Differential use of sensory information in sexual behavior as a function of gender

Olfactory information is critical to mammalian sexual behavior. Based on parental investment theory the relative importance of olfaction compared with vision, touch, and hearing should be different for human males and females. In particular, because of its link to immunological profile and offspring viability, odor should be a more important determinant of sexual choice and arousal for females than for males. To test this hypothesis a questionnaire was developed and administered to 332 adults (166 males, 166 females). Subjects used a 1–7 scale to indicate how much they agreed with a series of statements concerning the importance of olfactory, visual, auditory, and tactile information for their sexual responsivity. The data reveal that males rated visual and olfactory information as being equally important for selecting a lover, while females considered olfactory information to be the single most important variable in mate choice. Additionally, when considering sexual activity, females singled out body odor from all other sensory experiences as most able to negatively affect desire, while males regarded odors as much more neutral stimuli for sexual arousal. The present results support recent findings in mice and humans concerning the relation of female preferences in body odor and major histocompatibility complex (MHC) compatibility and can be explained by an evolutionary analysis of sex differences in reproductive strategies. This work represents the first direct examination of the role of different forms of sensory information in human sexual behavior.     

Bimorphism in Male Verreaux’s Sifaka in the Kirindy Forest of Madagascar

Male primates in species with pronounced secondary sexual adornments can exhibit reversible or irreversible bimorphism, i.e., striking variation in the degree to which males express the adornments. Verreaux’s sifaka (Propithecus verreauxi verreauxi) use scent marking as a form of communication and exhibit sex differences in scent glands. Some males exhibit a pronounced brown staining around their sternal gland, whereas others do not. We studied morphological and behavioral characteristics of males in 6 social groups in Kirindy Forest, Madagascar, from November 2000 to March 2002 to evaluate the hypotheses that the bimorphism in male sifaka chest status represents alternative mating tactics and is a badge of status. Males are clearly divided into 2 categories: clean and stained chests, with rare, but informative, intermediate males. The chest staining probably results from the males scent marking with their sternal glands, because stained-chested males scent marked significantly more often than clean-chested males. Though sample sizes are small, chest status did not appear to depend on body size. Chest status is reversible and related to dominance rank. In each group, only 1 male, the dominant, was stained-chested, whereas all other (subordinate) males were clean-chested. These findings suggest that stained chests are visual and olfactory signals of dominance rank and that clean chests signal lack of competitive intent. Thus, this bimorphism may reflect alternative mating tactics used by males to maximize their reproductive success based upon their social environment.     

Olfactory preferences, scent marking, and "proceptivity" in female hamsters

Two appetitive sexual behaviors of female hamsters, attraction to odors of males and vaginal scent marking, were investigated and the correlations of each to reproductive states were determined. Both estrous and diestrous females were more attracted to the odors of intact males than to the odors of females or castrated males; this differential attraction was more pronounced for estrous females. Lactating females, but not pregnant females, were also preferentially attracted to odors of intact males. Thus, odors alone provided sufficient information to allow sexual discrimination by females, and estrous, diestrous, and lactating females were preferentially attracted to odors of intact males whereas pregnant females were not. Reproductive condition had no influence on responses to odors of castrated males or diestrous females. Vaginal scent marking was strongly influenced by reproductive state: Marking frequency was low in estrous, pregnant, and early lactation females, but high in late lactation and diestrous females, suggesting a function of advertisement of approaching receptivity. Thus sexual preferences based on olfactory cues and vaginal scent-marking frequency differed in their relationships to reproductive conditions. It is suggested that in other species such relationships between appetitive sexual behaviors and reproductive condition will depend on the species social organization, ecological niche, and taxonomic group, and consequently that the concept of preceptive behaviors should be broadened to include all appetitive sexual behaviors of females, not just those that are correlated with the hormonal state characterizing estrus.     

Scent marking strategies of New World primates

This paper reviews recent findings on scent-marking behavior in wild New World primates. These findings are used to examine three functional hypotheses: territoriality, regulation of social and reproductive dominance, and mating competition/mate attraction. Available data provide little evidence for a territorial function of scent-marking behavior in New World primates. Evidence for a function in the regulation of social and reproductive dominance is ambiguous. The patterns of scent marking found so far (i.e., rates of scent marking according to sex and social or reproductive status, and the spatial distribution of scent marks), and the sparse information on responses to scent marks are consistent with a hypothesized function in intrasexual competition and intersexual mate choice. Suggestions for future research are made.     

Olfactory signals and the MHC: a review and a case study in Lemur catta

The major histocompatibility complex (MHC) is the most polymorphic genetic system known in vertebrates. Decades of research demonstrate that it plays a critical role in immune response and disease resistance. It has also been suggested that MHC genes influence social behavior and reproductive phenomena. Studies in laboratory mice and rats report that kin recognition and mate choice are influenced by olfactory cues determined at least in part by an individual's MHC genes. This issue has stimulated intense but controversial research. However, work in this field has only been carried out in rodents and humans. Thus far, no study has directly investigated the relationship between olfactory cues and MHC genotype in nonhuman primates. Furthermore, other genetic loci, including those linked to the MHC, have not been ruled out as the primary influence on odor profiles. To explore the relationship between individual odor profiles and MHC alleles, we are studying ring-tailed lemurs (Lemur catta). These animals are an ideal model species because they are extremely scent-oriented and their behaviors suggest that olfactory signals form an important part of their intra- and intergroup communication systems. Individual odor profiles from tail and scent gland samples were generated for six males using gas chromatography mass spectrometry (GC-MS). MHC genotypes were identified using polymerase chain reaction (PCR) and denaturing gradient gel electrophoresis (DGGE). The GC-MS analyses demonstrated a difference between profiles obtained from tail and scent gland samples. Although our sample size is relatively small and statistical significance could not be obtained, our analyses suggest a relationship between MHC and concentrations of volatile compounds. While these results are preliminary, they support the need for further studies of the MHC and olfactory signals in lemurs and other primates.     

Dynamics of Male–Female Multimodal Signaling Behavior across the Estrous Cycle in Giant Pandas (Ailuropoda melanoleuca)

Giant panda courtship behavior includes multimodal signaling assemblages consisting of olfactory, vocal, and postural elements. While signaling is generally conspicuous, successful copulation is inconsistently achieved in captivity, even when female behavioral and physiological data indicate that ovulation is imminent. We set out to characterize these complex patterns of social behavior by observing interactions between 26 unique pairs of giant pandas housed in adjoining pens throughout the females' reproductive cycle. We categorized social behaviors from a transactional perspective and examined social exchanges via analyses of the relative frequency of social behaviors, and via the sequential relationship between male and female social behavior. From non‐estrus to peak‐estrus, we found that the relative frequency of female affiliative and sexual behavior increased and that the relative frequency of ambivalent and aggressive behavior decreased. Male behavior was fairly constant, except for sexual behavior, which increased during peak‐estrus, when it was facilitated by female sexual behavior. Sequential analysis of social interactions showed that preceding behavior had a significant influence over the other panda's response behavior primarily during peak‐estrus, suggesting that pandas are most responsive to conspecific signaling during the peri‐ovulatory period. However, behavioral momentum was a dominant feature of the intra‐individual transitions. Females maintained sexual, ambivalent, and neutral behavior during interactions significantly more than would be expected by chance, with male behavior bearing little influence once the behavior was initiated. A similar pattern was also observed in males, who maintained affiliative, interested, and neutral behaviors. Overall, our data suggest that the multimodal signals used by giant pandas during courtship do not consistently evoke a discrete, immediate response from receivers. Instead, signals appear to advertise reproductive condition and influence potential mates over longer timeframes, suggesting the potential tonic role of communication.     

Social chemosignals from breastfeeding women increase sexual motivation

Human pheromones, a type of social chemosignal, modulate endocrine function by regulating the timing of ovulation. In animals, pheromones not only regulate ovulation but also female reproductive motivation and behavior. There is no extant evidence that humans produce social chemosignals that affect human sexual motivation or reproductive behavior as occurs in other mammals. Here, we demonstrate that natural compounds collected from lactating women and their breastfeeding infants increased the sexual motivation of other women, measured as sexual desire and fantasies. Moreover, the manifestation of increased sexual motivation was different in women with a regular sexual partner. Those with a partner experienced enhanced sexual desire, whereas those without one had more sexual fantasies. These results are consistent with previous pheromonal effects on endocrine function, and warrant further study of these social chemosignals as candidates for pheromonal processes, including their effects on other aspects of motivation and behavior.     

Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice

Reproductive behavior in male rodents is made up of anticipatory and consummatory elements which are regulated in the brain by sensory systems, reward circuits and hormone signaling. Gonadal steroids play a key role in the regulation of male sexual behavior via steroid receptors in the hypothalamus and preoptic area. Typical patterns of male reproductive behavior have been characterized, however these are not fixed but are modulated by adult experience. We assessed the effects of repeated sexual experience on male reproductive behavior of C57BL/6 mice; including measures of olfactory investigation of females, mounting, intromission and ejaculation. The effects of sexual experience on the number of cells expressing either androgen receptor (AR) or estrogen receptor alpha (ERα) in the primary brain nuclei regulating male sexual behavior was also measured. Sexually experienced male mice engaged in less sniffing of females before initiating sexual behavior and exhibited shorter latencies to mount and intromit, increased frequency of intromission, and increased duration of intromission relative to mounting. No changes in numbers of ERα-positive cells were observed, however sexually experienced males had increased numbers of AR-positive cells in the medial preoptic area (MPOA); the primary regulatory nucleus for male sexual behavior. These results indicate that sexual experience results in a qualitative change in male reproductive behavior in mice that is associated with increased testosterone sensitivity in the MPOA and that this nucleus may play a key integrative role in mediating the effects of sexual experience on male behavior.     

The effects of infant births on the sociosexual behavior and hormonal patterns of a cooperatively breeding primate (Cebuella pygmaea)

This study examined changes in the behavioral and hormonal patterns of cooperatively breeding pairs in a primate species with the passing of time and with specific reproductive events. We (1) compared patterns of sexual, agonistic, and affiliative behavior of newly paired pygmy marmosets with the same behavioral patterns immediately after the birth of their first set of infants; (2) determined if postpartum behavioral differences existed between pairs whose infants lived and those whose infants died; and (3) examined whether behavioral patterns changed over the course of ovarian cycles in parous pygmy marmosets as had been documented in nulliparous pairs. The behavior of pairs was recorded during daily half-hour focal samples for 60 days after pairing, and 30 or 60 days after the birth of infants for pairs whose litters died or lived, respectively. Daily urine samples from females during the study were analyzed for luteinizing hormone and pregnanediol glucuronide concentrations to determine dates of ovulation. The results indicated that males consistently altered their sexual behavior and olfactory monitoring of mates during periovulatory periods in the females' cycles both postpairing and postpartum, while similar rates of social and sexual behavior were maintained between the conditions. Sexual behavior occurred throughout the females' ovarian cycles. Peaks in sexual behavior during the periovulatory period in nulliparous pairs disappeared after the birth of infants. Pairs whose infants died showed higher rates of sexual behavior than pairs with surviving infants. Social and sexual behavior may function to maintain the relationship both during and outside of ovulation, especially with the loss of infants. © 1996 Wiley-Liss, Inc.     

Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures

The apocrine and sebaceous scent glands of ringtailed lemurs (Lemur catta) appear to serve different social functions. In behavioral experiments, lemurs modulate their responses to scent marks based on the type of odorant, their own physiological state, the signaler's physiological state, and prior social experience. To examine variation in odorant chemistry relative to olfactory behavior, we used gas chromatography and mass spectrometry to analyze over 86 samples of glandular secretion collected over 2 years from 15 adult lemurs. Labial and scrotal secretions contained organic acids and esters, whereas male brachial secretions were composed almost entirely of squalene and cholesterol derivatives. Principal component and linear discriminant analyses revealed glandular, individual-specific, and seasonal variation in chemical profiles but no relationship to the signaler's social status. The chemical composition of the various secretions provides further clues about the function of the different glands: the higher molecular weight compounds in genital and brachial secretions may increase signal longevity and provide lasting information to conspecifics, consistent with a role in advertising resource ownership or reproductive state. Conversely, the lower molecular weight compounds of antebrachial secretions produce ephemeral signals used primarily in social dominance displays and require integration of multiple sensory modalities for effective signal transmission.     

Attunement to the fertility status of same-sex rivals: women's testosterone responses to olfactory ovulation cues

Evolutionary theories of mating suggest that changes in fertility across the menstrual cycle play an important role in sexual selection. In line with this framework, the current research examined whether olfactory cues to the fertility of a same-sex rival would prompt hormonal signs of intrasexual competition in women. Women exposed to the scent of another woman close to ovulation subsequently displayed higher levels of testosterone than women exposed to the scent of a woman far from ovulation. Whereas women exposed to the scent of a woman in the mid-luteal phase displayed sizable decreases in testosterone over time, no such decline was observed among women exposed to the scent of a woman near ovulation. Thus, olfactory cues signaling a rival's heightened level of fertility were associated with endocrinological responses in women that could be linked to intrasexual competition.     

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.     

Murine scent mark microbial communities are genetically determined

Scent marking in mice allows males to communicate information such as territory ownership, male competitive ability and current reproductive, nutritional, social and health status. It has been suggested that female mice eavesdrop on these olfactory cues, using them as a means of selecting mates with dissimilar major histocompatibility complex (MHC) genes, known as H2 in mice. The mechanisms underpinning MHC-dependent olfactory communication remain unresolved. Using congenic mouse strains and molecular methods we explore the involvement of the microbial communities, a known source of odourants, in scent marks to test the hypothesis that the microbial communities and hence the olfactory signals are genetically determined. Here we show that the indigenous microbial community of murine scent marks is genetically determined. Both background genotype and H2 haplotype influence the community structure of the scent mark flora, removing the possibility that community composition is solely orchestrated by the MHC. Qualitative and quantitative components of the bacterial community associated with MHC haplotype and background genotype were identified. The analyses confirm that the four groups of congenic mice tested are distinguishable on basis of the microbiology of their scent marks alone, strengthening the role of microorganisms in the development of MHC-dependent odours.     

Sex differences in main olfactory system pathways involved in psychosexual function

We summarize literature from animal and human studies assessing sex differences in the ability of the main olfactory system to detect and process sex‐specific olfactory signals (“pheromones”) that control the expression of psychosexual functions in males and females. A case is made in non primate mammals for an obligatory role of pheromonal signaling via the main olfactory system (in addition to the vomeronasal‐accessory olfactory system) in mate recognition and sexual arousal, with male‐specific as well as female‐specific pheromones subserving these functions in the opposite sex. Although the case for an obligatory role of pheromones in mate recognition and mating among old world primates, including humans, is weaker, we review the current literature assessing the role of putative human pheromones (eg, AND, EST, “copulin”), detected by the main olfactory system, in promoting mate choice and mating in men and women. Based on animal studies, we hypothesize that sexually dimorphic effects of putative human pheromones are mediated via main olfactory inputs to the medial amygdala which, in turn, transmits olfactory information to sites in the hypothalamus that regulate reproduction.     

Bateman revisited: the reproductive tactics of female primates

The breeding system of an animal population is thought to depend on the ability of one sex (usually the male) to acquire mates, either directly through association with females or indirectly through defense of the resources desired by females. The sex that contributes most to infant care (usually the female) is constrained by parental involvement and thereby limits reproduction of the opposite sex. Accordingly, males, but not females, enhance their reproductive success by acquiring additional mates. This classical view has emphasized the role of male-male competition in sexual selection, at the expense of fully exploring the potential for female choice. A more recent shift in focus has revealed substantial variation in female reproductive success and increasingly accentuates the importance of female intrasexual competition and male mate choice. A comparative review of primate reproduction, therefore, challenges expectations of male control and female compliance, and calls for a comprehensive treatment of costs and benefits that extends beyond conventional mention of heavy female investment versus male negligence or absenteeism. For individuals that manipulate their social environment or reproductive output, consideration of more subtle, even cryptic, aspects of female behavior and physiology (e.g., social strategizing, sexual solicitation or rejection, sexual advertisement or concealed ovulation, multiple mating, and reproductive failure) raises the question of whether females can be effectively 'monopolized.' Widespread patterns that counter Bateman's paradigm call for a reexamination of the predictions generated by dichotomizing gametes into 'expensive eggs' and 'cheap sperm,' and encourage continued mechanistic research focused on conception quality rather than quantity.     

Self-Discrimination in Meadow Voles, Microtus pennsylvanicus

Particular features of the signaling characteristics of the scent marks of temperate zone, seasonally breeding mammals may reflect differences in their reproductive state and, hence, be variable. Consequently, an individual's perception of self may depend more on the condition independent than on the condition-dependent signaling characteristics of the scent marks. Yet, we do not know whether an individual responds to changes in the signaling characteristics of its own scent marks, such as those associated with changes in an individual's reproductive state. Such changes may affect how and where an animal scent marks. Here we report on a series of experiments designed to test the hypothesis that individual meadow voles, Microtus pennsylvanicus , distinguish between scent marks they deposited when they were in different reproductive states. Results showed that voles discriminated their own scent marks from those of unfamiliar, same-sex conspecifics, and the scent marks of siblings. Voles did not behave as if they could distinguish between their own scent marks if the marks were deposited when the voles were in the same reproductive state, although the two scent marks used as stimuli differed in age by 30 d. However, they did so distinguish if they were exposed to scent marks taken when they were in different reproductive states. Overall, these findings suggest that voles behave as if their novel and familiar scent marks shared the similar signaling features. If, however, the reproductive condition of the voles differed when it provided the two scent marks, they behaved as if their own scent marks had different signal characteristics, which may have induced voles to treat the two scent marks as not being the same or having been deposited by two different donors. We speculate that the scent marks of individuals may have unique signaling characteristics that may be associated with that individual's 'current template for self'.     

The sexual behavior of the primates]

The article presents the review of modern data of the field and laboratory investigations of primate sexual behavior, cyclicity, reproductive strategies and copulation in different primates taxa: strepsirrhini, platyrrhyni, catarrhini. The specific character, progressiveness and adaptation of some reproductive models are discussed by the authors. A problem of connection between dominance and reproductive success is also discussed, the role of sexual teaching in postnatal ontogenesis, age and hormonal status for expression of sexual behavior are analysed. Some forms of sexual declinations in primates are considered.     

SOCIAL BEHAVIOR OF OCHOTONA CANSUS: ADAPTATION TO THE ALPINE ENVIRONMENT

Field observations were carried out on the Gansu pikas, Ochotona cansus Lyon, in its natural habitat from July 1987 to November 1988 at Haibei Alpine Meadow Ecosystem Research Station, Qinghai Province,PRC. Communicative behavior, reproductive behavior, spatial and social organization of the Gansu pika were described, and their adaptive significance discussed. The major communicative methods are acoustical and olfactory.At least four types of call (long call,short call, trill and whine)were distinguished. The peculiar habits of vocalization of species in the genus Ochotona appear to be the result of adaptation to boreal and/or high altitude severe climates. Two types of scent marking patterns were observed, and faeces play an important role in olfactory communication. Mother-infant relationships differ from most small rodents, but resemble those of medium-sized lagomorphs. The suckling time is "scheduled", and the frequency seems positively related to litter-size. This mother-infant relationship is thoug     

Sex and context: hormones and primate sexual motivation

Gonadal hormones regulate the ability to copulate in most mammalian species, but not in primates because copulatory ability has been emancipated from hormonal control. Instead, gonadal hormones primarily influence sexual motivation. This separation of mating ability from hormonally modulated mating interest allows social experience and context to powerfully influence the expression of sexual behavior in nonhuman primates, both developmentally and in adulthood. For example, male rhesus monkeys mount males and females equally as juveniles, but mount females almost exclusively as adults. Having ejaculated with a female better predicted this transition to female mounting partners than did increased pubertal testosterone (T). It is proposed that increased pubertal T stimulates male sexual motivation, increasing the male's probability of sexual experience with females, ultimately producing a sexual preference for females. Eliminating T in adulthood reduces male sexual motivation in both humans and rhesus monkeys, but does not eliminate the capacity to engage in sex. In male rhesus monkeys the effects of reduced androgens on sexual behavior vary with social status and sexual experience. Human sexual behavior also varies with hormonal state, social context, and cultural conventions. Ovarian hormones influence female sexual desire, but the specific sexual behaviors engaged in are affected by perceived pregnancy risk, suggesting that cognition plays an important role in human sexual behavior. How the physical capacity to mate became emancipated from hormonal regulation in primates is not understood. This emancipation, however, increases the importance of motivational systems and results in primate sexual behavior being strongly influenced by social context.