Prosociality in a despotic society

Humans possess remarkable prosocial tendencies beyond the confinement of kinship, which may be instrumental in promoting cooperative interactions and sociality at large. Yet, prosociality is an evolutionary conundrum as it does not provide immediate benefits to the actor. The ‘domestication’ and ‘cooperative-breeding’ hypotheses postulated that enhanced social tolerance and inter-individual dependence could nonetheless facilitate the evolution of prosociality. However, inconsistent results due to varying experimental paradigms, and restricted focus of research on tolerant and cooperatively breeding species, have impeded our understanding so far. Albeit counterintuitively, despotic societies with relatively low social tolerance levels represent an excellent opportunity to investigate prosociality due to their kin favoritism and potential interdependence among individuals in terms of social support. Japanese macaques (Macaca fuscata) live in strictly hierarchical matrilineal societies, where kin members have strong social bonds. Additionally, support from non-kins can be crucial to form coalitions and rank up in the hierarchy. Using a group-service paradigm, we tested prosociality in a semi-free-ranging group of Japanese macaques. In contrast to currently existing evidence, we found that individuals (n=25) can act prosocially and at comparably high rates as cooperative breeding- or self-domesticated species. The macaques benefitted not only their kin members but other individuals to whom they showed relatively high social tolerance. We emphasize the roles of complex socio-ecological conditions in facilitating individual prosocial tendencies. Furthermore, these results call for a novel evolutionary framework regarding prosociality that focuses on different forms of interdependence and expands beyond cooperative breeding- and (self-)domesticated species. Significance statement What made humans so incredibly prosocial? Examining the evolutionary trajectory of prosocial acts led comparative psychologists to explore various taxa. Empirical evidence so far suggests that enhanced social tolerance and interdependence among individuals facilitate prosociality. Conventionally, despotism is characterized by low group-level tolerance, yet kin favoritism, nepotism, and high interdependence (in support and coalition formation) are also fundamental properties of despotic societies. Under such complex socio-ecological conditions, individual prosocial acts could thus be vital. We found, for the first time, high levels of prosociality in the very despotic Japanese macaques. Individuals benefitted both kin-relatives and others to whom they showed relatively high dyadic social tolerance. This study signifies that prosociality can be favored even in a highly despotic society.

press were discarded from this analysis. Overall, food provisions, i.e. prosocial presses that also led to a recipient getting the food, prosocial provisioning, we corrected this by using only the prosocial individuals who seemed 1 8 8 to understand the consequences of their actions in the group-service paradigm, and the value 1 8 9 was found to be 68.8%. Notably, even though it pressed more often in the test than in empty 1 9 0 control, one individual did not provide any food to others. Thus, we excluded her from the 1 9 1 list of prosocial individuals due to a lack of clear evidence of prosocial provisioning. Although the prosocial individuals seemed to also provision food at a sustained rate 1 9 3 ( Figure S3), there was a significant difference between session one (no. of provisions ± SD: 1 9 4 3.9 ± 9.02) and five (8.8 ± 9.67) of the test condition (GLMM: z = 2.478, p = 0.013), 1 9 5 indicating an increase in food provision from session one to five. Given the sustained rates of 1 9 6 pressing by the focal subjects/prosocial individuals across sessions, these results suggest 1 9 7 better coordination between actors and recipients. Furthermore, for prosocial individuals, we compared the number of food provisions 1 9 9 and food received ( Table S3). These individuals provided food to others (no. of provisions ± 2 0 0 SD: 19.11 ± 22.83) significantly more than the amount they received (4.11 ± 3.58, Wilcoxon 2 0 1 signed-rank test: z = -2.43, p = 0.01). This may indicate that the prosocial individuals indeed 2 0 2 cared for benefitting group members rather than gaining immediate advantages through 2 0 3 reciprocity. We found very few instances of aggression from helpers to receivers (6.59%) after 2 0 7 provisioning food (Goodness of fit Chi-square test: χ 2 = 137.16, p < 0.001). Also, active 2 0 8 solicitation in the form of interacting with the provisioning side (Pos. 1) and reaching-out behavior (i.e. holding the food pipe) were observed (16.48%) in significantly few instances 2 1 0 by receivers toward helpers (Goodness of fit Chi-square test: χ 2 = 81.78, p < 0.001).

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Furthermore, in 22% of the trials, individuals were already present within one arm's 2 1 2 distance from Pos. 1, i.e. at the receiving end when a prosocial individual pressed the handle 2 1 3 and provided food. In all other trials, i.e. in a significantly higher number of trials (Goodness 2 1 4 of fit Chi-square test: χ 2 = 57.16, p < 0.001), the prosocial act of pressing the handle seemed 2 1 5 more proactive and not specific for a particular partner, which may also explain why not 2 1 6 every press resulted in food provisioning. This is not to say that there were no links between 2 1 7 the provider and the individual who ultimately received the reward. To assess what might explain the likelihood and magnitude of prosociality among different 2 2 1 dyads, we examined the effects of kinship and dyadic social tolerance. Considering the large 2 2 2 number of participating individuals and among individual variations in prosocial tendencies, recipients. In other words, a prosocial individual could potentially help everyone. In this 2 2 6 analysis, kinship was found to influence the magnitude (GLMM: z = 2.990, p = 0.002; kin = 2 2 7 3.68 ± 7.18; non-kin = 0.32 ± 1.41; Figure 4b) but not the likelihood (GLMM: z = 3.534, p =  Figure   2 3 1 4b), independently from the effect of kin. We did not find any effect of age, sex and rank 2 3 2 differences on the likelihood and magnitude of prosocial provision (Figures 4a and 4b). We asked whether prosociality can be favored in a despotic society and, if so, what factors 2 3 6 necessarily regulate it. Our results show that Japanese macaques, a highly despotic species 2 3 7 that is neither self-domesticated nor cooperatively breeding, exhibits prosociality at prosocial tendencies were not restricted to kin-relatives, and non-kin dyads with relatively 2 4 0 high social tolerance also engaged in prosocial acts. Besides, the low aggression and behavior. In addition, our findings reveal substantial individual differences in prosocial 2 4 3 tendencies. Burkart and van Schaik (10) illustrated that to be proactively prosocial, some criteria need to 2 4 7 be fulfilled in the group service paradigm -higher frequency of press in the test than So far, there have been two influential hypotheses explaining the phylogenetic differences in 3 0 1 prosociality across taxa -the self-domestication hypothesis (6) and the cooperative breeding breeding. Yet, interestingly, the observed food provisioning rate (~ 69%) of the Japanese 3 0 4 macaques in our study resembled cooperative breeding and self-domesticated species' 3 0 5 prosocial provisioning (3, 5, 10), notably while using the exact same set-up and procedure. These results, together with the findings of prosociality (although used different set-up and/or 3 0 7 procedures) among other non-domesticated species and species that lack cooperative 3 0 8 breeding or allomaternal care (16,18,19,(54)(55)(56), call for additional hypotheses explaining  Both cooperative breeding and self-domestication hypothesis, to a reasonable extent, given their despotic social structure (57), very low group-level social tolerance, but we did 3 1 4 identify ample interdependencies among its members that may explain their prosocial 3 1 5 tendencies. We, therefore, call for a more general 'interdependency hypothesis' to explain the 3 1 6 evolutionary origins of prosocial tendencies and the phylogenetic differences observed. Note 3 1 7 that interdependency has also been postulated as an explanatory variable for variation in 3 1 8 inequity responses across and within species (58).

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Our results also question the premises of the covariation framework for macaques or 3 2 0 primates in general (11, 24), as it expects little to no cooperative behaviors in despotic 3 2 1 species with low group-level tolerance. We argue here that instead, in such despotic societies, 3 2 2 cooperation may be paramount to attain and maintain rank positions and that it, as such, (14, 15)). Our results are in stark contrast with previous reports on prosociality in captive Japanese 3 2 8 macaque (~ 0%, (10)). Consistent with the prediction that independently breeding free or 3 2 9 semi free-ranging primates have lower social tolerance than captive populations (59-62), our 3 3 0 study group showed lower group-level social tolerance (0.13) than the previously tested 3 3 1 population residing in a more restricted captive setting (0.32) (10). It must be noted that our 3 3 2 group level tolerance measure was limited to focal individuals and not the entire population. Nevertheless, this again suggests that group-level social tolerance may not be a good predictor of prosociality. Yet, striking variation at the dyadic social tolerance level was 3 3 5 observed among kin and non-kin group members, and as discussed above, they did predict Relatively large size and complexity of a group can drive cognitive processes, as proposed by the social intelligence hypothesis (15, 63, 64), even within single species (65).

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Such complexity might create opportunities for individuals to become "Machiavellian" and Finally, prosociality has been argued to be the foundation for inter-group conflict 3 5 1 (68); consequently, in-group prosociality and parochial cooperation can be favored. Our  We provide the first experimental report of proactive prosociality in semi free-ranging 3 6 0 Japanese macaques. We discussed how kin favoritism and dyadic social tolerance in a 3 6 1 despotic society could drive prosocial motivations. Although we did not find the age 3 6 2 difference of the individuals to influence prosociality significantly, participation of a 3 6 3 relatively large number of juveniles can not be neglected; for instance, due to their higher 3 6 4 social tolerance, bonobo sub-adults have been shown to be more prosocial than adults (32).

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Nonetheless, prosociality was not restricted to juveniles, and therefore, we speculate on the hypothesis', which can be systematically tested using an evolutionary framework. Finally, as previously stated by other researchers, we would also like to encourage exploring multiple 3 7 2 groups of a species with similar and different living conditions (i.e., captive, semi free-3 7 3 ranging, and free-ranging.) and structures, to come to a conclusion on that species' prosocial 3 7 4 tendencies. Similarly, it might be interesting to see whether population differences in 3 7 5 prosociality can be due to differential cultures with regard to societal norms in these   We adopted a modified version (5) of the group-service paradigm (10). The procedure 3 8 9 included several phases occurring in the following order -Phase 0 (habituation to apparatus), Phase 1 (initial training and habituation to procedure), Phase 2 (food distribution assessment), Information for details). It is important to note, however, that 25 individuals (adult female = 3 9 4 13, adult male = 3, juvenile female = 6, juvenile male = 3, Table S2) successfully passed the  To measure social tolerance at the group level, we ran a food distribution assessment 3 9 8 in phase 2. The seesaw mechanism was locked, and the board was tilted towards the  In the test sessions of phase 4, we assessed the prosocial tendency of the individuals. individual could only make food available for their group mates. In addition to the test 4 1 1 sessions, we conducted empty control sessions, identical to the test sessions, except that no 4 1 2 food was placed, even though the same movement (of placing food in Pos. 1) was made to 4 1 3 control for stimulus enhancement. We conducted five such tests and five empty control 4 1 4 sessions, alternately, each containing 125 trials.

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To investigate whether pressing in the test was only due to the presence of food, we 4 1 6 also performed a blocked control in Phase 5. Here, the access to the potentially available food 4 1 7 in Pos. 1 was blocked using plexiglass. As in Phase 4, we performed five blocked control  Finally, in Phase 6 (Re-test), two additional tests and two empty control sessions were 4 2 0 conducted alternately to eliminate the potential bias of the order of the phases in the 4 2 1 experiment.

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For phases 4-6, in each session, be it test or control, we added motivation trials where due to a lack of motivation to participate. Overall, the monkeys were very motivated as they 4 2 6 pressed in 96% of these trials, independent of the experimental conditions (Test -Empty influence pressing the handle in either condition. For the string-pulling (dyadic tolerance) task, we used a movable wooden platform 4 3 8 (length ~ 1.5 m) to which two ropes were attached at the two extremes (Movie S2). Two  descriptions of study subjects, experimental procedure, coding and data analyses. Acknowledgements and funding sources: We are thankful to the Affenberg Zoobetriebsgesellschaft mbH, and specifically to its     Chimpanzees. Science (1979) 311, 1301-1303 (2006).       18, 375-385 (1997). interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support.