Exposure to infant scent lowers serum testosterone in father common marmosets (Callithrix jacchus)

Common marmoset (Callithrix jacchus) males are bi-parental non-human primates that show extensive paternal behaviour. Fathers are in direct sensory contact with their infants during the natal period. We found that fathers exposed to isolated scents of their infant displayed a significant drop in serum testosterone levels within 20min after exposure, whereas parentally naive males did not. These data suggest that infant's scent may have a causal role in regulating paternal testosterone in their fathers. This is the first study to demonstrate that olfactory cues have an acute effect on paternal care.     

Differential endocrine responses to infant odors in common marmoset (Callithrix jacchus) fathers

Olfactory cues can exert priming effects on many mammalian species. Paternally experienced marmosets, Callithrix jacchus, exposed to direct isolated olfactory contact with their own infant's scent show rapid decreases in testosterone levels within 20 min, whereas paternally inexperienced males do not. The following study tests whether there is a differential steroid response to exposure of infant scent from dependent infants (own and novel) and independent infants (own and novel). We examined the serum levels of estradiol, estrone, testosterone, dihydrotestosterone (DHT), and combined estrogens and androgens in eight male marmosets 20 min after exposure to isolated infant scent. Testosterone and androgen levels combined were significantly lower with exposure to own infant scent than a novel infant scent when the infants were at a dependent age but not at an independent age. Estrogen levels elevated significantly in response to own infant scent when the infants were at a dependent age but not at an independent age. These results suggest that marmoset fathers are more responsive to priming cues from related infants and hormonal responses from fathers are greatest when the infant is at a dependent age.     

Reproductive Strategies in Lemur catta: Balance Among Sending,Receiving, and Countermarking Scent Signals

Our goal is to go deep into behavioral olfactory strategies possibly used by ring-tailed lemurs in reproductive competition and to shed some light on the function of female scent marks deposited outside the breeding season. We followed 16 captive adults at the Pistoia Zoo (Tuscany, Italy) for > 1,500 h from May 1997 to March 1999. Male direct and indirect olfactory investigation on females showed complementary distributions, the former peaking during the breeding and the latter during the birth season. Males are thus able to monitor female reproductive conditions throughout the whole year. During the birth season there was an increase of female genital marking. The olfactory advertisement probably guarantees that the extremely brief estrus does not remain unnoticed and allows male intrasexual competition a long period to operate. Male indirect olfactory monitoring and countermarking on female signals peaked during the birth season, which suggests that male intrasexual competition is achieved both by getting female chemical messages and by concealing them from other males. Female countermarking on other female genital marks peaked during the breeding season. High-ranking females had higher frequencies of countermarking than those of low-ranking females, which suggests that the advantage of obliterating scent signals of other females is greater than the disadvantage of revealing one's own reproductive condition.     

Adaptive attunement to the sex of individuals at a competition: the ratio of opposite- to same-sex individuals correlates with changes in competitors' testosterone levels

Evolutionary theories (e.g., the challenge hypothesis) suggest that testosterone plays an important role in intrasexual competition. In addition, those theories suggest that testosterone responses during competition should depend upon the presence of potential, immediate mating opportunities associated with the competition. The current research tested the hypothesis that the sex composition of individuals at a competition (ratio of opposite-sex, potential mates to same-sex individuals) would influence changes in competitors' testosterone levels. Consistent with our hypotheses, higher ratios of opposite- to same-sex individuals at an ultimate frisbee tournament were associated with greater increases in salivary testosterone among competitors. The relationship between sex ratio and increased salivary testosterone was observed for both male and female competitors and occurred regardless of whether competitors won or lost. Findings are consistent with the hypothesis that testosterone responses during competition are influenced by cues of potential, immediate mating opportunities.     

Body odor attractiveness as a cue of impending ovulation in women: evidence from a study using hormone-confirmed ovulation

Scent communication plays a central role in the mating behavior of many nonhuman mammals but has often been overlooked in the study of human mating. However, a growing body of evidence suggests that men may perceive women's high-fertility body scents (collected near ovulation) as more attractive than their low-fertility body scents. The present study provides a methodologically rigorous replication of this finding, while also examining several novel questions. Women collected samples of their natural body scent twice--once on a low-fertility day and once on a high-fertility day of the ovulatory cycle. Tests of luteinizing hormone confirmed that women experienced ovulation within two days of their high-fertility session. Men smelled each woman's high- and low-fertility scent samples and completed discrimination and preference tasks. At above-chance levels, men accurately discriminated between women's high- and low-fertility scent samples (61%) and chose women's high-fertility scent samples as more attractive than their low-fertility scent samples (56%). Men also rated each scent sample on sexiness, pleasantness, and intensity, and estimated the physical attractiveness of the woman who had provided the sample. Multilevel modeling revealed that, when high- and low-fertility scent samples were easier to discriminate from each other, high-fertility scent samples received even more favorable ratings compared with low-fertility scent samples. This study builds on a growing body of evidence indicating that men are attracted to cues of impending ovulation in women and raises the intriguing question of whether women's cycling hormones influence men's attraction and sexual approach behavior.     

Intrasexual competition and eating restriction in heterosexual and homosexual individuals

Restrictive eating attitudes and behaviors have been hypothesized to be related to processes of intrasexual competition. According to this perspective, within-sex competition for status serves the adaptive purpose of attracting mates. As such, status competition salience may lead to concerns of mating desirability. For heterosexual women and gay men, such concerns revolve around appearing youthful and, thus, thinner. Following this logic, we examined how exposure to high-status and competitive (but not thin or highly attractive) same-sex individuals would influence body image and eating attitudes in heterosexual and in gay/lesbian individuals. Results indicated that for heterosexuals, intrasexual competition cues led to greater body image dissatisfaction and more restrictive eating attitudes for women, but not for men. In contrast, for homosexual individuals, intrasexual competition cues led to worse body image and eating attitudes for gay men, but not for lesbian women. These findings support the idea that the ultimate explanation for eating disorders is related to intrasexual competition.     

Exposure to perceived male rivals raises men's testosterone on fertile relative to nonfertile days of their partner's ovulatory cycle

The challenge hypothesis posits that male testosterone levels increase in the presence of fertile females to facilitate mating and increase further in the presence of male rivals to facilitate male–male competition. This hypothesis has been supported in a number of nonhuman animal species. We conducted an experiment to test the challenge hypothesis in men. Thirty-four men were randomly assigned to view high-competitive or low-competitive male rivals at high and low fertility within their partner's ovulatory cycle (confirmed by luteinizing hormone tests). Testosterone was measured upon arrival to the lab and before and after the manipulation. Based on the challenge hypothesis, we predicted that a) men's baseline testosterone would be higher at high relative to low fertility within their partner's cycle, and b) men's testosterone would be higher in response to high-competitive rivals, but not in response to low-competitive rivals, at high relative to low fertility within their partner's cycle. Contrary to the first prediction, men's baseline testosterone levels did not differ across high and low fertility. However, consistent with the second prediction, men exposed to high-competitive rivals showed significantly higher post-test testosterone levels at high relative to low fertility, controlling for pre-test testosterone levels. Men exposed to low-competitive rivals showed no such pattern (though the fertility by competition condition interaction fell short of statistical significance). This preliminary support for the challenge hypothesis in men builds on a growing empirical literature suggesting that men possess mating adaptations sensitive to fertility cues emitted by their female partners.     

Menstrual cycle variation in women's preferences for the scent of symmetrical men.

Evidence suggests that female sexual preferences change across the menstrual cycle. Women''s extra-pair copulations tend to occur in their most fertile period, whereas their intra-pair copulations tend to be more evenly spread out across the cycle. This pattern is consistent with women preferentially seeking men who evidence phenotypic markers of genetic benefits just before and during ovulation. This study examined whether women''s olfactory preferences for men''s scent would tend to favour the scent of more symmetrical men, most notably during the women''s fertile period. College women sniffed and rated the attractiveness of the scent of 41 T-shirts worn over a period of two nights by different men. Results indicated that normally cycling (non-pill using) women near the peak fertility of their cycle tended to prefer the scent of shirts worn by symmetrical men. Normally ovulating women at low fertility within their cycle, and women using a contraceptive pill, showed no significant preference for either symmetrical or asymmetrical men''s scent. A separate analysis revealed that, within the set of normally cycling women, individual women''s preference for symmetry correlated with their probability of conception, given the actuarial value associated with the day of the cycle they reported at the time they smelled the shirts. Potential sexual selection processes and proximate mechanisms accounting for these findings are discussed.     

Factors influencing aggression toward females by male rats exposed to anabolic androgenic steroids during puberty

Previous results showed that male rats pubertally exposed to anabolic androgenic steroids (AAS) displayed aggression towards females in response to physical provocation. This experiment examined two factors that may modulate AAS-induced behavior towards females: olfactory cues and frustration. Gonadally intact males began one of three AAS treatments at puberty (D40): testosterone propionate (T), stanozolol (S), T+S, or vehicle control. To test for the relevance of olfactory cues in the elicitation of behavior toward females, a hidden neighbor paradigm was used. The proximal stimulus was an ovariectomized (OVX) female, estrogen plus progesterone (E+P) female, or an E+P female with tape-obstructed vagina (OBS). Distal olfactory cues from a hidden neighbor were delivered from a separate cage connected to the testing arena. The vaginally obstructed, sexually receptive female (OBS) was used to determine the effects of frustration on behavior by AAS males. Both sexual and aggressive behaviors were measured. The presence of distal olfactory cues had no effect on either sexual or aggressive behavior. In the presence of E+P and OBS females, all males displayed sex behaviors, not aggression. However, AAS males displayed significantly more aggression towards proximal OVX females than controls. AAS males mounted OBS females significantly more than controls, indicating a persistence of once rewarded behavior. These results suggest (1) proximal cues of the conspecific female are more salient than distal olfactory cues in determining behavior and (2) AAS males display frustration-induced persistence in response to vaginally obstructed receptive females.     

Hormonal contraceptive use lowers female intrasexual competition in pair-bonded women

The purpose of this study was to test the influence of hormonal contraceptive use on levels of female intrasexual competition. Twenty-eight women completed a scale for intrasexual competition on three occasions: when using hormonal contraceptives and when regularly cycling at a fertile and a non-fertile cycle stage. When using hormonal contraception, pair-bonded, but not single women, reported significantly lower levels of intrasexual competition than when regularly cycling at either fertile or non-fertile cycle stages. This effect remained significant when controlling for age, length of relationship and relationship satisfaction. Neither pair-bonded nor single women reported shifts in intrasexual competition across the menstrual cycle when fertile as compared to non-fertile. This study benefited from a within-subjects design and a more rigorous assessment of fertility status (transvaginal ultrasonography) than which is typical in the field. Results are discussed in consideration of the evolutionary literature on the stability of romantic relationships and fitness advantages associated with intrasexual competition.     

Women's estradiol predicts preference for facial cues of men's testosterone

A growing body of research has shown that women express stronger attraction to more masculine traits when they are tested near ovulation than when tested during other times in the menstrual cycle. Although these effects have been interpreted as increased preferences for markers of elevated testosterone during times in the cycle when conception is most likely, no previous studies have directly demonstrated that women express stronger attraction to higher testosterone men at different times in the cycle. In addition, little research has addressed which hormonal or other physiological mechanisms may regulate temporal shifts in women's attractiveness judgments. In this research, we demonstrate that women with higher estradiol concentrations exhibit stronger preferences for the faces of men with higher testosterone concentrations, and that women's testosterone preference and estradiol curves track one another across days of the cycle. The findings are the first direct demonstration in humans that hormone concentrations in one sex are associated with attraction to cues of hormonal status in the opposite sex. The results support a functional role for estradiol in calibrating women's mating psychology to indices of their current fertility, analogous to similar processes that have been documented in nonhuman species. A strong correlation between estradiol and testosterone preference specifically during the luteal phase further suggests that women's mate preferences may track their fertility between different cycles in addition to being calibrated to the timing of ovulation within individual cycles.     

Women Ornament Themselves for Intrasexual Competition near Ovulation,but for Intersexual Attraction in Luteal Phase

The present study examined women''s attentional bias toward ornamental objects in relation to their menstrual phase as well as to motivations of intersexual courtship or intrasexual competition. In Experiment 1, 33 healthy heterosexual women were tested in a bias-assessment visual cuing task twice: once on a high-fertility day (during the ovulatory phase) and once on a low-fertility day (during the luteal phase). They paid greater attention to pictures of ornamental objects than to pictures of non-ornamental objects near ovulation, but not during the luteal phase, suggesting an ornamental bias during the high-fertility phase. In Experiment 2, before the visual cuing task, 40 participants viewed 10 same-sex or opposite-sex facial photographs with either high or low attractiveness as priming tasks to activate the intrasexual competition or intersexual courtship motives. Results showed that women''s ornamental bias was dependent on the interaction of menstrual phase and mating motive. Specifically, the ornamental bias was observed on the high-fertility day when the subjects were primed with high-attractive same-sex images (intrasexual competition) and was observed on the low-fertility day when they were primed with high-attractive opposite-sex photographs (intersexual courtship). In conclusion, the present findings confirm the hypothesis that, during the high-fertility phase, women have an attentional bias toward ornamental objects and further support the hypothesis that the ornamental bias is driven by intrasexual competition motivation near ovulation, but driven by intersexual courtship motivation during the luteal phase.     

Testosterone and intrasexual competition in men: is there any relation with digit ratio (2D:4D)?

Digit ratio 2D:4D is a sexually dimorphic characteristic and it is believed that this difference is related to high levels of prenatal testosterone and circulating testosterone in men. High levels of testosterone are also associated with traits related to competitiveness. Therefore, this study aimed to examine the relation between intrasexual competition and 2D:4D in men. One hundred thirteen college men answered a questionnaire to measure their scores of intrasexual competition and donated a saliva sample to measure their testosterone levels; finally, the finger length from both hands was measured. It was found a positive correlation between testosterone levels and intrasexual competition scores, and a negative correlation between testosterone levels and left 2D:4D. Finally, we did not find a significant association between digit ratios 2D:4D and intrasexual competition scores. Our study shows that men with higher testosterone levels also have higher intrasexual competition scores and lower values of left digit ratio 2D:4D. Further studies will have to take into account fluctuations in testosterone over the time to observe if the relation between competitiveness scores and digit ratios 2D:4D becomes significant.     

Individual olfactory signatures in common marmosets (Callithrix jacchus)

Individual discrimination is likely a prerequisite for most primate social interactions. Olfactory cues are one set of stimuli used by primates to discriminate between individuals. Despite the importance of these olfactory signatures, there is little published research assessing the existence or function of individually unique odors among primates. This review systematically assesses behavioral and biochemical aspects of individual odors in a New World primate, the common marmoset (Callithrix jacchus). There are three objectives to this review: First, behavioral evidence for odors unique to the individual is evaluated in the context of results demonstrating that marmosets are able to discriminate between the scents from a familiar and a novel individual conspecific in behavioral bioassays under a variety of conditions. Second, biochemical evidence for individual scent signatures is debated with reference to studies examining qualitative and quantitative differences between the chemical compositions of scent-mark pools from adult females. A combined gas chromatography (GC) and mass spectrometry (MS) analysis demonstrated that each female had a unique ratio of highly volatile chemicals in the scent mark that could affect individual discrimination. Finally, the possible adaptive significance of individual odors in marmosets is debated. Individual odors may play a key role in regulating both female intrasexual competition and intersexual communication by providing a basis for the assessment of individual quality.     

Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus

Male mammals show rapid behavioral and hormonal responses to signals from sexually receptive females. However, rapid endocrine responses to female signals have not been observed in a nonhuman primate. Here, we tested the behavioral and hormonal response of male common marmosets (Callithrix jacchus) to isolated scent secretions from ovulatory females or to vehicle control scent. Fifteen males were tested in their home cage for behavioral and hormonal responses. These males showed increased investigative and arousal behaviors to the ovulatory scent compared to the vehicle scent. Time sniffing the scent substrate and the duration of erections were significantly elevated in relation to the vehicle scent. Thirty minutes after presentation of ovulatory scent, males showed a significant increase in testosterone compared to the vehicle, but there was no difference in cortisol values. To better control for scent presentation, 15 additional males were tested under a controlled scent exposure. Current social housing condition influenced the male's testosterone response to the ovulatory scent. Single and paired males showed significant increases in testosterone levels with the ovulatory scent but did not increase cortisol levels. Single males also showed the highest change in testosterone with the ovulatory scent, but fathers showed no changes. These results indicate that a rapid hormonal response to sexually arousing cues occurs in marmosets, and the data suggest that a male's social condition influences how he responds to sexually relevant cues.     

Sociosexual development,pair bond formation,and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus)

The effect of various social environments on sociosexual behavior was examined in six young female cotton-top tamarins (Saguinus oedipus oedipus) and in three established breeding females. Behavioral observations and hormonal samples were collected on young females while they were living with their families, when they were isolated from conspecifics, and after they were paired with an unrelated male. While living with the family, all females showed a suppression of fertility and low frequencies of sociosexual behavior. Following removal from the family, isolated females displayed an increase in rate of scent marking and an increase in hormonal levels. When young females were paired with males, they were exposed to scent secretions from their natal families, from an unfamilar family, and from a control for a total of 24 weeks. After pairing, hormonal levels increased dramatically, and ovarian cyclicity began. An increase in sociosexual behavior and elevated levels of scent marking accompanied this physiological change. Newly paired females had higher rates of affiliative behavior and scent marking than did established breeding females. However, both newly paired and established breeding males were more likely to initiate contact, grooming bouts, and social sniffing than were females. Time to first ovulation was later in females who were exposed to scent secretions from their natal families than it was in those females given a control for the first 8 weeks following pairing. No female conceived during exposure to scent secretions. However, once normal ovarian cycling had begun or a pregnancy was established, exposure to scent secretions had no effect. Thus, the social environment influences the fertility, sociosexual behavior, and pair bond formation of cotton-top tamarins. In addition, chemical stimuli found in the scent secretions produced by the natal family are most likely involved in reproductive suppression.     

A sex difference in the context-sensitivity of dominance perceptions

Although dominance perceptions are thought to be important for effective social interaction, their primary function is unclear. One possibility is that they simply function to identify individuals who are capable of inflicting substantial physical harm, so that the perceiver can respond to them in ways that maximize their own physical safety. Another possibility is that they are more specialized, functioning primarily to facilitate effective direct (i.e., violent) intrasexual competition for mates, particularly among men. Here we used a priming paradigm to investigate these two possibilities. Facial cues of dominance were more salient to women after they had been primed with images of angry men, a manipulation known to activate particularly strong self-protection motivations, than after they had been primed with images of angry women or smiling individuals of either sex. By contrast, dominance cues were more salient to men after they had been primed with images of women than when they had been primed with images of men (regardless of the emotional expressions displayed), a manipulation previously shown to alter men's impressions of the sex ratio of the local population. Thus, men's dominance perceptions appear to be specialized for effective direct competition for mates, while women's dominance perceptions may function to maximize their physical safety more generally. Together, our results suggest that men's and women's dominance perceptions show different patterns of context-sensitivity and, potentially, shed new light on the routes through which violence and intrasexual competition have shaped dominance perceptions.     

What role do olfactory cues play in chacma baboon mating?

The probability of ovulation in a number of primate species is associated with both visual and auditory cues. We use 18‐month behavioral data from two chacma baboon troops to provide the first systematic assessment of the possibility that olfactory cues are also involved. Using variance in the rate of olfactory inspection by males as a proxy for changes in the intensity of female vaginal odor, we found that rates of inspection were broadly correlated with changes in female fertility. Males inspected cycling females significantly more than anovulatory, noncycling females and swelling females significantly more than nonswollen cycling females. Rates of inspection peaked around the time at which males first started guarding females and were sustained until the detumescence of the female's sexual skin. We conclude, therefore, that olfactory cues represent one component of a multimodal signal of ovulation in chacma baboons. The possible reasons for such a multimodal signal are discussed. Am. J. Primatol. 71:493–502, 2009. © 2009 Wiley‐Liss, Inc.     

Fertility status,dominance, and scent marking behavior of family-housed female cotton-top tamarins (Saguinus oedipus) in absence of their mothers

The effect of the mother's absence on the fertility status and expression of scent marking behavior was examined in 12 sexually mature female cotton-top tamarins (Saguinus oedipus) living in four motherless families. Behavioral data and urine samples were collected on an average of five times per week and levels of estrone-glucuronide (E1G) were quantified directly by radioimmunoassay to establish whether the females showed ovarian cyclicity. Of the 12 females investigated only the dominant female in each motherless group exhibited regular E1G cycles. By contrast, low and acyclic hormonal profiles were found for subordinate sisters. In addition to differences in the patterns and levels of E1G, scent gland morphology and rates of scent marking differed between females: dominant, cycling females had elaborate glands and significantly higher rates of scent marking than subordinates. These results indicate that the presence of the mother (breeding female) is one important factor regulating ovarian function in cotton-top tamarin daughters. The findings also show that dominance status is a vital determinant of each female's subsequent physiological reproductive competence, with only the dominant female obtaining complete fertility and probably inhibiting ovulatory activity in her subordinate sisters. Scent marking behavior seems to be involved in the regulation of this phenomenon of intrasexual reproductive competition.     

The direct assessment of genetic heterozygosity through scent in the mouse

The role of individual genetic heterozygosity in mate choice is the subject of much current debate. Several recent studies have reported female preference for more heterozygous males, but the mechanisms underlying heterozygote preference remain largely unknown. Females could favor males that are more successful in intrasexual competition, but they could also assess male heterozygosity directly at specific polymorphic genetic markers. Here, we use a breeding program to remove the intrinsic correlation between genome-wide heterozygosity and two highly polymorphic gene clusters that could allow direct assessment of heterozygosity through scent in mice: the major histocompatibility complex (MHC) and the major urinary proteins (MUPs). When other sources of variation are controlled and intrasexual competition is minimized, female mice prefer to associate with MUP heterozygous over MUP homozygous males. MHC heterozygosity does not influence preference, and neither does heterozygosity across the rest of the genome when intrasexual competition between males is restricted. Female mice thus assess male heterozygosity directly through multiple MUP isoforms expressed in scent signals, independently of the effects of genome-wide heterozygosity on male competitiveness. This is the first evidence that animals may use signals of genetic heterozygosity that have no direct association with individual vigour.