Sexual Skin Research Articles

Are badges of status adaptive in large complex primate groups?

Sexual dimorphism in ornamentation in primates may have been sexually selected as signals of rank and dominance to males or by augmenting attractiveness to females. While male primates display tremendous variation in secondary sexual traits, such as sexual skin, capes of hair, and beards, which are often attributed to sexual selection, their phylogenetic distribution remains to be fully understood. Here we investigate the hypothesis that sexual dimorphism in ornaments is more pronounced in larger more ‘anonymous’ social organizations where quick reliable assessment of male quality, social status, dominance, and aggressiveness are selective pressures. Multiple regression analyses, including phylogenetic correction, were performed on 154 species representing 45 genera of simian primates. We found a positive relationship between degree of ornamental dimorphism and group size, even after controlling for other independent variables such as habitat type (i.e. openness of terrain) and fission–fusion dynamics. Dimorphism was also significantly associated with social organization, so that males from species with multilevel social organizations had the highest ratings for ornamentation. In sum, our analysis suggests that among primates with larger group sizes and multilevel social organizations, males have more developed visually conspicuous secondary sexual traits. This may reflect selection for amplified signals of individual identity, rank, dominance, or attractiveness in large and complex social organizations wherein social and physical conflict may arise frequently and individual recognition is limited.

Prolonged maximal sexual swelling in wild bonobos facilitates affiliative interactions between females

Perineal sexual skin swelling in relation to menstrual cycle occurs in a variety of primate taxa. However, sexual swelling with exaggerated size and colour is found only in some Old World monkeys and the two Pan species. Although several hypotheses have been proposed (e.g., reliable indicator hypothesis and graded signal hypothesis), it seems unlikely that a single explanation can account for the significance of the sexual swelling in all of these species. Bonobos (Pan paniscus) provide an excellent opportunity for studying sexual swelling since they have the most prolonged maximal swelling periods among primates. In this study we propose a new hypothesis that sexual swelling in female bonobos increases their attractiveness to other females and thereby facilitates affiliative social interaction with them. We found that free-ranging female bonobos with maximal sexual swelling engaged in affiliative social interactions with other females, including genito-genital rubbing, staying in close proximity and grooming, more frequently than females without maximal swelling. These tendencies suggest that females with maximal swelling were attractive to other females. The results also suggest that the benefits of maximal swelling might vary among females depending on their life-history stage. In particular, young females may get more benefits from prolonged maximal swelling through increased grooming reciprocity and staying in close proximity to other females. Thus our study supported the hypothesis that one function of prolonged maximal swelling in bonobos is to increase attractiveness to other females, thereby enhancing affiliative relationships between females in a male-philopatric social system.

Toward a better understanding of social learning, social deciding, and other-regarding preferences.

Toward a better understanding of social learning, social deciding, and other-regarding preferences.

Social relevance drives viewing behavior independent of low-level salience in rhesus macaques.

Quantifying attention to social stimuli during the viewing of complex social scenes with eye tracking has proven to be a sensitive method in the diagnosis of autism spectrum disorders years before average clinical diagnosis. Rhesus macaques provide an ideal model for understanding the mechanisms underlying social viewing behavior, but to date no comparable behavioral task has been developed for use in monkeys. Using a novel scene-viewing task, we monitored the gaze of three rhesus macaques while they freely viewed well-controlled composed social scenes and analyzed the time spent viewing objects and monkeys. In each of six behavioral sessions, monkeys viewed a set of 90 images (540 unique scenes) with each image presented twice. In two-thirds of the repeated scenes, either a monkey or an object was replaced with a novel item (manipulated scenes). When viewing a repeated scene, monkeys made longer fixations and shorter saccades, shifting from a rapid orienting to global scene contents to a more local analysis of fewer items. In addition to this repetition effect, in manipulated scenes, monkeys demonstrated robust memory by spending more time viewing the replaced items. By analyzing attention to specific scene content, we found that monkeys strongly preferred to view conspecifics and that this was not related to their salience in terms of low-level image features. A model-free analysis of viewing statistics found that monkeys that were viewed earlier and longer had direct gaze and redder sex skin around their face and rump, two important visual social cues. These data provide a quantification of viewing strategy, memory and social preferences in rhesus macaques viewing complex social scenes, and they provide an important baseline with which to compare to the effects of therapeutics aimed at enhancing social cognition.

Use of photogrammetry as a means to assess hybrids of rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques.

Rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques are the most commonly used non-human primate models for biomedical research, but it is difficult to identify these two species in the hybrid zone (15-20°N). In this work, we used morphological values obtained via photogrammetry to assess hybrids of rhesus and long-tailed macaques at Khao Khieow Open Zoo (KKZ; 13°21'N, 101°06'E), eastern Thailand. Long-tailed and rhesus macaques have species-specific tail lengths and contrasts of their yellowish pelages. The accuracy and precision of the relative tail length (%RTL) and the contrast of the yellow hue (Cb*) of the pelage, as obtained from photographs, were compared with the corresponding direct measurements (morphometrics). The photogrammetric and morphometric measurements of %RTL and Cb* were highly significantly correlated (r = 0.989 and 0.980, p < 0.001), and there were no significant differences between the two datasets (t test, p = 0.13 and 0.41; n = 42 and 17 for %RTL and Cb*, respectively). The reproducibilities of the %RTL and Cb* measurements (calculated in the photogrammetric case by taking photographs of the same macaques in two different environments) were significantly correlated between the datasets (r = 0.983 and 0.914, p < 0.001 and 0.005), and there were no significant differences between the datasets (t test, p = 0.539 and 0.344; n = 30 each for %RTL and Cb*, respectively). The %RTL and Cb* data were combined with data on the crown and cheek hair patterns and sex skin reddening of the macaques, and this combined data set was then analyzed by multiple correspondence analysis and agglomerative hierarchical cluster analysis, leading to the categorization of the rhesus macaques, long-tailed macaques, and hybrids at KKZ into five groups. Thus, photogrammetry can be utilized to identify macaque species or hybrids when species identification relies mainly on tail length and pelage color.

Indoor environmental factors associated with wheezing illness and asthma in South Korean children: phase III of the International Study of Asthma and Allergies in Childhood

Background: The relationship between exposure to indoor environmental pollutants and incidence of asthma and wheezing illness in children is unclear. This study aimed to clarify this relationship by identifying the risk factors associated with these conditions in South Korean children aged 6–7 years. Methods: The parents or guardians of 3810 children aged 6–7 years who had participated in the International Study of Asthma and Allergies in Childhood and met the study criteria completed validated questionnaires regarding their children's asthma and wheezing illness, risk factors and exposure to indoor pollutants. The data were subjected to chi-square and multivariate logistic regression analysis to identify the factors significantly associated with asthma and wheezing illness. Results: Parental history of allergic disease (odds ratio [OR]: 1.729; 95% confidence interval [CI]: 1.447–2.066), living on the basement or semi-basement floor (OR: 1.891; 95% CI: 1.194–2.996) and living in housing that had been remodeled within the last 12 months (OR: 1.376; 95% CI: 1.101–1.720) were found to be significantly associated with wheezing illness. Parental history of allergic disease (OR: 2.189; 95% CI: 1.483–3.231), male sex (OR: 1.971; 95% CI: 1.369–2.838) and positive skin prick test (SPT) result (OR: 1.583; 95% CI: 1.804–3.698) were found to be significantly associated with current asthma. Conclusions: Although the risk factors for current asthma appear to be more related to the non-modifiable risk factors like sex, parental history of allergic diseases, SPT, the two groups are associated with exposure to modifiable indoor environmental factors.

Colour and contrast of female faces: attraction of attention and its dependence on male hormone status in Macaca fuscata

Colour signals play a major role in social and sexual communication in a broad range of animal species. Previous studies on nonhuman primates showed that intense female skin coloration attracts male attention. We investigated (1) whether sexually active male Japanese macaques are attracted by intensely coloured female skin, (2) whether a preference for intense skin coloration results from the increased colour contrast between the skin area and its surroundings irrespective of the red chromaticity, and (3) whether the endocrine status of sexually active males affects their attentional selectivity (or preference) for salient female sexual skin coloration. We conducted two behavioural experiments in two consecutive mating seasons. First, we presented two female face images coloured in a natural range of red skin coloration on monitors. Second, we presented the same faces dissociated from the red chromaticity while maintaining their initial colour contrast properties. In both experiments we analysed male selective visual attention and approaches as a function of stimulus type. Faecal samples were collected after each experiment to analyse focal males' cortisol and testosterone excretion rates. We found that female facial skin coloration triggered selective behaviour in social-living male Japanese macaques. Variances in colour contrast also triggered males' selective orienting towards an intensely coloured face image but the red chromaticity remained essential to induce prolonged male interest. Furthermore, elevated cortisol facilitated male preferences for the intensely coloured female faces, sociosexual stimuli that are presumably highly relevant during the mating season. Future studies may pursue the principle of colour contrast in male attentional behaviour with respect to subtle colour changes expressed by females throughout the reproductive cycle. Cortisol-related physiological processes should be considered in studies on mating-relevant selective attention. • We investigated colour and colour contrast preferences in male Japanese macaques. • We analysed males' endocrine status in relation to their selective behaviour. • Female facial skin coloration triggers visual and behavioural selection of males. • Dissociated from the red colour, variances in colour contrast are less decisive. • Cortisol excretion rates correlate with males' selective behaviour.

Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior.

The past decade has seen an increasing shift in animal communication towards more studies that incorporate aspects of signaling in multiple modalities. Although nonhuman primates are an excellent group for studying the extent to which different aspects of condition may be signaled in different modalities, and how such information may be integrated during mate choice, very few studies of primate species have incorporated such analyses. Here, we present data from free-ranging male rhesus macaques on sex skin coloration (modeled to receiver perception), bark vocal signals, androgen levels, morphometric variables, dominance status, and female mate choice. We show that, consistent with data on females, most intra- and interindividual variation in sex skin appearance occurs in luminance rather than color. Sex skin luminance was significantly correlated across different skin regions. Sex skin luminance did not correlate with the majority of bark parameters, suggesting the potential for the two signals to convey different information. Sex skin appearance was not related to androgen levels although we found some evidence for links between androgen levels and bark parameters, several of which were also related to morphometric variables. We found no evidence that either signal was related to male dominance rank or used in female mate choice, though more direct measures of female proceptive behavior are needed. Overall, the function of male sex skin coloration in this species remains unclear. Our study is among the first nonhuman primate studies to incorporate measurements of multiple signals in multiple modalities, and we encourage other authors to incorporate such analyses into their work.

Social Signals in Primate Orbitofrontal Cortex

Primate evolution produced an increased capacity to respond flexibly to varying social contexts as well as expansion of the prefrontal cortex. Despite this association, how prefrontal neurons respond to social information remains virtually unknown. People with damage to their orbitofrontal cortex (OFC) struggle to recognize facial expressions, make poor social judgments, and frequently make social faux pas. Here we test explicitly whether neurons in primate OFC signal social information and, if so, how such signals compare with responses to primary fluid rewards. We find that OFC neurons distinguish images that belong to socially defined categories, such as female perinea and faces, as well as the social dominance of those faces. These modulations signaled both how much monkeys valued these pictures and their interest in continuing to view them. Far more neurons signaled social category than signaled fluid value, despite the stronger impact of fluid reward on monkeys' choices. These findings indicate that OFC represents both the motivational value and attentional priority of other individuals, thus contributing to both the acquisition of information about others and subsequent social decisions. Our results betray a fundamental disconnect between preferences expressed through overt choice, which were primarily driven by the desire for more fluid, and preferential neuronal processing, which favored social computations.

Boundary zone between northern and southern pig-tailed macaques and their morphological differences

Based on previous conflicting reports that the two forms of pig-tailed macaque (northern and southern) exist as separate species, subspecies, or forms, and that their boundary zone lies in Thailand, a survey of the distribution range and morphology of pig-tailed macaques in Thailand was conducted during 2003-2010. We first conducted a questionnaire survey. Questionnaires were sent to 7,410 subdistricts throughout Thailand. We then traveled to 72 of the 123 subdistricts reporting the presence of pig-tailed macaques. However, due to a lack of reports of the presence of free-ranging pig-tailed macaques living south of the Isthmus of Kra, a survey of pet pig-tailed macaques was also conducted during 16-24 September 2011. Furthermore, 35 wild northern pig-tailed macaques inhabiting northern Thailand (13°13'N, 101°03'E) were temporarily caught and their morphological characters were measured and then compared to those of the southern form captured from Sumatra, Indonesia. Although largely allopatric, the ranges of the northern and southern pig-tailed macaques in Thailand were found to have a partially sympatric boundary at the Surat Thani-Krabi depression (8-9°30'N). Morphologically, these two forms were very distinctive, with different morphological characters such as the crown patch, the white color of the triangle above the eyes, the red streak at the external rim of the eyes, pelage color, ischial callosity, tail length and carriage, facial height, and limb length in both sexes, and patterns of sex skin swelling and reddening in females. These differences in morphological characters between the northern and southern forms should help settle the problems of their taxonomy.

Visual preferences for sex and status in female rhesus macaques.

Most primates are both highly visual and highly social. These qualities predict that visual cues to social variables, such as identity, sex, social status, and reproductive quality, would be intrinsically valuable and systematically attract attention. Supporting this idea, thirsty male rhesus macaques (Macaca mulatta) will forego fluid reward to view images of the faces of high-ranking males and the sexual skin of females. Whether female rhesus macaques, who experience dramatically different social pressures and reproductive costs than male macaques, also systematically and spontaneously value visual cues to social information remains untested experimentally. We probed the preferences of female rhesus macaques, given the opportunity to display an image from a known class of social stimuli or touch a second target to display a blank screen. We found that females preferred faces of high-status males and also images of the perinea of both males and females, but were not motivated to display images of subordinate males or control stimuli. These findings endorse the view that both male and female rhesus macaques-and presumably other highly social primates-seek information about other individuals in a way that matches the adaptive value of that information for guiding social behavior.

Information content of female copulation calls in wild long-tailed macaques (Macaca fascicularis)

Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the female's fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.

Dominance, Coloration, and Social and Sexual Behavior in Male Drills Mandrillus leucophaeus

Sexual selection has driven the evolution and elaboration of a wide variety of displays and ornaments in male nonhuman primates, including capes, cheek flanges, and sexual coloration. Among the most sexually dimorphic of all primates is the drill (Mandrillus leucophaeus), the males of which can be 3 times the mass of females, possess large canines, and exhibit extremely bright sexual skin coloration. However, the function of male coloration in this species has never been examined. Here, we present data on male color (measured objectively using digital photography), dominance rank, measures of male-female association, and key sexual behaviors, of adult male drills (n = 17) living in four semi free-ranging enclosures at the Drill Rehabilitation and Breeding Center in Nigeria. We test the hypothesis that male coloration is a badge of status, indicating dominance rank, and the hypothesis that male coloration attracts females. We found that male coloration did indicate rank, and that high ranking, strongly colored males were more likely to associate with adult females, and more specifically with fully tumescent females. These males also engaged in more sexual activity. However, measures of male-female association and sexual behaviors were not related to male color once rank had been taken into consideration; i.e., for males of a given rank, females did not prefer those that were more colorful. We discuss the results in light of what is known about the wild drill social system, in which unfamiliar individuals may come together in “supergroups,” and in which quality indicators of competitive ability may be particularly important.

Factors Affecting the Distribution of Copulatory Plugs in Rhesus Monkeys (Macaca mulatta) on Cayo Santiago

Although the proximate mechanisms behind the formation of copulatory plugs are well understood, their distribution and function among primates remain largely unstudied. During a study of female rhesus macaque (Macaca mulatta) mating behaviour on Cayo Santiago, we examined the pattern of the distribution of visible copulatory plugs among females and their potential relationship to female reproductive traits and sexual skin colouration. Our results indicate that non-pregnant females were observed more frequently with visible copulatory plugs than were pregnant females. Female parity status, age and rank were unrelated to copulatory plug observation. Genital colouration components were higher among females observed with copulatory plugs. We suggest that although copulatory plugs are generally thought of in terms of male physiology, plug observation may also be affected by female reproductive status.

Sexual Skin Color Contains Information About the Timing of the Fertile Phase in Free-ranging Macaca mulatta

Females of several primate species undergo cyclical changes of their sexual skin, i.e., the development of a swelling or a change in color. The relationship between intracycle probability of fertility and the size of sexual swellings is well established, but in the only study to combine an objective measure of color with endocrinological data, researchers found no evidence that swelling color contains such information. To evaluate the role of female skin color in the context of sexual signaling further, we investigated whether changes in sexual skin color contain information about the timing of the fertile phase in rhesus macaques (Macaca mulatta), a species in which adult females do not develop sexual swellings, but do express visually detectable changes in the skin color of the face and hindquarters. Using an objective and quantitative measure of color, along with detailed data on fecal progestogen and estrogen metabolite levels collected from 8 females of the Cayo Santiago colony, we show that the ratio of red to green (R/G) for facial and hindquarter skin significantly varies throughout the ovarian cycle. In addition, facial skin R/G is significantly higher during the 5-d fertile phase versus the 5-d periods immediately before or after this time, but no such pattern occurs in hindquarter R/G. This suggests that skin color change in female rhesus macaques may potentially signal information about the intracycle probability of fertility to male receivers, but that only facial skin color may signal reliable information about its timing.

Ovarian response to gonadotropin stimulation in juvenile rhesus monkeys

The objective of this study was to investigate juvenile rhesus monkeys responding to various gonadotropin regimen stimulations. Thirty-two prepubertal rhesus monkeys were randomly allocated into five groups for ovarian stimulation as follows: Groups I, II, and III were given 35, 18, and 9 IU recombinant human follicle-stimulating hormone (rhFSH), respectively, twice daily for 8 d; Group IV was given 18 IU rhFSH twice daily until the appearance of maximal increase in sex skin during the breeding season; and Group V was treated identically to Group II but during the nonbreeding season. In addition, nine menarchial monkeys (Group VI) were treated identically to Group II. Menarchial monkeys yielded two- to fivefold the numbers of MII oocytes (24.1) and almost twice the development potential of in vitro–fertilized oocytes (blastocyst rate: 50.0%) compared with those of the other groups. Moreover, prepubertal monkeys in Group V had approximately double the numbers of MII oocytes and in Groups IV and V twice the development potential compared with those of Groups I and II, whereas Group III did not respond to stimulation. The most prominent sex skin swelling was in association with peak serum estradiol concentrations, and good responses to stimulation were associated with reduced body temperatures. All stimulated monkeys had normal reproductive performance at adulthood, except those in Group I. In conclusion, gonadotropin stimulation of menarchial monkeys could be appropriate for addressing the high cost and limited availability of rhesus monkeys in studying reproductive biology in primates.

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.

Secondary sexual coloration and CSF 5‐HIAA are correlated in vervet monkeys (Cercopithecus aethiops sabaeus)

Identifying indirect markers of the physiology or neuroendocrinology of a primate can provide a powerful tool to scientists. Anecdotal descriptions and recent experimental evidence suggests that the colorful sexual skin in adult male vervet monkeys (Cercopithecus aethiops sabaeus) might be sensitive to social changes, including dominance relationships, which could be related to serotonergic activity. The present study examined whether individual differences in scrotal coloration were related to cisternal cerebrospinal fluid concentrations of 5-hydroxyindoleacetic acid (CSF 5-HIAA) in a captive population of vervet monkeys. Darkly colored males had relatively higher CSF 5-HIAA concentrations than paler males, and scrotal color hue was also related CSF 5-HIAA concentrations. These preliminary data are compatible with the hypothesis that scrotal coloration serves as an indirect marker of serotonergic activity. These findings suggest that color assessments might be useful to consider for study design, as well as for animal welfare and captive management.

Development of the sexual skin with pubertal maturation in female chimpanzees

We examined the adolescent development of the sexual skin of chimpanzees (Pan troglodytes) by daily observation, evaluation of swelling, and weekly photogrametry. Although the size of swelling differed with the individual, the development of sexual swelling followed four stages: (1) initial stage, the labial region began to show a slight swelling and recovery; (2) labial stage, swelling at the labial region became maximal; (3) anal stage, another swelling center appeared in the anal region and enlarged; and (4) full maturity stage, the labial and anal regions merged into a full swelling. Menarche occurred after the beginning of the anal stage, and the regular cycle was then established. All of the swelling stages and the peak swelling size are regarded as good indicators of reproductive maturation in chimpanzees.

Females Pay Attention to Female Secondary Sexual Color: An Experimental Study in Macaca mulatta

Researchers have long considered the color of female sexual skin to play a role in attracting or inciting competition among males, or both; however, females may also use color in intrasexual communication. To assess this possibility, we examined whether variation in same-sex sexual skin color is salient to female rhesus macaques (Macaca mulatta). We exposed adult females to computerized images of conspecific female faces and hindquarters manipulated for color (red vs. non-red), within the natural range of color variation. Females visually attended more to both reddened faces and hindquarters over the non-red counterparts. We conclude that female color might be biologically meaningful to other females.