Humans are thought to possess a unique proclivity to share with others – including strangers. This puzzling phenomenon has led many to suggest that sharing with strangers originates from human-unique language, social norms, warfare and/or cooperative breeding. However, bonobos, our closest living relative, are highly tolerant and, in the wild, are capable of having affiliative interactions with strangers. In four experiments, we therefore examined whether bonobos will voluntarily donate food to strangers. We show that bonobos will forego their own food for the benefit of interacting with a stranger. Their prosociality is in part driven by unselfish motivation, because bonobos will even help strangers acquire out-of-reach food when no desirable social interaction is possible. However, this prosociality has its limitations because bonobos will not donate food in their possession when a social interaction is not possible. These results indicate that other-regarding preferences toward strangers are not uniquely human. Moreover, language, social norms, warfare and cooperative breeding are unnecessary for the evolution of xenophilic sharing. Instead, we propose that prosociality toward strangers initially evolves due to selection for social tolerance, allowing the expansion of individual social networks. Human social norms and language may subsequently extend this ape-like social preference to the most costly contexts.

Bonobos are known for relatively high-levels of tolerance within and between groups when compared to chimpanzees [34] , [39] – [43] . In the wild, bonobos have even been observed to have affiliative intergroup interactions. For example, females from neighboring communities have been seen traveling together for days, feeding in the same trees and even participating in socio-sexual behavior ( [39] , [40] , also see [44] ). In a preliminary experiment seven bonobos were given the opportunity to voluntarily share with another bonobo [12] . All three bonobos paired with a non-groupmate voluntarily shared their food while only one of the four bonobos paired with an in-group shared. No aggression of any form was ever observed. This suggests that with the relative tolerance of bonobos they can afford such prosociality with strangers. In turn, sharing with a stranger might aid them in extending their social network and in forming new “friendships” [5] , [45] . However, it remains unclear whether the observed prosociality represents a preference to share with strangers over groupmates. In addition, it is unclear if the voluntary sharing observed only represents a selfish tactic to obtain a novel social interaction or whether bonobos will also share with strangers if there is no immediate, tangible reward. Therefore, we conducted four experiments with 15 wild-born bonobos that are orphans of the bushmeat trade living at Lola Ya Bonobo Sanctuary in Kinshasa, Democratic Republic of Congo [46] . We designed these experiments based on the relative costs and benefits of the prosocial behavior to the actor and this serial design allowed us to identify whether the prosocial motivation is selfish or other-regarding ( Table 1 ). In experiment 1 and 2 we presented bonobos with a task in which they could choose whether to share food and physically interact with either a groupmate or stranger. In experiment 3 and 4 we presented bonobos with a second task in which they could either ignore or help another bonobo in obtaining out-of-reach food. In this second task helping allowed no immediate benefit to the actor (e.g. physical interactions) and the cost of helping was altered between experiment 3 and 4 (see Table 1 ).

Nonhuman primates are known to help and voluntarily share food with other groupmates (e.g. [10] – [16] ). This prosociality, or voluntary behavior that benefits others [17] – [21] , can be driven by selfish or other-regarding motivations [17] , [22] . Therefore, while a primate can be prosocial even if pursuing selfish goals, they only demonstrate other-regarding forms of prosociality if their actions do not result in immediate selfish benefit (see SI for disambiguation of prosocial, other-regarding and altruistic behaviors). A number of experiments have now shown that a variety of primates will even help another individual obtain food when there is no immediate, tangible reward for their help (chimpanzees: [4] , [23] – [27] ; old world monkeys: [28] ; new world monkeys: [29] – [31] ). This type of prosociality suggests in some contexts primates also have other-regarding motivations (but see critique of this interpretation by [9] ). However, there remains little evidence that nonhuman primates show any form of prosociality toward non-group members [7] , [9] , [13] , [31] , [32] . Primates typically compete against non-group members, resulting in agonistic intergroup relations [33] . This hostility goes to the extreme in chimpanzees that opportunistically kill neighbors [34] , [35] and sometimes even immigrants [36] – [38] . Therefore, it is unlikely that most primates have tolerance levels that would allow for prosocial or other-regarding tendencies toward strangers. Moreover, designing such an experiment for most primate species would be extremely difficult given the high potential for stress, injury and aggression.

One of the most puzzling human behaviors from an evolutionary perspective is our species' propensity to share with non-relatives and even strangers [1] , [2] . Across numerous cultures and early in development, humans engage in spontaneous helping and costly sharing with strangers [3] , [4] . Some have suggested this human form of sharing is inconsistent with the predictions of kinship theory and reciprocal altruism (see [1] , but see [5] ) while others have proposed our species has evolved unique motivation and cognition for sharing [6] – [9] .

Experiment 1

The purpose of experiment 1 was to determine whether bonobos share and prefer to share food with strangers based on [12]. The subjects entered a room baited with a pile of highly desirable food. They could either eat all the food alone or they could co-feed with a conspecific by removing a one-way key to release either a groupmate or a stranger who were each locked in separate adjacent rooms (Figure 1a).

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larger image TIFF original image Download: Figure 1. Experimental setups of experiment 1–4. In experiment 1 (a) and 2 (b), prosociality incurred a high cost (food loss) but potentially yielded immediate benefits (social interactions). In experiment 3 (c) and 4 (d), prosociality had no potential selfish benefits but always incurred a cost. Note that subjects always had complete control over the keys and therefore any prosocial behavior was voluntary. https://doi.org/10.1371/journal.pone.0051922.g001

Subjects Fourteen bonobos (8F∶6M) from Lola ya Bonobo sanctuary participated in this experiment (see SI). All experiments were approved by the Ministry of Research in the Democratic Republic of the Congo (#MIN.RS/SG/004/2009), Lola ya Bonobo sanctuary and Duke IACUC. All subjects are orphans of bushmeat trade, but a comparison of their psychological health to mother-reared individuals revealed no substantial differences [49]. Each subject was tested with two conspecific recipients – one a stranger and the other a current groupmate. Seven female subjects played the role of the recipient (see Table S1 for pairings). We did not use male recipients simply because we did not have enough available at the time of the experiment. The composition of all trios allowed no role-reversal and maximized combinations of available recipients (see SI). Additionally, because pre-existing relationships among groupmates might be a confounding factor, we included as many individuals into the recipient pool as possible and randomly paired each subject with a groupmate recipient. Strangers. were defined as unrelated individuals living in different social groups from one another. All subjects came from two different groups (see Table S1). Each group has a separate outdoor enclosure and set of indoor sleeping rooms. Strangers therefore did not have physical access to one another, because they were always physically separated by mesh and an electric fence. There was only possibility for vocal and visual communication, and this resembled the way wild bonobos from different populations interact [39]. Nine of fourteen of our stranger pairings were complete strangers who had never stayed in the same physical enclosure prior to the current experiment. We were able to examine individual records at the sanctuary to confirm which subjects were complete strangers. We tested the maximum number of complete strangers we could produce given sample size limitations and management constraints. Two pairings were not complete strangers because they met briefly during testing before they themselves were tested (i.e. they had served as recipients opposite one another for two previously tested subjects). For the last three pairings, they were former groupmates but had been transferred to different groups for at least one year (i.e. a period of time that in captive chimpanzees (Pan troglodytes) typically leads to a strong xenophobic response during reintegration attempts [50]).

Setup The experiment was conducted in three adjacent testing rooms (Figure 1a). These rooms (each 15 m2) were in the subjects' night building and were separated by open mesh. Manual sliding doors connected the middle room and the two side rooms where the recipients were placed for testing. The middle room also had a separate entrance (i.e. an overhead raceway) through which the subject could enter at the beginning of each test trial. A one-way key system was installed in each of the doors from the middle room into each of the side rooms. The keys consisted of wooden pegs that could be inserted on the subject's side of the door into a round metal hole in the track of the door. This blocked the path of the door unless the key was removed by the subject (see Figure S1a). Removing both keys simultaneously was impossible due to the distance between them. We thus created a setup in which bonobos in the middle room could determine whether to unlock a door(s) and which door to unlock first.

Procedure Food introduction. This was designed to demonstrate that subjects understood the one-way key system. One side room was baited with slices of apples or bananas and locked with the one-way key. Subjects had to successfully retrieve food out of the adjacent room in four out of five consecutive trials within 60 seconds. No-food introduction. This was designed to demonstrate that subjects' door-opening was not simply intrinsically motivating but instead goal-directed. The setup was identical to the food introduction except food was placed in the middle room instead of in one of the side rooms. Subjects needed to inhibit removing the key for 60 s in four out of five consecutive trials in less than 21 trials. Number pre-test. This was designed to demonstrate that subjects could make a choice between the contents of the two side rooms. Both side rooms were locked and one was baited with more food than the other. The locations of food were counterbalanced within and across subjects. Subjects had to first unlock the room with more food in four 1-minute trials of a five-trial session. Test. For the test a potential recipient was moved into each of the two side rooms – one being a stranger to the subject (as well as the second recipient) and the other being a groupmate of the subject (see Figure 1a). The location of the different recipients were switched between trials and counterbalanced within and across subjects. Following [12], a mixture of food was placed in a small pile in the center of the food room (i.e. the middle room) beyond the reach of the recipients (see SI). A trial started when the subject entered the food room and ended when all the desirable food was claimed or seven minutes after the entry of the subject. Subjects were tested in a five-trial session with the same two recipients throughout, and they were tested early in the morning before their first meal to maximize their food motivation.

Coding and analysis Based on [15], [16], we define sharing as joint use of monopolizable food. Sharing is a type of prosocial behavior if it is voluntary, i.e. the possessor has the intention to allow the recipient access to food. However, this intention is not necessarily other-regarding or altruistic (i.e. instead they intentionally give another bonobo access to food without concern for the recipient's well-being). As the measurement of sharing, door-opening was coded when a subject first removed the key to one of the doors but only if this occurred before all desirable food was claimed. Following [12], food being “claimed” was scored when a bonobo (both subjects and recipients) picked up each of the different pieces of food. This conservative criterion means only food that subjects did not pick up in the original food pile before releasing one of the recipients was scored as potentially sharable (i.e. food that subjects claimed but dropped might not represent their intention to share and would be excluded). Because a trial could take up to seven minutes, it was also possible for the second door to be opened releasing the second recipient before the end of the trial. A second door-opening was scored when either the subject or the first recipient removed the key to the second door - again only if this occurred before all the desirable food was claimed. We coded food consumption if an individual placed food into its mouth. Because the bonobos could take a handful of food at once, we were unable to track the exact amount of food each recipient consumed. As a proxy, we compared “shared” feeding-time (i.e. from when a recipient was released until when all food was consumed) to total feeding-time (i.e. from when the subject started feeding to when all food was consumed). Socio-sexual behavior was scored when genital-genital contact occurred between two individuals once a recipient door was opened and before all the desirable food was claimed. Similarly, aggression was also scored if one bonobo fought with another bonobo resulting in screaming, hitting and biting. To assess the effect of recipients' solicitation, we categorized the recipient in each trial as either 1) active if they made any attempt to open the locked door or to reach the food, or 2) passive if no such behavior was observed. Inter-coder reliability was high (door-opening, food consumption, socio-sexual behavior, aggression: Cohen's K = 1; signaling behavior: K = 0.720; feeding time: N = 12, r = 0.993, Spearman's correlation). Nonparametric, two-tailed statistics were used in all analyses.

Results See Figure 2a for results and Movie S1 for a sample video. The majority of the subjects (12 of 14) shared at least once and for a total of 51 trials (out of 70 or 72.9%). Subjects chose to release a complete stranger in preference to a groupmate before eating all the food (N = 9 (two ties), Z = 1.961, p = 0.05, Wilcoxon test), while having a strong tendency when all strangers are included (N = 14 (two ties), Z = 1.737, p = 0.081, Wilcoxon test). Nine subjects released the stranger first in more trials than the groupmate and only three subjects were in the opposite direction (see Table S1). Subjects also allowed the stranger but not the groupmate to co-feed for the majority of the total feeding time (stranger: N = 10, T = −2.090, p = 0.037; groupmate: N = 6, T = −0.105, p = 0.917, one-sample Wilcoxon signed rank test). Moreover, while unexpected, the second recipient was often released after the first even though there was remaining food that would need to be shared three ways. When the subject released the stranger first, the second recipient (the groupmate) was released by this first recipient (the stranger) more often than by the subject (N = 8 (one tie), Z = 1.983, p = 0.047, Wilcoxon test, Figure 2a). PPT PowerPoint slide

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larger image TIFF original image Download: Figure 2. Results of experiment 1–4. ** p≤0.10, * p≤0.05, Wilcoxon test. In experiment 1 (a), we used two-tailed statistics. Based on the directional results of experiment 1 and those of [12], we had a priori predictions bonobos are spontaneously and preferentially prosocial toward strangers. Therefore, in experiment 2 (b) and 3–4 (c) we were justified to use one-tailed statistics. https://doi.org/10.1371/journal.pone.0051922.g002 Subjects consumed part of the food before releasing a recipient in 86.3% of trials where sharing occurred (44 of 51). The released recipients obtained desirable food in 78% of the trials (40 of 51). No form of aggression was ever observed. Socio-sexual behavior between the subjects and the first recipient released was observed in 20 trials (39.2%). This behavior only occurred between strangers but not groupmates (N = 51, r = 0.494, p<0.001, Phi coefficient). We found no co-variation between socio-sexual behavior and consumption of food by the recipient within trials where subjects unlocked a door (N = 51, r = 0.128, p = 0.360, Phi coefficient). Recipients' signaling behavior also did not correlate with subjects' tendency to share (N = 60, r = 0.074, p = 0.573, Spearman's correlation). Finally, subjects' prosociality did not change between the first and the last two trials (tendency to release a recipient: N = 14, Z = −0.378, p = 0.705; preference for releasing the stranger: N = 14, Z = −0.427, p = 0.669, Wilcoxon test).