Constance Dubuc

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.

Social capital and physiological stress levels in free-ranging adult female rhesus macaques.

Social animals with greater access to social support, i.e. higher levels of social capital, may be able to cope better with the challenges they face in their day-to-day lives, and this may be reflected in lower physiological stress levels. Here, we examine the relationship between social capital and fecal glucocorticoid (GC) levels in pregnant free-ranging adult female rhesus macaques. In addition to social capital measures based on direct connections between social partners, which have been examined previously, we use social network analysis to generate measures of social capital based on indirect connections (i.e. connections between pairs of individuals which result from their mutual direct connection to a third party). We consider social capital based on three different types of affiliative association: grooming, the exchange of affiliative vocalizations and proximity. After controlling for variables known to affect GC output in primates (e.g. month of pregnancy), GC levels of females were significantly predicted by a social network measure of indirect connectedness in the proximity network, proximity reach, in interaction with dominance rank. High ranking females had significantly lower GC levels in months in which they had low levels of proximity reach (i.e. in months in which their proximity networks were smaller and therefore more focused). The results of our study add to a growing body of evidence which suggests that social capital may be an important means by which gregarious animals cope with day-to-day challenges. Our study also joins a small body of recent research which has demonstrated that indirect connections may be important factors in the lives of social animals.

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 males ability to assess that females 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 females 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 receivers ability to use a social partners signals to discern their reproductive status.

Is male rhesus macaque red color ornamentation attractive to females

Male sexually selected traits can evolve through different mechanisms: conspicuous and colorful ornaments usually evolve through intersexual selection, while weapons usually evolve through intra-sexual selection. Male ornaments are rare among mammals in comparison to birds, leading to the notion that female mate choice generally plays little role in trait evolution in this taxon. Supporting this view, when ornaments are present in mammals, they typically indicate social status and are products of male-male competition. This general mammalian pattern, however, may not apply to rhesus macaques (Macaca mulatta). Males of this species display conspicuous skin coloration, but this expression is not correlated to dominance rank and is therefore unlikely to have evolved due to male-male competition. Here, we investigate whether male color expression influences female proceptivity toward males in the Cayo Santiago free-ranging rhesus macaque population. We collected face images of 24 adult males varying in dominance rank and age at the peak of the mating season and modeled these to rhesus macaque visual perception. We also recorded female sociosexual behaviors toward these males. Results show that dark red males received more sexual solicitations, by more females, than pale pink ones. Together with previous results, our study suggests that male color ornaments are more likely to be a product of inter- rather than intra-sexual selection. This may especially be the case in rhesus macaques due to the particular characteristics of male-male competition in this species.

Sexually selected skin colour is heritable and related to fecundity in a non-human primate

Sexual selection promotes the prevalence of heritable traits that increase an individuals reproductive rate. Despite theoretically strong directional selection, sexually selected traits can show inter-individual variation. Here, we investigate whether red skin ornamentation, a rare example of a male mammalian trait involved in mate attraction, influences fecundity and is heritable in rhesus macaques (Macaca mulatta), and explore the mechanisms that are involved in maintaining trait variation. Interestingly, the trait is expressed by and is attractive to both sexes. We collected facial images of 266 free-ranging individuals and modelled skin redness and darkness to rhesus macaque vision. We used 20 years of genetic parentage data to calculate selection gradients on the trait and perform heritability analyses. Results show that males who were both darkly coloured and high-ranking enjoyed higher fecundity. Female skin redness was positively linked to fecundity, although it remains unclear whether this influences male selectiveness. Heritability explained 10–15% of the variation in redness and darkness, and up to 30% for skin darkness when sexes are considered separately, suggesting sex-influenced inheritance. Our results suggest that inter-individual variation is maintained through condition-dependence, with an added effect of balancing selection on male skin darkness, providing rare evidence for a mammalian trait selected through inter-sexual selection.

Social tolerance in a despotic primate: co-feeding between consortship partners in rhesus macaques.

Food sharing among nonkin-one of the most fascinating cooperative behaviors in humans-is not widespread in nonhuman primates. Over the past few years, a large body of work has investigated the contexts in which primates cooperate and share food with unrelated individuals. This work has successfully demonstrated that species-specific differences in temperament constrain the extent to which food sharing emerges in experimental situations, with despotic species being less likely to share food than tolerant ones. However, little experimental work has examined the contexts that promote food sharing and cooperation within a species. Here, we examine whether one salient reproductive context-the consortship dyad-can allow the necessary social tolerance for co-feeding to emerge in an extremely despotic species, the rhesus macaque (Macaca mulatta). We gave naturally formed male-female rhesus macaque pairs access to a monopolizable food site in the free-ranging population at Cayo Santiago, Puerto Rico. Using this method, we were able to show that tolerated co-feeding between unrelated adults can take place in this despotic species. Specifically, our results show that consort pairs co-fed at the experimental food site more than nonconsort control pairs, leading females to obtain more food in this context. These results suggest that co-feeding is possible even in the most despotic of primate species, but perhaps only in contexts that specifically promote the necessary social tolerance. Researchers might profit from exploring whether other kinds of within-species contexts could also generate cooperative behaviors.

Effect of mating activity and dominance rank on male masturbation among free-ranging male rhesus macaques.

The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non-human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale-multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non-functional by-product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free-ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower-ranking males mated less and tended to masturbate more frequently than higher-ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.

Who cares? Experimental attention biases provide new insights into a mammalian sexual signal

The effects of intrasexual and intersexual selection on male trait evolution can be difficult to disentangle, especially based on observational data. Male-male competition can limit an observers ability to identify the effect of female mate choice independently from sexual coercion. Here, we use an experimental approach to explore whether an ornament, the red facial skin exhibited by male rhesus macaques (Macaca mulatta), might be involved in both female mate choice and male-male competition. We used a noninvasive experimental approach based on the looking time paradigm in a free-ranging setting, showing images of differently colored male faces to both adult females (N = 91) and males (N = 77), as well as to juveniles (N = 94) as a control. Results show that both adult females and males looked longer at dark red faces compared with pale pink ones. However, when considering the proportion of subjects that looked longer at dark red faces regardless of preference strength, only females showed a significant dark red bias. In contrast, juveniles did not show any preferences between stimuli, suggesting that the adult bias is not a consequence of the experimental design or related to a general sensory bias for red coloration among all age-sex classes. Collectively, these results support the role the ornament plays in female mate choice in this species and provide the first evidence that this ornament may play a role in male-male competition as well, despite a general lack of observational evidence for the latter effect to date.

Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals

Primate trichromatic colour vision has been hypothesized to be well tuned for detecting variation in facial coloration, which could be due to selection on either signal wavelengths or the sensitivities of the photoreceptors themselves. We provide one of the first empirical tests of this idea by asking whether, when compared with other visual systems, the information obtained through primate trichromatic vision confers an improved ability to detect the changes in facial colour that female macaque monkeys exhibit when they are proceptive. We presented pairs of digital images of faces of the same monkey to human observers and asked them to select the proceptive face. We tested images that simulated what would be seen by common catarrhine trichromatic vision, two additional trichromatic conditions and three dichromatic conditions. Performance under conditions of common catarrhine trichromacy, and trichromacy with narrowly separated LM cone pigments (common in female platyrrhines), was better than for evenly spaced trichromacy or for any of the dichromatic conditions. These results suggest that primate trichromatic colour vision confers excellent ability to detect meaningful variation in primate face colour. This is consistent with the hypothesis that social information detection has acted on either primate signal spectral reflectance or photoreceptor spectral tuning, or both.

Is male rhesus macaque facial coloration under intrasexual selection

Exaggerated male traits can evolve under intra- or intersexual selection, but it remains less clear how often both mechanisms act together on trait evolution. While the males of many anthropoid primate species exhibit colorful signals that appear to be badges of status under intrasexual selection, the red facial coloration of male rhesus macaques (Macaca mulatta) appears to have evolved primarily under intersexual selection and female mate choice. Nonetheless, experiments show that red color is salient to males, raising the question of whether the signal may also be under intrasexual selection. Here, we examine whether males express this signal more strongly in competitive contexts. Facial images were collected on all 15 adult males of a free-ranging social group during the peak of the mating season, and coloration was quantified using visual models. Results show that males more similar in facial redness were more likely to interact aggressively than more dissimilar ones, suggesting that color may be involved in the assessment of rivals. Furthermore, males exhibited darker coloration on days they were observed copulating, and dominance rank predicted facial redness only on copulating days, suggesting that coloration may also advertise motivation to defend a mate. Male rhesus macaque facial coloration may thus mediate agonistic interactions with rivals during competition over reproductive opportunities, such that it is under both inter- and intrasexual selection. However, color differences were small, raising perceptibility questions. It remains possible that color variation reflects differences in male condition, which in turn alter investment towards male-male competition and mating effort.