Humans closely monitor others’ cooperative relationships []. Children and adults willingly incur costs to reward helpers and punish non-helpers—even as bystanders []. Already by 3 months, infants favor individuals that they observe helping others []. This early-emerging prosocial preference may be a derived motivation that accounts for many human forms of cooperation that occur beyond dyadic interactions and are not exhibited by other animals []. As the most socially tolerant nonhuman ape [] (but see []), bonobos (Pan paniscus) provide a powerful phylogenetic test of whether this trait is derived in humans. Bonobos are more tolerant than chimpanzees, can flexibly obtain food through cooperation, and voluntarily share food in captivity and the wild, even with strangers [] (but see []). Their neural architecture exhibits a suite of characteristics associated with greater sensitivity to others [], and their sociality is hypothesized to have evolved due to selection against male aggression []. Here we show in four experiments that bonobos discriminated agents based on third-party interactions. However, they did not exhibit the human preference for helpers. Instead, they reliably favored a hinderer that obstructed another agent’s goal (experiments 1–3). In a final study (experiment 4), bonobos also chose a dominant individual over a subordinate. Bonobos’ interest in hinderers may reflect attraction to dominant individuals []. A preference for helpers over hinderers may therefore be derived in humans, supporting the hypothesis that prosocial preferences played a central role in the evolution of human development and cooperation.

Subjects exhibited a significant preference for the dominant agent (n = 24, M = 0.604 ± 0.033, p = 0.008; Figure 2 D). No subjects chose the subordinate on a majority of trials, whereas eight favored the dominant. In the control, bonobos showed no preference for either agent (n = 24, M = 0.531 ± 0.023, p = 0.180; Figure 2 D). One favored the subordinate control and four the dominant control. Within-subject comparisons revealed that subjects selected the dominant agent significantly more than its control counterpart (related-samples Wilcoxon signed-rank test, n = 24, p = 0.035; Figure 2 D). When the sample was split into adults and subadults, the effects replicated only in adults, although the subadult sample size was notably smaller (n = 6; see STAR Methods ). Given that bonobos’ dominance preference is driven by eight subjects, it’s possible that this effect explains some, but not all, of the preference for hinderers documented in the first three experiments.

Experiment 4 was identical to experiment 1, except for the animations (n = 24, M= 10.83 years, range = 4–17 years, ten females; Table 1 Table S4 ). In the test session ( Movie S4 ), subjects watched a video in which two animated agents competed for access to a central location in the scene, with the dominant agent repeatedly displacing the subordinate one, a dominance interaction familiar to nonhuman primates (see also seminal work with humans by Heider and Simmel []). To ensure that a preference in the test session did not stem from perceptual features, in the control session ( Movie S4 ) subjects witnessed the same video (with new agents) except that the agents’ actions were separated in time such that they were no longer contingent and therefore the agents should not be perceived as being dominant or subordinate to one another. As in experiment 1, all subjects participated in both conditions on separate days, with condition order counterbalanced across individuals.

In experiment 4, we further tested the dominance hypothesis—that subjects’ hinderer preference might be explained by an attraction to individuals perceived as dominant, since dominant individuals may be the most desirable allies or social partners. Although in principle prosocial and antisocial individuals can be dominant or subordinate, antisocial behavior is often used to establish and maintain dominance, and the specific antisocial behaviors exhibited by hinderers in our studies and those with human infants resemble dominance interactions: the hinderer prevails over the neutral agent or the helper in reaching his goal (of descending the hill or acquiring the toy) []. Therefore, according to the dominance hypothesis, we predicted that bonobos would exhibit a preference for an antisocial dominant over a subordinate as they did for hinderers over helpers.

Bonobos exhibited a significant shift between the baseline and test phases in response to the social demonstrations (related-samples Wilcoxon singed-rank test: n = 18, p = 0.032; Figure 2 C). Specifically, ten of 18 individuals shifted from their baseline preference toward the hinderer, and only three exhibited the opposite shift. Taken together, these three experiments demonstrate that bonobos have a robust preference for individuals that behave antisocially over those that behave prosocially toward others.

Experiment 3 employed identical methods to experiment 2 ( Figure 3 ), except that subjects participated in four baseline trials before completing four test trials (n = 18 adult bonobos, M= 12.33 years, range = 10–18 years nine females; Table 1 Table S3 ) (see [] for a similar design). Baseline trials only involved the choice phase of the procedure from experiment 2, whereas test trials included the demonstration and choice phases. Additionally, after making their choice, subjects did not receive food from either experimenter. If subjects approached one experimenter during the majority of baseline trials, this experimenter was assigned the role of helper. If subjects approached the experimenters equally during baseline trials, roles were assigned semi-randomly, with the aim of counterbalancing the role played by each experimenter across subjects [].

In experiment 3, we further tested the robustness of adult bonobos’ preference for hinderers by replicating experiment 2 but including an additional baseline phase to assess and control for subjects’ arbitrary preferences for the experimenters. Experiment 3, therefore, tested whether bonobos would shift their initial preference toward the hinderer once he began to behave antisocially.

Overall, subjects tended to select the hinderer more frequently than the helper (M = 0.551 ± 0.036 of trials), but not significantly above chance (n = 22, p = 0.158; Figure 2 B). Since in experiment 1 only adults exhibited a hinderer preference, we again separated our sample into adults and subadults, replicating the age-dependent pattern. Adults, but not subadults, exhibited a significant preference for the hinderer (adults: n= 14, M = 0.607 ± 0.047, p = 0.047; subadults: n= 8, M = 0.453 ± 0.040, p = 0.257; Figure 2 B), extending the experiment 1 finding to a completely different real-world context.

Twenty-two bonobos (11 females, M= 10.63 years, range = 4–17 years; Table 1 Table S2 ) participated in experiment 2. Experiment 2 consisted of eight trials, each involving a demonstration phase and a choice phase ( Figure 3 Movie S3 ) modeled after a similar social preference task []. In the demonstration phase, subjects watched as a neutral actor dropped a toy out of reach, a helper retrieved the toy and attempted to return it to the neutral actor, and a hinderer prevented the transfer by aggressively snatching the toy. In the choice phase, which followed immediately, the helper and hinderer approached the bonobo simultaneously with a piece of apple in their hands. Subjects received food from whichever actor they approached first.

(B) Choice phase. Subjects could approach either the helper or hinderer, both of whom held a piece of apple in their outstretched hand.

(A) Demonstration phase. Subjects watched as E1 played with and ultimately dropped a stuffed animal out of reach. The helper retrieved the toy and attempted to return it to E1, until the hinderer intervened and aggressively stole the toy.

The preferences that we observed for arbitrary shapes acting with agency may translate into the natural social interactions of bonobos. However, in a previous experiment, bonobos did not discriminate between human experimenters that they observed either attempting to share food with or steal food from another experimenter []. Therefore, in experiment 2, we tested whether the hinderer preference from experiment 1 was robust enough to generalize to a real-world social interaction involving object-centered prosocial and antisocial behavior by unfamiliar human actors.

If bonobos were responding to perceptual rather than social features of the animations, they should prefer the downward agent whose movements mirrored those of the hinderer. However, subjects showed no preference for either agent in the control condition when grouped together (n = 24, M = 0.438 ± 0.035 choice of downward agent, p = 0.084; see Figure 2 A) or separated into adults and subadults (see STAR Methods ). A direct comparison of the experimental and control conditions also revealed a significant difference in choice patterns (related-samples Wilcoxon signed-rank test, z = −2.884, n = 24, T+ = 13, ties = 9, p = 0.004), with subjects selecting the hinderer significantly more than the downward control. Thus, perceptual features alone do not appear to explain bonobos’ preference for the hinderer.

The bonobos exhibited a significant bias for selecting the hinderer (n = 24, M = 0.625 ± SE = 0.043, p = 0.011; see Figure 2 A). Only two individuals chose the helper on a majority of trials whereas 11 favored the hinderer. This finding suggests that bonobos can discriminate between prosocial and antisocial agents but that they do not show the human preference for prosocial agents. Separate analysis of adult (age 9 and above) and subadult subjects revealed that only adults showed a significant preference ( Figure 2 A; see STAR Methods for details). Because the youngest testable bonobos were already 4 years old, we cannot be certain about the preferences of younger infants. However, we found no evidence that bonobos discriminate helpers from hinderers, or at least that they exhibit strong social preferences based on third-party interactions, until adulthood—in contrast to humans’ early emerging prosocial preference.

(A) Mean proportion of choices for the hinderer and control in experiment 1, overall and for adults and subadults.

Test and control sessions each involved four trials in which subjects first witnessed the two animations for that condition in a loop (i.e., test: helper and hinderer animations; control: upward and downward animations) and then were allowed to choose between paper cutouts of the agents placed on top of small pieces of apple ( Movie S2 ). Based on previous work with infants and nonhuman apes, we used reaching behavior as a measure of preference (e.g., []). To avoid shaping subjects’ preferences, we used non-differential rewarding. Subjects received the same quality and quantity of food regardless of their choice. The helping and hindering behavior in the test events did not involve food. Therefore, a preference, for example for helpers, could not be based on subjects evaluating the agent as a social tool for food acquisition. Unless otherwise noted, all analyses for all experiments represent two-tailed one-sample Wilcoxon signed-rank tests of the proportion of trials in which subjects chose a particular agent.

Following Hamlin et al. [], we designed two control animations to examine the influence of the nonsocial features of our experimental animations. Each control animation was a variant of an experimental video in which an agent pushed an eyeless, inanimate circle up or down the hill (see Figures 1 C and 1D). Unlike the climber in the experimental animations, the inanimate circle in these control videos exhibited no independent movement or goal-directed action. Otherwise, the upward animation ( Movie S1 ) mimicked the actions of the helper animation and the downward animation ( Movie S1 ) mimicked those of the hinderer animation.

Twenty-four bonobos participated in experiment 1 (12 females, mean age (M) = 10.42 years, range = 4–19 years; Table 1 Table S1 ), completing both a test and a control condition on separate days, with condition order counterbalanced across subjects. In each condition, the experimenter sat at a table just outside the subject’s enclosure, attracted them with food, and showed the subject two different animated videos on an iPad. The videos, modeled closely after the stimuli used by Hamlin et al. [] to test human infants, depicted a pair of two-dimensional shapes interacting. As cues to their agency, each shape had two eyes with white sclera and dark pupils and exhibited goal-directed movements []. Eyes were chosen since experiments have shown that apes are sensitive to eye contact and direction [], and bonobos are even more sensitive to eye gaze than are chimpanzees []. In the test condition, each video began with a circle, the climber, entering the scene and attempting but failing three times to climb a steep hill. On the third attempt, the climber encountered another agent. In the helper animation ( Figure 1 A; Movie S1 ), a second shape (i.e., the helper; e.g., a blue triangle) entered from below and pushed the climber up to the top of the hill before returning down the hill and exiting the screen. In the hinderer animation ( Figure 1 B; Movie S1 ), a different shape (i.e., the hinderer; e.g., a red square) entered from above and pushed the climber back down the hill before returning to the top of the hill and exiting the screen. Videos were of equal length, and the helper and hinderer each spent approximately the same amount of time on screen and in contact with the climber.

Helper animation (A), hinderer animation (B), upward animation (C), and downward animation (D). In both the helper (A) and hinderer (B) animations, the climber (circle) tries but fails to scale the hill (A1 and B1) three times before encountering another agent. In the helper animation, the helper (here, a triangle) enters from below (A2), pushes the climber up the hill (A3), and exits the screen (A4). In the hinderer animation, the hinderer (here, a square) enters from above (B2), pushes the climber down the hill (B3), and exits the screen (B4). The upward animation (C) begins with a static ball at the base of the hill (C1). The upward agent enters from below (C2), pushes the ball up the hill (C3), and exits the screen (C4). Conversely, the downward animation (D) begins with a static ball at the top of the hill (D1). The downward agent enters from above (D2), pushes the ball down the hill (D3), and exits the screen (D4). See also Movies S1 and S2 and Table S1

The prosocial preference hypothesis suggests that bonobos exhibit their distinct pattern of cooperation in part because they share a preference with humans for those who are prosocial toward others. Alternatively, the dominance hypothesis suggest that, although the outcome of bonobo cooperation is often human-like, bonobos, unlike humans, are more attracted to individuals that are antisocial in third-party interactions as these individuals are more likely to be dominant, powerful allies []. To test the prosocial preference and dominance hypotheses, we showed bonobos displays in which one actor behaved prosocially and another behaved antisocially toward a third party in one context. Then we allowed bonobos to choose between the actors in a completely unrelated context.

Discussion

6 Hamlin J.K.

Wynn K.

Bloom P. Social evaluation by preverbal infants. 7 Hamlin J.K.

Wynn K. Young infants prefer prosocial to antisocial others. 8 Hamlin J.K.

Wynn K.

Bloom P. Three-month-olds show a negativity bias in their social evaluations. 11 Hare B.

Melis A.P.

Woods V.

Hastings S.

Wrangham R. Tolerance allows bonobos to outperform chimpanzees on a cooperative task. 15 Tan J.

Hare B. Bonobos share with strangers. 38 Slocombe K.E.

Zuberbühler K. Chimpanzees modify recruitment screams as a function of audience composition. 39 Wittig R.M.

Crockford C.

Langergraber K.E.

Zuberbühler K. Triadic social interactions operate across time: a field experiment with wild chimpanzees. Our results support the predictions of the dominance hypothesis and raise the possibility that the motivation to prefer prosocial individuals evolved in humans after their divergence from the other apes. In three experiments, adult bonobos spontaneously chose a human or animated agent that hindered another individual over one that helped. In contrast, by 3 months of age, human infants already show the opposite preference in related paradigms []. Bonobos failed to show a human-like preference despite their relative tolerance and prosociality in dyadic interactions []. However, bonobos were sensitive to the actors’ goal-directed actions toward others, clearly discriminating between helpers and hinderers, even when they were just animated shapes with eyes. This finding suggests that bonobos do track interactions between third parties and evaluate potential social partners based on these interactions [].

Our main finding is reproducible, having been replicated in three different experiments involving multiple paradigms with both humans and animated agents as actors. Our experiments controlled for attraction to different colors, shapes, or motion patterns. Agent color and shape were counterbalanced between subjects and, when key social features were removed, bonobos showed no preference for control agents that exhibited similar motion patterns. The fact that bonobos showed consistent preferences across all of our studies also provides validation for the more artificial but completely novel animation-based experiments. Because we used non-differential or zero rewarding and few trials, subjects did not have an opportunity to form preferences based on food acquisition. Moreover, our use of both novel animated agents and unfamiliar human experimenters allowed us to eliminate biases in social preference based on social information that is unrelated to the goals of our study (such as sex, age, reproductive status, and size of the agents). Critically, bonobos’ preferences were tested in a context that differed from the one in which the actors’ prosocial and antisocial behavior was demonstrated, minimizing the possibility that, at the moment of choice, subjects were simply expecting to be able to use the actor as a context-specific social tool.

33 Schroepfer-Walker K.

Hare B.

Wobber V. Experimental evidence that grooming and play are social currency in bonobos and chimpanzees. 16 Yamamoto S. Non-reciprocal but peaceful fruit sharing in wild bonobos in Wamba. Although the results of experiment 1 could be interpreted as bonobos preferring to steal food from the hinderer (since food accompanied their choices), experiments 2–4 suggest that this was not the case. For one, this interpretation would suggest that, in experiment 4, bonobos also preferred to steal from a dominant, which is antithetical to the concept of dominance and thus unlikely. Moreover, experiments 2 and 3 were based on a paradigm in which bonobos preferred to approach an individual who had recently groomed or played with them over one who had not [], suggesting that these measures reflect social affinity rather than acts of punishment. Finally, the interpretation that bonobos prefer dominant hinderers accords with natural observations in which bonobos exhibit courtesy begging toward high-ranking individuals to build and test relationships [].

24 Vervaecke H.

de Vries H.

Van Elsaker L. Function and distribution of coalitions in captive bonobos (Pan paniscus). 40 Chapais B. Alliances as a means of competition in primates: evolutionary, developmental, and cognitive aspects. 41 Duffy K.G.

Wrangham R.W.

Silk J.B. Male chimpanzees exchange political support for mating opportunities. 16 Yamamoto S. Non-reciprocal but peaceful fruit sharing in wild bonobos in Wamba. 42 Surbeck M.

Langergraber K.E.

Fruth B.

Vigilant L.

Hohmann G. Male reproductive skew is higher in bonobos than chimpanzees. Bonobos may prefer hinderers because they appear to be more dominant than helpers. When intervening in third-party conflicts, primates often support the higher-ranking contestant or the one who is already winning (i.e., “winner support”), and they may gain reproductive benefits from doing so []. For example, high-ranking male chimpanzees, who often prevent others from mating, have been shown to be more tolerant of mating by their supporters []. In food sharing contexts, wild bonobos preferentially beg for food from dominants even when they can easily obtain the same food themselves, perhaps to test their social tolerance []. Recent evidence also suggests that female bonobos may exert especially high levels of choice in mating decisions, selecting the highest-ranking males []. In support of this dominance preference interpretation, in experiment 4, bonobos favored a dominant agent over a subordinate one. Hindering and dominance are not inextricably linked, however, and, as such, research with humans and nonhuman animals should continue to investigate understanding of these qualities and the relationship between preferences for prosocial versus antisocial agents and for dominants versus subordinates.

43 Anderson J.R.

Kuroshima H.

Takimoto A.

Fujita K. Third-party social evaluation of humans by monkeys. 26 Herrmann E.

Keupp S.

Hare B.

Vaish A.

Tomasello M. Direct and indirect reputation formation in nonhuman great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus) and human children (Homo sapiens). 27 Russell Y.I.

Call J.

Dunbar R.I. Image scoring in great apes. 28 Subiaul F.

Vonk J.

Okamoto-Barth S.

Barth J. Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers. Future work should also examine whether there are contexts in which bonobos do prefer prosocial individuals (e.g., in response to conspecifics). Our spontaneous measures can also be extended to a range of species. Capuchin monkeys (Cebus apella) would be a good prospect since in some contexts they show a preference for helpers over non-helpers. However, they have yet to be tested for their preference between helpers and hinderers []. Our work will also need to be extended to other apes to provide more resolution on the phylogenetic history of this trait in our lineage. For example, chimpanzees and orangutans spontaneously requested food from a human they had observed sharing food with a third party over one who had refused to share []. However, it is unclear whether this potential prosocial preference would generalize to cases, like those investigated in our experiments and experiments with human infants, where participants must evaluate others based on prosocial and antisocial interactions that are not immediately relevant to the participants. Chimpanzees prefer to seek food from an individual who has shared food moments before, but would they also prefer to interact with an individual who has previously helped a third party to access a goal object, as human infants do, or would they instead prefer to interact with someone who has previously thwarted a third party’s goal, like bonobos? Further work on chimpanzees’ social preferences and evaluative cognition is necessary to clarify whether bonobos or humans show the more derived preference.