large room. Each female in a group was treated in turn first with estradiol alone and then with estradiol and progesterone in combination. When hormone-treated, the female was also observed during pair tests with the male in the same large observation room (four males, eight females, 240 group tests, 240 pair tests). The dominance ranks of females during group tests were determined post hoc by means of the dominance index [Zumpe & Michael, American Journal of Primatology 10:291–300, 1986]. In all six groups, the most dominant female virtually monopolized the male, and the subordinate females' interactions with the male, assessed during pair tests, were almost completely suppressed during group tests. This “dominant female effect” was a robust phenomenon that depended solely on female dominance rank. It was independent of the identity and hormonal status of females and of the social preferences of males as expressed in pair tests. These findings demonstrate the existence of female mate competition in an Old World primate.     

Does neonatal gonadectomy affect the sexual differentiation of quail?

This experiment was designed to determine the contribution, if any, of posthatching gonadal hormones to sexual differentiation of behavior in Japanese quail (Coturnix coturnix japonica). Males and females were gonadectomized or sham-operated (controls) prior to age 7 days posthatching. At age 4-9 weeks controls were gonadectomized. All birds were then given 2 weeks of testosterone propionate injections and tested for sexual behavior with female partners. Neonatally gonadectomized females exhibited more male-typical copulatory behavior than control females, but this effect was not statistically significant. Neonatal gonadectomy had no effect on males, and neonatally gonadectomized males exhibited significantly more male-typical copulatory behavior than neonatally gonadectomized females. Although the process of sexual differentiation may extend to a minor degree into the posthatching period in females, nonetheless it is largely complete at hatching in this species.     

Male mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioural and molecular genetics data

Sand lizard Lacerta agilis females characteristically mate with several males which, in staged mating experiments, results in multiple paternity of the offspring. In order to investigate multiple paternity in a natural population and interpret male reproductive behaviours in terms of sired young, we sampled the blood of females, potential fathers and hatchlings, and determined paternity using multilocus DNA fingerprinting as well as the variation at a single locus detected by the probe (TC) _n . The paternity analyses were preceded by a laboratory experiment in which we established that the parental alleles identified by the single locus probe were inherited in a Mendelian way. Our molecular data demonstrated that 12 out of 13 males (92%) that sired offspring were correctly identified from the 56 sexually mature males in the population. Also smaller males were accepted as sexual partners by the females, but sired fewer young in competition with larger males and were less able to maintain prolonged post-copulatory mate guarding. This may result in that some sexually successful males are only observed inside a female's home range, but never in pair-association with the female.     

Masculinized sexual partner preference in female zebra finches with sex-reversed gonads

Previous research in the zebra finch, a socially monogamous pair-bonding species, suggests that the preference for opposite-sex partners may arise in part through the organizing actions of sex steroids. To further investigate this process, zebra finch eggs were injected with 20 microg fadrozole, a potent estrogen synthesis inhibitor, or with the saline vehicle on embryonic day 5. As adults they were given two-choice sexual partner preference tests followed by group aviary tests. Fadrozole females had masculinized beak color and had testes or ovotestes instead of ovaries. Males were not affected by fadrozole; they did not differ from controls on any measure. In contrast, sexual partner preference was substantially masculinized in fadrozole females in the group aviary tests. Untreated males given a choice between fadrozole and untreated females preferred the untreated females, but this was equally the case when they were given a choice between saline-treated and untreated females. These results suggest that males do not specifically avoid females with testes and that male avoidance is unlikely to explain why fadrozole-treated females pair with other females. The present data add to the evidence that actions of gonadal steroids during development contribute to adult sex differences in partner preference in this pair-bonding species. Furthermore, because fadrozole-treated females do not produce audible song, the mechanisms regulating partner preference and song system development are dissociated.     

The contrasting role of male relatedness in different mechanisms of sexual selection in red junglefowl

In structured populations, competition for reproductive opportunities should be relaxed among related males. The few tests of this prediction often neglect the fact that sexual selection acts through multiple mechanisms, both before and after mating. We performed experiments to study the role of within‐group male relatedness across pre‐ and postcopulatory mechanisms of sexual selection in social groups of red junglefowl, Gallus gallus, in which two related males and one unrelated male competed over females unrelated to all the males. We confirm theoretical expectations that, after controlling for male social status, competition over mating was reduced among related males. However, this effect was contrasted by other sexual selection mechanisms. First, females biased male mating in favor of the unrelated male, and might also favor his inseminations after mating. Second, males invested more—rather than fewer—sperm in postcopulatory competition with relatives. A number of factors may contribute to explain this counterintuitive pattern of sperm allocation, including trade‐offs between male investment in pre‐ versus postcopulatory competition, differences in the relative relatedness of pre‐ versus postcopulatory competitors, and female bias in sperm utilization in response to male relatedness. Collectively, these results reveal that within‐group male relatedness may have contrasting effects in different mechanisms of sexual selection.