Selective attention toward female secondary sexual color in male rhesus macaques

Pink-to-red anogenital and facial sexual skin occurs in females of many primate species. Since female sexual skin color varies with reproductive state, it has long been assumed that color acts to stimulate male sexual interest. Although there is supportive evidence for this as regards anogenital skin, it is unclear whether this is also the case for facial sexual skin. In this study we experimentally manipulated digital facial and hindquarter images of female rhesus macaques (Macaca mulatta) for color within the natural range of variation. The images were presented to adult male conspecifics to assess whether the males exhibited visual preferences for red vs. non-red female coloration, and whether preferences varied with anatomical region. The males displayed significantly longer gaze durations in response to reddened versions of female hindquarters, but not to reddened versions of faces. This suggests that female facial coloration may serve an alternative purpose to that of attracting males, and that the signal function of sexual skin and the intended recipients may vary across anatomical regions.     

Pregnancy coloration in macaques may act as a warning signal to reduce antagonism by conspecifics

Instances of bright, hormonally induced coloration among females during gestation have been reported in a few reptile and primate genera. Gravid coloration in lizards has been linked to female aggression but the influence of color changes associated with pregnancy has not yet been experimentally pursued for primates. As a first step to determine whether the crimson to magenta hues common to pregnancy coloration in rhesus macaques (Macaca mulatta) contains information, to which conspecifics of either sex attend, we evaluated whether male and female rhesus macaques discriminate between pregnant and non-pregnant female faces. To these ends, we presented 19 adult rhesus macaques with color-manipulated digital images of female faces where pregnancy coloration was present or absent, and measured visual attention and behavioral reactions. Males were significantly more attentive to female faces with pregnancy coloration over those without pregnancy coloration. Both sexes engaged in higher levels of appeasement behavior toward stimulus with pregnancy coloration, and males showing signs of anxiety did so exclusively when exposed to faces with pregnancy coloration. Our results suggest that pregnancy coloration might be an attention grabbing stimulus to males and a warning stimulus to both male and female rhesus macaques. The findings provide a comparative perspective on the use of color in intra-specific communication, and suggest similarity in female similarity in signalling properties in distantly related taxa.     

An experimental examination of female responses to infant face coloration in rhesus macaques

In many primates, infants possess distinctive coloration that changes as a function of age. This colour is thought to serve the purpose of eliciting caretaking behaviour from the mother as well as other conspecifics. The present study investigated the responses of adult female rhesus macaques (Macaca mulatta) to pictures of infant faces in relation to infant age and facial coloration. Study animals were shown digitized images of neonates and 5-6-month-old infants displaying either unaltered facial colour, pink neonatal colour, or novel (green) facial colour. While infant and neonate faces of all colours elicited the attention of adult females, pink neonatal facial coloration did not appear to be especially attractive to subjects in contrast with the findings from an earlier study [Higley, J.D., Hopkins, W.D., Hirsch, R.M. Marra, L.M. Suomi S.J., 1987. Preferences of female rhesus monkeys (Macaca mulatta) for infantile coloration. Dev. Psychobiol. 20, 7-18]. The results suggest that infant facial colour is not particularly important in mediating infant attractiveness to rhesus macaque females as previously suggested or that other infantile facial characteristics might be more important than colour in eliciting caretaking behaviours amongst females.     

Preferences for Symmetry in Conspecific Facial Shape Among Macaca mulatta

In human males and females, bilateral symmetry of facial shape influences assessments of attractiveness. It is possible, however, that other primate species also possess preferences for conspecific facial symmetry. To assess this experimentally, we presented 13 adult rhesus macaques (8 females, 5 males) with computer-manipulated images of symmetrical and asymmetrical versions of opposite-sexed conspecific faces. We utilized looking behavior to assess visual preferences for these factors. We found significant preferences for symmetry, raising the possibility that human preferences for facial symmetry are more deeply rooted in our evolutionary history than previously realized. Our results also have implications for the use of facial shape as a mechanism for attractiveness appraisals across the Primates.     

Testing for links between face color and age,dominance status,parity, weight,and intestinal nematode infection in a sample of female Japanese macaques

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.     

Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration

This study evaluated whether diversity in male ornamental traits between populations is associated with a corresponding diversity in female preferences, or whether males can evolve divergent ornamentation even when female preferences remain relatively consistent. Video editing techniques were used to manipulate the coloration of recorded images of male three-spined sticklebacks, Gasterosteus aculeatus, and these images were presented to female sticklebacks from populations with black or red male nuptial coloration. Overall, females responded preferentially to images of males with black or red coloration over images with the dull coloration of females and some males; although preferences differed between populations, these differences were not statistically significant. Thus divergence in male ornaments was probably not caused by a corresponding divergence in female preferences. The results do not, however, allow clear discrimination between the various hypotheses for the evolution of female mating preferences.     

Cultural differences in preferences for facial coloration

Effects of facial coloration on facial attractiveness judgments are hypothesized to be “universal” (i.e., similar across cultures). Cross-cultural similarity in facial color preferences is a critical piece of evidence for this hypothesis. However, only two studies have directly compared facial color preferences in two cultures. Both of those studies reported that White UK and Black African participants showed similar preferences for facial coloration. By contrast with the cross-cultural similarity reported in those studies, here we show cultural differences in the effects of facial coloration on Chinese and White UK participants' facial attractiveness judgments. While Chinese participants preferred faces with decreased yellowness to faces with increased yellowness, White UK participants preferred faces with increased yellowness to faces with decreased yellowness. Chinese participants also demonstrated weaker preferences for facial redness and stronger preferences for facial lightness than did White UK participants. These results suggest that preferences for facial coloration are not universal.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Females Pay Attention to Female Secondary Sexual Color: An Experimental Study in <Emphasis Type="Italic">Macaca mulatta</Emphasis>

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.     

MHC-assortative facial preferences in humans

Individuals tend to choose mates who are sufficiently genetically dissimilar to avoid inbreeding. As facial attractiveness is a key factor in human mate preference, we investigated whether facial preferences were related to genetic dissimilarity. We asked female volunteers to rate the attractiveness of men from photographs and compared these results with individual genotypes at the major histocompatibility complex (MHC). In contrast to previously reported preferences based on odour, we found a non-significant tendency for women to rate MHC-similar faces as more attractive, suggesting a preference for cues to a self-similar MHC in faces. Further analysis revealed that male faces received higher attractiveness scores when rated by women who were MHC-similar than by MHC-dissimilar women. Although unexpected, this MHC-similar facial preference is consistent with other studies documenting assortative preferences in humans, including for facial phenotype.     

The Costs of Reproductive Success in Male Rhesus Macaques (Macaca mulatta) on Cayo Santiago

Sexual selection acts to increase the success of males possessing advantageous traits in competition over females. In primates, interspecific variability in social and mating systems creates highly variable selective pressures on males, changing the relative strength of both intra- and intersexual selection, and the relative degree of direct vs. indirect male–male competition. Rhesus macaques are an interesting species for studying intrasexual selection and male–male competition, because they exhibit relatively low (for Papionini) body and canine size dimorphism, and exhibit large testes, suggesting reduced direct competition and strong indirect competition. We have undertaken several studies of male rhesus macaques on Cayo Santiago, from analyses of long-term life-history data to shorter term projects that combined noninvasive measures of physiological markers such as concentrations of urinary C-peptide of insulin and androgen and glucocorticoid (GC) concentrations, with measures of behavior and of sexually selected signals (male red facial coloration). We here review these studies, combining data from short-term studies with long-term mortality data to present an integrated picture of both the short- and long-term gross costs of male mating competition. We find that males exhibit many signs of the costs of indirect competition, such as energetic consequences of reduced feeding and high copulation rates. During periods of more direct contest, such as during dominance instability, males are also characterized by high androgen and GC concentrations among high-ranking individuals. Consistent with relatively weak direct male–male competition, male red skin coloration appears to be more related to female choice (intersexual selection) than the signaling of dominance status (intrasexual selection). Forty-five years of life-history data show that male mortality is higher during the mating than the birth season, a pattern we hypothesize to be linked to the costs associated with mating activity. We finish by discussing unresolved issues, such as the costs of sperm competition and the data that are needed to address them.     

Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques

Animals signal their reproductive status in a range of sensory modalities. Highly social animals, such as primates, have access not only to such signals, but also to prior experience of other group members. Whether this experience affects how animals interpret reproductive signals is unknown. Here, we explore whether familiarity with a specific female affects a male's ability to assess that female's reproductive signals. We used a preferential looking procedure to assess signal discrimination in free-ranging rhesus macaques, a species in which female facial luminance covaries with reproductive status. We collected images of female faces throughout the reproductive cycle, and using faecal hormone analysis to determine ovulation, categorized images as coming from a female's pre-fertile, ovulating, or post-fertile period. We printed colour-calibrated stimuli of these faces, reproducing stimuli perceptually the same in colour and luminance to the original appearance of females. These images were presented to males who were either unfamiliar or familiar with stimuli females. Overall, males distinguished ovulatory from pre-ovulatory faces. However, a significant proportion of males did so only among males familiar with stimuli females. These experiments demonstrate that familiarity may increase a receiver's ability to use a social partner's signals to discern their reproductive status.     

Change in male coloration associated with artificial selection on foraging colour preference

Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour‐based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour‐based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour‐based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.     

Fitness correlates of male coloration in a Lake Victoria cichlid fish

Sexual selection by female choice has contributed to the rapidevolution of phenotypic diversity in the cichlid fish speciesflocks of East Africa. Yet, very little is known about the ecologicalmechanisms that drive the evolution of female mating preferences.We studied fitness correlates of male nuptial coloration ina member of a diverse Lake Victoria cichlid lineage, Pundamilianyererei. In this species, male red coloration is subject tointraspecific sexual selection by female mate choice. Male nuptialcoloration plays a critical role also in reproductive isolationbetween this species and the closely related sympatric speciesP. pundamilia. Here, we show that P. nyererei male colorationis carotenoid based, illustrating the potential for honest signalingof individual quality. In a wild population, we found that variationin male coloration was not associated with variation in a setof strongly intercorrelated indicators of male dominance: malesize, territory size, and territory location. Instead, the 2male characters that predominantly determine female choice,territory size and red coloration, may be independent predictorsof male quality: males with bright red coloration and largeterritories had lower parasite infestation rates. As a result,female preferences tended to select against heavily parasitizedmales. Consistent with parasite-mediated sexual selection, maleshad higher and more variable parasite loads than females.     

Sexual Skin Color Contains Information About the Timing of the Fertile Phase in Free-ranging <Emphasis Type="Italic">Macaca mulatta</Emphasis>

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.     

Cross-Cultural Agreement in Facial Attractiveness Preferences: The Role of Ethnicity and Gender

Previous work showed high agreement in facial attractiveness preferences within and across cultures. The aims of the current study were twofold. First, we tested cross-cultural agreement in the attractiveness judgements of White Scottish and Black South African students for own- and other-ethnicity faces. Results showed significant agreement between White Scottish and Black South African observers'' attractiveness judgements, providing further evidence of strong cross-cultural agreement in facial attractiveness preferences. Second, we tested whether cross-cultural agreement is influenced by the ethnicity and/or the gender of the target group. White Scottish and Black South African observers showed significantly higher agreement for Scottish than for African faces, presumably because both groups are familiar with White European facial features, but the Scottish group are less familiar with Black African facial features. Further work investigating this discordance in cross-cultural attractiveness preferences for African faces show that Black South African observers rely more heavily on colour cues when judging African female faces for attractiveness, while White Scottish observers rely more heavily on shape cues. Results also show higher cross-cultural agreement for female, compared to male faces, albeit not significantly higher. The findings shed new light on the factors that influence cross-cultural agreement in attractiveness preferences.     

Phylogenetic Correlation Between Male Nuptial Color and Behavioral Responses to Color Across a Diverse and Colorful Genus of Freshwater Fish (Etheostoma spp., Teleostei: Percidae)

Sexual selection theory predicts that preferences in both sexes select for the elaboration of male nuptial coloration, with empirical evidence supporting these predictions. Empirical studies are often limited in their taxonomic inclusiveness, however, and typically do not examine how male and female preferences contribute to macroevolutionary patterns of male color variation across multiple lineages in a clade. This study examined color preferences in a group of dichromatic freshwater fishes known as darters (genus Etheostoma) that vary in the presence of male coloration. The strengths of attraction to black, blue, gray, and red models were tested in females of 18 species, in addition to males of five species. We found a positive association between the presence of red or orange on the body and the amount of time associating with red models, suggesting color variation is at least in part due to variation in female preferences between species. Males also spent more time associating with colors that most closely resembled conspecifics, suggesting that preferential responses to color in males also can contribute to the diversity of nuptial coloration in darters.     

Female Preferences for Male Vocal and Facial Masculinity in Videos

Vocal and facial masculinity are cues to underlying testosterone in men and influence women’s mate preferences. Consistent with the proposal that facial and vocal masculinity signal common information about men, prior work has revealed correlated female preferences for male facial and vocal masculinity. Previous studies have assessed women’s preferences for male facial and vocal masculinity by presenting faces and voices independently and using static face stimuli. By contrast, here we presented women with short video clips in which male faces and voices were simultaneously manipulated in masculinity. We found that women who preferred masculine faces also preferred masculine voices. Furthermore, women whose faces were rated as relatively more attractive preferred both facial and vocal masculinity more than did women whose faces were rated as less attractive. These findings complement other evidence for cross‐modal masculinity preferences among women and demonstrate that preferences observed in studies using still images and/or independently presented vocal stimuli are also observed when dynamic faces and voices are displayed simultaneously in video format.     

Male red ornamentation is associated with female red sensitivity in sticklebacks

Sexual selection theory proposes correlated evolutionary changes in mating preferences and secondary sexual characters based on a positive genetic correlation between preference and the preferred trait. Empirical work has provided support for a genetic covariation between female preference and male attractiveness in several taxa. Here, we study parent and offspring visual traits in threespine sticklebacks, Gasterosteus aculeatus. While focusing on the proximate basis of mating preferences, we compare the red breeding coloration of males, which strongly contributes to female choice, with their daughters' red sensitivity measured by optomotor response thresholds. We show that the red color expression of fathers correlates well with their daughters' red sensitivity. Given that a within-population genetic correlation between signal and preference was experimentally confirmed for the red coloration in sticklebacks, our results indicate a proximate mechanism in terms of perceptual sensitivity being involved in the co-evolution of female preferences and male mating signals.     

Social correlates of testosterone and ornamentation in male mandrills

We investigated relationships between fecal androgen concentrations, facial coloration and behaviour in semi-free-ranging male mandrills. We found that fecal androgen levels were significantly positively related to dominance rank, independent of rank stability and the mating period, suggesting that male mandrills live in a permanently aggressive context in which they must actively maintain their dominance status. Facial red coloration was also significantly related to both fecal androgen levels and rank, with high ranking males having both higher androgen levels and redder faces, although dominant males did not always have the highest androgen levels or the reddest faces. Predictive relationships between androgen levels, coloration and rank were short-term. Androgen concentrations and facial redness both increased in the presence of receptive females, as did the former during periods of rank instability. We conclude that male facial redness is likely to represent an honest signal (to other males) of current androgen status, competitive ability and willingness to engage in fights and that females may also use this to assess male condition. Further, our findings provide support for the “challenge hypothesis” as originally proposed for birds by Wingfield.