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Socioecological factors are associated with life-history patterns and growth trajectories among primates. Under certain conditions, selection may favor a temporal decoupling of growth and major life-history events such as sexual maturation or natal dispersal. Yet, empirical tests of these associations in wild populations remain scarce owing to the lack of non-invasive methods to capture growth trajectories. In this study, we first compared two non-invasive methods of digital photogrammetry. Then, we used parallel laser photogrammetry to investigate forearm growth of wild Assamese macaque males and females in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand to test life-history and socio-ecological hypotheses. Across 48 males and 44 females, we estimated growth trajectories and pseudo-velocity curves by applying quadratic plateau models and non-parametric LOESS regressions. We assessed the development of sexual dimorphism by comparing the sexes at five different ages. Females had completed 96% of their growth at the age at first birth (5.9 years) and ceased growing at 7.1 years of age. Males, in contrast, grew until well after their average age of natal dispersal: they reached 81% of their size at the age of natal dispersal (4.0 years), and ceased growing only at 9.0 years of age, much later than females. Sexual dimorphism in forearm length was driven by an extended growth period in males, which is expected for males dispersing between multimale and multifemale groups and not facing the risk of being ousted by other larger males. Our results contradict the neonatal investment hypothesis that predicts a desynchronization of investment in growth and reproduction only in female baboons, but not other papionins producing cheaper neonates. Furthermore, male Assamese macaques do not delay natal dispersal until they are fully grown, in accordance with predictions of the male-career-framework for species with low to medium level of direct competition.

Objectives: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. Materials and methods: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. Results: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%–3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, latestage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. Discussion: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods. Canadian Institute for Advanced Research/[]/CIFAR/Canadá UCR::Vicerrectoría de Docencia::Ciencias Básicas::Facultad de Ciencias::Escuela de Biología

Social animals invest time and resources into building and adapting their social environment, which emerges not only from their own but also from the decisions of other group members. Thus, individuals have to monitor interactions between others and potentially decide when and how to interfere to prevent damage to their own investment. These interventions can be subtle, as in the case of affiliative interactions such as grooming, but they can inform us about how animals structure their world and influence other group members. Here, we used interventions into grooming bouts in 29 female rhesus macaques (Macaca mulatta) to determine who intervened into which grooming bouts, why, and what determined intervention outcomes, based on kinship, dominance rank, and affiliative relationships between groomers and (potential) interveners. Using 1132 grooming bouts and 521 interventions, we show that high dominance rank of groomers reduced the risk of intervention. Bystanders, particularly when high-ranking, intervened in grooming of their kin, close affiliates, and close-ranked competitors. Interveners gained access to their close affiliates for subsequent grooming. Affiliative relationship and rank determined intervention outcomes, with reduced aggression risk facilitating grooming involving three individuals. Thus, interventions in this species involved the monitoring of grooming interactions, decision-making based on several individual and dyadic characteristics, and potentially allowed individuals to broaden their access to grooming partners, protect their own relationships, and influence their social niche.

Recognizing emotions is an essential ability for successful interpersonal interaction. Prior research indicates some links between the endocrine system and emotion recognition ability, but only a few studies focused on within-subject differences across distinct ovulatory cycle phases and this ability. These studies have demonstrated mixed results that might be potentially due to heterogeneity in experimental tasks, methodologies, and lacking ecological validity. In the current study, we investigated associations between within-subject differences in ovarian hormones levels and emotion recognition from auditory, visual, and audiovisual modalities in N = 131 naturally cycling participants across the late follicular and mid-luteal phase of the ovulatory cycle. We applied a within-subject design with sessions in the late follicular and mid-luteal cycle phase, and also assessed salivary progesterone and estradiol in these sessions. Our findings did not reveal any significant difference in emotion recognition ability across two cycle phases. Thus, they emphasize the necessity of employing large-scale replication studies with well-established study designs along with proper statistical analyses. Moreover, our findings indicate that the potential link between ovulatory cycle phases (late follicular and mid-luteal) and emotion recognition ability might have been overestimated in previous studies, and may contribute to theoretical and practical implications of socio-cognitive neuroendocrinology.

Abstract It has long been recognized that the patterning of social interactions within a group can give rise to a social structure that holds very different places for different individuals. Such within-group variation in sociality correlates with fitness proxies in fish, birds, and mammals. Broader integration of this research has been hampered by the lack of agreement on how to integrate information from a plethora of dyadic interactions into individual-level metrics. As a step towards standardization, we collected comparative data on affinitive and affiliative interactions from multiple groups each of five species of primates to assess whether the same aspects of sociality are measured by different metrics and indices. We calculated 16 different sociality metrics used in previous research and thought to represent three different sociality concepts. We assessed covariation of metrics within groups and then summarized covariation patterns across all 15 study groups, which varied in size from 5 to 41 adults. With some methodological and conceptual caveats, we found that the number of weak ties individuals formed within their groups represented a dimension of sociality that was largely independent from the overall number of ties as well as from the number and strength of the strong ties they formed. Metrics quantifying indirect connectedness exhibited strong covariation with strong tie metrics and thus failed to capture a third aspect of sociality. Future research linking affiliation and affinity to fitness or other individual level outcomes should quantify inter-individual variation in three aspects: the overall number of ties, the number of weak ties, and the number or strength of strong ties individuals form, after taking into account effects of social network density. Significance statement In recent years, long-term studies of individually known animals have revealed strong correlations between individual social bonds and social integration, on the one hand, and reproductive success and survival on the other hand, suggesting strong natural selection on affiliative and affinitive behavior within groups. It proved difficult to generalize from these studies because they all measured sociality in slightly different ways. Analyzing covariation between 16 previously used metrics identified only three rather independent dimensions of variation. Thus, different studies have tapped into the same biological phenomenon. How individuals are weakly connected within their group needs further attention.

Group-living animals often maintain a few very close affiliative relationships-social bonds-that can buffer them against many of the inevitable costs of gregariousness. Kinship plays a central role in the development of such social bonds. The bulk of research on kin biases in sociality has focused on philopatric females, who typically live in deeply kin-structured systems, with matrilineal dominance rank inheritance and life-long familiarity between kin. Closely related males, in contrast, are usually not close in rank or familiar, which offers the opportunity to test the importance of kinship per se in the formation of social bonds. So far, however, kin biases in male social bonding have only been tested in philopatric males, where familiarity remains a confounding factor. Here, we studied bonds between male Assamese macaques, a species in which males disperse from their natal groups and in which male bonds are known to affect fitness. Combining extensive behavioural data on 43 adult males over a 10-year period with DNA microsatellite relatedness analyses, we find that postdispersal males form stronger relationships with the few close kin available in the group than with the average nonkin. However, males form the majority of their bonds with nonkin and may choose nonkin over available close kin to bond with. Our results show that kinship facilitates bond formation, but is not a prerequisite for it, which suggests that strong bonds are not restricted to kin in male mammals and that animals cooperate for both direct and indirect fitness benefits.

The formation of male-female social bonds and the resulting competition among females for male partners is a core element of human societies. While female competition for a male partner outside the mating context is well studied in humans, evidence from non-human primates is scarce, and its evolutionary roots remain to be explored. We studied two multi male – multi female groups of wild Assamese macaques (Macaca assamensis), a species where females gain benefits from selectively affiliating with particular males. Using a behavioral data set collected over several years, we tested whether females competed over access to male social partners, whether success in competition was driven by female dominance rank, and which male traits were most attractive for females. We found assortative bonding by dominance rank between females and males, which together with females initiating and maintaining contact suggests direct female competition over males. Two male traits independently predicted male attractiveness to females: (1) current dominance rank, a measure of 'power' or a male's ability to provide access to resources, and (2) prior male affiliation with immatures, a measure of a male's potential paternal proclivity or 'commitment' to infant care. Both traits have been consistently identified as drivers of female partner choice in humans. Our study adds to the evidence that female competition for valuable male partners is not unique to humans, suggesting deep evolutionary origins of women's mate choice tendencies for ‘power’ and ‘commitment’.

Forming strong social bonds can lead to higher reproductive success, increased longevity, and/or increased infant survival in several mammal species. Given these adaptive benefits, understanding what determines partner preferences in social bonding is important. Maternal relatedness strongly predicts partner preference across many mammalian taxa. The role of paternal relatedness, however, has received relatively little attention, even though paternal and maternal kin share the same number of genes, and theoretically similar preferences would therefore be expected for paternal kin. Here, we investigate the role of maternal and paternal relatedness in female affiliation in Assamese macaques (Macaca assamensis), a species characterized by a relatively low male reproductive skew. We studied a wild population under natural conditions using extensive behavioral data and relatedness analyses based on pedigree reconstruction. We found stronger affiliative relationships and more time spent grooming between maternal kin and paternal half-sisters compared with nonkin, with no preference of maternal over paternal kin. Paternally related and nonrelated dyads did not form stronger relationships when they had less close maternal kin available, but we would need a bigger sample size to confirm this. As expected given the low reproductive skew, affiliative relationships between paternal half-sisters closer in age were not stronger than between paternal half-sisters with larger age differences, suggesting that the kin bias toward paternal kin was not mediated by age similarity. An alternative way through which paternal kin could get familiarized is mother- and/or father-mediated familiarity.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

The assessment of mucosal immunity as a component of animal health is an important aspect for the understanding of variation in host immunity, and its tradeoff against other life-history traits. We investigated immunoglobulin A (IgA), the major type of antibody associated with mucosal immunity, in relation to changes in parasitic burden following anthelminthic treatment in noninvasively collected fecal samples in a semi-free ranging group of Barbary macaques (Macaca sylvanus). We measured IgA in 340 fecal samples of fourteen females and nine males. As IgA has been found to be responsive to stressors, we also related fecal IgA (fIgA) levels to fecal glucocorticoid metabolites (fGCM) measured in the same samples as part of a previous study. We found a high variability within and between individual fIgA levels over time. Running generalized additive mixed models, we found that fIgA levels were higher in males than in females, but did not change in response to the anthelmintic treatment and the resulting reduction in worm burden. Instead, fIgA level changes were significantly correlated to changes in fGCM levels. Our findings indicate that due to the strong responsiveness of fIgA to HPA-axis activity, the measurement of fIgA may have certain limitations with respect to reflecting gastrointestinal parasitic burden. Moreover, the responsiveness of fIgA to stressors interferes with the interpretation of IgA levels in fecal samples as a measure of mucosal immunity, at least in our study population of the Barbary macaques.

Abstract The source of maternal energy supporting reproduction (i.e., stored or incoming) is an important factor determining different breeding strategies (capital, income or mixed) in female mammals. Key periods of energy storage and allocation might induce behavioral and physiological shifts in females, and investigating their distribution throughout reproduction helps in determining vulnerable phases shaping female reproductive success. Here, we examined the effects of reproductive state on activity budget, feeding behavior, and urinary C-peptide (uCP) levels, a physiological marker of energy balance, in 43 wild female Assamese macaques (Macaca assamensis). Over a 13-month study period, we collected 96,266 instantaneous records of activity and 905 urine samples. We found that early lactating females and non-gestating–non-lactating females follow an energy-saving strategy consisting of resting more at the expense of feeding and consuming mostly fruits which contributed to enhancing their energy intake and feeding efficiency. We found an opposite pattern in gestating and late lactating females who feed more at the expense of resting and consume mostly seeds, providing a fiber-rich diet. Storing food into cheek pouches increased throughout gestation while it decreased all along with lactation. Lastly, we found the highest uCP levels during late gestation. Our results reflect different feeding adaptations in response to the energetic costs of reproduction and suggest a critical role of fat accumulation before conception and metabolizing fat during gestation and lactation. Overall, our study provides an integrative picture of the energetics of reproduction in a seasonal species and contributes to our understanding of the diversity of behavioral and physiological adaptations shaping female reproductive success. Significance statement To offset their substantial energetic investment in reproduction, mammalian females may modify their behavior and the way they extract energy from their environment. In addition, as a result of heightened energy expenditure, female reproduction might trigger physiological shifts. To date, most studies investigated the energetic costs of female reproduction using either a behavioral or a physiological approach. To arrive at a more comprehensive picture, we combined behavioral data with a physiological marker of energy balance, i.e., urinary C-peptide, in a seasonal primate species in its natural habitat. Our results indicate that throughout the reproductive cycle, behavioral and physiological adaptations operate concomitantly, inducing modifications in female activity budget, feeding behavior, and suggesting shifts in fat use. Overall, our results illustrate the relevance of combining data on behavior and hormones to investigate breeding strategies in coping with the energetic costs of reproduction.

The abstract is available here: https://uscholar.univie.ac.at/o:1220815

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships. Publisher PDF

Infant care from adult males is unexpected in species with high paternity uncertainty. Still, males of several polygynandrous primates engage in frequent affiliative interactions with infants. Two non‐exclusive hypotheses link male infant care to male mating strategies. The paternal investment hypothesis views infant care as a male strategy to maximize the survival of sired offspring, while the mating effort hypothesis predicts that females reward males who cared for their infant by preferably mating with them. Both hypotheses predict a positive relationship between infant care and matings with a particular female. However, the paternal investment hypothesis predicts that increased matings come before infant care whereas the mating effort hypothesis predicts that infant care precedes an increase in matings. Both hypotheses are usually tested from the perspective of the proportion of matings and care that individual females engage in and receive, rather than from the perspective of the care and mating behaviour of individual males. We tested the relationships between care and mating from both female and male perspectives in Barbary macaques. Mating predicted subsequent care and care predicted subsequent mating when viewed from the male but not the female perspective. Males mainly cared for infants of their main mating partners, but infants were not mainly cared for by their likely father. Males mated more with the mothers of their favourite infants, but females did not mate more with the main caretakers of their infants. We suggest that females do not choose their mating partners based on previous infant care, increasing paternity confusion. Males might try to increase paternal investment by distributing the care according to their own instead of female mating history. Further, males pursue females for mating opportunities based on previous care.

Animal social bonds are defined as stable, equitable and strong affiliative and cooperative relationships similar to human friendships. Just as human friendships, social bonds are thought to function as alliances that generate adaptive benefits via support in critical situations. In humans, similarity in many sociodemographic, behavioural and intrapersonal characteristics leads to trust and is predictive of friendships. Specifically, personality homophily, that is the tendency of individuals to form social bonds with others who have a similar personality, may increase predictability and facilitate trust and reciprocity among partners with compatible behavioural tendencies. While evidence for social bonding in nonhumans is accumulating, far less is known about its predictors. Here, personality homophily effects on the formation and maintenance of social bonds are shown in twenty-four wild male Assamese macaques (Macaca assamensis), at Phu Khieo Wildlife Sanctuary, Thailand. Dyadic bond strength increased with increased similarity in the trait Connectedness (i.e. frequent and diverse neighbours in 5m proximity and pronounced social tolerance, as high rates of friendly approaches to and by others). To differentiate whether homophily indeed predicted bond formation or whether bonded males’ personalities became more similar over time, we tested the stability of the connectedness traits in a subset of immigrating males that had to form new bonds. Connectedness in these males remained stable suggesting that males do not adapt their personality to their partner. Our results support the idea of a shared evolutionary origin of homophily as a partner choice strategy in human and non-human animals. The main selective advantage of personality similarity in animal social bonds may result from a more reliable cooperation among individuals with similar cooperative behavioural tendencies.

In several cercopithecine species males exhibit a specific type of male–infant–male interaction during which two males briefly manipulate an infant. These interactions typically occur after a male carrying an infant (infant holder) approaches or is approached by another male who is not holding an infant (infant nonholder). The agonistic buffering and relationship management hypotheses explain these interactions as a tool to establish and maintain social bonds among males. Both hypotheses predict that males preferentially use the opportunity to interact and bond with males dominant to themselves. However, the agonistic buffering hypothesis predicts that males preferentially initiate male–infant–male interactions with the highest ranking males available, whereas the relationships management hypothesis predicts that males are more likely to interact with males that are close to them in rank. To test these predictions, we collected data on 1562 male–infant–male interactions during 1430 hours of focal observation of 12 infants in one group of wild Barbary macaques (Macaca sylvanus) in Morocco. Using generalized linear mixed-effect models we found that males preferably initiated interactions with males that were dominant to them. However, we observed this effect only for interactions initiated by the infant holder. In interactions initiated by non-holders, the receiver’s relative rank did not predict the frequency of interactions. Males also initiated more interactions with males close in rank to themselves than distantly ranked males. Our results support the relationship management hypothesis, but also indicate that the different types of male–infant–male interactions may require different explanations.

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.

Social contagion of non-interactive behaviour is widespread among animals including humans. It is thought to facilitate behavioural synchronization and consequently group cohesion, coordination and opportunities for social learning. Contagion of interactive behaviour—particularly affiliation—has received much less attention. Here, we investigated in female rhesus macaques ( Macaca mulatta ) the effect of observing group members groom on a subject's subsequent grooming behaviour and the potential modulation of contagion by relationship quality and social status. We recorded behaviour after subjects witnessed a grooming event and compared it to behaviour in a control condition with the same individuals in proximity but in the absence of a stimulus grooming event. Compared to the control condition, after observing others groom, females engaged in a grooming interaction sooner, and were more likely to be the initiator and to take on the active groomer role. Dominance rank of the focal individual and more weakly also of the stimulus individuals affected the latency to the next grooming interaction of the focal subject. Latency to the next grooming interaction decreased with increasing rank of the subject potentially reflecting lower social constraints faced by high ranking individuals in this highly despotic species. Relationship quality between the subject and the stimulus individuals had no effect on latency to grooming. Collectively, our findings provide evidence for visual contagion of affiliation in rhesus macaques. Future studies should explore the systematic variation in contagion of interactive behaviour in relation to a gradient of social tolerance.

Microsatellite genotyping is an important genetic method for a number of research questions in biology. Given that the traditional fragment length analysis using polyacrylamide gel or capillary electrophoresis has several drawbacks, microsatellite genotyping‐by‐sequencing (GBS) has arisen as a promising alternative. Although GBS mitigates many of the problems of fragment length analysis, issues with allelic dropout and null alleles often remain due to mismatches in primer binding sites and unnecessarily long PCR products. This is also true for GBS in catarrhine primates where cross‐species amplification of loci (often human derived) is common.We therefore redesigned primers for 45 microsatellite loci based on 17 available catarrhine reference genomes. Next, we tested them in singleplex and different multiplex settings in a panel of species representing all major lineages of Catarrhini and further validated them in wild Guinea baboons (Papio papio) using fecal samples.The final panel of 42 microsatellite loci can efficiently be amplified with primers distributed into three amplification pools.With our microsatellite panel, we provide a tool to universally genotype catarrhine primates via GBS from different sample sources in a cost‐ and time‐efficient way, with higher resolution, and comparability among laboratories and species., Even with genotyping‐by‐sequencing (GBS) of microsatellites issues with allelic dropout, null alleles and off‐target amplifications often remain due to poor primer design or using primers for cross‐species amplification. We re‐designed and validated a panel of 42 microsatellites providing a tool to universally genotype catarrhine primates via GBS from different sample sources in a cost‐ and time‐efficient way, with higher resolution, and comparability among laboratories and species.

We designed a genotyping panel for the investigation of the genetic underpinnings of inter-individual differences in aggression and the physiological stress response. The panel builds on single nucleotide polymorphisms (SNPs) in genes involved in the three subsystems of the hypothalamic-pituitary-adrenal (HPA)-axis: the catecholamine, serotonin and corticoid metabolism. To promote the pipeline for use with wild animal populations, we used non-invasively collected faecal samples from a wild population of Assamese macaques (Macaca assamensis). We targeted loci of 46 previously reported SNPs in 21 candidate genes coding for elements of the HPA-axis and amplified and sequenced them using next-generation Illumina sequencing technology. We compared multiple bioinformatics pipelines for variant calling and variant effect prediction. Based on this strategy and the application of different quality thresholds, we identified up to 159 SNPs with different types of predicted functional effects among our natural study population. This study provides a massively parallel sequencing panel that will facilitate integrating large-scale SNP data into behavioural and physiological studies. Such a multi-faceted approach will promote understanding of flexibility and constraints of animal behaviour and hormone physiology.

Recent evidence suggests that in sexual selection on human males, intrasexual competition plays a larger role than female choice. In a sample of men ( N = 164), we sought to provide further evidence on the effects of men's physical dominance and sexual attractiveness on mating success and hence in sexual selection. Objective measures and subjective ratings of male sexually dimorphic traits purportedly under sexual selection (height, vocal and facial masculinity, upper body size from 3D scans, physical strength, and baseline testosterone) and observer perceptions of physical dominance and sexual attractiveness based on self-presentation video recordings were assessed and associated with mating success (sociosexual behaviour and number of potential conceptions) in a partly longitudinal design. Results from structural equation models and selection analyses revealed that physical dominance, but not sexual attractiveness, predicted mating success. Physical dominance mediated associations of upper body size, physical strength, as well as vocal and facial physical dominance and attractiveness with mating success. These findings thus suggest a greater importance of intrasexual competition than female choice in human male sexual selection.

Energy availability drives an individual's fitness and can be affected by diverse energetic challenges. The assessment of hormones involved in metabolic activity and energy mobilization provides a gateway to the study of physiological adaptations in response to changes in energy availability. Here, we investigated immunoreactive urinary total triiodothyronine (uTT3, thyroid hormone secreted through the hypothalamus-pituitary-thyroid axis and regulating the basal metabolic rate) alongside glucocorticoids (i.e. urinary cortisol, uCort, secreted through the hypothalamus-pituitary-adrenal axis and mediating energy mobilization) in wild female Assamese macaques (Macaca assamensis). Combining more than 2900; of behavioral data from 42 adult females with physiological data from 382 urine samples, we evaluated both uTT3 and uCort in relation to potential energetic challenges encountered by a female, namely fluctuations in energy intake, travel distance, reproductive state and minimum ambient temperature. As predicted, levels of both hormones changed in response to variation in energy intake with a tendency toward a positive effect on uTT3 and a significant negative effect on uCort levels. Unexpectedly, neither hormone was influenced by variation in travel distance. Reproductive state affected both hormones with higher levels of uTT3 and uCort in the second half of gestation. Finally, a decrease of minimum temperature triggered an increase in uCort but unexpectedly not in uTT3. Collectively, our results highlight the respective contribution of two endocrine axes when facing energetic challenges and the underlying metabolic strategies to cope with them. Overall, assessing thyroid hormones together with glucocorticoids provides an integrative picture in the evaluation of an individual's energy status.

Regulation of energy allocation and metabolic rate plays an important role in determining behavior and fitness in wild animals, calling for the validation of non-invasive markers of energetic condition. Recently, the thyroid hormone triiodothyronine (T3) has emerged as a promising marker as concentrations decrease to lower the metabolic rate during energetically challenging periods. However, it remains largely unclear whether T3 merely represents an alternative or provides additional information compared to other compounds involved in the regulation of energy acquisition and allocation, like cortisol and C-peptide, as few joint measurements have been conducted to date in non-invasively collected samples. We aimed to validate the non-invasive measurement of immunoreactive urinary total T3 (uTT3), in comparison to urinary cortisol (uCort) and urinary C-peptide (uCP), as a marker of metabolic response to variation in food intake in macaques, and to address a number of issues regarding the collection, storage and processing of samples which are important for application of uTT3 measurements under field conditions. We used daily samples and body mass measures from a prior food restriction-refeeding experiment over 4 weeks with six captive macaques and analyzed concentrations of uTT3 and uCort in samples collected prior to (fasting) and after morning feeding (non-fasting). Concentrations of uTT3 decreased in response to restriction in food supply and were also lower during weeks of food restriction compared to weeks of refeeding. Variation in uTT3 also correlated positively with variation in body mass and concentrations of uCP. As expected, uCort showed the reverse pattern, increasing during food restriction and decreasing following refeeding, but was not associated with variation in body mass. Generally, compared to fasting samples, concentrations were higher in post-morning feeding, i.e. non-fasting, samples for uTT3 but not uCort. Contamination of urine samples with fecal matter, but not soil, and exposure to UV light led to a decrease in uTT3. uTT3 was largely unaffected by repeated freeze–thaw cycles and by refrigeration for medium-term storage (2 days) but degraded substantially when stored at ambient temperature for the same period. In conclusion, uTT3 measurements inform on the effect of food intake and its associated metabolic response to variation in energetic status. Since uTT3 is reasonably robust to many issues associated with collection and storage of urine samples under field conditions, it is a promising biomarker for studies of energetic condition and basal metabolic rate in wild macaques.

In polygynandrous mammals, females rarely form affiliative relationships with unrelated males outside the mating context. The antiharassment hypothesis provides one explanation for why such relationships have evolved in some gregarious primates: it states that females receive less aggression from group members in the presence of a male partner and gain his support when being harassed by others. This lowers the costs of competition and increases the female's access to resources, as it also reduces interruptions to feeding. Our aim was to test this hypothesis by investigating the benefits that wild female Assamese macaques, Macaca assamensis, in Thailand derive from bonding with particular males. In support of the antiharassment hypothesis, we found that the strength of affiliative relationships lowered the aggressiveness of a male towards a female, and predicted how much support a female received from a particular male in agonistic interactions with other group members. Additionally, relationship strength predicted the time that females spent co-feeding with a particular male as well as her feeding efficiency in the presence of that male. Hence, female Assamese macaques benefit from forming a social bond with a particular male by reducing the costs of competition.

Prenatal developmental plasticity in response to various environmental and social adversities can affect multiple aspects of offspring phenotype including social behavior strategies with effects that can last into adulthood. Here, we (1) identify adaptive social behavior strategies and their underlying mechanisms as potential targets of developmental plasticity in primates, (2) derive predictions about social behavior outcomes of prenatal adversity from different types of evolutionary models, (3) review the primate evidence for prenatal stress effects on offspring cognitive function, social, and non-social behavior, and (4) discuss avenues for future research. The scarce evidence currently available points towards increased distress behavior, particularly in infant offspring, and reductions of activity, exploration, and affiliative behavior in response to experimental prenatal adversity. Not all effects are stable, the results do not replicate well, and, for the most part, the current data cannot be used to test predictions of evolutionary models because relevant aspects of social behavior were not quantified and not assessed in the complex social environments they evolved for. More comprehensive research in developmental plasticity needs to incorporate sex differences and the interaction of effects from different sensitive periods including adolescence. Moreover, future research needs to assess the role of social buffering in mediating intergenerational effects and trade-offs between the pace of life and social cognitive performance.

In nonhuman animals, individuals of the same sex and age differ in their behavior patterns consistently across time, comparable with human personality differences. To draw conclusions about the adaptive value of behavior traits, it is essential to study them in the wild where animals are subject to the ecological pressures that promoted the evolution of behavior strategies. This study was conducted in the Phu Khieo Wildlife Sanctuary, Thailand, on 4 groups of habituated wild Assamese macaques by observers who had familiarized themselves with the subjects over the course of an ongoing long-term study. We used a multimethod approach enabling the most comprehensive understanding of variation in stable interindividual differences in a species-typical ecological setting. We combined trait ratings (TRs), assessed with observer-report questionnaires (54-item Hominoid Personality Questionnaire) of 107 individuals of diverse age-sex classes, with behavior codings (BCs) of 24 adult males. We found male and female personality constructs to be congruent and examined reliability and construct validity. Combining trait rating and behavioral coding, we found two solutions with five factors to best describe the personality structure of the males: one structure comprised the dimensions GregariousnessBC, AggressivenessBC, SociabilityBC and VigilanceBC, complemented by a ConfidenceTR domain and the other structure OpportunismTR, ConfidenceTR, FriendlinessTR, ActivityTR complemented with VigianceBC. We discuss our findings with regard to the importance of construct validity and reproducibility in the context of method development and standardization in nonhuman animal personality research. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best‐studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x̅ = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort—measured as the number of publications—had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.

Monitoring conspecifics is a crucial process in social learning and a building block of social cognition. Selective attention to social stimuli results from interactions of subject and stimulus characteristics with dominance rank often emerging as an important predictor. We extend previous research by providing as stimuli naturally occurring affiliative interactions between group members instead of pictorial or auditory representations of conflicts, and by extending to the affiliative relationship, i.e. social bond, between subject and stimulus instead of just their dominance relations. Our observational data on adult female rhesus macaques support the prediction that subjects pay more attention to affiliative interactions of others than to solitary controls. Exceedingly more attention was paid to conflicts unfolding in the group which can have more prompt and direct consequences than others’ friendly interactions. The valence of the stimulus (affiliative vs. agonistic) affected biases towards individuals dominant over the subject, but not the ubiquitous bias towards close affiliates of the subject. Keeping track of the whereabouts and interactions of key social partners has been proposed as a prerequisite for behavioral coordination among bonded partners. In groups of socially very active monkeys, social attention is gated by both social dominance and social bonding.

Gastrointestinal nematodes are intensely studied models for host-pathogen interactions in wildlife, yet consequences of infections are not fully understood. Among the potential costs of nematode infection are physiological changes caused by immune system activation, reduction or reallocation of available energy, as well as potential social consequences in terms of decreased social activity or avoidance of infected individuals. We used experimental anthelmintic treatment to investigate effects of strongyle nematode infection in Barbary macaques (Macaca sylvanus), comparing 56 treated to 17 untreated individuals. Deworming success was monitored by coproscopy and infection probability estimated from patch occupancy models. Increasing strongyle infection probabilities were associated with increased fecal glucocorticoid metabolite levels and slightly decreased activity and had no significant effect on energy balance quantified as urinary C-Peptide levels. The frequency to approach into close spatial proximity of a partner was predicted by the partner's, but not focal individual's infection status, with a tendency toward infected individuals being approached less frequently. Although effects were weak, they suggest a co-occurrence of sickness behavior and avoidance of infected conspecifics, both possibly shaping social interaction patterns with potential consequences for an individual's social relationships. This study adds to the growing body of research on the complex interactions of sociality, health, and fitness in a group living species.

The development of methods to quantify hormones from non-invasively collected samples such as urine or feces has facilitated endocrinology research on wild-living animals. To ensure that hormone measurements are biologically meaningful, method validations are strongly recommended for each new species or sample matrix. Our aim was to validate three commonly used enzyme immunoassays (EIA), one for analysis of cortisol and two for analysis of testosterone, to assess adrenocortical and gonadal endocrine activity, respectively, from the urine of male Barbary macaques. We compared EIA and liquid chromatography-mass spectrometry (LC-MS) results to determine if the EIA measurements truly reflect levels of the target hormone and to determine if antibody cross-reactivities with other steroids were potentially confounding results. Furthermore, we conducted a biological validation of testosterone to ensure that both EIA and LC-MS were able to capture physiologically meaningful differences in hormone levels. We found that cortisol measured by EIA correlated strongly with cortisol measured by LC-MS in both adult and immature males, without the need for deconjugation of steroids in the urine. Both testosterone EIAs correlated strongly with LC-MS in adult males, but only if steroids in the urine were deconjugated by enzymatic hydrolysis prior to analysis. However, in immature males, EIA and LC-MS results did not correlate significantly. Further correlation analyses suggest this is likely due to cross-reactivity of the testosterone antibodies with other adrenal steroids such as cortisol, DHEA, and likely others, which are present at much higher concentrations relative to testosterone in immature males. Testosterone levels were significantly higher in adult compared to immature males as measured by LC-MS but not as measured by EIA. Taken together, our results suggest that the testosterone EIAs are suitable to assess gonadal activity in adult but not immature males, and only if a hydrolysis of the urine is conducted prior to analysis.

In large multimale-multifemale primate groups, individual adult males and females may form close social relationships that extend beyond the mating context, a surprising finding for polygynandrous mammals. The patterns of these associations can be relatively stable across time. Here we investigate whether dyadic social relationships between the sexes transcend mere association in wild Assamese macaques and may be characterized as strong, equitable, and stable affiliative relationships or social bonds. We collected >9,000 hr of focal animal data on adult males and females from two groups of wild Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, Thailand. Using dyadic composite sociality indices, we found male-female affiliative relationships to be highly differentiated. The stronger the relationships were, the more likely partners were to reciprocate grooming and the more stable were the relationships. In addition, the strongest dyadic relationships remained stable over multiple years as long as both partners remained in the group. These results indicate that in a polygynous species particular males and females form strong, equitable, and enduring affiliative relationships qualitatively similar to the same-sex bonds described for female baboons and male chimpanzees. Am. J. Primatol. 78:872-882, 2016. © 2016 Wiley Periodicals, Inc.

In multimale multifemale primate groups, the strength and stability of affiliative relationships have been shown to affect an individual's long-term fitness such as offspring survival and longevity. Studies investigating the fitness benefits of close social relationships and the underlying mechanisms have mainly focused on the philopatric sex. The strong relationships of philopatric chimpanzee males and baboon females share important characteristics with human friendships in that increased strength of affiliative relationships is associated with increased equitability in service exchanges and relationship stability. So far, it has remained unclear whether the strong relationships of dispersing males share these characteristics as well and can thus be labelled as social bonds. Here we provide results on the variation in affiliative relationship strength and its relation to equitability and relationship stability from two wild groups of male Assamese macaques, Macaca assamensis, at Phu Khieo Wildlife Sanctuary, Thailand collected over 2 and 7 years, respectively. Our analyses of almost 9000 h of focal animal data show that males formed differentiated affiliative relationships and that the strength of a relationship affected how likely males returned a grooming service within a single bout and how equally males were responsible for the maintenance of close proximity. Partner stability among the three strongest relationships was higher than among weaker relationships which suggests that top partners were not retained simply because of a lack of alternatives. Together, these results suggest that dispersing male Assamese macaques form differentiated affiliative relationships that increase in equitability and stability with increasing relationship strength. This is the first study showing long-term partner stability in males as the dispersing sex. Our results thus add to the growing body of literature indicating that nonhuman animals form close social relationships similar to human friendships. peerReviewed

Mammals living in stable social groups often mitigate the costs of group living through the formation of social bonds and cooperative relationships. The neuropeptide hormone oxytocin (OT) has been proposed to promote both bonding and cooperation although only a limited number of studies have investigated this under natural conditions. Our aim was to assess the role of OT in bonding and cooperation in male Barbary macaques (Macaca sylvanus). First we tested for an effect of affiliation - grooming and triadic male-infant-male interactions - with bond and non-bond partners on urinary OT levels. Secondly we aimed to test whether grooming interactions (and thus increased OT levels) increase a male’s general propensity to cooperate in polyadic conflicts. We collected behavioral data via full-day focal animal protocols on 14 adult males and measured endogenous OT levels from 139 urine samples collected after affiliation and non-social control periods. Urinary OT levels were higher after grooming with any partner. By contrast, OT levels after male-infant-male interactions with any partner or with bond partners were not different from controls but were higher after interactions with non-bond partners. Previous grooming did not increase the likelihood of males to support others in conflicts. Collectively, our results support research indicating that OT is involved in the regulation of adult social bonds, including in non-reproductive contexts. However, our male-infant-male interaction results go against previous studies suggesting that it is affiliation with bond rather than non-bond partners that trigger the release of OT. Alternatively, OT levels may have been elevated prior to male-infant-male interactions thus facilitating interaction between non-bond partners. The lack of an association of grooming (and by extension increased OT levels) and subsequent support speaks against an OT linked increase in the general propensity to cooperate, yet further studies are needed for a more direct test including the possibility of partner-specific contingent cooperation.

Inter- and intra-specific variation in the propensity to form coalitions has been explained by variation in the availability of suitable partners, distribution of fighting ability, coalition profitability, and costs of coordination. Male coalition formation can be an alternative reproductive strategy to one-on-one competition to maximize male reproductive success. Here we focus on age as a state variable to explain within-group variation in individual propensity to form coalitions against other group members. We specifically test the prediction that males conditionally switch from a solo strategy for achievement of high mating success to a cooperative strategy after reaching post-prime age in male Barbary macaques (Macaca sylvanus). We combined new observations with data collected in 2006 and 2008 on the same individuals from one captive group living in semi-natural conditions at Affenberg Salem, Germany, and found that in all years males between 5 and 13 years formed significantly fewer coalitions than males 14 years and older (post-prime). More importantly, we found those males that aged into the post-prime phase to have switched their reproductive strategy and to form significantly more coalitions in 2014 compared to 2008. These first longitudinal data together with earlier cross-sectional analyses in this and other primate species suggest that group-level measures of coalition propensity may be strongly affected by the age composition of groups and that male coalition formation can be a conditional reproductive strategy.

Human aggression can be differentiated into reactive aggression (RA), displayed in face of a real or perceived threat and associated with high levels of anxiety, and proactive aggression (PA), displayed to achieve a certain goal and linked to lower anxiety levels. To study the origins of these aggression subtypes and their relation to anxiety, we tested if both subtypes can be distinguished in a nonhuman primate species, characterized their occurrence within the study group, and examined the link between aggression subtype and anxiety. Data were collected on 29 individuals of a semi-free ranging group of Barbary macaques (Macaca sylvanus) at Affenberg Salem, Germany, via focal animal (303 hr) and event sampling (1,222 agonistic events). Using a priori definitions, each aggressive event was classified as either reactive or proactive. We found both aggression types in our study population as well as individual differences in the proportion at which they occurred. The predominant use of one subtype of aggression was linked to the individual's dominance rank, age and sex, but not related to standard behavioral and physiological measures of anxiety. Our results suggest that reactive and proactive subtypes of aggression also exist in Barbary macaques, indicating a deeper evolutionary history of these aggression types observed in humans.