Progesterone levels in seasonally breeding,free-ranging male <Emphasis Type="Italic">Macaca thibetana</Emphasis>

Progesterone, a “female” hormone, modulates sexual behaviors in male mammals. This modulation is well documented in laboratory animals, but it is as yet unknown whether progesterone is associated with testosterone and/or sexual behaviors in primates living in their natural environments. In this study, we collected a total of 426 fecal samples and approximately 453 h of behavioral data from five male Tibetan macaques (Macaca thibetana) to study relationships between males’ progesterone and testosterone levels and sexual behaviors. Our results showed a negative correlation between fecal testosterone and progesterone levels. Both hormones seasonally varied. For three of the five subjects, we also found that copulatory and sexually motivated behaviors were negatively correlated with fecal progesterone levels. While not significant for the other two males, this study provides insight into the relationship between progesterone and the sexual behaviors of male primates living in a natural environment.     

Sex difference in L-glutamine D-fructose-6-phosphate aminotransferase activity of mouse submandibular gland

L-Glutamine D-fructose-6-phosphate aminotransferase (2-amino-2-deoxy-D-glucose-6-phosphate ketol-isomerase (amino transferring), EC 5.3.1.19) activities in the three main salivary glands of male and female mice were measured. It was found that the activity in the submandibular gland was about 10 times more in females than in males, whereas the activities in the sublingual and parotid glands of males and females were similar. The activity in the submandibular gland of female mice was not affected appreciably by ovariectomy but it decreased to the level in males on injection of testosterone. The activity in males was not affected appreciably by injection of progesterone or 17β-estradiol, but it increased to the level in females after castration. The increased acitivity in castrated male mice was decreased again to the normal level by testosterone injection. Thus, this sex difference is caused by androgen, not by female hormones. On the basis of in vivo experiments using actinomycin D, it was suggested that testosterone produced an “enzyme inhibitor”, which suppressed the enzyme activity in the submandibular glands of androgen-rich animals.     

Endocrine events associated with spawning behavior in the sea lamprey (Petromyzon marinus)

Levels of estradiol, progesterone, and testosterone were determined in plasma of sea lamprey (Petromyzon marinus) undergoing certain behaviors associated with spawning in natural and artificial stream environments. Significantly higher levels of estradiol, progesterone, and testosterone were found in males than in females. In the artificial spawning channel, levels of estradiol were significantly higher in females exhibiting resting and swimming behaviors than in fanning, nest building, and spawning behaviors. No significant correlation was found with either progesterone or testosterone levels and the various reproductive behaviors. The data presented are the first experimental evidence that suggest gonadal steroids may be correlated with certain reproductive behaviors in the sea lamprey.     

Initiation of copulatory behavior in castrated male rats injected with critically adjusted doses of testosterone

In castrated male rats it was possible by means of administration of adequate testosterone propionate doses to induce a state in which the males did not initiate copulatory behavior with a stimulus female displaying no (Lordotic female) or weak (Presenting female) intensity of precopulatory behavior. On the other hand, such males started to copulate and finished copulatory series when a stimulus female exhibiting the complete pattern of precopulatory behavior (Darting female) was offered. The males “prepared” in this manner displayed regularly precopulatory behavior directed toward all the stimulus females. The requisite testosterone doses differed individually. However, in the majority of cases they were in the range of 500–700 μg of testosterone injected once a week.     

The reward value of infant facial cuteness tracks within-subject changes in women's salivary testosterone

“Baby schema” refers to infant characteristics, such as facial cues, that positively influence cuteness perceptions and trigger caregiving and protective behaviors in adults. Current models of hormonal regulation of parenting behaviors address how hormones may modulate protective behaviors and nurturance, but not how hormones may modulate responses to infant cuteness. To explore this issue, we investigated possible relationships between the reward value of infant facial cuteness and within-woman changes in testosterone, estradiol, and progesterone levels. Multilevel modeling of these data showed that infant cuteness was more rewarding when women's salivary testosterone levels were high. Moreover, this within-woman effect of testosterone was independent of the possible effects of estradiol and progesterone and was not simply a consequence of changes in women's cuteness perceptions. These results suggest that testosterone may modulate differential responses to infant facial cuteness, potentially revealing a new route through which testosterone shapes selective allocation of parental resources.     

Sex-specific interactions between aggressive and sexual behavior in the rat: Effects of testosterone and progesterone

The influence of progesterone on sexual and aggressive behaviors during aggressive encounters was investigated in pairs of TP-treated male and female rats. Gonadectomized females, chronically injected with testosterone propionate (TP), showed low but consistent levels of feminine sexual behavior which alternated with aggression. Progesterone when given in addition to TP facilitated receptive and proceptive behaviors, but reduced levels of aggression. In TP-treated males, levels of aggression were the same as observed in TP-treated females. However, TP-treated males seldomly showed sexual behavior during aggressive encounters and additional treatment with progesterone did not affect their behavior. After the aggression tests, animals were tested in a social preference test in which an ovariectomized female cage mate and the opponent from the aggressive encounter served as incentives. Positive correlations between levels of aggression and social preference for an opponent were found in both sexes, although correlations only reached statistical significance when progesterone was given in addition to TP. These correlations were found in both sexes, despite the fact that group analysis revealed pronounced sex differences in social preference: males preferred to spend their time near ovariectomized female cage mates, whereas females divided their time equally among female cage mates and opponents.     

Age- and sex-related variations in vocal-tract morphology and voice acoustics during adolescence

Distinct differences in the human voice emerge during adolescence, with males producing deeper and more resonant voices than females by the end of sexual maturation. Using magnetic resonance images of heads and voice recordings obtained in 532 typically developing adolescents, we investigate what might be the drivers of this change in voice, and the subjective judgment of the voice “maleness” and “femaleness”.We show clear sex differences in the morphology of voice-related structures during adolescence, with males displaying strong associations between age (and puberty) and both vocal-fold and vocal-tract length; this was not the case in female adolescents. At the same time, males (compared with females) display stronger associations between age (and puberty) with both fundamental frequency and formant position. In males, vocal morphology was a mediator in the relationship between bioavailable testosterone and acoustic indices.Subjective judgment of the voice sex could be predicted by the morphological and acoustic parameters in males only: the length of vocal folds and its acoustic counterpart, fundamental frequency, is a larger predictor of subjective “maleness” of a voice than vocal-tract length and formant position.     

Activity pattern, reproductive behaviors and gonadal hormones in the raccoon dog (Nyctereutes procyonoides)

The objectives of this study were to (1) assess year-round behaviors and activity patterns of captive raccoon dogs (Nyctereutes procyonoides) and (2) characterize the species' reproductive endocrinology. Behaviors and activity patterns of 12 (5.7) animals were recorded over a 1-year period. During that time, fecal samples were collected 2-7 times/week from 16 (7.9) individuals (six of these were included in the behavioral study) for the analysis of testosterone, progesterone and estrogen metabolite concentrations. Activity pattern and excretion of gonadal steroids followed a seasonal pattern. Specifically, dogs were cathemeral in summer, and primarily nocturnal in winter. In the males, testosterone concentrations were at baseline from April through September, began to rise in October and reached peak concentrations in February (P<0.05). In the females, elevated estrogen (P<0.05) was observed in March followed by an increase in progestagen concentrations from March through May (P<0.05) in both pregnant and pseudopregnant animals. Gender significantly influenced monthly testosterone/estrogen ratio (P<0.01); values were higher in males than in females throughout the year with overall percentage of overlapping values between males and females being 28%. In summary, this study characterized cirannual fluctuations in behaviors and gonadal steroid metabolites in the raccoon dog maintained in captivity. Because there is no obvious sexual dimorphism, the differences in testosterone/estrogen ratio may be useful for gender differentiation (72% accuracy), especially among individuals living in the wild.     

Presence of mother and unfamiliar female alters levels of testosterone,progesterone, cortisol,adrenocorticotropin, and behavior in maturing Guinea pigs

Although the guinea pig is characterized by precocial physical development and minimal active maternal care, studies suggest the presence of the mother can influence neuroendocrine and behavioral activity of offspring even well beyond weaning. Previous results may have been influenced by the procedure of housing weaned subjects with the mother to within 2 days of testing. The present study examined approximately 40-day-old guinea pigs housed apart from the mother for 0 (not rehoused), 2, or 10 days. Rehousing without the mother led to elevations in plasma testosterone (measured in males), progesterone (measured in females), cortisol, and adrenocorticotropin (ACTH) (both measured in males and females). Offspring housed without the mother for 10 days had the highest progesterone, cortisol, and ACTH levels. Testosterone elevations were observed in 2-day-, but not 10-day-, rehoused animals. Regardless of rehousing condition, 60 min isolation in a novel test cage elevated progesterone, cortisol, and ACTH, and reduced testosterone. These effects were all moderated if the subject was tested with the mother or another female. Sexual behavior toward the mother was observed frequently, but only in males housed apart from her prior to testing. Overall, males and females that had been housed apart from the mother interacted with her as they would an unfamiliar female. Our results corroborate previous findings, suggest the effect of housing apart from the mother on male testosterone is transitory, and indicate that continuous housing with the mother past weaning suppresses circulating progesterone in females and cortisol and ACTH in both sexes.     

Physical provocation of pubertal anabolic androgenic steroid exposed male rats elicits aggression towards females

Human studies suggest that anabolic androgenic steroid (AAS) users are aggressive towards women. This study used a rat model to evaluate whether AAS potentiated aggression towards females and the conditions under which this occurs. Gonadally intact pubertal male rats received one of the following AAS treatments (5 mg/kg s.c. 5 days/week for nine weeks): testosterone (T), stanozolol (S), testosterone + stanozolol (T + S), or vehicle control. Each rat was tested with 3 conspecific stimuli: ovariectomized females (OVX), estrogen only females (E), and estrogen + progesterone females (E + P). The response to physical provocation was tested under three conditions: without physical provocation, provocation of the experimental male, and provocation of the conspecific female. Provocation was a mild tail pinch. Both aggressive and sexual behaviors were measured during each test. In the absence of physical provocation, AAS males were not aggressive towards females. However, provocation significantly increased aggression in males treated with testosterone but only towards OVX females. In the presence of E or E + P females, all animals displayed sex behavior, not aggression. Thus, factors such as the nature of the AAS and the hormonal status of the females are important in determining whether male rats will be aggressive towards females. However, the most salient factor determining aggression towards females is the presence of provocation in combination with high levels of testosterone.     

Plasma steroid hormones in relation to behavioral sex role reversal in the spotted sandpiper, Actitis macularia

Plasma samples collected from spotted sandpipers during the reproductive season were analyzed for testosterone, dihydrotestosterone (DHT), estradiol-17 beta and progesterone. Prior to incubation, plasma testosterone and DHT levels were significantly greater in males than in females. Estradiol levels of paired females were significantly greater than those of paired males. Testosterone and DHT levels of unpaired resident and paired males were significantly greater than those of incubating and brooding males. A 25-fold decline in testosterone occurred in males from the 1- or 2-egg stage to the 3-egg stage, when incubation is initiated. In females, testosterone values were low in unpaired, brooding, and transient birds. Paired females had levels 7-fold greater than unpaired birds. In both sexes, there was a strong correlation between testosterone and DHT levels. Prolactin values were negatively correlated with testosterone and DHT in males. These results indicate that the high level of intrasexual competition for mates among female spotted sandpipers is not based upon a total reversal of the normal male/female levels of androgens and estradiol. Territoriality and intense competition for mates in females may be based upon enhanced receptivity of neural centers to moderate hormone levels. Relative changes in testosterone between unpaired and paired females indicates that this hormone may play a role in mate acquisition and territoriality of these sex role-reversed females.     

Testosterone and reproductive effort in male primates

Considerable evidence suggests that the steroid hormone testosterone mediates major life-history trade-offs in vertebrates, promoting mating effort at the expense of parenting effort or survival. Observations from a range of wild primates support the “Challenge Hypothesis,” which posits that variation in male testosterone is more closely associated with aggressive mating competition than with reproductive physiology. In both seasonally and non-seasonally breeding species, males increase testosterone production primarily when competing for fecund females. In species where males compete to maintain long-term access to females, testosterone increases when males are threatened with losing access to females, rather than during mating periods. And when male status is linked to mating success, and dependent on aggression, high-ranking males normally maintain higher testosterone levels than subordinates, particularly when dominance hierarchies are unstable. Trade-offs between parenting effort and mating effort appear to be weak in most primates, because direct investment in the form of infant transport and provisioning is rare. Instead, infant protection is the primary form of paternal investment in the order. Testosterone does not inhibit this form of investment, which relies on male aggression. Testosterone has a wide range of effects in primates that plausibly function to support male competitive behavior. These include psychological effects related to dominance striving, analgesic effects, and effects on the development and maintenance of the armaments and adornments that males employ in mating competition.     

Serum steroid hormones including 11-ketotestosterone, 11-ketoandrostenedione, and dihydroprogesterone in juvenile and adult bonnethead sharks, Sphyrna tiburo.

Previous studies in the placental viviparous bonnethead shark, Sphyrna tiburo, have correlated 17 beta-estradiol, progesterone, testosterone, and dihydrotestosterone with reproductive events in both males and females. However, several key reproductive events, including implantation, maintenance of pregnancy, and parturition, did not correlate with these four steroid hormones. Therefore, the present study investigated three steroid hormones, 11-ketotestosterone, 11-ketoandrostenedione, and dihydroprogesterone, which have demonstrably important roles in the reproductive cycles of teleosts. It was hypothesized that one or more of these three hormones would correlate with specific reproductive events in S. tiburo. Concurrently, developmental (growth and/or maturation) analyses of these three steroids plus 17 beta-estradiol, progesterone, testosterone, and dihydrotestosterone were investigated in juvenile bonnethead sharks. Serum dihydroprogesterone concentrations were highest in mature females and 11-ketotestosterone concentrations were highest in mature males. In mature females, 11-ketoandrostenedione levels were elevated from the time of mating, through six months of sperm storage and another four months of gestation. At parturition concentrations became significantly lower and remained lower until mating occurred again in another two to three months. Serum 11-ketotestosterone concentrations were the highest at implantation though not significant. In mature males, significantly elevated serum levels of dihydroprogesterone occurred in April and May, near the start of annual testicular development. During growth in males, testosterone and dihydrotestosterone increased progressively and in females, testosterone increased progressively. At maturity in males, significant increases occurred in testosterone and 11-ketotestosterone concentrations while, in females, dihydroprogesterone, 11-ketotestosterone, 17 beta-estradiol, progesterone, testosterone, and dihydrotestosterone concentrations increased. This study shows that although testosterone may be the primary androgen in the bonnethead shark, other derived androgens may have important functions in growth, maturation, and reproduction. J. Exp. Zool. 284:595-603, 1999.     

The development of seasonal variation in gonadal hormones and body weight in the maturing squirrel monkey

Captive-born squirrel monkeys of three different subtypes (Colombian, Bolivian, Peruvian), ranging in age from 1 to 4.5 years for males and 1 to 3.5 years for females, were examined at 3-month intervals throughout the year for seasonal changes in levels of plasma testosterone and progesterone and in body weight. Cyclical activity of testosterone in males began between 2 and 3 years of age but became more defined by the time the animals were 3–4 years old. Peak values occurred in February and May and corresponded to the the time of year in which adults normally mate. Elevations of progesterone occurred initially at approximately 2.5 years of age in February and May, and mainly infernales of the Colombian subtype. However,unlike levels of testosterone in males of this age, which declined in August and November (following the typical breeding season), levels of progesterone in females continued to increase during these months. Seasonal changes in body weight were also found in males but these changes were less evident than, and did not correlate with, hormonal changes.     

Effects of gonadectomy and steroid treatment on renal prostaglandin 9-ketoreductase activity in the rat

The effect of gonadectomy and treatment with sex-steroids on renal prostaglandin 9-ketoreductase activity in 10-11 week old male and female rats was determined. Rats were gonadectomized or subjected to sham operation at 3 weeks of age. During week 7, rats were injected s.c. twice over a 6-day interval with vehicle (peanut oil, 0.5 ml X kg-1) or with depot forms of testosterone (5 mg X kg-1), estradiol (0.02 mg X kg-1), progesterone (5 mg X kg-1), or estradiol and progesterone combined. Renal prostaglandin 9-ketoreductase activity was about 50% higher in female rats than in males. Gonadectomy decreased 9-ketoreductase activity in females, but not in males, and eliminated the gender difference in enzyme activity. Treatment with estradiol elevated 9-ketoreductase activity in males and females, while treatment with testosterone or progesterone was without effect. Progesterone did, however, antagonize the elevation in 9-ketoreductase activity produced by estradiol.     

Some endocrine traits of transgenic rabbits. I. Changes in plasma and milk hormones

The aim of these studies was to compare some endocrine and non-endocrine characteristics of transgenic (carrying mammary gland-specific mWAP-hFVIII gene construct) and non-transgenic rabbits. The concentrations of corticosterone, progesterone, testosterone, estradiol, insulin-like growth factor I (IGF-I) and human factor VIII (hFVIII) in the blood plasma of adult females (9 months of age, third generation transgenic animals), adult males, and young females (1-2 months of age, fourth generation of transgenic animals), as well as in the milk of lactating adult females, were analyzed by using RIA. In addition, litter size and body mass of pups born by transgenic and non-transgenic females from the third generation were compared. Transgenic animals were compared with their non-transgenic siblings (the same genetic and epigenetic background). Transgenesis did not influence plasma hFVIII, but significantly increased corticosterone (in all animals), reduced IGF-I (in adult males and females), testosterone and estradiol, (in young females) and altered progesterone (increase in adult males and decrease in adult females) concentrations in blood plasma. In addition, transgenic females had higher milk concentrations of testosterone, but not progesterone or IGF-I than their non-transgenic sisters. These endocrine changes were not associated with changes in litter size. Transgenic male (but not female) pups have smaller body mass than control animals. These observations demonstrate the influence of transgenesis per se on the animal growth and endocrine system (secretion of reproductive and stress steroid hormones as well as growth factors) over four generations.     

Sexual orientation, proceptivity, and receptivity in the male rat as a function of neonatal hormonal manipulation

The influence of neonatal androgen on the potential to exhibit feminine sexual behavior was investigated. Male rats castrated on Day 0 but not those castrated on Day 4 or later showed hop/darting, ear wiggling, and lordotic behavior in response to treatment with estrogen and progesterone in adulthood at a frequency equal to that of females. Neonatal treatment with testosterone propionate (1 mg/rat for 4 days) abolished the capacity to show these behaviors. In subsequent experiments, involving castration of male rats at 0 or 4 hr after cesarean delivery, the effect of the postnatal surge of testicular secretions on the expression of female sexual behavior was investigated. No differences were seen in the frequency of hop/darting, ear wiggling, and receptivity between males castrated immediately or 4 hr after delivery. In a preference test where the experimental male could choose between an estrous female and a sexually active male, the neonatally castrated males preferred the company of a male when treated with estrogen and progesterone. The implantation of testosterone resulted in a preference for an estrous female. It was concluded that testicular secretions in the newborn male influence adult sexual orientation and suppress the ability to show proceptive and receptive behaviors.     

The effects of progesterone on sexual behavior in male green anole lizards (Anolis carolinensis).

It is well known that androgen-dependent sexual behaviors in male mammals and birds are inhibited by exogenous progesterone (P). However, recent research on male whiptail lizards (Cnemidophorus inornatus) indicates that P can stimulate sexual and copulatory behavior. We report here both antiandrogenic and synandrogenic actions of P on sexual behavior in males of another reptile, the green anole lizard (Anolis carolinensis). Earlier reports on birds and mammals are reviewed and discussed in relation to a possible physiological role of P in influencing sexual behavior in male vertebrates.     

Regulation of Male Sexual Behavior by Progesterone Receptor, Sexual Experience, and Androgen

Recent studies have demonstrated that physiological doses of progesterone may facilitate the androgen-dependent display of male sexual behavior in laboratory rats and three species of lizard. We used mice with a targeted disruption of the progesterone receptor to investigate whether such interactions exist in male mice and whether they may be modified by sexual experience. We found that naive intact male progesterone receptor knockout (PRKO) mice exhibit reduced mount frequencies compared to wild-type (WT) mice. Also unlike WT mice, sexually experienced PRKO males show profound losses in many measures of sexual behavior following castration. In a second experiment, we tested whether male mice heterozygous for a null mutation at the progesterone receptor locus were responsive to testosterone and progesterone treatment. We found that heterozygous males showed a reduced response to testosterone. The data are consistent with experiments indicating that the progesterone receptor is able to facilitate male-typical sex behaviors in other species and suggest novel mechanisms underlying the interaction of androgens and experience.     

Progesterone modulates aggression in sex-role reversed female African black coucals

Testosterone is assumed to be the key hormone related to resource-defence aggression. While this role has been confirmed mostly in the context of reproduction in male vertebrates, the effect of testosterone on the expression of resource-defence aggression in female vertebrates is not so well established. Furthermore, laboratory work suggests that progesterone inhibits aggressive behaviour in females. In this study, we investigated the hormonal changes underlying territorial aggression in free-living female African black coucals, Centropus grillii (Aves; Cuculidae). Females of this sex-role reversed polyandrous bird species should be particularly prone to be affected by testosterone because they aggressively defend territories similar to males of other species. We show, however, that territorial aggression in female black coucals is modulated by progesterone. After aggressive territorial challenges female black coucals expressed lower levels of progesterone than unchallenged territorial females and females without territories, suggesting that progesterone may suppress territorial aggression and is downregulated during aggressive encounters. Indeed, females treated with physiological concentrations of progesterone were less aggressive than females with placebo implants. This is one of the first demonstrations of a corresponding hormone-behaviour interaction under challenged and experimental conditions in free-living females. We anticipate that our observation in a sex-role reversed species may provide a more general mechanism, by which progesterone--in interaction with testosterone--may regulate resource-defence aggression in female vertebrates.