Anja Widdig

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

Kin selection promotes the evolution of social behavior that increases the survival and reproductive success of close relatives. Among primates, maternal kinship frequently coincides with a higher frequency of grooming and agonistic aiding, but the extent to which paternal kinship influences adult female social relationships has not yet been investigated. Here, we examine the effect of both maternal and paternal kinship, as well as age proximity, on affiliative interactions among semifree-ranging adult female rhesus macaques, Macaca mulatta. Kinship was assessed by using both microsatellites and DNA-fingerprinting. Our study confirms that the closest affiliative relationships characterize maternal half-sisters. We provide evidence that adult females are significantly more affiliative with paternal half-sisters than with nonkin. Furthermore, paternal kin discrimination was more pronounced among peers than among nonpeers, indicating that age proximity has an additional regulatory effect on affiliative interactions. We propose that kin discrimination among cercopithecine primates emerges from ontogenetic processes that involve phenotype matching based on shared behavioral traits, such as inherited personality profiles, rather than physiological or physical characteristics.

Restricted accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article 2004A longitudinal analysis of reproductive skew in male rhesus macaquesProc. R. Soc. Lond. B.271819–826http://doi.org/10.1098/rspb.2003.2666SectionSupplemental MaterialRestricted accessA longitudinal analysis of reproductive skew in male rhesus macaques Published:22 April 2004https://doi.org/10.1098/rspb.2003.2666AbstractOne of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi–free–ranging population of rhesus macaques (Macaca mulatta), using Nonac's B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half–sibling in their own birth cohort. Reproductive success was greatest for high–ranking males, males who spent the whole mating season in the troop and males of 9–11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extra–group paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the ‘limited–control’ model, with multiple factors interacting to regulate individual reproductive output. 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Bonier F, Martin P and Wingfield J (2007) Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird, Behavioral Ecology, 10.1093/beheco/arm075, 18:6, (1045-1050), Online publication date: 1-Nov-2007., Online publication date: 1-Nov-2007. Charpentier M, Widdig A and Alberts S (2007) Inbreeding depression in non-human primates: a historical review of methods used and empirical data, American Journal of Primatology, 10.1002/ajp.20445, 69:12, (1370-1386), Online publication date: 1-Dec-2007. Nutt K (2007) Genetic reconstruction of breeding patterns in gundis (Rodentia: Ctenodactylidae), Behavioral Ecology and Sociobiology, 10.1007/s00265-007-0396-0, 61:11, (1651-1663), Online publication date: 6-Aug-2007. Intrasexuelle Selektion: wie Männchen konkurrieren Verhaltensbiologie, 10.1007/3-540-29977-7_8, (241-309) Engelhardt A, Heistermann M, Hodges J, Nürnberg P and Niemitz C (2006) Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?, Behavioral Ecology and Sociobiology, 10.1007/s00265-005-0104-x, 59:6, (740-752), Online publication date: 1-Apr-2006. Kutsukake N and Nunn C (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control, Behavioral Ecology and Sociobiology, 10.1007/s00265-006-0213-1, 60:5, (695-706), Online publication date: 1-Sep-2006. ROSSITER S, RANSOME R, FAULKES C, DAWSON D and JONES G (2006) Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism, Molecular Ecology, 10.1111/j.1365-294X.2006.02987.x, 15:10, (3035-3043) Widdig A, Streich W, Nürnberg P, Croucher P, Bercovitch F and Krawczak M (2006) Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta), Behavioral Ecology and Sociobiology, 10.1007/s00265-006-0251-8, 61:2, (205-214), Online publication date: 22-Nov-2006. Heg D, Bergmüller R, Bonfils D, Otti O, Bachar Z, Burri R, Heckel G and Taborsky M (2006) Cichlids do not adjust reproductive skew to the availability of independent breeding options, Behavioral Ecology, 10.1093/beheco/arj056, 17:3, (419-429), Online publication date: 1-May-2006. Piertney S and Oliver M (2005) The evolutionary ecology of the major histocompatibility complex, Heredity, 10.1038/sj.hdy.6800724, 96:1, (7-21), Online publication date: 1-Jan-2006. WIDDIG A, NÜRNBERG P, BERCOVITCH F, TREFILOV A, BERARD J, KESSLER M, SCHMIDTKE J, STREICH W and KRAWCZAK M (2006) Consequences of group fission for the patterns of relatedness among rhesus macaques, Molecular Ecology, 10.1111/j.1365-294X.2006.03039.x, 15:12, (3825-3832) ERIKSSON J, SIEDEL H, LUKAS D, KAYSER M, ERLER A, HASHIMOTO C, HOHMANN G, BOESCH C and VIGILANT L (2006) Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus), Molecular Ecology, 10.1111/j.1365-294X.2006.02845.x, 15:4, (939-949) Deaner R, Khera A and Platt M (2005) Monkeys Pay Per View: Adaptive Valuation of Social Images by Rhesus Macaques, Current Biology, 10.1016/j.cub.2005.01.044, 15:6, (543-548), Online publication date: 1-Mar-2005. Bercovitch F (2005) Book review, Animal Behaviour, 10.1016/j.anbehav.2004.11.001, 69:2, (508-509), Online publication date: 1-Feb-2005. Krawczak M, Trefilov A, Berard J, Bercovitch F, Kessler M, Sauermann U, Croucher P, Nürnberg P, Widdig A and Schmidtke J (2005) Male Reproductive Timing in Rhesus Macaques Is Influenced by the 5HTTLPR Promoter Polymorphism of the Serotonin Transporter Gene1, Biology of Reproduction, 10.1095/biolreprod.104.038059, 72:5, (1109-1113), Online publication date: 1-May-2005. Setchell J, Charpentier M and Wickings E (2005) Mate guarding and paternity in mandrills: factors influencing alpha male monopoly, Animal Behaviour, 10.1016/j.anbehav.2005.02.021, 70:5, (1105-1120), Online publication date: 1-Nov-2005. Bradley B, Robbins M, Williamson E, Steklis H, Steklis N, Eckhardt N, Boesch C and Vigilant L (2005) Mountain gorilla tug-of-war: Silverbacks have limited control over reproduction in multimale groups, Proceedings of the National Academy of Sciences, 10.1073/pnas.0502019102, 102:26, (9418-9423), Online publication date: 28-Jun-2005. Robbins A and Robbins M (2005) Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei), Behavioral Ecology and Sociobiology, 10.1007/s00265-005-0917-7, 58:3, (295-309), Online publication date: 1-Jul-2005. Charpentier M, Peignot P, Hossaert-McKey M, Gimenez O, Setchell J and Wickings E (2005) Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx), Behavioral Ecology, 10.1093/beheco/ari034, 16:3, (614-623), Online publication date: 1-May-2005. Kazem A, Widdig A and Noë R (2013) Visual Phenotype Matching: Cues to Paternity Are Present in Rhesus Macaque Faces, PLoS ONE, 10.1371/journal.pone.0055846, 8:2, (e55846) Dama M, Singh N, Rajender S and Singh A (2011) High Fat Diet Prevents Over-Crowding Induced Decrease of Sex Ratio in Mice, PLoS ONE, 10.1371/journal.pone.0016296, 6:1, (e16296) Carnes L, Nunn C, Lewis R and Waterman J (2011) Effects of the Distribution of Female Primates on the Number of Males, PLoS ONE, 10.1371/journal.pone.0019853, 6:5, (e19853) Minkner M, Young C, Amici F, McFarland R, Barrett L, Grobler J, Henzi S and Widdig A (2018) Assessment of Male Reproductive Skew via Highly Polymorphic STR Markers in Wild Vervet Monkeys, Chlorocebus pygerythrus, Journal of Heredity, 10.1093/jhered/esy048 Ward H, Ransome R, Jones G, Rossiter S and Russo D (2014) Determinants and Patterns of Reproductive Success in the Greater Horseshoe Bat during a Population Recovery, PLoS ONE, 10.1371/journal.pone.0087199, 9:2, (e87199) Lardy S, Cohas A, Desouhant E, Tafani M, Allainé D and Rands S (2012) Paternity and Dominance Loss in Male Breeders: The Cost of Helpers in a Cooperatively Breeding Mammal, PLoS ONE, 10.1371/journal.pone.0029508, 7:1, (e29508) Madlon-Kay S, Brent L, Montague M, Heller K and Platt M (2017) Using Machine Learning to Discover Latent Social Phenotypes in Free-Ranging Macaques, Brain Sciences, 10.3390/brainsci7070091, 7:12, (91) Langos D, Kulik L, Ruiz-Lambides A, Widdig A and Engelhardt A (2015) Does Male Care, Provided to Immature Individuals, Influence Immature Fitness in Rhesus Macaques?, PLOS ONE, 10.1371/journal.pone.0137841, 10:9, (e0137841) Norman V, Pamminger T, Nascimento F and Hughes W (2019) The role of juvenile hormone in regulating reproductive physiology and dominance in Dinoponera quadriceps ants , PeerJ, 10.7717/peerj.6512, 7, (e6512) This Issue22 April 2004Volume 271Issue 1541 Article InformationDOI:https://doi.org/10.1098/rspb.2003.2666PubMed:15255100Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Published online22/04/2004Published in print22/04/2004 License: Citations and impact Keywordsmate choiceheterozygote advantagerhesus macaqueskin structuremale reproductive skew Large datasets are available through Proceedings B's partnership with Dryad

One of the most important assumptions of kin selection theory is that individuals behave differently towards kin than non-kin. In mammals, there is strong evidence that maternal kin are distinguished from non-kin via familiarity. However, little is known about whether or not mammals can also recognize paternal kin as many female mammals, including primates, mate with multiple males near the time of conception, potentially concealing paternal kinship. Genetic data in several mammalian species with a promiscuous mating system and male-biased dispersal reveal a high skew in male reproduction which leads to co-residing paternal half-siblings. In most primates, individuals also form stable bisexual groups creating opportunities for males to interact with their offspring. Here I consider close paternal kin co-resident in the same social group, such as father-offspring and paternal half-siblings (i.e. animals sharing the same father but who were born to different mothers) and review mammalian studies of paternal kin discrimination. Furthermore, I summarize the most likely mechanisms of paternal kin discrimination (familiarity and phenotype matching). When familiarity is the underlying mechanism, mothers and/or the sire could mediate familiarity among paternal half-siblings as well as between fathers and offspring assuming mothers and/or fathers can assess paternity. When animals use phenotype matching, they might use their fathers' template (when the father is present) or self (when the father is absent) to assess paternal kinship in others. Available evidence suggests that familiarity and phenotype matching might be used for paternal kin discrimination and that both mechanisms might apply to a wide range of social mammals characterized by a high skew in male reproduction and co-residence of paternal kin. Among primates, suggested evidence for phenotype matching can often have an alternative explanation, which emphasizes the crucial importance of controlling for familiarity as a potential confounding variable. However, the mechanism/s used to identify paternal kin might differ within a species (as a function of each individual's specific circumstances) as well as among species (depending upon the key sensory modalities of the species considered). Finally, I discuss the possible cues used in paternal kin discrimination and offer suggestions for future studies.

Personality dimensions capturing individual differences in behavior, cognition, and affect have been described in several species, including humans, chimpanzees, and orangutans. However, comparisons between species are limited by the use of different questionnaires. We asked raters to assess free-ranging rhesus macaques at two time points on personality and subjective well-being questionnaires used earlier to rate chimpanzees and orangutans. Principal-components analysis yielded domains we labeled Confidence, Friendliness, Dominance, Anxiety, Openness, and Activity. The presence of Openness in rhesus macaques suggests it is an ancestral characteristic. The absence of Conscientiousness suggests it is a derived characteristic in African apes. Higher Confidence and Friendliness, and lower Anxiety were prospectively related to subjective well-being, indicating that the connection between personality and subjective well-being in humans, chimpanzees, and orangutans is ancestral in catarrhine primates. As demonstrated here, each additional species studied adds another fold to the rich, historical story of primate personality evolution.

The relatively new research discipline of Eco-Metabolomics is the application of metabolomics techniques to ecology with the aim to characterise biochemical interactions of organisms across different spatial and temporal scales. Metabolomics is an untargeted biochemical approach to measure many thousands of metabolites in different species, including plants and animals. Changes in metabolite concentrations can provide mechanistic evidence for biochemical processes that are relevant at ecological scales. These include physiological, phenotypic and morphological responses of plants and communities to environmental changes and also interactions with other organisms. Traditionally, research in biochemistry and ecology comes from two different directions and is performed at distinct spatiotemporal scales. Biochemical studies most often focus on intrinsic processes in individuals at physiological and cellular scales. Generally, they take a bottom-up approach scaling up cellular processes from spatiotemporally fine to coarser scales. Ecological studies usually focus on extrinsic processes acting upon organisms at population and community scales and typically study top-down and bottom-up processes in combination. Eco-Metabolomics is a transdisciplinary research discipline that links biochemistry and ecology and connects the distinct spatiotemporal scales. In this review, we focus on approaches to study chemical and biochemical interactions of plants at various ecological levels, mainly plant–organismal interactions, and discuss related examples from other domains. We present recent developments and highlight advancements in Eco-Metabolomics over the last decade from various angles. We further address the five key challenges: (1) complex experimental designs and large variation of metabolite profiles; (2) feature extraction; (3) metabolite identification; (4) statistical analyses; and (5) bioinformatics software tools and workflows. The presented solutions to these challenges will advance connecting the distinct spatiotemporal scales and bridging biochemistry and ecology.

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.

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.

Several studies have documented the importance of social bonding for the enhancement of individual fitness. However, little is known about how social relationships develop through ontogeny, and whether their development follows the same trajectory in males and females. Here we analyzed affiliative interactions (proximity, social grooming, play) combined with demographic and genetic data in semi-free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago over their first 4 yr of life (from birth to sexual maturation) to understand how these interactions change through development in both sexes. Generalized linear mixed models revealed that social behaviors mostly followed different developmental trajectories in males and females and were highly dependent on the social context. In particular, sex differences in social behavior varied through development depending on the partner's sex and age. Females engaged in more social interactions than males, especially with other females, and were more involved in grooming around the time of maturation. In contrast, males interacted more with males and age peers, especially around maturation. Sex differences in social behavior varied through development, but also depended on rank, partner's rank, and kin line, although not consistently. High-ranking individuals, especially older females, were generally preferred as social partners. Moreover, both male and female individuals interacted mostly with maternal kin, although males also preferred paternal kin over nonkin. Importantly, most developmental changes in sociality happened when individuals were ca. 2 yr old, suggesting that this might be a milestone in the development of sociality in rhesus macaques. The only notable exception to this pattern was play, which was more pronounced in males from the beginning of their lives. We propose that play might serve as a trigger of sex differences in social behavior, with sex differences emerging early in development and increasing through time as males and females gradually grow into their adult social roles.

Abstract 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.

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.

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.

Infant survival is a major determinant of individual fitness and constitutes a crucial factor in shaping species' ability to maintain viable populations in changing environments.1 Early adverse conditions, such as maternal loss, social isolation, and ecological hazards, have been associated with reduced rates of infant survivorship in wild primates.2,3,4 Agricultural landscapes increasingly replacing natural forest habitats may additionally threaten the survival of infants through exposure to novel predators,5 human-wildlife conflicts,6,7 or the use of harmful chemicals.8,9 Here, we investigated potential links between agricultural habitat use and high infant mortality in wild southern pig-tailed macaques (Macaca nemestrina) inhabiting a mosaic landscape of rainforest and oil palm plantation in Peninsular Malaysia. Longitudinal data revealed that 57% of all infants born during the study period (2014-2023) died before the age of 1 year, far exceeding mortality rates reported for other wild primates.10,11,12,13,14 Importantly, prolonged time spent in the plantation during infancy decreased the likelihood of infant survival by 3-fold, likely caused by increased exposure to the threats inherent to this environment. Further, mortality risk was elevated for infants born to primiparous mothers and predicted by prolonged maternal interbirth intervals, suggesting potential long-term effects attributed to the uptake and/or accumulation of pesticides in mothers' bodies.15,16,17 Indeed, existing literature reports that pesticides may cross the placental barrier, thus impacting fetal development during pregnancy.18,19,20 Our findings emphasize the importance of minimizing anthropogenic threats to wildlife in agricultural landscapes by establishing environmentally friendly cultivation practices that can sustain wildlife populations in the long term.

Abstract 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.

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.

Kin recognition can enhance inclusive fitness via nepotism and optimal outbreeding. Mechanisms allowing recognition of patrilineal relatives are of particular interest in species in which females mate promiscuously, leading to paternity uncertainty. Humans are known to detect facial similarities between kin in the faces of third parties, and there is some evidence for continuity of this ability in nonhuman primates . However, no study has yet shown that this propensity translates into an ability to detect one's own relatives, one of the key prerequisites for gaining fitness benefits. Here we report a field experiment demonstrating that free-ranging rhesus macaques (Macaca mulatta) spontaneously discriminate between facial images of their paternal half-siblings and unrelated individuals, when both animals are unfamiliar to the tested individual. Specifically, subjects systematically biased their inspection time toward nonkin when the animals pictured were of their own sex (potential threats), relative to when they were of the opposite sex (potential mates). Our results provide strong evidence for visual phenotype matching and the first demonstration in any primate that individuals can spontaneously detect their own paternal relatives on the basis of facial cues under natural conditions.

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. 78:78–91, 2016. © 2016 Wiley Periodicals, Inc.

When close relatives mate, offspring are expected to suffer fitness consequences due to inbreeding depression. Inbreeding has previously been quantified in two ways: using a sufficiently large panel of markers or deep and complete pedigrees over several generations. However, the application of both approaches is still limited by the challenge of compiling such data for species with long generation times, such as primates. Here, we assess inbreeding in rhesus macaques living on Cayo Santiago (Puerto Rico), a population genetically isolated since 1938, but descendant of a large set of presumably unrelated founders. Using comprehensive genetic data, we calculated inbreeding coefficients (F) for 2669 individuals with complete three generation pedigrees and 609 individuals with complete four generation pedigrees. We found that 0.79 and 7.39% of individuals had an F > 0 when using data from three and four generation pedigrees, respectively. No evidence of an increase in inbreeding over the study period (up to 23 years) was found. Furthermore, the observed mean relatedness of breeding pairs differed significantly from the distribution of parental relatedness expected as simulated based on previous reproductive data, suggesting that kin generally avoid breeding with each other. Finally, inbreeding was not a predictor of early mortality measured as survival until weaning and sexual maturation, respectively. Our results remain consistent with three estimators of inbreeding (standardized heterozygosity, internal relatedness, and homozygosity by loci) using up to 42 highly polymorphic microsatellites for the same set of individuals. Together, our results demonstrate that close inbreeding may not be prevalent even in populations isolated over long periods when mechanisms of inbreeding avoidance can operate.When close relatives mate, offspring may suffer from such inbreeding, e.g., via lower survival and/or fertility. Using (i) a large panel of genetic markers and (ii) complete three or four generation pedigrees, respectively, we show that incidences of inbreeding in a long-lived primate population are rare, even after genetic isolation for 75 years. Moreover, our simulations suggest that kin in our population generally avoid breeding with each other. Finally, the few inbred individuals detected in our large sample did not suffer from lower survival. Given that many animal species face dramatic habitat loss combined with critical population declines, our study provides important implications for conservation biology in general and for population management in particular.

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.

Dispersal has been suggested to be challenging, especially for species that heavily rely on social learning for knowledge acquisition. One of the obstacles that migrants face is learning how to cope with an unfamiliar, new habitat, which may involve learning from resident individuals. So far, only very few studies have looked at social learning in migrants after dispersal. Here we examine how migrant male orangutans use a behavior called “peering” (an indicator of observational social learning), to learn from local individuals. In total, we analyzed 4,009 daily dyadic associations with and without peering events of 77 males of the highly sociable Sumatran orangutans ( Pongo abelii ) at the Suaq population and 75 males of the less sociable Bornean orangutans ( Pongo pygmaeus wurmbii ) at the Tuanan population, covering a combined study time of 30 years. Analysis using generalized linear mixed models supported our prediction that migrant males in Suaq preferentially peered at the local adult females. However, in Tuanan, migrants peered mostly at other adult males and local immatures. Migrants’ peering rates were highest shortly after their arrival, and significantly decreased with increasing time spent in the area. Migrants in both sites peered significantly more at peering targets’ feeding on food items that are rarely eaten within the locals’ diet, than at commonly eaten ones and peered significantly more at skill-intense food items than easy-to-process ones. Further, migrants interacted significantly more with the peered-at food item after the peering event, than before, suggesting that they practice the observed behavior. Our results therefore suggest that migrant males use peering to learn new ecological knowledge after dispersal (e.g., where and what to feed on), and continue to learn complex skills even within adulthood , (e.g., how to feed on skill-intense food items). To do so, migrants selectively attend to the most knowledgeable and/or available individuals, practice the new skill afterwards and even flexibly adjust their learning, e.g., when confronted with intolerant locals or when the need for learning decreases. Together, our study provides important evidence that social learning in great apes expands towards adulthood, an ability which critically impacted also human evolution.

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.

Animal personalities, i.e. consistent differences in behavior across time and/or context, have received increased attention of behavioral biologists over the last years. Recent research shows that personalities represent traits on which natural and sexual selection work and which can have substantial fitness consequences. The aim of this study is to establish the personality structure of crested macaque (Macaca nigra) males as foundation for future studies on its adaptive value. We collected behavioral data through focal animal sampling and additionally conducted two sets of playback experiments. Results of a factor analysis on the behavioral data revealed a four factor structure with components we labeled Anxiety, Sociability, Connectedness and Aggressiveness. Results from the experiments revealed an additional and independent Boldness factor but the absence of Neophilia. Overall, this structure resembles other macaque and animal species with the exception of Connectedness, which might be a consequence of the species' tolerant social style. Our results thus not only form the basis for future studies on the adaptive value of personality in crested macaques but also contribute an important data point for investigating the evolution of personality structure from a comparative perspective by refining, for example, which personality factors characterized the last common ancestor of hominids and 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.

Widespread evidence exists that when relatives live together, kinship plays a central role in shaping the evolution of social behaviour. Previous studies showed that female rhesus macaques ( Macaca mulatta ) recognize familiar maternal kin using vocal cues. Recognizing paternal kin might, however, be more difficult as rhesus females mate promiscuously during the possible conception period, most probably concealing paternity. Behavioural observations indicate that semi free-ranging female rhesus macaques prefer to associate with their paternal half-sisters in comparison to unrelated females within the same group, particularly when born within the same age cohort. However, the cues and mechanism/s used in paternal kin discrimination remain under debate. Here, we investigated whether female rhesus macaques use the acoustic modality to discriminate between paternal half-sisters and non-kin, and tested familiarity and phenotype matching as the underlying mechanisms. We found that test females responded more often to calls of paternal half-sisters compared with calls of unrelated females, and that this discrimination ability was independent of the level of familiarity between callers and test females, which provides, to our knowledge, the first evidence for acoustic phenotype matching. Our study strengthens the evidence that female rhesus macaques can recognize their paternal kin, and that vocalizations are used as a cue.

Premature loss of offspring decreases direct fitness of parents. In gregarious mammals, both ecological and social variables impact offspring survival and may interact with each other in this regard. Although a number of studies have investigated factors influencing offspring loss in mammals, we still know very little on how different factors interact with one another. We therefore investigated fetal and infant mortality in 3 large groups of wild crested macaques ( Macaca nigra ) over a period of up to 5 years by including potential social causes such as maternal dominance rank, male immigration, between group encounters, and ecological conditions such as rainfall in a multivariate survival analysis using Cox proportional hazards model. Infant but not fetal survival was most impaired after a recent takeover of the alpha-male position by an immigrant male. Furthermore, infant survival probability increased when there was an increase in number of group adult females and rainfall. Fetal survival probability also increased with an increase of these 2 factors, but more in high-ranking than low-ranking females. Fetal survival, unlike that of infants, was also improved by an increase of intergroup encounter rates. Our study thus stresses the importance of survival analyses using a multivariate approach and encompassing more than a single offspring stage to investigate the determinants of female direct fitness. We further provide evidence for fitness costs and benefits of group living, possibly deriving from high pressures of both within- and between-group competition, in a wild primate population.

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.

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.

Abstract Offspring born to related parents may show reduced fitness due to inbreeding depression. Although evidence of inbreeding depression has accumulated for a variety of taxa during the past two decades, such analyses remain rare for primate species, probably because of their long generation time. However, inbreeding can have important fitness costs and is likely to shape life‐history traits in all living species. As a consequence, selection should have favored inbreeding avoidance via sex‐biased dispersal, extra‐group paternity, or kin discrimination. In this paper, we review empirical studies on the effects of inbreeding on fitness traits or fitness correlates in primate species. In addition, we report the methods that have been used to detect inbreeding in primate populations, and their development with the improvement of laboratory techniques. We focus particularly on the advantages and disadvantages using microsatellite loci to detect inbreeding. Although the genetic data that are typically available (partial pedigrees, use of microsatellite heterozygosity as an estimate of genomewide inbreeding) tend to impose constraints on analyses, we encourage primatologists to explore the potential effects of inbreeding if they have access to even partial pedigrees or genetic information. Such studies are important because of both the value of basic research in inbreeding depression in the wild and the conservation issues associated with inbreeding, particularly in threatened species, which include more than half of the currently living primate species. Am. J. Primatol. 69:1370–1386, 2007. © 2007 Wiley‐Liss, Inc.

The relationship between an individual’s genotype and its phenotype is a central issue in biology, but one that is largely unexplored for the important phenotype of complex social behavior. Here we examine the relationship between heterozygosity and social behavior among unrelated adult female rhesus macaques living on the island of Cayo Santiago (Puerto Rico). We show that female macaques with lower mean neutral heterozygosity were discriminated against by their unrelated conspecifics: less heterozygous females received aggressive behavior at higher rates and received affiliation at lower rates than more heterozygous females. We demonstrate that these results are likely due to local genomic effects associated with particular microsatellite loci. Our study suggests that genetic characteristics can impact the way an individual experiences its social environment and that female macaques that are homozygous at two microsatellite loci appear to be less attractive social partners based on grooming and aggression received by unrelated conspecifics.

The ability to recognize kin and thus behaviourally discriminate between conspecifics based on genetic relatedness is of importance both in acquiring inclusive fitness benefits and to enable optimal inbreeding. In primates, mechanisms allowing recognition of paternal relatives are of particular interest, given that in these mating systems patrilineal information is unlikely to be available via social familiarity. Humans use visual phenotype matching based on facial features to identify their own and other's close relatives, and recent studies suggest similar abilities may be present in other species. However it is unclear to what extent familial resemblances remain detectable against the background levels of relatedness typically found within demes in the wild – a necessary condition if facial cues are to function in kin recognition under natural conditions. Here, we experimentally investigate whether parent-offspring relationships are discernible in rhesus macaque (Macaca mulatta) faces drawn from a large free-ranging population more representative of the latter scenario, and in which genetic relatedness has been well quantified from pedigrees determined via molecular markers. We used the human visual system as a means of integrating multiple types of facial cue simultaneously, and demonstrate that paternal, as well as maternal, resemblance to both sons and daughters can be detected even by human observers. Experts performed better than participants who lacked previous experience working with nonhuman primates. However the finding that even naïve individuals succeeded at the task underlines the strength of the phenotypic cues present in faces.

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.

Previous studies showed that olfactory cues are important for mammalian communication. However, many specific compounds that convey information between conspecifics are still unknown. To understand mechanisms and functions of olfactory cues, olfactory signals such as volatile compounds emitted from individuals need to be assessed. Sampling of animals with and without scent glands was typically conducted using cotton swabs rubbed over the skin or fur and analysed by gas chromatography-mass spectrometry (GC-MS). However, this method has various drawbacks, including a high level of contaminations. Thus, we adapted two methods of volatile sampling from other research fields and compared them to sampling with cotton swabs. To do so we assessed the body odor of common marmosets (Callithrix jacchus) using cotton swabs, thermal desorption (TD) tubes and, alternatively, a mobile GC-MS device containing a thermal desorption trap. Overall, TD tubes comprised most compounds (N = 113), with half of those compounds being volatile (N = 52). The mobile GC-MS captured the fewest compounds (N = 35), of which all were volatile. Cotton swabs contained an intermediate number of compounds (N = 55), but very few volatiles (N = 10). Almost all compounds found with the mobile GC-MS were also captured with TD tubes (94%). Hence, we recommend TD tubes for state of the art sampling of body odor of mammals or other vertebrates, particularly for field studies, as they can be easily transported, stored and analysed with high performance instruments in the lab. Nevertheless, cotton swabs capture compounds which still may contribute to the body odor, e.g. after bacterial fermentation, while profiles from mobile GC-MS include only the most abundant volatiles of the body odor.

Conversion of tropical forests into oil palm plantations reduces the habitats of many species, including primates, and frequently leads to human-wildlife conflicts. Contrary to the widespread belief that macaques foraging in the forest-oil palm matrix are detrimental crop pests, we show that the impact of macaques on oil palm yield is minor. More importantly, our data suggest that wild macaques have the potential to act as biological pest control by feeding on plantation rats, the major pest for oil palm crops, with each macaque group estimated to reduce rat populations by about 3,000 individuals per year (mitigating annual losses of 112 USD per hectare). If used for rodent control in place of the conventional method of poison, macaques could provide an important ecosystem service and enhance palm oil sustainability.

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.

Neophobia (the fearful reaction to novel stimuli or situations) has a crucial effect on individual fitness and can vary within and across species. However, the factors predicting this variation are still unclear. In this study, we assessed whether individual characteristics (rank, social integration, sex) and species socio-ecological characteristics (dietary breadth, group size, domestication) predicted variation in neophobia. For this purpose, we conducted behavioral observations and experimental tests on 78 captive individuals belonging to 10 different ungulate species-an ideal taxon to study inter-specific variation in neophobia given their variety in socio-ecological characteristics. Individuals were tested in their social groups by providing them with familiar food, half of which had been positioned close to a novel object. We monitored the individual latency to approach and eat food and the proportion of time spent in its proximity. Using a phylogenetic approach and social network analyses, we showed that across ungulate species neophobia was higher in socially more integrated individuals, as compared to less integrated ones. In contrast, rank and sex did not predict inter-individual differences in neophobia. Moreover, species differed in their levels of neophobia, with Barbary sheep being on average less neophobic than all the other study species. As group size in Barbary sheep was larger than in all the other study species, these results support the hypothesis that larger group size predicts lower levels of neophobia, and confirm ungulates as a highly promising taxon to study animal behavior and cognition with a comparative perspective.In several species, individuals may respond fearfully to novel stimuli, therefore reducing the risks they may face. However, it is yet unclear if certain individuals or species respond more fearfully to novelty. Here, we provided food to 78 individual ungulates with different characteristics (e.g., sex, rank, social integration, group size, domestication, dietary breadth) in different controlled conditions (e.g., when food was close to novel or to familiar objects). Across species, we found that socially integrated individuals responded more fearfully in all species. Moreover, being in larger groups decreased the probability of fearfully responding to novelty.The online version contains supplementary material available at 10.1007/s00265-021-03041-0.

Among mammals, individuals form strong social bonds preferentially with their kin. Differences in these relationships are linked to differential kin availability due to sex-specific dispersal patterns, but there is some indication that differential bonding among sexes already occurs prior to maturation. However, little is known about how these patterns arise during individual development. Here we investigated sex differences in the development of mother-offspring bonds in rhesus macaques (Macaca mulatta). Our results revealed that mothers showed sex-biased bonding toward their offspring. Sons had a distinctly higher probability of receiving aggression from their mothers than did daughters in the first year of life, while no differences were found with respect to affiliative interactions. After the first year, probabilities of all affiliative and aggressive behaviours investigated were higher for daughters than for sons, although generally declining. Furthermore, sons spending less time with their mother and receiving more maternal aggression tended to disperse earlier. The results of our study suggest that mothers influence their bonding strength with offspring by interacting less affiliative with sons than daughters.

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 significant behavioural modifications in sociality of southern pig-tailed macaques visiting Malaysian oil palm plantations in search of food despite elevated predation risk. Specifically, we found critical reductions of key positive social interactions but higher rates of aggression in the plantation interior compared to the plantation edge (i.e. plantation areas bordering the forest) and the forest. At the plantation edge, affiliation even increased compared to the forest, while central positions in the macaques' social network structure shifted from high-ranking adult females and immatures to low-ranking individuals. Further, plantations also affected mother-infant relationships, with macaque mothers being more protective in the open plantation environment. We suggest that although primates can temporarily persist in human-altered habitats, their ability to permanently adapt requires the presence of close-by forest and comes with a trade-off in sociality, potentially hampering individual fitness and infant 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.

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.The online version contains supplementary material available at 10.1007/s10764-023-00356-9.

Abstract When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half‐siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half‐siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half‐siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co‐segregation of paternal half‐sibs in our study reflects active choice or is a by‐product of the group‐specific kin structures, prior to fission.

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.

In promiscuous primates, interactions between adult males and infants have rarely been investigated. However, recent evidence suggests that male affiliation towards infants has an influence on several aspects of the infants' life. Furthermore, affiliations may be associated with male reproductive strategy. In this study, we examined which social factors influenced male-infant affiliation initiated by either male or infant, in wild crested macaques (Macaca nigra). We combined behavioral data and genetic paternity analysis from 30 infants living in three wild groups in Tangkoko Reserve, Indonesia. Our results indicate that adult males and infants do not interact at random, but rather form preferential associations. The social factors with the highest influence on infant-initiated interactions were male rank and male association with the infant's mother. While infants initiated affiliations with males more often in the absence of their mothers, adult males initiated more affiliations with infants when their mothers were present. Furthermore, males initiated affiliations more often when they were in the same group at the time the infant was conceived, when they held a high dominance rank, or when they had a close relationship with the mother. Interestingly, paternity did not affect male-infant affiliation despite being highly skewed in this species. Overall, our results suggest that adult males potentially associate with an infant to secure future mating with the mother. Infants are more likely to associate with a male to receive better support, suggesting a strategy to increase the chance of infant survival in a primate society with high infant mortality. We explore social relationships between males and infants in a promiscuous primate, the wild crested macaque. Our novel approach addresses the nature of affiliations both from males' and infants' perspectives. The results show that males and infants form preferential associations. Male-female affiliation, but not paternity, was a significant predictor of interactions initiated both by males and infants. Males initiated more interactions towards infants when the mother was in proximity, while infants initiated more interactions in her absence. Finally, high-ranking males were more likely to initiate interactions towards infants. We demonstrated that paternity is not a good predictor of male-infant affiliations, even in a species with a high reproductive skew and a relatively high confidence of paternity. Our paper is one of the first to show that infants are active agents in establishing and maintaining preferential relationships with males.

Abstract 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. In this 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. 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. 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.

Abstract Innovation is the ability to solve novel problems or find novel solutions to familiar problems, and it is known to affect fitness in both human and non-human animals. In primates, innovation has been mostly studied in captivity, although differences in living conditions may affect individuals’ ability to innovate. Here, we tested innovation in a wild group of Barbary macaques ( Macaca sylvanus ). In four different conditions, we presented the group with several identical foraging boxes containing food. To understand which individual characteristics and behavioural strategies best predicted innovation rate, we measured the identity of the individuals manipulating the boxes and retrieving the food, and their behaviour during the task. Our results showed that success in the novel task was mainly affected by the experimental contingencies and the behavioural strategies used during the task. Individuals were more successful in the 1-step conditions, if they participated in more trials, showed little latency to approach the boxes and mainly manipulated functional parts of the box. In contrast, we found no effect of inhibition, social facilitation and individual characteristics like sex, age, rank, centrality, neophobia and reaction to humans, on the individuals’ ability to innovate.

Abstract With increasing anthropogenic pressure, interactions between humans and wildlife may become more frequent, including conflictual ones. To reduce conflicts, it is important to understand how different factors (e.g. education, previous experience, demographic variables) interplay with each other and contribute to the emergence of negative attitudes and behaviours toward wildlife in humans. To address this issue, we conducted a large-scale questionnaire in Malaysia, focusing on potential conflicts between human and other primates. We used generalized linear mixed models to assess how formal education, knowledge about primates, negative experience and potential competition affected participants’ negative attitudes to primates (i.e. how humans perceive primates), their behavioural intentions (i.e. opinion on how to reduce conflicts) and behaviour (i.e. measures taken to reduce negative interactions). We found that negative experience and potential competition had a negative impact on participants’ attitude and behavior (i.e. primates were more likely perceived as filthy, as negatively affecting residents’ health and safety, and as an increasing problem, with participants more likely to use invasive methods, including captures). Both higher education and better knowledge of primates predicted more positive behavioural intentions (i.e. primates should be protected, non-invasive interventions should be used). Higher education, however, was also linked to more negative attitudes (i.e. primates negatively affect residents’ health and safety), and partly to negative behavior (e.g. use of invasive methods). In contrast, better knowledge about primates predicted positive behaviour (i.e. exclusive use of non-invasive methods). Therefore, although better knowledge of primates had no clear effect on human attitudes, it may impact on their decisions to reduce potential conflicts with wildlife, and might be the most powerful tool to mitigate conflicts between humans and other species.

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.

Abstract In animals, high fission-fusion dynamics characterize groups in which individuals frequently split into subgroups of different size and composition, and may be linked to the enhancement of cognitive skills. However, this hypothesis has rarely been tested. Here, we compared two zebra species with different levels of fission-fusion dynamics, Chapman’s zebras ( Equus burchelli chapmanni ) and Grévy’s zebras ( Equus grevyi ), to assess potential differences in their cognitive skills. We tested 8 individuals of each species in experimental tasks assessing their object permanence, short-term memory, inference and quantity discrimination skills. Our results showed that Grévy’s zebras, which are characterized by higher levels of fission-fusion dynamics, performed better than Chapman’s zebras in tasks requiring inference and quantity discrimination skills. These findings provide preliminary support to the hypothesis that high fission-fusion dynamics are linked to the enhancement of specific cognitive skills also in taxa other than primates.

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 = 682 offspring; randomization P = 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.

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 ± <25% RSD (R2 > 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.

Following over 20 years of research on the climatic effects on biodiversity we now have strong evidence that climate change affects phenology, fitness, and distribution ranges of different taxa, including birds. Bird phenology likely responds to changes in local weather. It is also affected by climatic year-to-year variations on larger scales. Although such scale-related effects are common in ecology, most studies analyzing the effects of climate change were accomplished using climatic information on a single spatial scale. In this study, we aimed at determining the scale-dependent sensitivity of breeding phenology and success to climate change in a migratory passerine bird, the barn swallow (Hirundo rustica). For both annual broods, we investigated effects of local weather (local scale) and the North Atlantic Oscillation (NAO, large scale) on the timing of breeding and breeding success. Consistent with previous studies in migratory birds we found that barn swallows in Eastern Germany bred progressively earlier. At the same time, they showed reduced breeding success over time in response to recent climatic changes. Responses to climatic variation were observed on both local and large climatic scales, but they differed with respect to the ecological process considered. Specifically, we found that the timing of breeding was primarily influenced by large-scale NAO variations and to a lesser extent by local weather on the breeding grounds. Conversely, climatic conditions on the local scale affected breeding success, exclusively. The observed decrease in breeding success over years is likely a consequence of scale-related mismatches between climatic conditions during different breeding phases. This provides further evidence that a species' response of earlier breeding may not be enough to cope with climate change. Our results emphasize the importance of considering the response of ecological processes along different climatic scales in order to better understand the complexity of climate change effects on biodiversity.

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.

An increasing number of studies suggest that olfaction is important for communication throughout the order of primates. Callitrichids, in particular, have well-developed olfactory systems and use anogenital glands to produce scent marks. Behavioural studies have shown that male common marmosets (Callithrix jacchus) distinguish between odours from the peri-ovulatory and luteal phase of females. However, large gaps remain in understanding the chemical underpinnings of olfactory cues. To investigate whether chemical cues vary with female fertility and reproductive quality, our study combined behavioural bioassays with chemical analyses of the anogenital odours of female common marmosets using gas chromatography-mass spectrometry. We found that cycle states, age and parity have an impact on chemical profiles and further identified affected chemical substances. Our results confirm and expand on previous behavioural evidence for cues of fertility. Our results indicate that cycle-related substances likely act as chemical cues. Males could use such olfactory fertility cues to optimize their mating effort and thereby increase their paternity certainty. This certainty could enhance paternal care for their infants. The results of our study open a promising avenue to find the metabolic pathways from which chemical cues of fertility arise and to unravel their importance during primate evolution in future comparative studies.

Abstract 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.

High social status is the primary determinant of reproductive success among group-living male mammals. Primates living in multimale-multifemale groups show the greatest variation in the strength of this link, with marked variation in reproductive skew by male dominance among species, dependent on the degree of female fertile phase synchrony, and the number of competing males. Here, we present data on two groups of wild crested macaques (Macaca nigra), living in the Tangkoko Reserve, Sulawesi, Indonesia. We investigated male monopolization of fertile females in 31 cycles of 19 females, and genetic paternity of 14 offspring conceived during the study period. We show that female fertile phase synchrony was low, that females had few mating partners in their fertile phase, and that dominant males monopolized a high proportion of consortships and matings, resulting in marked and steep mating and reproductive skew. We conclude that female cycle asynchrony provides the opportunity for strong direct male-male competition in crested macaques, resulting in monopolization of females by dominant males, consistent with their marked sexual dimorphism. Our study provides a test of the underlying factors that determine the relative occurrence and strength of different mechanisms of sexual selection, and the phenotypes that evolve as a result.

Biological relatedness is a key consideration in studies of behavior, population structure, and trait evolution. Except for parent-offspring dyads, pedigrees capture relatedness imperfectly. The number and length of DNA segments that are identical-by-descent (IBD) yield the most precise estimates of relatedness. Here, we leverage novel methods for estimating locus-specific IBD from low coverage whole genome resequencing data to demonstrate the feasibility and value of resolving fine-scaled gradients of relatedness in free-living animals. Using primarily 4-6× coverage data from a rhesus macaque (Macaca mulatta) population with available long-term pedigree data, we show that we can call the number and length of IBD segments across the genome with high accuracy even at 0.5× coverage. The resulting estimates demonstrate substantial variation in genetic relatedness within kin classes, leading to overlapping distributions between kin classes. They identify cryptic genetic relatives that are not represented in the pedigree and reveal elevated recombination rates in females relative to males, which allows us to discriminate maternal and paternal kin using genotype data alone. Our findings represent a breakthrough in the ability to understand the predictors and consequences of genetic relatedness in natural populations, contributing to our understanding of a fundamental component of population structure in the wild.

Humans' colonization of diverse habitats relied on our ancestors' abilities to innovate and share innovations with others.While ecological impacts on innovations are well studied, their effect on social learning remains poorly understood.We examined how food availability affects social learning in migrant orangutan unflanged males, who may learn from local orangutans through peering (i.e., observational social learning).We analyzed 1,384 dyadic associations, including 360 peering events, among 46 wild Sumatran orangutan and 25 Bornean orangutan males, collected over 18 years.Migrants' peering rates significantly increased with higher food availability and time spent in proximity to others.Furthermore, migrants in the more sociable Sumatran population exhibited significantly higher peering rates compared to the Borneans, suggesting intrinsic and/or developmental effects of food availability on social learning.These findings emphasize the importance of investigating ecological effects on social learning on the immediate, developmental, and intrinsic levels for our understanding of cultural evolution.

Abstract 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 catarrhines. We observed the sniffing behavior of semi‐free ranging Barbary macaques, Macaca sylvanus , at Affenberg Salem, Germany, to assess how frequently macaques sniff and in which contexts, and how sniffing is affected by sex and age. Focal observations of 24 males and 24 females aged 1–25 years showed that Barbary macaques sniffed, on average, 5.24 times per hour, with more than 80% of sniffs directed at food. Irrespective of the context, younger individuals sniffed more often than older ones. Females’ sniffs were more often directed at food than male sniffs, while males sniffed more often than females in a social context. Sniffs at conspecifics occurred primarily 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 may play a role in male mating decisions, but the role of olfaction in sexual interactions warrants further investigations. In sum, results show that Barbary macaques routinely use olfaction during feeding, but also in a socio‐sexual context, corroborating the relevance of the olfactory sense in the lives of catarrhine primates.

Abstract In their natural environment, animals face a variety of ecological and social challenges, which might be linked to the emergence of different cognitive skills. To assess inter-specific variation in cognitive skills, we used ungulates as a study model, testing a total of 26 captive individuals across 5 different species (i.e., dwarf goats, Capra aegagrus hircus , llamas, Lama glama , guanacos, Lama guanicoe , zebras, Equus grevyi , and rhinos, Diceros bicornis michaeli ). Across species, we used the same well-established experimental procedures to test individuals’ object permanence, short-term memory, causality, understanding of object properties, and gravity. Our results revealed that study subjects showed object permanence, were able to remember the position of hidden food after up to 60 seconds, and inferred the position of hidden food from the sound produced or not produced when shaking containers. Moreover, they showed an understanding of basic object properties, being able to locate objects hidden behind occluders based on their size and inclination, and could reliably follow the trajectory of falling objects across different conditions. Finally, inter-specific differences were limited to the understanding of object properties, and suggest that domesticated species as goats might perform better than non-domesticated ones in tasks requiring these skills. These results provide new information on the cognitive skills of a still understudied taxon and confirm ungulates as a promising taxon for the comparative study of cognitive evolution.

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.

In most primate species, females remain in the natal group with kin while males disperse away from kin around the time of puberty. Philopatric females bias their social behavior toward familiar maternal and paternal kin in several species, but little is known about kin bias in the dispersing sex. Male dispersal is likely to be costly because males encounter an increased risk of predation and death, which might be reduced by dispersing together with kin and/or familiar males (individuals that were born and grew up in same natal group) or into a group containing kin and/or familiar males. Here we studied the influence of kinship on familiar natal migrant rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico, by combining demographic, behavioral, and genetic data. Our data suggest that kinship influences spatial proximity between recent natal immigrants and males familiar to them. Immigrants were significantly nearer to more closely related familiar males than to more distantly related individuals. Within a familiar subgroup, natal migrants were significantly closer to maternal kin, followed by paternal kin, then non-kin, and finally to males related via both the maternal and paternal line. Spatial proximity between natal immigrants and familiar males did not decrease over time in the new group, suggesting that there is no decline in associations between these individuals within the first months of immigration. Overall, our results might indicate that kinship is important for the dispersing sex, at least during natal dispersal when kin are still available.

Abstract Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills ( M andrillus sphinx ), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.

Extra-group paternity (EGP) has been described in various mammalian species; however, little is known about which factors contribute to the variation in EGP, as the majority of studies were restricted in time and the number of groups considered. Using longitudinal demographic and genetic data, we aim to investigate which factors predict rates of EGP in the free-ranging rhesus macaque population of Cayo Santiago, Puerto Rico (USA). Of the 1649 infants considered which were born into six social groups over 9 years, we identified an average of 16% of infants resulting from EGPs. We tested the influence of group size, breeding group sex ratio, female reproductive synchrony, and group instability on the occurrence of EGPs. Our results suggest a tendency for EGPs to increase as the proportion of females increased in larger groups, but no such effect in smaller groups. Furthermore, as group instability and female reproductive synchrony decreased, the number of EGPs tended to increase. Our results support the hypothesis that group structure affects the occurrence of EGPs, which might be mediated by male mating opportunities, male monopolization potential, and/or female choice. In several species, both sexes seek alternative reproductive strategies to enhance their reproductive success. For instance, females may pursue EGPs to potentially increase genetic compatibility with males, or males may seek EGPs to improve their mating opportunities. Our longitudinal analysis, including demographic and genetic data over 9 years of six social groups of rhesus macaques, revealed high variation in the occurrence of EGPs across groups and years, and this variation tended to depend on group characteristics such as breeding group size, sex ratio, female synchrony, and group instability. The data suggest that group structure affects the number of EGPs in this group-living primate. Our results show that EGPs can affect the distribution of paternity within social groups and should be taken into account when assessing reproductive success.

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.

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.

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.

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. 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.

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.

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.

Abstract 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.

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.

Abstract Background In the first years of their lives, children develop the cognitive, social and emotional skills that will provide the foundations for their lifelong health and achievements. To increase their life prospects and reduce the long-term effects of early aversive conditions, it is therefore crucial to understand the risk factors that negatively affect child development and the factors that are instead beneficial. In this study, we tested (i) the effects of different social and environmental stressors on maternal stress levels, (ii) the dynamic relationship between maternal stress and child behavior problems during development, and (iii) the potential promotive (i.e. main) or protective (i.e. buffering) effect of siblings on child behavior problems during development. Methods We used longitudinal data from 373 mother–child pairs (188 daughters, 185 sons) from pregnancy until 10 years of age. We assessed maternal stress and child behavior problems (internalizing and externalizing) with validated questionnaires, and then used linear mixed models, generalized linear mixed models and longitudinal cross-lagged models to analyze the data. Results Our results showed that higher maternal stress levels were predicted by socio-environmental stressors (i.e. the lack of sufficient social areas in the neighborhood). Moreover, prenatal maternal stress reliably predicted the occurrence of behavior problems during childhood. Finally, the presence of older siblings had a promotive function, by reducing the likelihood that children developed externalizing problems. Conclusions Overall, our results confirm the negative effects that maternal stress during pregnancy may have on the offspring, and suggest an important main effect of older siblings in promoting a positive child development.

Abstract Males may increase their fitness by providing care to offspring or to unrelated infants of female “friends” to maximise future mating. The potential for paternal care depends on paternity certainty, particularly in multi-male, multi-female groups with polygynandrous mating. In crested macaques ( Macaca nigra ), there seems to be high potential for paternity certainty and need for paternal protection. However, male-mother affiliation (or “friendships”), not paternity, predicts male-infant affiliation, questioning whether males can identify their offspring reliably. Using a Bayesian approach, we investigated male responses to infant screams (N = 2,637) emitted during agonistic interactions with males being the friend of the infant, the friend of the infants’ mother, and/or the father of the infant. Overall, male responses to infant screams were low. Bayesian estimates showed considerable uncertainty; hence, results should be interpreted cautiously. However, males were slightly more likely to react if the infant or its mother was a friend of the male or if the infant was his offspring. Additionally, higher-ranking males were slightly more likely to respond than lower-ranking ones, and screams from infants of lower-ranking females were more likely to be responded to. This might indicate that males assess paternity based on their rank and that they assess the need to intervene. Given the limitations of our study and the uncertainty surrounding our results, future studies are needed before we can draw solid conclusions for crested macaques. Overall, our results are in line with other studies suggesting that male primates provide care to related and unrelated infants.

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.

In social animals, kin relations strongly shape the social structure of a group. In female-bonded species, maternal relatedness is likely to be mediated via familiarity, but evidence is accumulating that non-human primates are able to recognize kin that they are not familiar with and adjust their behavior accordingly. In playback experiments, female rhesus macaques showed increased interest in ‘coo’ calls produced by unfamiliar paternal half-sisters compared to ‘coo’ calls produced by unfamiliar unrelated females, suggesting that these calls should have some common structural characteristics that facilitate the discrimination of kin from non-kin. Here we analyzed ‘coo’ calls of 67 adult female rhesus macaques from four groups and seven matrilines living on the island of Cayo Santiago (Puerto Rico). We tested whether the call structure of closely maternal and/or paternal related females, as determined from extensive pedigree data, differed from the call structure of unrelated females, while controlling for familiarity (i.e., group-matrilineal membership and age difference) of subjects. In contrast to our expectation, kinship did not predict similarities in ‘coo’ call structure, whereas ‘coo’ structure was more similar when produced by females of similar age as well as by females with higher familiarity, suggesting that experience is more decisive than genetic background. The high number of individuals in the analysis and the high accuracy of the assignment of calls to individuals render a lack of power as an unlikely explanation. Thus, based on the results of this study, kin recognition in rhesus monkeys does neither appear to be based on the assessment of self-similarity, nor on the comparison among related subjects (i.e., acoustic phenotype matching), but appears to be mediated by different or multiple cues. Furthermore, the results support the notion that frequent social interactions result in increasing acoustic similarity within largely innate call types (‘vocal accommodation’).

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.

Abstract In the animal kingdom, conspicuous colors are often used for inter- and intra-sexual communication. Even though primates are the most colorful mammalian taxon, many questions, including what potential information color signals communicate to social partners, are not fully understood. Vervet monkeys ( Chlorocebus pygerythrus ) are ideal to examine the covariates of color signals. Males have multi-colored genitals, which they present during distinctive male-male interactions, known as the “Red-White-and-Blue” (RWB) display, but the genitals are also visible across a variety of other contexts, and it is unclear what this color display signals to recipients. We recorded genital color presentations and standardized digital photos of male genitals ( N = 405 photos) over one mating season for 20 adult males in three groups at the Samara Private Game Reserve, South Africa. We combined these with data on male characteristics (dominance, age, tenure length, injuries, and fecal glucocorticoid metabolite concentrations). Using visual modeling methods, we measured single colors (red, white, blue) but also the contrasts between colors. We assessed the frequency of the RWB genital display and male variation in genital coloration and linked this to male characteristics. Our data suggest that the number of genital displays increased with male dominance. However, none of the variables investigated explained the inter- and intra-individual variation in male genital coloration. These results suggest that the frequency of the RWB genital display, but not its color value, is related to dominance, providing valuable insights on covariation in color signals and their display in primates. Significance statement Conspicuous colors in animals often communicate individual quality to mates and rivals. By investigating vervet monkeys, a primate species in which males present their colorful genitals within several behavioral displays, we aim to identify the covariates of such colorful signals and their behavioral display. Using visual modeling methods for the color analysis and combining behavioral display data and color data with male characteristics, we found that high-ranking males displayed their colorful genitals more frequently than lower-ranking ones. In contrast, color variation was not influenced by male dominance, age, tenure length, or health. Our results can serve as a basis for future investigations on the function of colorful signals and behavioral displays, such as a badge of status or mate choice in primates.

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.

Abstract 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.

In mammalian species, olfactory cues are important for within and between species communication. These cues can be part of multimodal signals indicating, for example, female fertility potentially perceived by male conspecifics. However, a large gap exists in our understanding of multimodal signaling in non-human catarrhines. Chimpanzees ( Pan troglodytes ) live in fission-fusion societies, mate promiscuously and express high levels of male-male competition. Females show a striking visual signal, an exaggerated sexual swelling, known to be a proxy of ovulation, while the maximum swelling is not matching the exact time of ovulation. The question remains if males use additional olfactory cues when being able to approach females closely. This would allow males to pinpoint the exact timing of ovulation and could be one reason why high-ranking males sire offspring more successfully than other males. Here, we present the first systematic test of such multimodal signaling by investigating male sniffing behavior directed to females in relation to their fertility in a group of 13 captive chimpanzees. Our results show that male sniffing behavior significantly increased with female swelling size, with female age as well as when fewer male competitors were present. Hence, odors might be part of a multimodal fertility cue, supporting the idea that males monitor both visual and olfactory cues to gain comprehensive information on female fertility.

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.

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.

[This corrects the article DOI: 10.3389/fpsyg.2021.666166.].

ABSTRACT Most catarrhine primates are considered to be strongly visually oriented, 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 several taxa ranging from insects to humans. Here, 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. We presented monkeys with pipes containing food (peanuts, popcorn), non-food (stones, feces) or no items in transparent or opaque containers, and assessed whether animals looked, sniffed and/or grabbed into the pipes depending on visibility of the contents (experiment 1). Visual information had no robust effect on sniffing probability, but it did affect sniffing behavior with respect to the timing of olfactory inspections (i.e. whether sniffing occurred first). Both visual and olfactory information affected, whether or not monkeys attempted to retrieve the items from the pipes. Furthermore, we manipulated the visual appearance of familiar food items (popcorn) with food colorant (experiment 2), which resulted in substantially increased olfactory inspections compared to unmanipulated popcorn. Taken together, 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.

Humans’ colonization of diverse habitats relied on our ancestors' abilities to innovate and share innovations with others. While ecological impact on innovations is well studied, its effect on social learning remains poorly understood. We examined how food availability affects social learning in migrant orangutan unflanged males, who may learn from local orangutans through peering (i.e., observational social learning). We analysed 1384 dyadic associations, including 360 peering events, among 46 wild Sumatran orangutan and 25 Bornean orangutan males, collected over 18 years. Migrants’ peering rates significantly increased with higher food availability and time spent in proximity to others. Furthermore, migrants in the more sociable Sumatran population exhibited significantly higher peering rates compared to the Bornean`s, suggesting intrinsic and/or developmental effects of food availability on social learning. These findings emphasize the importance of investigating ecological effects on social learning on the immediate, developmental, and intrinsic levels for our understanding of cultural evolution.

Data supporting the findings of the study 'Agricultural habitat use affects infant survivorship in an endangered macaque species'

Data supporting the findings of the study 'Agricultural habitat use affects infant survivorship in an endangered macaque species'

Dataset for Chanvin, M., Lamarque, F., Diko, N., Agil, M., Micheletta, J., Widdig, A. (2023). Ten years of positive impact of a conservation education program on children's knowledge and behaviour towards crested macaques (Macaca nigra) in the Greater Tangkoko Area, North Sulawesi, Indonesia. International Journal of Primatology.

Dataset for Chanvin, M., Lamarque, F., Diko, N., Agil, M., Micheletta, J., Widdig, A. (2023). Ten years of positive impact of a conservation education program on children's knowledge and behaviour towards crested macaques (Macaca nigra) in the Greater Tangkoko Area, North Sulawesi, Indonesia. International Journal of Primatology.

Dataset for Chanvin, M., Lamarque, F., Diko, N., Agil, M., Micheletta, J., Widdig, A. (2023). Ten years of positive impact of a conservation education program on children's knowledge and behaviour towards crested macaques (Macaca nigra) in the Greater Tangkoko Area, North Sulawesi, Indonesia. International Journal of Primatology.

Dataset for Chanvin, M., Lamarque, F., Diko, N., Agil, M., Micheletta, J., Widdig, A. (2023). Ten years of positive impact of a conservation education program on children's knowledge and behaviour towards crested macaques (Macaca nigra) in the Greater Tangkoko Area, North Sulawesi, Indonesia. International Journal of Primatology.

Although primates have long been regarded as microsmatic, recent studies indicate that olfaction is an important sensory mode of primate communication, e.g., in the context of reproduction. However, large gaps remain in our understanding of primate olfactory traits, especially in the great apes. Female chimpanzees (Pan troglodytes) possess an exaggerated sexual swelling, which is an imprecise signal of fertility that is thought to serve to confuse paternity. However, some high-ranking males that copulate most frequently on the days when females are most fertile seem to have more precise information on the timing of ovulation, which suggests the existence of an olfactory fertility trait. In order to examine, and provide evidence for, fertility-related chemical information in female chimpanzees, we used gas chromatography-mass spectrometry to analyze the chemical composition of female body odor collected across the menstrual cycle during various stages of sexual swelling (97 samples of six females). The chemical composition was significantly affected by swelling stage, and eight substances were detected that were strongly related to the latter. The existence of an additional, olfactory, fertility trait may help males to fine-tune their sexual behavior or allow females to strengthen concealment of the exact timing of ovulation, and needs to be further investigated in follow-up studies. The results of our study provide much-needed evidence for the existence of an olfactory cue related to reproduction in chimpanzees, and form a basis for future studies on the interplay between visual and olfactory information on female fertility.

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.