The intertwined nature of peace and war.

Glowacki discusses how humans regularly face collective action problems that may result in either peaceful or aggressive between-group interactions. Peace and war probably coevolved in humans. Using a gene-culture evolutionary framework is a powerful way to analyse why, when, and how humans have the capacity to build and maintain long-term peaceful interactions between groups and also to wage deadly wars.

Warfare in an evolutionary perspective.

The importance of warfare for human evolution is hotly debated in anthropology. Some authors hypothesize that warfare emerged at least 200,000-100,000 years BP, was frequent, and significantly shaped human social evolution. Other authors claim that warfare is a recent phenomenon, linked to the emergence of agriculture, and mostly explained by cultural rather than evolutionary forces. Here I highlight and critically evaluate six controversial points on the evolutionary bases of warfare. I argue that cultural and evolutionary explanations on the emergence of warfare are not alternative but analyze biological diversity at two distinct levels. An evolved propensity to act aggressively toward outgroup individuals may emerge irrespective of whether warfare appeared early/late during human evolution. Finally, I argue that lethal violence and aggression toward outgroup individuals are two linked but distinct phenomena, and that war and peace are complementary and should not always be treated as two mutually exclusive behavioral responses.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Triadic awareness predicts partner choice in male-infant-male interactions in Barbary macaques.

Social knowledge beyond one's direct relationships is a key in successfully manoeuvring the social world. Individuals gather information on the quality of social relationships between their group companions, which has been termed triadic awareness. Evidence of the use of triadic awareness in natural contexts is limited mainly to conflict management. Here we investigated triadic awareness in wild Barbary macaques (Macaca sylvanus) in the context of bridging interactions defined as male-infant-male interactions whereby a male (initiator, holder) presents an infant to another male (receiver, non-holder) in order to initiate an affiliative interaction with that male. Analyses based on 1263 h of focal observations on ten infants of one wild social group in Morocco supported the hypothesis that males use their knowledge of the relationship between infants and other adult males when choosing a male as a partner for bridging interactions. Specifically, (i) the number of bridging interactions among holder-infant-receiver triads was positively affected by the strength of the infant-receiver relationship and (ii) when two males were available as bridging partners, a male was more likely to be chosen as the receiver the stronger his social relationship with the infant relative to the other available male. This demonstrates that non-human primates establish triadic awareness of temporary infant-male relationships and use it in a naturally occurring affiliative context. Our results contribute to the discussion about the mechanism underlying the acquisition of triadic awareness and the benefits of its usage, and lend support to hypotheses linking social complexity to the evolution of complex cognition.

Evidence of direct reciprocity, but not of indirect and generalized reciprocity, in the grooming exchanges of wild Barbary macaques (Macaca sylvanus).

Reciprocity is one of the mechanisms that have been proposed to explain the exchange of social behaviors, such as grooming, in animals. Reciprocity assumes that individuals act as the donor and recipient of grooming and switch roles over time to balance the benefits and costs of this behavior. Three main patterns of reciprocity may follow a grooming given: (i) direct reciprocity, where the former recipient returns the grooming to the former donor; (ii) indirect reciprocity, where another individual returns the grooming to the former donor; and (iii) generalized reciprocity, where the former recipient returns the grooming to another individual. While there is evidence that direct reciprocity plays an important role in various species of animals, the role of indirect and generalized reciprocity is less clear and has been rarely analyzed. We tested the role of direct, indirect, and generalized reciprocity in explaining grooming exchanges of wild Barbary macaques, by analyzing the temporal contingency between giving and receiving grooming. We collected the occurrence and latency of the three types of grooming reciprocation during 1 hr long focal sessions run simultaneously on two partners who just stopped grooming (post-grooming session) or who were in proximity (i.e., within 1.5 m) without grooming each other (control session). We ran the analyses on 284 post-grooming and 63 control sessions. The results revealed a temporal contingency of grooming interactions exchanged according to direct reciprocity but not according to indirect or generalized reciprocity. Our results indicate that grooming distribution in Barbary macaques is partner-specific. We discuss the possible role of cognition and emotions in explaining direct reciprocity in animals.

Correlates of androgens in wild male Barbary macaques: Testing the challenge hypothesis.

Investigating causes and consequences of variation in hormonal expression is a key focus in behavioral ecology. Many studies have explored patterns of secretion of the androgen testosterone in male vertebrates, using the challenge hypothesis (Wingfield, Hegner, Dufty, & Ball, 1990; The American Naturalist, 136(6), 829-846) as a theoretical framework. Rather than the classic association of testosterone with male sexual behavior, this hypothesis predicts that high levels of testosterone are associated with male-male reproductive competition but also inhibit paternal care. The hypothesis was originally developed for birds, and subsequently tested in other vertebrate taxa, including primates. Such studies have explored the link between testosterone and reproductive aggression as well as other measures of mating competition, or between testosterone and aspects of male behavior related to the presence of infants. Very few studies have simultaneously investigated the links between testosterone and male aggression, other aspects of mating competition and infant-related behavior. We tested predictions derived from the challenge hypothesis in wild male Barbary macaques (Macaca sylvanus), a species with marked breeding seasonality and high levels of male-infant affiliation, providing a powerful test of this theoretical framework. Over 11 months, 251 hr of behavioral observations and 296 fecal samples were collected from seven adult males in the Middle Atlas Mountains, Morocco. Fecal androgen levels rose before the onset of the mating season, during a period of rank instability, and were positively related to group mating activity across the mating season. Androgen levels were unrelated to rates of male-male aggression in any period, but higher ranked males had higher levels in both the mating season and in the period of rank instability. Lower androgen levels were associated with increased rates of male-infant grooming during the mating and unstable periods. Our results generally support the challenge hypothesis and highlight the importance of considering individual species' behavioral ecology when testing this framework.

Responses to social and environmental stress are attenuated by strong male bonds in wild macaques.

In humans and obligatory social animals, individuals with weak social ties experience negative health and fitness consequences. The social buffering hypothesis conceptualizes one possible mediating mechanism: During stressful situations the presence of close social partners buffers against the adverse effects of increased physiological stress levels. We tested this hypothesis using data on social (rate of aggression received) and environmental (low temperatures) stressors in wild male Barbary macaques (Macaca sylvanus) in Morocco. These males form strong, enduring, and equitable affiliative relationships similar to human friendships. We tested the effect of the strength of a male's top three social bonds on his fecal glucocorticoid metabolite (fGCM) levels as a function of the stressors' intensity. The attenuating effect of stronger social bonds on physiological stress increased both with increasing rates of aggression received and with decreasing minimum daily temperature. Ruling out thermoregulatory and immediate effects of social interactions on fGCM levels, our results indicate that male Barbary macaques employ a tend-and-befriend coping strategy in the face of increased environmental as well as social day-to-day stressors. This evidence of a stress-ameliorating effect of social bonding among males under natural conditions and beyond the mother-offspring, kin or pair bond broadens the generality of the social buffering hypothesis.

Within-group behavioural consequences of between-group conflict: a prospective review.

Conflict is rife in group-living species and exerts a powerful selective force. Group members face a variety of threats from extra-group conspecifics, from individuals looking for reproductive opportunities to rival groups seeking resources. Theory predicts that such between-group conflict should influence within-group behaviour. However, compared with the extensive literature on the consequences of within-group conflict, relatively little research has considered the behavioural impacts of between-group conflict. We give an overview of why between-group conflict is expected to influence subsequent behaviour among group members. We then use what is known about the consequences of within-group conflict to generate testable predictions about how between-group conflict might affect within-group behaviour in the aftermath. We consider the types of behaviour that could change and how the role of different group members in the conflict can exert an influence. Furthermore, we discuss how conflict characteristics and outcome, group size, social structure and within-group relationship quality might modulate post-conflict behavioural changes. Finally, we propose the need for consistent definitions, a broader range of examined behaviours and taxa, individual-focused data collection, complementary observational and experimental approaches, and a consideration of lasting effects if we are to understand fully the significant influence of between-group conflict on social behaviour.

Cooperation in wild Barbary macaques: factors affecting free partner choice.

A key aspect of cooperation is partner choice: choosing the best available partner improves the chances of a successful cooperative interaction and decreases the likelihood of being exploited. However, in studies on cooperation subjects are rarely allowed to freely choose their partners. Group-living animals live in a complex social environment where they can choose among several social partners differing in, for example, sex, age, temperament, or dominance status. Our study investigated whether wild Barbary macaques succeed to cooperate using an experimental apparatus, and whether individual and social factors affect their choice of partners and the degree of cooperation. We used the string pulling task that requires two monkeys to manipulate simultaneously a rope in order to receive a food reward. The monkeys were free to interact with the apparatus or not and to choose their partner. The results showed that Barbary macaques are able to pair up with a partner to cooperate using the apparatus. High level of tolerance between monkeys was necessary for the initiation of successful cooperation, while strong social bond positively affected the maintenance of cooperative interactions. Dominance status, sex, age, and temperament of the subjects also affected their choice and performance. These factors thus need to be taken into account in cooperative experiment on animals. Tolerance between social partners is likely to be a prerequisite for the evolution of cooperation.

Metabolic strategies in wild male Barbary macaques: evidence from faecal measurement of thyroid hormone.

Selection is expected to favour the evolution of flexible metabolic strategies, in response to environmental conditions. Here, we use a non-invasive index of basal metabolic rate (BMR), faecal thyroid hormone (T3) levels, to explore metabolic flexibility in a wild mammal inhabiting a highly seasonal, challenging environment. T3 levels of adult male Barbary macaques in the Atlas Mountains, Morocco, varied markedly over the year; temporal patterns of variation differed between a wild-feeding and a provisioned group. Overall, T3 levels were related to temperature, foraging time (linked to food availability) and intensity of mating activity, and were higher in the provisioned than in the wild-feeding group. In both groups, T3 levels began to increase markedly one month before the start of the mating season, peaking four to six weeks into this period, and at a higher level in the wild-feeding group. Our results suggest that while both groups demonstrate marked metabolic flexibility, responding similarly to ecological and social challenges, such flexibility is affected by food availability. This study provides new insights into the way Barbary macaques respond to the multiple demands of their environment.

The functions of non-reproductive mounts among male Barbary macaques (Macaca sylvanus).

Same-sex, non-reproductive mounts have been observed in a number of primate species and in various social contexts. However, the function of non-reproductive mounts is still largely unknown. We aimed to test whether non-reproductive mounts function to assert dominance and as appeasement behavior in male Barbary macaques. We analyzed post-mount behavior in 54 macaques belonging to two captive groups at Trentham Monkey Forest in Staffordshire, using 10 min post-mount/matched-control focal sessions collected either on the mounter or the mountee. In support of the dominance assertion hypothesis, the higher-ranking male within a mounting pair was more likely to be the mounter than the mountee, and to mock bite the lower-ranking male. In support of the appeasement hypothesis, the former mounting partners were more likely to exchange grooming and to have a lower frequency of self-scratching (a measure of social tension) after a non-reproductive mount than in control sessions. Our study indicates that non-reproductive mounts have different and not mutually exclusive functions and can modulate the quality of social interactions among group members. We discuss the possible factors that can affect the occurrence of non-reproductive mounts within and between species.

Male mating behaviour in relation to female sexual swellings, socio-sexual behaviour and hormonal changes in wild Barbary macaques.

In many cercopithecine primates females display probabilistic cues of fertility to indicate the periovulatory period to males. These cues may include female behaviour, acoustic signals, and morphological signs such as the anogenital swelling. However, the extent to which males can utilise this information varies between species. We describe male sexual behaviour in relation to changes in anogenital swelling size, timing of ovulation and female socio-sexual behaviour in wild Barbary macaques (Macaca sylvanus). We further compare male sexual behaviour during conception and post-conception cycles to evaluate if males differentiate between these qualitatively different cycle types. Our results show that during conception cycles male mating behaviour was concentrated around the fertile phase implying that males inferred information from more than swelling size alone. Male mating frequency increased in line with female socio-sexual behaviour, namely female presenting and the frequency of copulations with copulation calls. Most strikingly our results show that males invested equally in mating during fertile and non-fertile, i.e. post-conception, maximum swelling phases. Whether post-conception swellings were merely a result of changes in hormone concentrations during pregnancy or part of a female reproductive strategy remains elusive. In sum, this study adds to the body of research on the evolution of female sexual signals and how males may infer information from these cues.

Coping with the cold: predictors of survival in wild Barbary macaques, Macaca sylvanus.

We report the death of 30 wild Barbary macaques, living in two groups, during an exceptionally cold and snowy winter in the Middle Atlas Mountains, Morocco. We examined whether an individual's time spent feeding, the quality and number of its social relationships, sex and rank predicted whether it survived the winter or not. The time an individual spent feeding and the number of social relationships that an individual had in the group were positive and significant predictors of survival. This is the first study to show that the degree of sociality affects an individual's chance of survival following extreme environmental conditions. Our findings support the view that sociality is directly related to an individual's fitness, and that factors promoting the establishment and maintenance of social relationships are favoured by natural selection.

Corrigendum: Intra-specific variation in the social behavior of Barbary macaques (Macaca sylvanus).

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

Cooperation and group similarity in children and young adults in the UK.

For cooperation to be beneficial, cooperators should be able to differentiate individuals who are willing to cooperate from free-riders. In the absence of kin or of familiar individuals, phenotypic similarity (e.g. in terms of language) can be used as a cue of how likely two or more individuals are to behave similarly (whether they will cooperate or free-ride). Thus, phenotypic similarity could affect cooperation. However, it is unclear whether humans respond to any type of phenotypic similarity or whether only salient phenotypic traits guide cooperation. We tested whether within-group, non-salient phenotypic similarity affects cooperation in 280, 3 to 10 year old children and in 76 young adults (mean 19.8 years old) in the UK. We experimentally manipulated the degree of phenotypic similarity in three computer-based experiments. We found no evidence of a preference for, or greater cooperation with, phenotypically similar individuals in children, even though children displayed ingroup preference. Conversely, young adults cooperated more with phenotypically similar than with phenotypically diverse individuals to themselves. Our results suggest that response to non-salient phenotypic similarity varies with age and that young adults may pay more attention to non-salient cues of diversity then children.

Hierarchical steepness, counter-aggression, and macaque social style scale.

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four-grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style-two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter-aggression)-to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter-aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter-aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species' phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness.

The Habituation Process in Two Groups of Wild Moor Macaques (Macaca maura).

When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly used to ensure that animals do not perceive researchers as a direct threat and do not alter their behavior in their presence. However, habituation can have significant effects on the welfare and conservation of the animals. Studying how nonhuman primates react to the process of habituation can help to identify the factors that affect habituation and implement habituation protocols that allow other researchers to speed up the process while maintaining high standards of health and safety for both animals and researchers. In this study, we systematically described the habituation of two groups of wild moor macaques (Macaca maura), an Endangered endemic species of Sulawesi Island (Indonesia), to assess the factors that facilitate habituation and reduce impact on animal behavior during this process. During 7 months, we conducted behavioral observations for more than 7,872 encounters and an average of 120 days to monitor how macaque behavior toward researchers changed through time in the two groups under different conditions. We found that both study groups (N = 56, N = 41) became more tolerant to the presence of researchers during the course of the habituation, with occurrence of neutral group responses increasing, and minimum distance to researchers and occurrence of fearful group responses decreasing through time. These changes in behavior were predominant when macaques were in trees, with better visibility conditions, when researchers maintained a longer minimum distance to macaques and, unexpectedly, by the presence of more than one researcher. By identifying these factors, we contribute to designing habituation protocols that decrease the likelihood of fearful responses and might reduce the stress experienced during this process.

Intra-specific Variation in the Social Behavior of Barbary macaques (Macaca sylvanus).

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.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

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.

Innovation in wild Barbary macaques (Macaca sylvanus).

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.