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On-site analysis of volatile organic compounds (VOCs) with miniaturized gas chromatography–mass spectrometry (GC–MS) systems is a very rapidly developing field of application. While, on the one hand, major technological advances are improving the availability of these systems on the market, on the other hand, systematic studies to assess the performance of such instruments are still lacking. To fill this gap, we compared three portable GC–MS devices to a state-of-the-art benchtop (stationary) system for analysis of a standard mixture of 18 VOCs. We systematically compared analytical parameters such as the sensitivity and similarity of the signal response pattern and the quality of the obtained mass spectra. We found that the investigated mobile instruments (i) showed different response profiles with a generally lower number of identified analytes. Also, (ii) mass spectral reproducibility (% relative standard deviation (RSD) of the relative abundance of selective fragments) was generally worse in the mobile devices (mean RSD for all targeted fragments ~9.7% vs. ~3.5% in the stationary system). Furthermore, mobile devices (iii) showed a poorer mass spectral similarity to commercial reference library spectra (>20% deviation of fragment ion relative intensity vs. ~10% in the stationary GC–MS), suggesting a less reliable identification of analytes by library search. Indeed, (iv) the performance was better with higher-mass and/or more abundant fragments, which should be considered to improve the results of library searches for substance identification. Finally, (v) the estimation of the signal-to-noise ratio (S/N) in mobile instruments as a measure of sensitivity revealed a significantly lower performance compared to the benchtop lab equipment (with a ratio among medians of ~8 times lower). Overall, our study reveals not only a poor signal-to-noise ratio and poor reproducibility of the data obtained from mobile instruments, but also unfavorable results with respect to a reliable identification of substances when they are applied for complex mixtures of volatiles. Graphical Abstract

Most catarrhine primates are considered to be strongly visually oriented animals, obtaining information about conspecifics and their environment from a diversity of visual cues. Other sensory modalities may provide information that is redundant and/or complimentary to visual cues. When cues from multiple sensory modalities are available, these may reinforce or suppress each other, as shown in a range of taxa from insects to humans. In the present study, we tested how the presence and ambiguity of visual information affects the use of olfactory cues when exploring food and non-food items in semi-free ranging Barbary macaques at Affenberg Salem, Germany. In experiment 1, we presented monkeys with pipes containing food (peanuts, popcorn), non-food (stones, feces) or no items. The ends of the pipes were either transparent or opaque, and we assessed whether animals looked, sniffed and/or grabbed into the pipes depending on visibility of the contents. In experiment 2, we manipulated the visual appearance of familiar food items (popcorn) with food colorant and scored if monkeys sniffed at and/or ate the popcorn depending on whether it was uncolored or dyed. In both experiments, the available visual information modulated sniffing behavior. Both visual as well as olfactory information further affected, whether or not monkeys attempted to retrieve the items from the pipes in experiment 1, while data were insufficient to assess this in experiment 2. Hence, reliance on the olfactory sense was modulated by the available visual information, emphasizing the interplay between different sensory modalities for obtaining information about the environment.

In areas where primates are threatened, environmental education interventions are a key way to increase the local population’s knowledge of their environment and encourage positive attitudes and habits to preserve the environment and wildlife on a local and global scale. This study assesses the impact of Tangkoko Conservation Education (TCE), the Macaca Nigra Project’s conservation education programme, running since 2011 in North Sulawesi for school children, teachers, and the local population. TCE’s goal is to help people increase their knowledge of their environment and develop more positive habits and behaviours towards their local environment, especially the Critically Endangered and endemic crested macaques (Macaca nigra). We measured the efficacy of TCE’s programme for pupils using questionnaires provided one month before and one month after a year-long conservation education programme at school. Pupils’ knowledge and behaviour scores increased significantly after their participation in the programme. Their habits score also increased but this increase was not statistically significant. Girls scored significantly higher than boys in terms of positive behaviour towards wildlife. Children participating in the programme more than once seemed to obtain higher scores in their second participation, although the sample size was too small for formal analysis. Despite some limitations, this study demonstrates the positive impact of our programme on young people living in an area where primates are threatened. We hope that this research will inspire similar programmes in Sulawesi and elsewhere by providing methods and activities to help prevent primate extinction.

Olfaction is one of the evolutionarily oldest senses and plays a fundamental role in foraging and social interactions across mammals. In primates, the role of olfaction is now well recognized, but better investigated in strepsirrhine and platyrrhine primates than in catarrhine primate species. We therefore observed the sniffing behavior of semi-free ranging Barbary macaques,Macaca sylvanus, at Affenberg Salem, Germany, to assess how frequently macaques use olfaction and in which contexts, and how olfaction is affected by sex and age. Focal observations of 24 males and 24 females aged 1 to 25 years showed that Barbary macaques sniffed, on average, 5.3 times per hour, with more than 80% of sniffs directed at food. Irrespective of the context, younger individuals used olfaction more often than older ones. Females sniffed more often on food than males did, while males used olfaction more often in a social context than females did. Sniffs at conspecifics primarily occurred in a sexual context, with 70% of social sniffs directed at female anogenital swellings performed by males. Of the observed 176 anogenital inspections, 51 involved sniffing of the swelling. Olfactory inspections were followed by copulation significantly less often than merely visual inspections, suggesting that anogenital odors provided additional information guiding male mating decisions. In sum, results show that Barbary macaques routinely use olfaction during feeding, but also in a social context. Our study further suggests that odors may guide mating decisions, but the role of olfaction in sexual interactions warrants further investigations.

Coalition formation is one of the most striking forms of cooperation found in animals. Yet, there is substantial variation between taxa regarding the mechanisms by which coalitions can result in fitness consequences. Here, we investigate the influence of coalitions on dominance rank trajectories and subsequently on reproductive success in wild male crested macaques ( Macaca nigra ) at Tangkoko Nature Reserve (Sulawesi, Indonesia). We observed 128 coalition events involving 28 males and tested how a variety of coalition properties and factors related to the social environment influenced future male rank. We further used genetic paternity analysis of 19 infants conceived during the study to assess male reproductive success. Our results show that males participating in coalitions achieved higher-than-expected future ranks, while coalition targets had lower-than-expected future ranks. Additionally, all-up coalitions had stronger effects on rank than all-down and bridging coalitions, and these were modulated by the relative strength of coalition partners versus targets. Finally, higher ranking males were more likely to sire infants than lower ranking males. These results provide important insights regarding the mechanisms underlying coalition formation and support the idea that one major path by which coalitions can affect fitness is through influencing male dominance trajectories.

The ability to innovate and the social transmission of innovations have played a central role in human evolution. However, innovation is also crucial for other animals, by allowing them to cope with novel socioecological challenges. Although innovation plays such a central role in animals’ lives, we still do not know the conditions required for innovative behaviour to emerge. Here, we focused on interindividual differences in innovation by (1) extensively reviewing existing literature on innovative behaviour in animals and (2) quantitatively testing the different evolutionary hypotheses that have been proposed to explain interindividual variation in innovation propensity during foraging tasks. We ran a series of phylogenetically controlled mixed-effects meta-regression models to determine which hypotheses (if any) are supported by currently available empirical studies. Our analyses show that innovation is more common in individuals that are older and belong to the larger sex, but also in more neophilic and/or explorative individuals. Moreover, these effects change depending on the study setting (i.e. wild versus captive). Our results provide no clear support to the excess of energy or the bad competitor hypotheses and suggest that study setting and interindividual differences in traits related to personality are also important predictors of innovation.

Non-human primates show an impressive behavioral diversity, both across and within species. However, the factors explaining intra-specific behavioral variation across groups and individuals are yet understudied. Here, we aimed to assess how group size and living conditions (i.e., captive, semi-free-ranging, wild) are linked to behavioral variation in 5 groups of Barbary macaques (N=137 individuals). In each group, we collected observational data on the time individuals spent in social interactions and on the group dominance style, along with experimental data on social tolerance over food and neophobia. Our results showed that differences in group size predicted differences in the time spent in social interactions, with smaller groups spending a higher proportion of time in close spatial proximity, but a lower proportion of time grooming. Moreover, group size predicted variation in dominance style, with smaller groups being more despotic. Social tolerance was affected by both group size and living conditions, being higher in smaller groups and in groups living in less natural conditions. Finally, individual characteristics also explained variation in social tolerance and neophobia, with socially integrated individuals having higher access to food sources, and higher-ranking ones being more neophobic. Overall, our results support the view that intra-specific variation is a crucial aspect in primate social behavior and call for more comparative studies to better understand the sources of within-species variation.

Este artículo se encuentra disponible en la siguiente URL: https://www.nature.com/articles/s41598-020-79246-6.pdf En este artículo también participan: Karimullah Karimullah, Risma Illa Maulany, Putu Oka Ngakan, Andi Siady Hamzah y Bonaventura Majolo. Primates live in complex social systems with social structures ranging from more to less despotic. In less despotic species, dominance might impose fewer constraints on social choices, tolerance is greater than in despotic species and subordinates may have little need to include novel food items in the diet (i.e. neophilia), as contest food competition is lower and resources more equally distributed across group members. Here, we used macaques as a model to assess whether different dominance styles predict differences in neophilia and social tolerance over food. We provided familiar and novel food to 4 groups of wild macaques (N = 131) with different dominance styles (Macaca fuscata, M. fascicularis, M. sylvanus, M. maura). Our study revealed inter- and intra-specific differences in individuals’ access to food, which only partially reflected the dominance styles of the study subjects. Contrary to our prediction, social tolerance over food was higher in more despotic species than in less despotic species. Individuals with a higher dominance rank and being better socially integrated (i.e. higher Eigenvector centrality) were more likely to retrieve food in all species, regardless of their dominance style. Partially in line with our predictions, less integrated individuals more likely overcame neophobia (as compared to more integrated ones), but only in species with more tolerance over food. Our study suggests that individual characteristics (e.g. social integration or personality) other than dominance rank may have a stronger effect on an individual’s access to resources.

Human-induced habitat alterations globally threaten animal populations, often evoking complex behavioural responses in wildlife. This may be particularly dramatic when negatively affecting social behaviour, which fundamentally determines individual fitness and offspring survival in group-living animals. Here, we provide first evidence for critical behavioural modifications in sociality of Southern pig-tailed macaques visiting Malaysian oil palm plantations in search of food. Specifically, we found significant reductions of positive social interactions, an increase of aggression and shifts in the macaques' social network structure, with the central positions of high-ranking adult females and immatures being passed to low-ranking individuals, likely resulting from socio-ecological risks posed by plantations. Deviations from natural behaviour also affected the smallest but crucial social units within groups, mother-infant pairs, with increased maternal protectiveness at plantations. We suggest that although primates can persist in human-altered habitats, their ability to adapt comes with a trade-off for their natural sociality, potentially hampering infant development and individual survival. Studies like ours remain critical for understanding species’ adaptability to anthropogenic landscapes, which may ultimately contribute to facilitating their coexistence with humans and preserving biodiversity.

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.

Extragroup paternity (EGP) is found across a wide range of species and may entail reproductive benefits, but may also entail costs to both sexes. While population and group parameters affecting the degree of EGPs are relatively well established, less is known about the individual characteristics that make males and females engage in alternative reproductive tactics such as EGP. Applying a combination of long-term demographic and genetic data from the rhesus macaque population of Cayo Santiago (Puerto Rico, U.S.A.), we investigate which male and female characteristics influence the probability of EGP to better understand the circumstances that shape the distribution and occurrence of EGP. Our results show that, against our expectations, higher-ranking females were more likely to produce EGP offspring than lower- ranking females. The probability of producing extragroup offspring was not significantly related to female or male age, male tenure or previous reproductive success. Furthermore, genetic relatedness between the parents did not affect the production of extragroup offspring, but extragroup offspring were more frequently produced early rather than late in a given mating season. Altogether, our analysis suggests that individual attributes and seasonal aspects create different opportunities and preferences for engaging in EGP as an alternative reproductive tactic. The observed patterns of EGP in rhesus macaques appear to be consistent with female mate choice for genetic benefits, which needs to be confirmed in future studies.

Summary 1. Olfaction is a central aspect of mammalian communication, providing information about individual attributes such as identity, sex, group membership or genetic quality. Yet, the chemical underpinnings of olfactory cues remain little understood, one of the reasons being the difficulty in obtaining high quality samples for chemical analysis. 2. In the present study we adjusted and evaluated the use of thermal desorption (TD) tubes, commonly used in plant metabolomic and environmental studies, for non-invasive sampling of mammalian body odour. We obtained chemical profiles of meerkat (Suricata suricatta) body odour samples using TD tubes analysed with gas chromatography – mass spectrometry (GC-MS). 3. TD tubes captured a wide range of volatile and semi-volatile organic compounds including compounds likely originating from the target animals. Adjustment of sampling parameters (distance, volume, flow rate, interruption of sampling) to increase the feasibility for a non-invasive application yielded samples of adequate quality. However, to minimize the variability between samples, sampling parameters should be kept constant and samples should be collected when no conspecifics are close-by. 4. The method was sensitive enough to pick up population differences in the chemical profiles of two captive groups of meerkats, demonstrating its applicability to biological questions. With sufficiently habituated animals, the method is applicable non-invasively, allowing short- and long-term studies on a wide range of questions, including e.g. chemical signatures of kinship, diet, individual health or reproductive state. This article is protected by copyright. All rights reserved.

Genetic analyses based on noninvasively collected samples have become an important tool for evolutionary biology and conservation. Crested macaques (Macaca nigra), endemic to Sulawesi, Indonesia, are important for our understanding of primate evolution as Sulawesi macaques represent an exceptional example of primate adaptive radiation. Crested macaques are also Critically Endangered. However, to date we know very little about their genetics. The aim of our study was to find and validate microsatellite markers useful for evolutionary, conservation, and other genetic studies on wild crested macaques. Using fecal samples of 176 wild macaques living in the Tangkoko Reserve, Sulawesi, we identified 12 polymorphic microsatellite loci through cross-species polymerase chain reaction amplification with later modification of some of these primers. We tested their suitability by investigating and exploring patterns of paternity, observed heterozygosity, and evidence for inbreeding. We assigned paternity to 63 of 65 infants with high confidence. Among cases with solved paternity, we found no evidence of extragroup paternity and natal breeding. We found a relatively steep male reproductive skew B index of 0.330 ± 0.267; mean ± SD) and mean alpha paternity of 65% per year with large variation across groups and years (29–100%). Finally, we detected an excess in observed heterozygosity and no evidence of inbreeding across our three study groups, with an observed heterozygosity of 0.766 ± 0.059 and expected heterozygosity of 0.708 ± 0.059, and an inbreeding coefficient of −0.082 ± 0.035. Our results indicate that the selected markers are useful for genetic studies on wild crested macaques, and possibly also on other Sulawesi and closely related macaques. They further suggest that the Tangkoko population of crested macaques is still genetically variable despite its small size, isolation, and the species’ reproductive patterns. This gives us hope that other endangered primate species living in small, isolated populations may also retain a healthy gene pool, at least in the short term. Electronic supplementary material The online version of this article (doi:10.1007/s10764-017-9973-x) contains supplementary material, which is available to authorized users.

Although personality has been widely studied among animal species, only a few studies have investigated the long-term development of personality during early ontogeny. In fact, no study of nonhuman primates has consistently mapped personality development from birth to adulthood. Our study aimed at closing this gap by examining the development of personality among free-ranging rhesus macaques, Macaca mulatta, using longitudinal behavioural data of 24 subjects (3758 h) collected from birth to 7 years of age on the island of Cayo Santiago, Puerto Rico, U.S.A. In our analyses we combined different frameworks of animal personality research to discuss behavioural differences in terms of latent personality models, behavioural syndromes and behavioural characters. The results showed that a core model of rhesus macaque personality, comprising three latent factors (Fearfulness, Aggression, Sociability), can already be established over the course of the first 7 years of life. However, only Fearfulness emerged consistently throughout development. While the factor of Sociability diffused during maturation, Aggression stabilized towards adulthood after having inconsistent loadings during infancy. When assessing correlations among behaviours separately on the within- and between-individual level, again only Fearfulness showed significant results averaged over the entire study period and can therefore be classified as behavioural syndrome or behavioural character. We discuss differences in correlations, interactions between sex and age and the effect of maternal rank as potential source of differences in stability of latent traits. Furthermore, we assessed plasticity of behaviour with regard to first maternity in females and natal dispersal of males. While the latter was accompanied by an increase of fearful behaviour and decrease of physical aggression, first maternity was marked by a mixed pattern of changes. Overall, our results suggest that rhesus macaques are not born into their personality, but grow into it.

It is now well established that sociality plays a crucial role in primates. For example, among non-human primates, individuals with strong social bonds significantly increase their fecundity, reproductive success, offspring survival and longevity. Also in humans, social integration positively affects psychological stress, health and survival. However, despite the evidence that sociality is a fundamental fitness trait, relatively little is known about how sociality develops. Previous studies are mainly limited to the development of human sociality in Western cultures. Hence, to increase our knowledge about important human developmental milestones, an inter-specific and inter-cultural approach is needed. In particular, to understand the evolutionary roots of human sociality, studies on non-human primates are of large importance. The present Topical Collection is divided into four parts addressing (i) the effect of main bonding partners (mothers, siblings, peers) on social development in non-human primates; (ii) other factors affecting social development, such as sex differences, genetic constraints and personality; (iii) how social cognition and multimodal communication develop through early life in non-human primates and (iv) how human sociality develops through ontogeny, with a special focus on cross-cultural differences. In this paper, we introduce the development of sociality from an evolutionary perspective, briefly summarise each contribution of this Topical Collection and close with possible future directions. We aim to summarise the current state of research on the development of primate sociality, stimulate inter-disciplinary research and provide insight into the outstanding variability in social development across non-human primate species and human cultures. This paper opens a Topical Collection on the development of primate sociality. Here, we introduce the topic, summarise contributions to this collection and outline future directions. To understand the evolutionary roots of human sociality, we consider the social development across different non-human primate species and human cultures.

Fast active sampling of volatile organic compounds (VOCs) under field conditions still is a great challenge especially when the exposure time to the source of emissions is a restricting factor. Hence, to identify ideal conditions for such applications, we systematically compared fast active sampling of VOCs collected on two common adsorbents under two regimes: first, very low gas volumes (from 300 mL) sampled at nominal flow rate and, second, sampling at the maximal applicable flow rate (0.5 L/min) before loss of sorbent material was experienced. For XAD-2 and Tenax TA, efficient sorbents for on-site VOC-sampling followed by thermal desorption GC–MS, significant differences in the signal response of volatile compounds were related not only to the varied experimental factors alone, but also to their interactions and to compound volatility. In the first regime, volatiles (∼0.004–3.13 mM) from Tenax TA gave the highest signal response only above 800 mL sampled gas volume while at low concentrations (∼0.004–0.12 mM), satisfactory recovery from XAD-2 required longer analyte-sorbent interaction. For the second regime, the relative recovery was severely impaired down to 73 ± 23%, n = 56 for Tenax TA and 72 ± 17%, n = 56 for XAD-2 at intermediate concentration, and 79 ± 11%, n = 84 for Tenax TA at high concentration compared to the relative recovery at standard flow rate. Neither Tenax TA nor XAD-2 provided a 100% total recovery (calculated using breakthrough values) for any of the evaluated compounds. Finally, two-way and three-way interactions identified in a multi-variable model, explained not only the dependence of the signal response on different experimental variables, but also their complex interplay affecting the recovery of the VOCs. In conclusion, we show for the first time that XAD-2, a material only recently introduced for the adsorption of volatiles from the gas phase, competes well with the standard material Tenax TA under conditions of fast sampling. Due to the similar absolute recovery with Tenax TA even at low concentration and with regard to the better detection limits, we consider XAD-2 the better choice for fast sampling of VOCs, particularly with low sample volumes at regular flow. For fast sampling with high flow rate, however, both sorbents might be selected only if the corresponding recovery loss can be accepted for the study.

Preferential affiliative relationships, or social bonds, play a crucial role in primate social life, but little is known about their development. Here, we review macaque studies investigating the social development of both sexes. Firstly, we highlight the emergence of sex differences in mother–offspring bonds, as macaque mothers form stronger bonds with daughters, while being more aggressive towards sons, possibly contributing to maintain female philopatry and/or male dispersal. Secondly, despite paternity uncertainty, we discuss studies reporting that fathers of several macaque species preferentially engage with their offspring, but less than mothers and only in periods of high infant mortality. Thirdly, we show that immature females, the philopatric sex in macaques, already form stronger bonds with close maternal kin than immature males, mirroring social patterns during adulthood. However, this bias seems not caused by kin availability, as kin availability is similar for both sexes prior to male dispersal. Moreover, immature males might preferentially affiliate with paternal kin over non-kin, possibly because of lower maternal integration in their maternal family and/or in preparation of dispersal. Fourthly, we discuss how immature females engage in grooming and proximity with female partners as they grow older, while immature males preferentially interact with adult males and peers, playing more than females from early on. Finally, we show that most developmental changes in sociality happen around 2–3 years of age, probably representing a milestone in macaque social development. We conclude that sex differences in sociality emerge early in development and increase through time, with sexes gradually growing into their adult roles.

Extragroup paternity (EGP) is found across a wide range of species and may entail reproductive benefits, but may also entail costs to both sexes. While population and group parameters affecting the degree of EGPs are relatively well established, less is known about the individual characteristics that make males and females engage in alternative reproductive tactics such as EGP. Applying a combination of long-term demographic and genetic data from the rhesus macaque population of Cayo Santiago (Puerto Rico, U.S.A.), we investigate which male and female characteristics influence the probability of EGP to better understand the circumstances that shape the distribution and occurrence of EGP. Our results show that, against our expectations, higher-ranking females were more likely to produce EGP offspring than lower- ranking females. The probability of producing extragroup offspring was not significantly related to female or male age, male tenure or previous reproductive success. Furthermore, genetic relatedness between the parents did not affect the production of extragroup offspring, but extragroup offspring were more frequently produced early rather than late in a given mating season. Altogether, our analysis suggests that individual attributes and seasonal aspects create different opportunities and preferences for engaging in EGP as an alternative reproductive tactic. The observed patterns of EGP in rhesus macaques appear to be consistent with female mate choice for genetic benefits, which needs to be confirmed in future studies.

We assessed the suitability of a frequently used sampling method employing cotton swabs for collecting animal body odor for gas chromatography-mass spectrometry (GC-MS) analysis of volatile organic compounds (VOCs). Our method validation showed that both sampling material and sampling protocols affect the outcome of the analyses. Thus, among the tested protocols swabs of pure viscose baked before use and extracted with hexane had the least blank interferences in GC-MS analysis. Most critical for the recovery of VOCs was the handling time: the significant recovery losses of volatiles experienced with this sampling procedure suggest that a rapid processing of such samples is required. In a second part, we used swab sampling to sample the body odor of rhesus macaques (Macaca mulatta), which lack scent glands. First results after GC-MS analysis of the samples collected from these nonhuman primates emphasize that proper analytical performance is an indispensable prerequisite for successful automated data evaluation of the complex GC-MS profiles. Moreover, the retention times and the nature of the identified chemical compounds in our samples suggest that the use of swabs is generally more appropriate for collecting semivolatile rather than VOCs.

Olfaction is important across the animal kingdom for transferring information on, for example, species, sex, group membership, or reproductive parameters. Its relevance has been established in primates including humans, yet research on great apes still is fragmentary. Observational evidence indicates that great apes use their sense of smell in various contexts, but the information content of their body odor has not been analyzed. Our aim was therefore to compare the chemical composition of body odor in great ape species, namely Sumatran orangutans (Pongo abelii (Lesson, 1827), one adult male, five adult females, four nonadults), Western lowland gorillas (Gorilla gorilla gorilla (Savage, 1847), one adult male, two adult females, one nonadult), common chimpanzees (Pan troglodytes (Blumenbach, 1775), four adult males, nine adult females, four nonadults), and bonobos (Pan paniscus (Schwarz, 1929), two adult males, four adult females, two nonadults). We collected 195 samples (five per individual) of 39 captive individuals using cotton swabs and analyzed them using gas chromatography mass spectrometry. We compared the sample richness and intensity, similarity of chemical composition, and relative abundance of compounds. Results show that species, age, and potentially sex have an impact on the variance between odor profiles. Richness and intensity varied significantly between species (gorillas having the highest, bonobos the lowest richness and intensity), and with age (both increasing with age). Richness and intensity did not vary between sexes. Odor samples of the same species were more similar to each other than samples of different species. Among all compounds identified some were associated with age (N = 7), sex (N = 6), and species-related (N = 37) variance. Our study contributes to the basic understanding of olfactory communication in hominids by showing that the chemical composition of body odor varies across species and individuals, containing potentially important information for social communication.

Male reproductive strategies have been well studied in primate species where the ability of males to monopolize reproductive access is high. Less is known about species where males cannot monopolize mating access. Vervet monkeys (Chlorocebus pygerythrus) are interesting in this regard as female codominance reduces the potential for male monopolization. Under this condition, we assessed whether male dominance rank still influences male mating and reproductive success, by assigning paternities to infants in a population of wild vervets in the Eastern Cape, South Africa. To determine paternity, we established microsatellite markers from noninvasive fecal samples via cross-species amplification. In addition, we evaluated male mating and reproductive success for 3 groups over 4 mating seasons. We identified 21 highly polymorphic microsatellites (number of alleles = 7.5 ± 3.1 [mean ± SD], observed heterozygosity = 0.691 ± 0.138 [mean ± SD]) and assigned paternity to 94 of 97 sampled infants (96.9%) with high confidence. Matings pooled over 4 seasons were significantly skewed across 3 groups, although skew indices were low (B index = 0.023-0.030) and mating success did not correlate with male dominance. Paternities pooled over 4 seasons were not consistently significantly skewed (B index = 0.005-0.062), with high-ranking males siring more offspring than subordinates only in some seasons. We detected 6 cases of extra-group paternity (6.4%) and 4 cases of natal breeding (4.3%). Our results suggest that alternative reproductive strategies besides priority of access for dominant males are likely to affect paternity success, warranting further investigation into the determinants of paternity among species with limited male monopolization potential.

Scents play an important role in the life of most terrestrial mammals and may transmit valuable information about conspecifics. Olfaction was long considered of low importance in Old World monkeys due to their relative reduction of olfactory structures and low incidence of scent-marking behavior but has been increasingly recognized for mediating social relationships in recent years. Yet, studies investigating the composition of their chemical cues remain scarce. In the present study, we analyzed the potential information content of chemicals present on the skin of rhesus macaques (Macaca mulatta). We collected axillary secretions from 60 animals of the semifree-ranging population on Cayo Santiago (Puerto Rico, USA) with precleaned cotton swabs from which the secretions were subsequently extracted and analyzed by gas chromatography–mass spectrometry. Rhesus macaque axillary odorants varied in their overall similarity and composition. This variation was attributable to differences in sex, group membership, and kinship and further appeared to reflect age and rank in parts of our sample. The compounds most strongly associated with this variation primarily comprised larger molecular weight aldehydes and steroids. Such compounds are considered to be perceivable by the primate olfactory system through close-range interactions or through breakdown into smaller molecules by bacterial fermentation. Overall, our results provide additional evidence that odors of Old World monkeys reflect a wealth of potential information about their carrier, which provides the basis for chemical communication via body odors; however, its use by conspecifics needs to be confirmed in bioassays. Significance statement One prerequisite for olfactory communication is the presence of systematic variation in animal odors that is related to attributes such as age, sex, or kinship. The composition of odors has been examined in numerous mammals but, with the exception of humans, remains poorly understood in Old World monkeys and apes, taxonomic groups in which most species do not show scent-marking behavior. In the present study, we show that the composition of axillary secretions of an Old World monkey, the rhesus macaque, reflects sex, group membership, relatedness, and possibly also age and rank. This variation thus provides a basis for olfactory communication in Old World monkeys. Electronic supplementary material The online version of this article (10.1007/s00265-018-2479-5) contains supplementary material, which is available to authorized users.

The importance of smell in humans is well established but we know little about it in regard to our closest relatives, the great apes, as systematic studies on their olfactory behavior are still lacking. Olfaction has long been considered to be of lesser importance in hominids given their relatively smaller olfactory bulbs, fewer functional olfactory receptor genes than other species and absence of a functional vomeronasal organ. Therefore, the aim of this study was to evaluate the use of olfaction in hominids. In particular, we observed sniffing behavior in captive groups of four species (Sumatran orangutans, Pongo abelii; Western lowland gorillas, Gorilla gorilla gorilla; Western chimpanzees, Pan troglodytes verus; bonobos, Pan paniscus) and evaluated in which contexts sniffing was used. Our results show that all investigated species frequently used the sense of smell, and that the sniffing frequency varied with species, sex, age, and context. Most sniffing events were observed in gorillas in comparison to the three other species. Sniffing frequencies were also influenced by sex, with males sniffing slightly more often than females. Furthermore, our results revealed an effect of age, with younger individuals sniffing more often than older individuals. All species mainly sniffed in the non-social context (i.e., toward food and other environmental items) rather than in the social context (i.e., at conspecifics), suggesting that the evaluation of the environment and the nutritional value of food items is of major importance to all great ape species investigated here. In contrast to the other species and female chimpanzees, however, male chimpanzees most often used olfaction to inspect their conspecifics. Together, our study suggests that olfaction is likely to be more important in great apes than previously appreciated.

The ability to distinguish group members from conspecifics living in other groups is crucial for gregarious species. Olfaction is known to play a major role in group recognition and territorial defense in a wide range of mammalian taxa. Although primates have been typically regarded as microsmatic (having a poor sense of smell), increasing evidence suggests that olfaction may play a greater role in primates’ social life than previously assumed. In this study, we carried out behavioral bioassays using a signaler-receiver paradigm to investigate whether rhesus macaques (Macaca mulatta) can discriminate between body odors of female group members and females from different social groups. We conducted the study on the research island Cayo Santiago, Puerto Rico, in the non-mating season and controlled for kinship and familiarity using extensive pedigree and demographic data. Our results indicate that both males and females inspect out-group odors significantly longer than in-group odors. Males licked odors more often than females, and older animals licked more often than younger ones. Furthermore, individuals tended to place their nose longer towards odors when the odor donor’s group rank was higher than the rank of their own group. Reuse of odor samples decreased odor intensity (rated by human experimenters) during the course of a given test day and with longer exposure to ambient air; however, the reuse of odor samples did not significantly influence the response behaviors. Our findings uncover key roles of olfactory communication in a species not possessing distinct scent glands and thus shed light into the evolution of primate olfactory communication.

Aggressive behavior plays a central role in primate life, having a crucial effect on their reproductive performance and survival and possibly affecting the formation and maintenance of social bonds. Although aggressive behavior might serve a different function in males and females, and sex differences in aggressive behavior seem to emerge early during development, very few studies have investigated whether aggressive patterns follow different developmental trajectories in male and female primates. However, the developmental perspective is crucial to understanding when differences in adults’ aggression emerge and which factors trigger them. We here analyzed aggressive interactions in rhesus macaques from birth to sexual maturation (before male dispersal), including male and female focal subjects. We further considered the partner’s sex, age, and rank, as well as maternal and paternal kinship, and used powerful multivariate statistical analysis. The probability to initiate aggression was largely similar for both sexes and throughout development. Both males and females were more aggressive toward partners of the same sex and similar age. In contrast, the probability of receiving aggression mostly differed between sexes across development and depended on the social context. The probability of receiving aggression increased through development. Finally, important developmental changes appeared between 2 and 3 yr of age, indicating that this period is crucial for the development of adult social roles. Our results suggest that aggressive behavior largely serves a similar function for both sexes during the first years of development, only partially anticipating adult aggressive patterns.

Recognizing close kin and adjusting one’s behavior accordingly (i.e., favor kin in social interactions, but avoid mating with them) would be an important skill that can increase an animals’ inclusive fitness. Previous studies showed that philopatric female rhesus macaques (Macaca mulatta) bias their social behavior toward maternal and paternal kin. Benefits gained from selecting kin should, however, not only apply to the philopatric sex, for which the enduring spatial proximity facilitates kin discrimination. Given that dispersal is costly, the dispersing sex may benefit from migrating together with their kin or into groups containing kin. In male rhesus macaques, natal migrants bias their spatial proximity toward familiar male kin rather than familiar non-kin. Here, we set up playback experiments to test if males use the acoustic modality to discriminate familiar female kin from non-kin in a non-sexual context. Males responded differently to the presentation of “coo” calls of related and unrelated females, with their reaction depending on the interaction between kin-line (maternal vs paternal kin) and degree of relatedness (r = 0.5, 0.25). Specifically, males were more likely to respond to close kin compared to more distant kin or unrelated females, with this effect being significant in the maternal, but not paternal kin-line. The present study adds to our knowledge of kin recognition abilities of the dispersing sex, suggesting that male rhesus macaques are also able to identify kin using the acoustic modality. We discuss that the probability of response might be affected by the potential benefit of the social partner.

Genetic studies not only contribute substantially to our current understanding of the natural variation in behavior and health in many species, they also provide the basis of numerous in vivo models of human traits. Despite the many challenges posed by the high level of biological and social complexity, a long lifespan and difficult access in the field, genetic studies of primates are particularly rewarding because of the close evolutionary relatedness of these species to humans. The free-ranging rhesus macaque (Macaca mulatta) population on Cayo Santiago (CS), Puerto Rico, provides a unique resource in this respect because several of the abovementioned caveats are of either minor importance there, or lacking altogether, thereby allowing long-term genetic research in a primate population under constant surveillance since 1956. This review summarizes more than 40 years of genetic research carried out on CS, from early blood group typing and the genetic characterization of skeletal material via population-wide paternity testing with DNA fingerprints and short tandem repeats (STRs) to the analysis of the highly polymorphic DQB1 locus within the major histocompatibility complex (MHC). The results of the paternity studies also facilitated subsequent studies of male dominance and other factors influencing male reproductive success, of male reproductive skew, paternal kin bias, and mechanisms of paternal kin recognition. More recently, the CS macaques have been the subjects of functional genetic and gene expression analyses and have played an important role in behavioral and quantitative genetic studies. In addition, the CS colony has been used as a natural model for human adult-onset macular degeneration, glaucoma, and circadian rhythm disorder. Our review finishes off with a discussion of potential future directions of research on CS, including the transition from STRs to single nucleotide polymorphism (SNP) typing and whole genome sequencing. (C) 2016 Wiley Periodicals, Inc.

Dispersal and mating patterns are known to affect the availability of both maternal and paternal kin within social groups, with important effects on the evolution of sociality. It is generally assumed that the philopatric sex forms stronger social bonds than the dispersing sex, possibly as a result of reduced kin availability for the dispersing sex after departure. However, few primate studies have directly compared whether sex differences in association patterns, particular with kin, are already present prior to dispersal when kin availability should be the same for both sexes. Here, we compared affiliative and aggressive interactions in a female philopatric species, the rhesus macaque (Macaca mulatta), to test whether sex differences in kin bias already occur around the age of maturation, when both sexes still live together with kin in their natal group. Our data confirmed that kin availability was the same for both sexes prior to male dispersal. Similar kin availability was partially reflected by comparable association patterns, as both females and males preferentially interacted with maternal kin. However, females had stronger affiliative bonds with maternal kin than males of the same age, indicating that kin associations not only depended upon kin availability, but were also sex-specific. Similarly, males were significantly more likely to affiliate with paternal kin than non-kin, as compared to females, suggesting that males discriminated paternal kin from non-kin earlier in life than females. Males might have a stronger need than females to affiliate with paternal kin due to a reduced integration in the matrilineal family prior to dispersal and the high availability of paternally related age-peers, with whom males could potentially migrate. Females, in contrast, form stronger affiliations with maternal kin, which may enhance their offspring's survival. More comparative studies are needed to understand the impact of different dispersal regimes on patterns of kin associations. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.

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.

Patterns of within-group relatedness are expected to affect the prospects for cooperation among group members through kin selection. It has long been established that dispersal patterns determine the availability of kin and there is ample evidence of matrilineal kin biases in social behavior across primate species. However, in 1979, Jeanne Altmann(1) suggested that mating patterns also influence the structure of within-group relatedness; high male reproductive skew and the frequent replacement of breeding males leads to relatively high levels of paternal relatedness and age-structured paternal sibships within groups. As a consequence of frequent replacement of breeding males, relatedness among offspring of a given female will be reduced to the half- rather than full-sibling level. Depending on the number of sires and degree of relatedness among mothers, members of the same birth cohort may be as closely related as maternal siblings. If animals are able to recognize their paternal kin and exhibit biases in favor of them, this may influence the distribution of cooperation and the intensity of competition within groups of primates. Here, I summarize the evidence that serves as the basis for Altmann's predictions and review evidence regarding whether or not the availability of paternal kin also leads to paternal kin bias among primates.

In multimale groups where females mate promiscuously, male–infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father’s presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant’s mother. Hence, infant care might provide fitness gain for males. Here, we investigate male–infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate-guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi-free-ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0–4 years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male– infant interactions were affiliative, indicating the rareness of male–infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother’s proximity and emphasized during early infancy. Male–infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male–infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low-cost paternal care.

Volatile organic compounds (VOCs) are commonly collected from gaseous samples by adsorption to materials such as the porous polymer Tenax TA. Adsorbed compounds are subsequently released from these materials by thermal desorption (TD) and separated then by gas chromatography (GC) with flame ionization (FID) or mass spectrometry (MS) detection. Tenax TA is known to be particularly suitable for non-polar to semipolar volatiles, however, many volatiles from environmental and biological samples possess a rather polar character. Therefore, we tested if the polymer XAD-2, which so far is widely used to adsorb organic compounds from aqueous and organic solvents, could provide a broader coverage for (semi)polar VOCs during gas-phase sampling. Mixtures of volatile compounds covering a wide range of volatility (bp. 20–256 °C) and different chemical classes were introduced by liquid spiking into sorbent tubes with one of the two porous polymers, Tenax TA or XAD-2, and analyzed by TD/GC–MS. At first, an internal standard mixture composed of 17 authentic standards was used to optimize desorption temperature with respect to sorbent degradation and loading time for calibration. Secondly, we tested the detectability of a complex standard mixture composed of 57 volatiles, most of them common constituents of the body odor of mammals. Moreover, the performance of XAD-2 compared with Tenax TA was assessed as limit of quantitation and linearity for the internal standard mixture and 33 compounds from the complex standard mixture. Volatiles were analyzed in a range between 0.01–∼250 ng/tube depending on the compound and material. Lower limits of quantitation were between 0.01 and 3 ng ± 0.9). Interestingly, we found different kinetics for compound adsorption with XAD-2, and a partially better sensitivity in comparison with Tenax TA. For these analytes, XAD-2 might be recommended as an alternative of Tenax TA for TD/GC–MS analysis.

Natal dispersal may have considerable social, ecological and evolutionary consequences. While species-specific dispersal strategies have received much attention, individual variation in dispersal decisions and its fitness consequences remain poorly understood. We investigated causes and consequences of natal dispersal age in rhesus macaques (Macaca mulatta), a species with male dispersal. Using long-term demographic and genetic data from a semi-free ranging population on Cayo Santiago, Puerto Rico, we analysed how the social environment such as maternal family, group and population characteristics affected the age at which males leave their natal group. While natal dispersal age was unrelated to most measures of group or population structure, our study confirmed earlier findings that sons of high-ranking mothers dispersed later than sons of low-ranking ones. Natal dispersal age did not affect males’ subsequent survival, but males dispersing later were more likely to reproduce. Late dispersers were likely to start reproducing while still residing in their natal group, frequently produced extra-group offspring before natal dispersal and subsequently dispersed to the group in which they had fathered offspring more likely than expected. Hence, the timing of natal dispersal was affected by maternal rank and influenced male reproduction, which, in turn affected which group males dispersed to.

Light-dark coat color variation is a common aspect of color diversity within and across mammalian taxa. This variation in pelage brightness is associated with aspects of evolutionary ecology, particularly for primates, but little is known about the genetic mechanisms underlying light-dark differences in pelage pigmentation. Previous work, focusing particularly on macaques (Genus Macaca), has found no clear relationship between color variation and coding sequences of key pigmentation genes. This suggests that other loci and/or gene regulatory differences underlie this variation and raises the question of how patterns of gene expression differ in light verses dark hair follicles. Here, we examine relative expression levels of pigmentation genes in hair follicles from free-ranging rhesus macaques (Macaca mulatta) showing stark light-dark coat color variation. We quantified the brightness (reflectance) of plucked hair tufts using a spectrophotometer. We extracted RNA from the follicles and used quantitative RT-PCR to measure the relative amounts of gene product (mRNA) for seven candidate pigmentation genes (MITF, MC1R, MGRN1, ATRN, SLC24A5, TYRP1, and DCT). Expression values were normalized with the house-keeping gene ACTB. All candidate genes were expressed at similar levels in dark, intermediate, and light hair, and thus, light-dark variation in macaque coat color is unlikely to be due to differences in the expression of these key pigmentation genes. This study represents the first examination of gene expression and natural color variation in a non-human primate population. Our results indicate that even in a system, like pigmentation, where a candidate-gene approach is promising, identifying important intra-specific gene regulatory differences remains challenging.

Highlights\ud \ud ► Elo-rating generates reliable dominance hierarchies and circumvents drawbacks of established ranking methods. \ud ► It allows visualizing dominance relationships and the detection of rank dynamics. \ud ► An index to objectively assess the stability of a dominance hierarchy is proposed.

In group living animals, especially among primates, there is consistent evidence that high-ranking males gain a higher reproductive output than low-ranking males. Primate studies have shown that male coalitions and sociality can impact male fitness; however, it remains unclear whether males could potentially increase their fitness by preferentially supporting and socializing with females. Here we investigate patterns of male interventions and the effect of coalitions and sociality on male fitness in rhesus macaques (Macaca mulatta) with particular focus on male‐female interactions. We combined behavioural observations collected on Cayo Santiago with genetic data analysed for male reproductive output and relatedness. Our results revealed that the ten top-ranking males provided the majority of all male support observed. In contrast to other primates, male rhesus macaques mainly formed all-down coalitions suggesting that coalitions are less likely used to enhance male dominance. Males supporting females during and before their likely conception were not more likely to fertilize those females. We also found no evidence that males preferably support their offspring or other close kin. Interestingly, the most important predictor of male support was sociality, since opponents sharing a higher sociality index with a given male were more likely to be supported. Furthermore, a high sociality index of a given male‐female dyad resulted in a higher probability of paternity. Overall, our results strengthen the evidence that sociality affects fitness in male primates, but also suggest that in species in which males queue for dominance, it is less likely that males derive fitness benefits from coalitions.

Kin recognition is a key ability which facilitates the acquisition of inclusive fitness benefits and enables optimal outbreeding. In primates, phenotype matching is considered particularly important for the recognition of patrilineal relatives, as information on paternity is unlikely to be available via social familiarity. Phenotypic cues to both paternal and maternal relatedness exist in the facial features of humans and other primates. However, theoretical models suggest that in systems with uncertainty parentage it may be adaptive for offspring to conceal such cues when young, in order to avoid potential costs of being discriminated against by unrelated adults. Using experienced human raters, we demonstrate in a computer-based task that detection of parent–offspring resemblances in the faces of rhesus macaques ( Macaca mulatta ) increases significantly with offspring age. Moreover, this effect is specific to information about kinship, as raters were extremely successful at discriminating individuals even among the youngest animals. To our knowledge, this is the first evidence in non-humans for the age-dependent expression of visual cues used in kin recognition.

Why regularities in personality can be described with particular dimensions is a basic question in differential psychology. Nonhuman primates can also be characterized in terms of personality structure. Comparative approaches can help reveal phylogenetic constraints and social and ecological patterns associated with the presence or absence of specific personality dimensions. We sought to determine how different personality structures are related to interspecific variation in social style. Specifically, we examined this question in 6 different species of macaques, because macaque social style is well characterized and can be categorized on a spectrum of despotic (Grade 1) versus tolerant (Grade 4) social styles. We derived personality structures from adjectival ratings of Japanese (Macaca fuscata; Grade 1), Assamese (M. assamensis; Grade 2), Barbary (M. sylvanus; Grade 3), Tonkean (M. tonkeana; Grade 4), and crested (M. nigra; Grade 4) macaques and compared these species with rhesus macaques (M. mulatta; Grade 1) whose personality was previously characterized. Using a nonparametric method, fuzzy set analysis, to identify commonalities in personality dimensions across species, we found that all but 1 species exhibited consistently defined Friendliness and Openness dimensions, but that similarities in personality dimensions capturing aggression and social competence reflect similarities in social styles. These findings suggest that social and phylogenetic relationships contribute to the origin, maintenance, and diversification of personality.

The 5HTTLPR polymorphism in the promoter region of the human serotonin transporter (SLC6A4) gene is known to be associated with various stress-related psychological and psychiatric phenomena. We observed that a similar diallelic polymorphism in the orthologous gene of rhesus macaques (Macaca mulatta) was related to the reproductive life history of 580 males residing in the free-ranging colony of Cayo Santiago, Puerto Rico, between 1985 and 1998. At first glance, the polymorphism appeared to be selectively neutral because no difference in total reproductive output was noted between males of different 5HTTLPR genotypes. However, whereas heterozygotes were significantly more reproductive than homozygotes at intermediate age (10‐13 yr), the opposite held true before and after this period (n 5 682 offspring; randomization P 5 0.014). This association, which explains approximately 7% of the observed variation in sire age, most likely reflects different natal dispersal patterns and represents the first reported instance of a genetic influence on reproductive timing in mammals. behavior, male reproductive timing, male sexual function, neurotransmitters, rhesus macaques, serotonin transporter

Rhesus macaque females regularly copulate with a number of partners, and produce a single offspring per reproductive cycle in over 99% of cases. We used genotyping of 10 STR markers to determine paternity in the Cayo Santiago population of rhesus macaques. About 1,500 monkeys have been analyzed to date, with their marker genotypes entered into a computerized database. These data enable us to report the first documented case in any cercopithecine nonhuman primate species of the production of twin offspring sired by different males.

Kin selection promotes the evolution of social behaviour that increases the survival and reproductive success of close relatives. One prerequisite for kin selection is that individuals have the ability to discriminate between kin and nonkin. Studies incorporating data on paternal kinship are still rare, but in species with a high male reproductive skew, many adult females will be paternal half siblings. Using both microsatellites and DNA-fingerprinting, we here analyse data on paternal relatedness in order to compare the influence of maternal and paternal kinship on rates of affiliative and aggressive interactions among semi free-ranging adult female rhesus macaques (Macaca mulatta). Because paternal half siblings tend to be peers whereas maternal half siblings are almost always nonpeers, we also examine the interactions between age proximity and genetic relatedness on social behaviour. Genetic analyses show that male reproductive success is strongly skewed with 75% of infants within the troop having a paternal half sibling in the same age cohort. The highest rates of both affiliation and aggression occur among maternal half sisters. Adult females are significantly more affiliative, but not more aggressive, with paternal half sisters than with nonkin. Affiliative relationships declined in conjunction with increasing age difference among paternal half sisters, but the reverse effect was found for affiliative relationships among maternal half siblings. No association emerged among nonkin. Among both maternal and paternal kin, rates of affiliative and aggressive interactions increase as the degree of relatedness increased, thereby questioning the concept of a relatedness threshold as a mediator of social interactions in rhesus macaques. The asymmetry in affiliation and aggression between maternal and paternal half siblings, and the effect of age proximity on partitioning social interactions suggests that context-dependent kin discrimination characterises rhesus macaques. Paternal kin discrimination probably results from an interaction between phenotype matching and familiarity, rather than from one process or the other.

Genetic studies not only contribute substantially to our current understanding of the natural variation in behavior and health in many species, they also provide the basis of numerous in vivo models of human traits. Despite the many challenges posed by the high level of biological and social complexity, a long lifespan and difficult access in the field, genetic studies of primates are particularly rewarding because of the close evolutionary relatedness of these species to humans. The free-ranging rhesus macaque (Macaca mulatta) population on Cayo Santiago (CS), Puerto Rico, provides a unique resource in this respect because several of the abovementioned caveats are of either minor importance there, or lacking altogether, thereby allowing long-term genetic research in a primate population under constant surveillance since 1956. This review summarizes more than 40 years of genetic research carried out on CS, from early blood group typing and the genetic characterization of skeletal material via population-wide paternity testing with DNA fingerprints and short tandem repeats (STRs) to the analysis of the highly polymorphic DQB1 locus within the major histocompatibility complex (MHC). The results of the paternity studies also facilitated subsequent studies of male dominance and other factors influencing male reproductive success, of male reproductive skew, paternal kin bias, and mechanisms of paternal kin recognition. More recently, the CS macaques have been the subjects of functional genetic and gene expression analyses and have played an important role in behavioral and quantitative genetic studies. In addition, the CS colony has been used as a natural model for human adult-onset macular degeneration, glaucoma, and circadian rhythm disorder. Our review finishes off with a discussion of potential future directions of research on CS, including the transition from STRs to single nucleotide polymorphism (SNP) typing and whole genome sequencing.

Dispersal and mating patterns are known to affect the availability of both maternal and paternal kin within social groups, with important effects on the evolution of sociality. It is generally assumed that the philopatric sex forms stronger social bonds than the dispersing sex, possibly as a result of reduced kin availability for the dispersing sex after departure. However, few primate studies have directly compared whether sex differences in association patterns, particular with kin, are already present prior to dispersal when kin availability should be the same for both sexes. Here, we compared affiliative and aggressive interactions in a female philopatric species, the rhesus macaque (Macaca mulatta), to test whether sex differences in kin bias already occur around the age of maturation, when both sexes still live together with kin in their natal group. Our data confirmed that kin availability was the same for both sexes prior to male dispersal. Similar kin availability was partially reflected by comparable association patterns, as both females and males preferentially interacted with maternal kin. However, females had stronger affiliative bonds with maternal kin than males of the same age, indicating that kin associations not only depended upon kin availability, but were also sex-specific. Similarly, males were significantly more likely to affiliate with paternal kin than non-kin, as compared to females, suggesting that males discriminated paternal kin from non-kin earlier in life than females. Males might have a stronger need than females to affiliate with paternal kin due to a reduced integration in the matrilineal family prior to dispersal and the high availability of paternally related age-peers, with whom males could potentially migrate. Females, in contrast, form stronger affiliations with maternal kin, which may enhance their offspring's survival. More comparative studies are needed to understand the impact of different dispersal regimes on patterns of kin associations.

Among many mammals, maternal care strongly impacts infant survival; however, less is known about whether adult males also affect infant fitness. Paternal care is expected when providing care enhances offspring survival and reproduction, which likewise increases fathers' fitness. Males might also care for unrelated immature individuals to increase their mating probability with the immature individuals' mothers. Studies in multimale primate groups showed that sires enhance food access for offspring and provide protection in conflicts. Furthermore, fathers' presence during infancy has been suggested to accelerate offspring sexual maturation. However, no study has yet directly linked the degree of father-offspring bonds to offspring fitness in primates. We previously reported father-offspring affiliation in rhesus macaques, pronounced during early infancy and independent of mothers' presence. The present study aims at investigating whether affiliation with fathers or other males affects proxies of immature fitness (body mass gain, body fat and testis size). First, we combined behavioral, genetic and morphometric data from 55 subjects of one group. Second, using demographic and genetic data, we investigated for 92 individuals of the population whether mother- and father-offspring co-residence during immaturity influenced offspring lifetime reproductive success (LRS). Our results show that focal rank and higher amounts of affiliation with high-ranking males during infancy tend to positively impact body mass gain of female, but not male focal animals. In contrast, body mass gain of male focal individuals, but not females', appeared to be higher when affiliation of male immature individuals was evenly distributed across their adult male partners. Moreover, we found mothers', but not fathers', presence during immaturity to predict offspring LRS. Our results suggest that male-immature affiliation, but not father-offspring co-residence, potentially impacts proxies of immature fitness. However, future studies should investigate the underlying mechanisms of male-immature relationships and their impact on immature fitness in more detail.

Gene conversion and balancing selection have been invoked to explain the ubiquitous diversity of the antigen-presenting proteins encoded in the vertebrate major histocompatibility complex (MHC). In the present study, direct evidence for over-dominant selection promoting MHC diversity in primates is provided by the observation that, in a large free-ranging population of rhesus macaques, males heterozygous at MHC class II locus Mamu-DQB1 sired significantly more offspring than homozygotes (the male-specific selection coefficient s equals 0.34). This heterozygote advantage appeared to be independent of the actual male Mamu-DQB1 genotype. No similar effect emerged for a captive group of monkeys of similar genetic background but under veterinary care.

Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness.

A coalition is formed when one animal intervenes in an ongoing conflict between two parties to support one side. Since support of one party is also an act against the other party, coalitions are triadic interactions involving a supporter, a recipient, and a target. The purpose of this study was to test which of three possible theories explains coalition formation among male Barbary macaques: 1) Males support kin to enhance their indirect fitness (kin selection). 2) Males support nonkin to receive future reciprocal support (reciprocal altruism). 3) Males pursue self-interests and immediately benefit via nonkin support (cooperation). Coalition formation was investigated among 31 semi-free male Barbary macaques in the Salem Monkey Park, Germany during the mating season. The results show: 1) Males intervened more often in dyadic conflicts in which a related opponent was involved and supported related opponents more than unrelated opponents. Close kin supported each other more often than distant kin. 2) Some evidence for reciprocal support was found. However, reciprocity was probably a by-product of targeting the same individuals for dominance. 3) Coalition formation among nonkin is best interpreted as cooperation, based on self-interests. Male Barbary macaques seem to intervene more often to stabilize and less often to improve their rank. Although our data were limited, the results revealed that kin support, reciprocal support, and cooperative support were all involved in coalition formation among male Barbary macaques.

Establishing kinship relations in primates using modern molecular genetic techniques has enhanced the ability to scrutinize a number of fundamental biological issues. We screened 51 human short tandem repeats (STRs) for cross-species PCR amplification in rhesus macaques (Macaca mulatta) and identified 11 polymorphic loci with heterozygosity rates of at least 0.6. These markers were used for paternity testing in three social groups (M, R, and S) of rhesus macaques from Cayo Santiago, Puerto Rico. Several consecutive birth cohorts were analyzed in which approximately 200 males were tested for paternity against more than 100 mother/ infant pairs. Despite a combined exclusion rate of more than 99.9% in all three groups, some cases could not be solved unequivocally with the STR markers and additional testing of the MHC-associated DQB1 polymorphism. A final decision became possible through multilocus DNA fingerprinting with one or more of the oligonucleotide probes (GATA)4, (CA)8, and (CAC)5. Paternity assessment by multilocus DNA analysis with probe (CAC)5 alone was found to have limitations in rhesus macaques as regards the number of potential sires which might be involved in a given case. Multilocus DNA fingerprinting requires large amounts of DNA, and the ensuing autoradiographic patterns present difficulties in comparisons across gels and even within the same gel across remote lanes. Computer-assisted image analysis was incapable of eliminating this problem. Therefore, a dual approach to DNA typing has been adopted, using STR markers to reduce the number of potential sires to a level where all remaining candidates can be tested by multilocus DNA fingerprinting on a single gel, preferably in lanes adjacent to the mother/infant pair.