Facial and genital color ornamentation, testosterone, and reproductive output in high-ranking male rhesus macaques.

Males in many vertebrate species have colorful ornaments that evolved by sexual selection. The role of androgens in the genesis and maintenance of these signals is unclear. We studied 21 adult high-ranking male rhesus macaques from nine social groups in the free-ranging population on Cayo Santiago, Puerto Rico, and analyzed facial and genital skin luminance and redness, fecal androgens, rates of mating behaviors, and offspring sired. Facial and genital coloration varied in relation to age, mating behavior, reproductive success, and testosterone concentration. Our results indicate that skin coloration in high-ranking male rhesus macaques is a sexually-selected trait mediated by androgens. These results add to the growing literature on the proximate and ultimate causes of male sexual signals and highlight the need to examine how these characteristics change with age in other species.

Female ornaments: is red skin color attractive to males and related to condition in rhesus macaques?

Sexual selection produces extravagant male traits, such as colorful ornaments, via female mate choice. More rarely, in mating systems in which males allocate mating effort between multiple females, female ornaments may evolve via male mate choice. Females of many anthropoid primates exhibit ornaments that indicate intraindividual cyclical fertility, but which have also been proposed to function as interindividual quality signals. Rhesus macaque females are one such species, exhibiting cyclical facial color variation that indicates ovulatory status, but in which the function of interindividual variation is unknown. We collected digital images of the faces of 32 rhesus macaque adult females. We assessed mating rates, and consortship by males, according to female face coloration. We also assessed whether female coloration was linked to physical (skinfold fat, body mass index) or physiological (fecal glucocorticoid metabolite [fGCM], urinary C-peptide concentrations) condition. We found that redder-faced females were mated more frequently, and consorted for longer periods by top-ranked males. Redder females had higher fGCM concentrations, perhaps related to their increased mating activity and consequent energy mobilization, and blood flow. Prior analyses have shown that female facial redness is a heritable trait, and that redder-faced females have higher annual fecundity, while other evidence suggests that color expression is likely to be a signal rather than a cue. Collectively, the available evidence suggests that female coloration has evolved at least in part via male mate choice. Its evolution as a sexually selected ornament attractive to males is probably attributable to the high female reproductive synchrony found in this species.

Higher early life mortality with lower infant body mass in a free-ranging primate.

Traits that reflect the amount of energy allocated to offspring by mothers, such as infant body mass, are predicted to have long-lasting effects on offspring fitness. In very long-lived species, such as anthropoid primates, where long-lasting and obligate parental care is required for successful recruitment of offspring, there are few studies on the fitness implications of low body mass among infants. Using body mass data collected from 253 free-ranging rhesus macaque Macaca mulatta infants on Cayo Santiago, Puerto Rico, we examined if lower infant body mass predicts lower chance of survival through to reproductive maturation (4th year of life). We also used data on inter-birth intervals and suckling behaviours to determine whether the duration of maternal care was adjusted to infant body mass. Rhesus macaque infants experienced on average 5% reduced hazard of death for an increase in body mass of 0.1 SD (~100 g) above the mean within their age-sex class. The positive association between body mass and early life survival was most pronounced in the 1st year of life. Infant body mass tended to be lower if mothers were young or old, but the link between infant body mass and early life survival remained after controlling for maternal age. This finding suggests that maternal effects on early life survival such as maternal age may act through their influence on infant body mass. Mothers of heavier infants were less likely to be delayed in subsequent reproduction, but the estimated association slightly overlapped with zero. The timing of the last week of suckling did not differ by infant body mass. Using infant body mass data that has been rarely available from free-ranging primates, our study provides comparative evidence to strengthen the existing body of literature on the fitness implications of variation in infant body mass.

Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate.

Sexual selection favours traits that increase reproductive success via increased competitive ability, attractiveness, or both. Male rhesus macaque (Macaca mulatta) morphological traits are likely to reflect the effects of multiple sexual selection pressures. Here, we use a quantitative genetic approach to investigate the production and maintenance of variation in male rhesus macaque morphometric traits which may be subject to sexual selection. We collected measurements of body size, canine length, and fat, from 125 male and 21 female free-ranging rhesus macaques on Cayo Santiago. We also collected testis volumes from males. We used a genetic pedigree to calculate trait heritability, to investigate potential trait trade-offs, and to estimate selection gradients. We found that variation in most male morphometric traits was heritable, but found no evidence of trait trade-offs nor that traits predicted reproductive success. Our results suggest that male rhesus macaque morphometric traits are either not under selection, or are under mechanisms of sexual selection that we could not test (e.g. balancing selection). In species subject to complex interacting mechanisms of selection, measures of body size, weaponry, and testis volume may not increase reproductive success via easily-testable mechanisms such as linear directional selection.

Sexual selection in the Kinda baboon.

Due to wide variation in the presence and degree of expression of a diverse suite of sexually-selected traits, the tribe Papionini represents an outstanding model for understanding how variation in sexual selection pressures and mechanisms leads to trait evolution. Here, we discuss the particular value of Papio as a model genus for studies of sexual selection, emphasizing the presence of multiple mating systems, and differences in the expression of sexually-selected traits among closely-related species. We draw particular attention to the Kinda baboon (Papio kindae), a comparatively less-studied baboon species, by providing a primer to Kinda baboon morphology, genetics, physiology, and behavior. Based on observations of large group sizes, combined with low degrees of sexual dimorphism and large relative testis size relative to other baboon species, we test the hypothesis that Kinda baboons have evolved under reduced direct, and increased indirect, male-male competition. We present the first long-term data on wild Kinda baboons in Zambia. Kinda baboon females show seasonal peaks in births and reproductive receptivity, and males exhibit a queing-rather than contest-based dominance acquisition with long alpha-male tenure lengths. We finish by making a number of explicit testable predictions about Kinda baboon sexual signals and behaviors, and suggest that Kinda baboons have potential to offer new insights into the selective environments that may have been experienced during homininization.

The development of individual differences in cooperative behaviour: maternal glucocorticoid hormones alter helping behaviour of offspring in wild meerkats.

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats ( Suricata suricatta), the circulating glucocorticoid (GC) hormones of pregnant females affect the growth and cooperative behaviour of their offspring. We performed a 3-year experiment in wild meerkats to test the hypothesis that GC-mediated maternal effects reduce the potential for offspring to reproduce directly and therefore cause them to exhibit more cooperative behaviour. Daughters (but not sons) born to mothers treated with cortisol during pregnancy grew more slowly early in life and exhibited significantly more of two types of cooperative behaviour (pup rearing and feeding) once they were adults compared to offspring from control mothers. They also had lower measures of GCs as they aged, which could explain the observed increases in cooperative behaviour. Because early life growth is a crucial determinant of fitness in female meerkats, our results indicate that GC-mediated maternal effects may reduce the fitness of offspring, but may elevate parental fitness as a consequence of increasing the cooperative behaviour of their daughters. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Male immigration triggers increased growth in subordinate female meerkats.

There is increasing evidence that some vertebrates can adjust their growth rate in relation to changes in the social context that affect their probability of breeding. Here, we show that, in meerkats (Suricata suricatta), which are singular cooperative breeders, subordinate females increase in body mass after their father is replaced as the dominant male in their natal group by an immigrant male, giving them regular access to an unfamiliar and unrelated mating partner, while their brothers showed no similar increase nor did subordinate females living in other stable groups (where male immigration did not occur did) in this time period. Moreover, subordinate females showed a greater increase in growth rate when their father was succeeded by an unfamiliar immigrant male than when he was replaced by a familiar male who was already resident. These results suggest that female meerkats can adjust their rate of growth to changes in the kinship composition of their groups that provide them with increased access to unrelated breeding partners, which may occur in other mammals as well when breeding opportunities change.

Experimental evidence that female rhesus macaques (Macaca mulatta) perceive variation in male facial masculinity.

Among many primate species, face shape is sexually dimorphic, and male facial masculinity has been proposed to influence female mate choice and male-male competition by signalling competitive ability. However, whether conspecifics pay attention to facial masculinity has only been assessed in humans. In a study of free-ranging rhesus macaques, Macaca mulatta, we used a two-alternative look-time experiment to test whether females perceive male facial masculinity. We presented 107 females with pairs of images of male faces-one with a more masculine shape and one more feminine-and recorded their looking behaviour. Females looked at the masculine face longer than at the feminine face in more trials than predicted by chance. Although there was no overall difference in average look-time between masculine and feminine faces across all trials, females looked significantly longer at masculine faces in a subset of trials for which the within-pair difference in masculinity was most pronounced. Additionally, the proportion of time subjects looked toward the masculine face increased as the within-pair difference in masculinity increased. This study provides evidence that female macaques perceive variation in male facial shape, a necessary condition for intersexual selection to operate on such a trait. It also highlights the potential impact of perceptual thresholds on look-time experiments.

The influence of stress hormones and aggression on cooperative behaviour in subordinate meerkats.

In cooperative breeders, aggression from dominant breeders directed at subordinates may raise subordinate stress hormone (glucocorticoid) concentrations. This may benefit dominants by suppressing subordinate reproduction but it is uncertain whether aggression from dominants can elevate subordinate cooperative behaviour, or how resulting changes in subordinate glucocorticoid concentrations affect their cooperative behaviour. We show here that the effects of manipulating glucocorticoid concentrations in wild meerkats (Suricata suricatta) on cooperative behaviour varied between cooperative activities as well as between the sexes. Subordinates of both sexes treated with a glucocorticoid receptor antagonist (mifepristone) exhibited significantly more pup protection behaviour (babysitting) compared to those treated with glucocorticoids (cortisol) or controls. Females treated with mifepristone had a higher probability of exhibiting pup food provisioning (pup-feeding) compared to those treated with cortisol. In males, there were no treatment effects on the probability of pup-feeding, but those treated with cortisol gave a higher proportion of the food they found to pups than those treated with mifepristone. Using 19 years of behavioural data, we also show that dominant females did not increase the frequency with which they directed aggression at subordinates at times when the need for assistance was highest. Our results suggest that it is unlikely that dominant females manipulate the cooperative behaviour of subordinates through the effects of aggression on their glucocorticoid levels and that the function of aggression directed at subordinates is probably to reduce the probability they will breed.

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.

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 observer's 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.

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 individual's 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.

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 inter-sexual 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 towards 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 socio-sexual behaviors towards 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.

Variance in male lifetime reproductive success and estimation of the degree of polygyny in a primate.

The degree of polygyny is predicted to influence the strength of direct male-male competition, leading to a high variance in male lifetime reproductive success and to reproduction limited to the prime period of adulthood. Here, we explore the variance in male lifetime reproductive success and reproductive time in an anthropoid primate forming multimale-multifemale groups. Males of this species form dominance hierarchies, which are expected to skew reproduction toward few high-ranking males. At the same time, however, females mate with multiple males (polygynandry), which should limit the degree of polygyny. Using 20 years of genetic and demographic data, we calculated lifetime reproductive success for the free-ranging rhesus macaque (Macaca mulatta) population of Cayo Santiago for subjects that died naturally or reached senescence. Our results show that 1) male lifetime reproductive success was significantly skewed (range: 0-47 offspring; males reproducing below average: 62.8%; nonbreeders: 17.4%), 2) variance in male lifetime reproductive success was 5 times larger than in females, and 3) male lifetime reproductive success was more influenced by variation in fecundity (60%) than longevity (25%), suggesting that some direct male-male competition takes place. However, the opportunity for selection (i.e., standardized variance in male lifetime reproductive success) is low compared with that in other large mammal species characterized by a high degree of polygyny. Moreover, male reproductive life extended much beyond the prime period, showing that physical strength was not required to acquire mates. We conclude that rhesus macaques exhibit a moderate degree of polygyny and, therefore, low levels of direct male-male competition for fertile females, despite the fact that males form linear dominance hierarchies.

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.

Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques?

In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogen-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30-40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females' fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.

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.

Testing the priority-of-access model in a seasonally breeding primate species.

In mammals, when females are clumped in space, male access to receptive females is usually determined by a dominance hierarchy based on fighting ability. In polygynandrous primates, as opposed to most mammalian species, the strength of the relationship between male social status and reproductive success varies greatly. It has been proposed that the degree to which paternity is determined by male rank decreases with increasing female reproductive synchrony. The priority-of-access model (PoA) predicts male reproductive success based on female synchrony and male dominance rank. To date, most tests of the PoA using paternity data involved nonseasonally breeding species. Here, we examine whether the PoA explains the relatively low reproductive skew in relation to dominance rank reported in the rhesus macaque, a strictly seasonal species. We collected behavioral, genetic, and hormonal data on one group of the free-ranging population on Cayo Santiago (Puerto Rico) for 2 years. The PoA correctly predicted the steepness of male reproductive skew, but not its relationship to male dominance: the most successful sire, fathering one third of the infants, was high but not top ranking. In contrast, mating success was not significantly skewed, suggesting that other mechanisms than social status contributed to male reproductive success. Dominance may be less important for paternity in rhesus macaques than in other primate species because it is reached through queuing rather than contest, leading to alpha males not necessarily being the strongest or most attractive male. More work is needed to fully elucidate the mechanisms determining paternity in rhesus macaques.