Does the Bonobo Have a (Chimpanzee-Like) Theory of Mind?

Chapter 6 Does the bonobo have a (chimpanzee-like) theory of mind?

Christopher Krupenye, Evan L. MacLean and Brian Hare

Abstract Theory of mind—the ability to reason about the thoughts and emotions of others—is central to what makes us human. Chimpanzees too appear to understand some psychological states. While less is known about bonobos, several lines of evidence suggest that the social-cognitive abilities of the two sister taxa may differ in key respects. This chapter outlines a framework to guide future research on bonobo social cognition based on the predictions of two potentially complementary hypotheses. The self-domestication hypothesis suggests that selection against aggression and for prosociality in bonobos may have impacted the ontogeny of their social-cognitive skills relative to chimpanzees. The empathizing–systemizing hypothesis links degree of prenatal brain masculinization, a potential result of self-domestication, to adult cognition. Specifically, relative feminization may yield more flexible theory of mind skills in bonobos than chimpanzees. Finally, directions for future study, including development of new paradigms that maximize ecological validity for bonobos, are discussed. La théorie de l’esprit—le pouvoir de raisonner les pensées et émotions des autres—est centrale à notre nature humaine. Il parait que les chimpanzés peuvent comprendre quelques états psychologiques. Tandis que nous savons moins des bonobos, plusieurs té- moignages suggèrent que les capacités socio-cognitives des deux taxons soeur peuvent différer dans des aspects clefs. Nous traçons un cadre pour guider les prochaines recherches sur la cognition sociale des bonobos, basé sur les prédictions de deux hypothèses potentiellement complémentaires. L’hypothèse d’auto-domestication suggère que l’anti-agression et la prosocialité des bonobos a influé leur ontogenèse et leur capacités socio-cognitives relativement aux chimpanzés. L’hypothèse d’empathie systématique (Empathizing–Systemizing) forme un lien entre le degré de masculinisation prénatale du cerveau, le résultat potentiel d’auto- domestication, et la cognition adulte. Spécifiquement, la féminisation relative génère des théories de l’esprit plus flexibles chez les bonobos que chez les chimpanzés. Enfin, nous discutons le directions pour les prochaines études, inclut le développement de nouveaux paradigmes qui maximisent la validité écologique des bonobos.

Introduction even the limited comparisons that are now possible between the two species are helping to test hypoth- Humans are adept at making inferences about the eses about how such skills might evolve across spe- psychological states of others, including their emo- cies, including our own (Hare, 2011). tions, desires and beliefs. These inferences then In 1978, Premack and Woodruff first posed the inform our attempts to cooperate, resolve conflicts question, ‘Does the chimpanzee have a theory and communicate effectively. Such theory of mind of mind?’ At the time, chimpanzees were a clear (ToM) abilities, as they are known, were long be- choice for the first comparative investigations of lieved to be unique to humans but there is now human social cognition. Humans have two clos- evidence that in some contexts chimpanzees are est relatives. However, bonobos were discovered capable of attributing to others a range of psycho- much later than chimpanzees, in large part because logical states (Hare, 2011; Tomasello and Call, 1997). they inhabit a much more restricted range, south Less work has been accomplished with bonobos but of the Congo River, compared to chimpanzees’

Krupenye, C., MacLean, E. L., and Hare, B., Does the bonobo have a (chimpanzee-like) theory of mind? In: Bonobos: Unique in Mind, Brain, and Behavior. Edited by Brian Hare and Shinya Yamamoto: Oxford University Press (2017). © Oxford University Press. DOI: 10.1093/oso/9780198728511.003.0006

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Figure 6.1 Several lines of evidence suggest that bonobos may be more empathic than chimpanzees but further social cognitive comparisons are critical. (Plusieurs sources de données suggèrent que les bonobos montreraient plus d’empathie que les chimpanzés, mais d’autres comparaisons cognitives sociales relativisent cette observation.)

distribution throughout East, Central and West depicted humans facing a variety of problems (e.g. Africa. Bonobos were still barely known to science a banana was out of reach, or the actor shivered in 1978 while chimpanzees were relatively common because the heater was broken). Sarah was then in captivity and were already the subject of several allowed to choose among photographs of various captive and field research programs. However, even objects, only one of which would solve the problem after field sites were established to study bonobos presented in the video (e.g. a stick to retrieve the ba- in the wild, they remained little studied in captivity. nana, or a lit wick for the heater). Sarah consistently We currently find ourselves at an exciting moment chose the correct photograph, leading the authors to in bonobo research since there has been more work conclude that she understood the goals of the actors on bonobo cognition in the past ten years than the in the videos. Later, Povinelli and colleagues (1990) previous hundred. For the first time, quantitative reported a study in which chimpanzees discrimi- and qualitative comparisons between bonobos and nated between a knowledgeable and an ignorant in- chimpanzees are possible. Here we summarize what formant and selectively followed pointing gestures has been learned about ToM in chimpanzees since from the knowledgeable informant in order to find Premack and Woodruff’s seminal investigations. We hidden food. However, Heyes (1993) offered compel- then present two hypotheses relevant to the selective ling alternative interpretations for existing data on pressures that have shaped—and proximate mecha- animal mindreading, and in the years that followed nisms that underlie—ape social cognition. From these a number of studies reported that chimpanzees hypotheses, we generate predictions about possible did not follow the communicative cues of a knowl- differences in social cognition between chimpanzees edgeable human or conspecific when searching for and bonobos. Finally, we evaluate our hypotheses food. These data led Tomasello and Call (1997) to against existing data and discuss the most pressing conclude, in their landmark book Primate Cognition, directions for future research (Figure 6.1). that ‘there is no solid evidence that nonhuman primates understand the intentionality or mental states of others’ (p. 340). ToM was therefore an aspect of Theory of mind in chimpanzees human cognition in which the differences between Historical perspective humans and other animals were thought to be qualitative, rather than quantitative, in nature. Premack and Woodruff (1978) showed videos to a This view began to change when Hare (2001) human-raised chimpanzee, Sarah. These videos noted that primate social life is highly competitive

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and suggested that since primate cognitive abilities from them, chimpanzees will walk around to the have most likely been adapted for such a setting, front of the agent before attempting to communi- it may be in competitive situations that primates cate (Liebal et al., 2004). They also shift their use of are most motivated to exhibit their cognitive skills. gestural versus vocal communication depending on Additionally, Tomasello and colleagues (2003) sug- whether their target is facing towards or away from gested that chimpanzees’ failure to follow the com- them (Hostetter et al., 2001, Leavens et al., 2004). municative cues of a knowledgeable informant may To test the idea that chimpanzees can assess what not owe to a lack of ToM abilities in general but another individual can see, Hare and colleagues rather to a specific inability to understand the coop- (2000) examined how chimpanzees compete against erative intentions underlying such communicative one another over food in an experimental setting. cues. If chimpanzees do not produce cooperative Two chimpanzees were situated in separate testing communicative cues themselves, why should they rooms on either side of a central room where food understand such cues when others produce them? was hidden. Each could see her competitor on the Through more ecologically valid paradigms—that other side of the central room. Dominant individu- used some combination of spontaneous behavio- als are able to monopolize visible food. However, ral measures, larger sample sizes and competitive in each experiment, there was a critical condition in social contexts—substantial evidence for chimpan- which both pieces of food were visible to the sub- zees’ understanding of others’ perception, knowl- ordinate competitor but only one of the pieces was edge and goals has accumulated. visible to the dominant in the pair. In these condi- tions, subordinates preferentially targeted the food that the dominant could not see. In these crucial Understanding of perception tests subordinates were given a slight head-start, Much work has explored what chimpanzees un- and could not see the dominant when they made derstand of others’ perception. This research has their choice of direction to approach. This ensured largely focused on seeing and to some extent hear- that subjects were not simply responding to the being. Like many species, chimpanzees are capable of havior or gaze direction of their competitor. These following the gaze of conspecific or human social studies provided the first compelling evidence that partners (Brauer et al., 2005; Povinelli and Eddy, chimpanzees may be sensitive to others’ visual 1996; Tomasello et al., 1998). Gaze following could perspectives. reflect an appreciation of the other’s visual perspec- Building on this initial success, competitive ex- tive or it could be a simple reflexive response that periments were then designed to examine whether evolved for its clear adaptive benefits (Tomasello apes can intentionally manipulate what others per- et al., 1998). Co-orienting to match the target of ceive (Hare et al., 2006). Chimpanzees were given another’s attention may alert the gaze follower to the opportunity to steal food from a human com- important resources, such as food or mates, as well petitor who pulled the food out of reach if he de- as threats, such as predators or aggressive conspe- tected the subject’s approach. Chimpanzees were cifics. In chimpanzees at least, gaze following ap- then given a choice between paths that either pears to be more than just a reflexive response. This visually concealed or exposed their approach. The species follows gaze geometrically, around barri- chimpanzees spontaneously preferred a hidden ers and checks back with the actor when it cannot path avoiding the competitor’s face, behind an identify the target of her gaze (Brauer et al., 2005; opaque barrier rather than a transparent one, and Tomasello et al., 1999). Chimpanzees are also sen- behind a complete barrier rather than a partial one. sitive to an agent’s attentional state. For example, They also used indirect approaches in which they when begging for food, they spontaneously use initially moved away from the food and out of the more gestures when their target’s face or body is view of their competitor before they approached the oriented towards them than when it is oriented food behind an occluder. In a similar setup in which away (Kaminski et al., 2004). When attempting to chimpanzees could remain concealed until the fi- communicate with an agent who is facing away nal step of their approach in which they needed to

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reach through an opaque or transparent tube to re- (2015b) used a competitive setup very similar to trieve the food, they reliably chose the opaque tube Melis and co-workers (2006). Chimpanzees at- that concealed their reach (Melis et al., 2006). tempted to steal food from a human experimenter Further, Karg and colleagues (2015a) showed that who could not see them until they reached their chimpanzees strategically manipulate whether they hand into the tubes where the food was located. themselves can be seen by another agent and what From a distance, both tubes appeared to block the other features of the environment the agent can see. human’s view but one was actually see-through. Food was located in several small trays. The chim- Before the test phase, subjects were shown pea- panzees could move the individual trays behind nuts behind each surface so that they could expe- or in front of an occluder, but could not retrieve rience the occlusive properties of the tubes. In the the food themselves. Subjects left food concealed test phase, they avoided the see-through tube, even more often when interacting with a competitor who though from afar both looked identical. These re- would steal the food than when interacting with a sults suggest that chimpanzees were able to infer cooperator who would retrieve it for them. They what their competitor could see based on their own exposed more food to the cooperator than the com- self-experience with these novel occluders. petitor; however, they did not actively hide visible food from the competitor. Attributing knowledge, ignorance and false Research has also explored whether chimpan- belief to others zees are sensitive to what others can hear. Melis and colleagues (2006) showed that, when visually In addition to reasoning about what others can concealed from their competitor, chimpanzees pre- perceive in the present, experimental evidence ferred to steal food using an approach that was si- suggests that chimpanzees are capable of under- lent over one that that was noisy. However, Brauer standing what others have perceived in the past. In and co-workers (2008) found that when chimpan- a competitive paradigm, subordinate chimpanzees zees competed with conspecifics for hidden food in were more likely to approach hidden food when a manner similar to that reported by Hare and col- their competitor was uninformed or misinformed leagues (2000), they did not appear to infer which about its location than when he was knowledge- piece of food their competitor was aware of based able (Hare et al., 2001). Similarly, chimpanzees were on what their competitor could hear. They were reluctant to approach food when their competi- equally likely to approach a piece of food that their tor had witnessed it being hidden but not if their competitor could not see but could hear during competitor was switched out for a new dominant baiting and one that their competitor could neither individual who had not seen the baiting process see nor hear. (Hare et al., 2001). In the ‘chimp chess’ paradigm To determine whether chimpanzees were re- in which food was baited in several cups and two sponding to others’ visual perspectives and not chimpanzees took turns searching for that food— just using a behavior rule (e.g. that agents pursue each blind to the other’s choices—subjects adjusted anything in their environment as long as a direct their behavior depending on whether their compet- line can be drawn between the agent and the tar- itor was knowledgeable or ignorant of the food’s get, Heyes, 1993; Heyes, 1998; Penn and Povinelli, location (Kaminski et al., 2008). When the subject 2007, but see Table 1 in Hare, 2011 for a summary of chose second, she avoided food that her competitor evidence against this and other alternative explana- knew about (inferring that the competitor would tions), critics proposed giving subjects unique self- have already retrieved this item). MacLean and experience with unfamiliar equipment that alters Hare (2012) presented chimpanzees with a series of one’s perceptual access. Then these subjects could experiments in which subjects witnessed an experi- be tested to evaluate whether their self-experience menter become aware of or remain ignorant to an aided their ability to correctly predict the effect of object that was placed in his vicinity (by visually this same equipment on the visual experience of orienting to it or not). The experimenter later looked others (Heyes, 1998). To do so, Karg and colleagues in the direction of the object and mimicked surprise.

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Subjects recognized when the experimenter already goals and intentions. Chimpanzees treat the actions of knew about the object, and in these cases were more a human, but not a mechanical claw, as goal-directed likely to follow the experimenter’s line of sight be- and anticipate the outcomes of these goal-directed yond the object in search of an alternate target of his actions (Kano and Call, 2014b; Myowa-Yamakoshi attention. Finally, in a field experiment, Crockford et al., 2012). They correctly identify an actor’s goal and colleagues (2012) showed that chimpanzees in based on the context of his actions (Buttelmann et al., the presence of a snake were more likely to alert 2012). Chimpanzees are also able to complete others’ an incoming groupmate to the snake if she had not failed actions (Tomasello and Carpenter, 2005). They yet seen it than if she was already knowledgeable. provide targeted help to conspecific and human part- Together, these studies show that chimpanzees can ners based on a specific understanding of their part- discriminate between knowledgeable and ignorant ner’s needs (Melis and Tomasello, 2013; Warneken individuals, they have different expectations of et al., 2007; Yamamoto et al., 2012). Chimpanzees also how these agents will behave, and they use this in- discriminate intentional from accidental actions (Call formation both to outcompete ignorant groupmates and Tomasello, 1998; Tomasello and Carpenter, 2005) and potentially even to inform them of danger. and respond differently to an experimenter when To-date, however, no experimental demonstra- he is unwilling to help them versus unable to do so, tion is consistent with chimpanzees explicitly at- even though the experimenter performs very similar tributing false beliefs to others (Call and Tomasello, actions in each case (Call et al., 2004). Taken together, 1999; Hare et al., 2001; Kaminski et al., 2008; Krachun these studies suggest that chimpanzees have a ro- et al., 2009). A false belief exists when an individual bust understanding of the goals and intentions that believes something that is different from reality. govern others’ actions. Unlike knowledge or ignorance, understanding Given the cooperative nature of human society, false beliefs requires representing not only whether humans are also known to exhibit shared intention- or not the individual is aware of the true state of ality (Tomasello et al., 2005). Shared intentionality the world but also specifically the way in which describes our ability to hold, and attribute to oth- she construes the world to be different than it is. ers, shared goals and intentions that structure col- In humans, this ability appears to be tightly linked laborative or joint activities. For example, when to language development (Milligan et al., 2007). performing a collaborative activity, all collabora- In one study with chimpanzees, an experimenter tors are aware of their shared goal as well as each baited food in one of two containers out of view of other’s complementary roles required to accom- the subject but within view of a human competi- plish the goal. Although chimpanzees engaged in tor (Krachun et al., 2009). In the critical condition, triadic turn-taking activities with humans and even the competitor then either turned around or left elicited further interaction after the activities were the room and the experimenter switched the loca- terminated, it remains unknown if these activities tions of the cups. When the competitor returned she are supported by an understanding of shared inten- reached effortfully for the now incorrect location. tions (MacLean and Hare, 2013; Warneken et al., While in one experiment chimpanzees tended to 2006). Some evidence suggest that chimpanzees are look at the baited container in false belief trials, they aware of their partners’ role in collaborative activi- still followed the competitor’s reaching gesture and ties and even the means that are necessary for the selected the incorrect cup. Although their looking partner to accomplish that role, suggesting that dif- behavior may reflect some implicit understanding ferences in motivation rather than cognition may of belief, unlike human children, chimpanzees were underlie species differences in shared intentionality unable to act on this understanding. (Melis and Tomasello, 2013).

Recognizing others’ goals and intentions Summary

A variety of experiments suggest that chimpanzees Chimpanzees have at least a basic understanding of and other apes have some understanding of others’ others’ perspectives: they know whether or not an

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agent can see or hear a stimulus. They also know chimpanzees on most cognitive tasks, this is not al- whether or not an agent is knowledgeable or ig- ways the case (Herrmann et al., 2010). Only through norant about that stimulus, and they can reason studying the three species can we confidently infer about the goals and intentions that underlie agents’ which aspects of our cognition are shared evolu- actions. However, they may not possess explicit tionarily, and which are unique to each species. Per- comprehension of others’ false beliefs, or the co- haps even more importantly, there is much reason to operative motivations that are necessary for shared believe that bonobos will offer some very different intentionality. This cognitive profile may also be clues than chimpanzees about human evolutionary shared by the last common ancestor of humans and history (Hare, 2011). Below, we outline a frame- chimpanzees. However, such an evolutionary in- work that guides our analysis of existing compara- ference requires either assuming commonality be- tive studies and our suggested directions for future tween bonobo and chimpanzee ToM or that the last work. We describe the self-domestication and em- common ancestor was more similar cognitively to pathizing–systemizing hypotheses, which comple- chimpanzees than bonobos. ment one another and provide testable ultimate and proximate explanations for differences in chimpan- Bonobo cognitive evolution zee and bonobo social cognition (Figure 6.2).

The singular focus on chimpanzees as a model for The self-domestication hypothesis human cognitive evolution is problematic because, like humans, chimpanzees too have experienced The self-domestication hypothesis is based on the 5–7 million years of evolution since our lineages di- observation that domestication—which frequently verged. Likewise, bonobos and chimpanzees have involves artificial selection against aggression— experienced around a million years of independent consistently produces a suite of changes in mor- evolution. Although the general assumption has phology, physiology, behavior and cognition rela- often been that bonobos will perform similarly to tive to a species’ wild counterpart (Hare et al.,

Empathizing-Systemizing Hypothesis

Bonobos Chimpanzees lower prenatal androgen higher

lower masculinization of the brain higher – +

higher empathizing lower empathizing empathizing systemizing lower systemizing higher systemizing

Bonobos Predictions Chimpanzees

higher Social Tolerance lower higher Theory of Mind Skills lower lower Casual Reasoning and Tool Use higher lower Signs of Masculinization higher

Figure 6.2 diagram and predictions of the Empathizing–Systemizing hypothesis. (Diagramme et prédictions de l’hypothèse Empathizing-Systemizing.)

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2012). Importantly, in many cases of domestica- Specifically, domesticates show juvenilization or re- tion, including that of dogs from wolves, a phase of tention of paedomorphic traits into adulthood that self-domestication has been proposed to have pre- in non-domesticates are only present in infants and ceded domestication by artificial selection.D uring juveniles. They also often exhibit delayed patterns self-domestication of dogs, natural selection most of development. Since relaxed feeding competition likely favoured individuals who were more socially is believed to have facilitated selection against ag- tolerant and less fearful of humans, as these indi- gression in bonobos, delays are expected to impact viduals could live in closer proximity to humans behaviors related to feeding competition. Such de- and exploit new resources such as human refuse. In lays have been shown relative to chimpanzees in this way, selection against aggression is thought to the ontogeny of social intolerance, social inhibition have exerted pressures on canine evolution through and spatial memory (Rosati and Hare, 2012; Wobber natural selection even before the intervention of ar- et al., 2010b). tificial selection. Therefore, the chief prediction that we can draw Relative to chimpanzees, bonobos exhibit many from the self-domestication hypothesis is that there of the characteristic changes associated with the will be a relationship between delayed patterns of de- domestication syndrome, and are hypothesized to velopment and ToM abilities in bonobos. However, have been self-domesticated via natural selection there are several competing hypotheses about the for prosociality and against extreme forms of ag- specific influence that delayed development will have gression (Hare et al., 2012). Bonobos exhibit higher on adult ToM. Additionally, it is not clear whether all levels of tolerance while co-feeding than chimpan- ToM skills will be impacted in the same way. zees and consequently are more flexible cooperators One possibility is that social cognitive traits in instrumental tasks (Hare et al., 2007). Whereas themselves will be delayed. Nevertheless, despite chimpanzees are highly xenophobic, bonobos are the delay, bonobos may eventually demonstrate known to be prosocial even with strangers (Tan and comparable performance to chimpanzees on ToM Hare, 2013). Researchers have also documented tasks (e.g. as is the case with social inhibition, species differences in apes’ neuroanatomy and hor- Wobber et al., 2010b). Alternatively, developmental monal profiles and a delayed pattern of social devel- delay may result in adult bonobos failing to show opment in bonobos relative to chimpanzees, which comparable social cognitive flexibility to chim- most likely constitute the proximate underpinnings panzees (e.g. as is the case with spatial memory, of bonobos’ greater social tolerance and prosocial Rosati and Hare, 2012). It is also possible that de- flexibility (Rilling et al., 2012; Stimpson et al., 2015; layed development may result in a longer period Wobber et al., 2010a; Wobber et al., 2010b). Impor- of developmental plasticity and permit bonobos to tantly, although both species live in similar large develop skills that chimpanzees do not. Indeed, hu- multi-male, multi-female, promiscuous, fission– mans have evolved an extended period of juvenil- fusion societies, bonobos are believed to have ex- ity and adolescence that is associated with greater perienced more relaxed feeding competition than cognitive flexibility (Kaplan et al., 2000). Consistent chimpanzees throughout their evolutionary history with this hypothesis, there is evidence that bono- (Wrangham, 1993). Reduced competition may have bos reach certain developmental milestones beyond allowed selection to favour increased social toler- the typical period of chimpanzee development. For ance and ultimately produce the other correlated example, chimpanzees experience changes in TT3 by-products of the self-domestication process. thyroid hormone levels at the end of their somatic From the self-domestication hypothesis, we growth, and bonobos exhibit juvenile levels of these can derive a key prediction about the social cog- hormones ten years longer than chimpanzees do nitive abilities of chimpanzees and bonobos. (Behringer et al., 2014). The self-domestication hypothesis posits hetero- Another alternative is that social cognition may chonic shifts—changes in the timing or pattern of not have been directly shaped by self-domestication; development—as a major proximate mechanism however, traits that were shaped by selection against underlying species differences (Hare et al., 2012). aggression may still influence the ontogeny of social

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cognition. For example, retention of juvenile levels of Bonobos have more human-like 2D:4D ratios social tolerance into adulthood (Wobber et al., 2010b) than chimpanzees, suggesting lower prenatal an- may provide more opportunities for bonobos to learn drogen exposure and less masculinization of the about the behavior and mental states of their conspe- brain during development (McIntyre et al., 2009). If cifics, ultimately resulting in more flexible ToM skills non-human apes adhere to the pattern of individual in bonobos. Research in human children has already differences seen in humans, bonobos should exhibit linked temperament to ToM, showing in particular greater skill in empathizing but less skill in system- that children who are less aggressive, more shy and izing than chimpanzees (MacLean, 2016). Neuro- more observant at age three perform better on false logical evidence further supports this claim: relative belief tasks at age five (Wellman et al., 2011). These to chimpanzees, bonobos have more grey matter findings also align with the empathizing–systemiz- in the right dorsal amygdala and the right ante- ing hypothesis’ prediction that bonobos will exhibit rior insula—areas that function to perceive distress more attuned ToM skills as a result of reduced mas- (Rilling et al., 2012). They also have stronger con- culinization, a trait which most likely arose through nections between the amygdala and the ventral an- self-domestication (see later in this chapter). terior cingulate cortex, a pathway that contributes to aversion to others’ harm, as well as greater serotonergic innervation of the amygdala than chim- The empathizing–systemizing hypothesis panzees (Rilling et al., 2012; Stimpson et al., 2015). A potentially complementary hypothesis—this one Relative to other apes, humans and bonobos also relevant to the proximate origins of chimpanzee have a larger and more diversified posterior orbito- and bonobo species differences—comes from the frontal cortex, which has been implicated in emo- literature on autism spectrum disorders. This hy- tional responsiveness to social stimuli (Semendeferi pothesis, the empathizing–systemizing hypothesis, et al., 1998). Thus, both physiological and neurolog- links degree of masculinization of the brain during ical evidence support the empathizing–systemizing prenatal development to differences in adult ToM hypothesis and suggest that bonobos may be more skills. Variation in masculinization has been docu- sensitive to others’ mental states than chimpanzees. mented between chimpanzees and bonobos, per- Recent human evolution has been characterized haps resulting from self-domestication. According by a reduction in androgen activity, as reflected in to the empathizing–systemizing hypothesis, this the feminization of craniofacial morphology (Cieri variation may lead to differences in ToM abilities et al., 2014). This shift is believed to partially ex- between the two species (Figure 2). plain our unusual levels of within-group social tol- The empathizing–systemizing hypothesis was erance (Cieri et al., 2014). It may therefore be that originally developed to provide an explanation the same forces involved in bonobo evolution have for why people with autism spectrum disorders shaped the cognitive and behavioral phenotype of are characterized by deficits in empathizing and our species. If the predictions of the self-domestica- average or above-average abilities in systemizing tion and empathizing–systemizing hypothesis are (Baron-Cohen, 2009). Empathizing in this context supported in bonobos and chimpanzees, there is refers to the ability to understand others’ mental reason to believe that humans’ unique social cogni- states and to respond appropriately to their emo- tive abilities also evolved, at least in part, through a tions. Systemizing refers to a propensity for creating process of feminization in response to selection for and analysing predictable, rule-governed systems. prosociality and against aggression. Men tend to exhibit higher levels of systemizing and lower levels of empathizing than women, and Theory of mind in bonobos the even more extreme pattern of high systemizing and low empathizing seen in autism spectrum The self-domestication hypothesis predicts de- disorder is thought to result from hyper-masculin- velopmental delays that may impact the emer- ization of the brain during prenatal development gence of bonobos’ ToM abilities. Consistent with (Baron-Cohen, 2009). this prediction, MacLean and Hare (2012) found

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that chimpanzees succeeded in three related associated with greater sensitivity to others’ men- perspective-taking tasks involving reasoning about tal states (e.g. Phillips et al., 1992) and in other what an actor has previously seen whereas bonobos species appears to be a product of domestication succeeded in only one. MacLean and Hare (2012) (Miklosi et al., 2003). suggested that this differential performance might However, in most other ToM skills for which reflect a developmental delay in bonobos relative both species have been tested, their performance to chimpanzees (Wobber et al., 2010b). However, has been comparable (except MacLean and Hare, this potential species difference must be interpreted 2012, reviewed earlier). For example, in basic un- with extreme caution for several reasons. First, the derstanding of attention and agency, it appears that bonobos tested in the task were, on average, three there are no differences between species. Both spe- years younger than the chimpanzees and roughly cies, as well as the other great apes, interpret others’ half were non-adults. Second, in a control pre-test, actions as goal-directed (Buttelmann et al., 2012; bonobos did not respond as strongly as chimpan- Kano and Call, 2014b). They also follow gaze geo- zees to human vocalizations, which were a key com- metrically and check back with the actor when they ponent of test stimuli, making it unclear whether cannot identify the target of her gaze (Brauer et al., the methods were simply more ecologically valid 2005; Povinelli and Eddy, 1996; Tomasello et al., for chimpanzees. Beyond this study, which was not 1999). In addition, all great apes will walk to the directly aimed at exploring developmental differ- front of an agent before attempting to communicate ences in chimpanzee and bonobo social cognition, with her (Liebal et al., 2004), and use more gestural there is no published work that directly addresses communication when the recipient of their gestures this question. is oriented towards them rather than away (Kamin- The principal prediction of the empathizing– ski et al., 2004). systemizing hypothesis is that, due to reduced mas- In object choice tasks where subjects must follow culinization perhaps as a result of self-domestication, a human’s gesture to locate hidden food, bonobos bonobos will show more flexibility than chimpan- have always performed similarly to chimpanzees zees on ToM tasks and less on systemizing tasks. (Herrmann et al., 2010). The one study that tested Herrmann and colleagues (2010) administered a bonobos on their explicit understanding of others’ cognitive test battery of 16 tasks to a large sample beliefs also did not find positive evidence in either of bonobos and chimpanzees. As predicted by the bonobos or chimpanzees (Krachun et al., 2009). empathizing–systemizing hypothesis, the results In addition to controlled cognitive experiments, showed that chimpanzees are more skilled than several studies have investigated in each species be- bonobos on tasks requiring understanding of phys- haviors that may be related to empathy. Though no ical causality and tool use (traits associated with studies have quantitatively compared the two spe- systemizing), whereas bonobos performed more cies in these behaviors, bonobos and chimpanzees skilfully than chimpanzees on tasks related to ToM, both exhibit consolation behavior, affiliative contact especially gaze following (traits linked to empathiz- towards victims of aggression, as well as contagious ing). However, a much wider range of tasks than yawning (Campbell and de Waal, 2011; Demuru and presented in Herrmann and co-workers (2010) is Palagi, 2012; Fraser et al., 2008; Palagi and Norscia, needed to characterize more fully the differences in 2013). These behaviors are generally directed at ToM abilities between chimpanzees and bonobos. bond partners and close kin, and have been argued For example, bonobos consistently appear to to reflect rudimentary forms of empathy. be more sensitive than chimpanzees to certain Taken together, the existing qualitative and quan- types of social information. They gaze follow titative work on bonobo and chimpanzee ToM sug- more reliably and more flexibly than chimpan- gests comparable skills in both species. The major zees (Herrmann et al., 2010), including in response exception is that bonobos have shown greater sen- to allospecific models (Kano and Call, 2014a). sitivity than chimpanzees to eye contact and gaze— They also make more eye contact than chimpan- foundational traits that are used for gathering social zees (Kano et al., 2015), which in humans may be information that informs inferences about others’

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psychological states. Eye contact is also associated Table 6.1 Theory of mind skills in chimpanzees and bonobos. with lower levels of prenatal testosterone in hu- (Capacités de la théorie de l’esprit chez les chimpanzés et les bonobos.) man infants (Lutchmaya et al., 2002). Meanwhile, chimpanzees exhibit more skill in tasks relating Understanding of others’ Chimpanzees Bonobos to causal reasoning or reasoning about unobserv- 1 able properties of the physical world. These data Gaze direction ✓ ✓ provide preliminary support for the empathizing– Attention2 ✓ ✓ systemizing hypothesis that, within the Pan clade, Seeing3 ✓ ? chimpanzees are more the systemizers and bonobos Hearing4 ✓? ? the empathizers. These findings are also consistent Knowledge and Ignorance5 ✓ ✓? with the self-domestication hypothesis. However, False beliefs (Implicit)6 ✓? ✓? developmental comparisons (as well as compari- False beliefs (Explicit)7 X X sons between adults of each species) thus far sug- 8 gest, for the most part, that if self-domestication has Goals ✓ ✓ shaped bonobo ToM abilities, any developmental Intentions9 ✓ ✓? delay that bonobos experience may be overcome Shared goals10 ? ? by adulthood through the developmental plasticity that such a delay affords. Future work will be 1 (Brauer et al., 2005; Povinelli and Eddy, 1996; Tomasello et al., 1999); essential in further testing the predictions of these 2 (Hostetter et al., 2001; Kaminski et al., 2004; Leavens et al., 2004; Liebal et al., 2004); hypotheses. 3 (Hare et al., 2000; Hare et al., 2006; Karg et al., 2015a; Karg et al., 2015b; Melis et al., 2006); 4 (Brauer et al., 2008; Melis et al., 2006); Moving forward 5 (Crockford et al., 2012; Hare et al., 2001; Kaminski et al., 2008; MacLean and Hare, 2012); 6 (Krupenye et al., 2016); ToM abilities are among the defining features of our 7 (Call and Tomasello, 1999; Hare et al., 2001; Kaminski et al., 2008; Krachun species yet there remain many unanswered ques- et al., 2009); tions about their evolutionary origins. Comparative 8 (Buttelmann et al., 2012; Kano and Call, 2014b; Melis and Tomasello, 2013; Myowa-Yamakoshi et al., 2012; Tomasello and Carpenter, 2005; Warneken research involving humans’ two closest relatives, et al., 2007; Yamamoto et al., 2012); chimpanzees and bonobos, provides the most pow- 9 (Call et al., 2004; Call and Tomasello, 1998; Krupenye and Hare, in preparation; Tomasello and Carpenter, 2005); erful tool for understanding the evolution of these 10 (MacLean and Hare, 2013; Melis and Tomasello, 2013; Warneken skills in the lineage leading to humans. While work et al., 2006). in chimpanzees has demonstrated that they possess many, but certainly not all, of the ToM skills that also be responsible for reduced masculinization of are exhibited by humans, many more gaps exist in the brain during prenatal development in bonobos our knowledge of these abilities in bonobos (see relative to chimpanzees. The empathizing–system- Table 6.1). These gaps hinder inferences about the izing hypothesis, in turn, suggests that these dif- cognitive phenotype of the last common ancestor of ferences in masculinization may be responsible for chimpanzees, bonobos and humans as well as the greater flexibility in empathizing (i.e. ToM abilities) selective forces that shaped the cognitive abilities of in bonobos and in systemizing (i.e. physical causal each species. understanding) in chimpanzees. We have outlined two hypotheses—the self- There are several key areas that should be ex- domestication hypothesis and the empathizing– plored in order to test these hypotheses and pro- systemizing hypothesis—that together provide vide the most direct insights into the evolutionary testable predictions that will hopefully inspire history of humans and their closest relatives. First, future comparisons. The self-domestication hy- if the social cognitive abilities of these species have pothesis suggests that selection against aggres- been shaped by a self-domestication process, de- sion and for prosociality may have resulted in layed development relative to chimpanzees may heterochronic changes that impact the emergence impact the ToM skills of bonobos. Therefore, a criti- of ToM skills. These same selective pressures may cal test of this hypothesis requires a comparative

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developmental investigation of chimpanzee and engage in, competition. In contrast, bonobos have bonobo ToM. Second, as a result of reduced mas- been shown to perform a handful of cooperative be- culinization (predicted by the self-domestication haviors more flexibly than chimpanzees, owing to hypothesis), the empathizing–systemizing hypoth- their heightened social tolerance (Hare et al., 2007; esis predicts that bonobos will exhibit greater com- Tan and Hare, 2013). Therefore, it may be in non- petence than chimpanzees in employment of some, competitive contexts that bonobos are most moti- if not all, ToM abilities. Thus, future work must vated to demonstrate their cognitive skill. Future address the existing gaps in our understanding of work should take advantage of such contexts to in- ToM in both species. vestigate social cognition in bonobos. For example, To address these gaps, several concurrent strat- studies of targeted helping and sharing could shed egies are necessary. On the one hand, it will be light on bonobos’ understanding of other’s goals important to replicate with bonobos ToM studies and intentions. Krupenye and colleagues (in prepa- that have been completed with chimpanzees. For ration) have found that bonobos actively transfer example, almost no work has investigated their food, even doing so proactively (without request by perspective-taking skills, including their under- the recipient)—prosocial behaviors not exhibited standing of what others perceive and what others by chimpanzees—although, unlike chimpanzees, know. In other areas, such as understanding of oth- bonobos do not transfer tools or other objects. These ers’ goals and intentions, bonobos have only been findings suggest that while bonobos and chimpan- tested on a minority of paradigms. It will also be zees have a similar understanding of others’ needs, critical to develop new paradigms that maximize motivational differences impact their tendency to ecological validity for bonobos. Previous experi- demonstrate that understanding. ments that have been designed to study social Human infants discriminate between agents cognition in chimpanzees may not hold the same based on their prosocial and antisocial actions ecological validity for bonobos, and poor perfor- and intentions (Hamlin, 2013), and these abilities mance by bonobos in such tasks could reflect spe- may also be particularly pronounced in bonobos. cies differences in experimental motivation more Indeed, Krupenye and Hare (in preparation-a; in than cognitive ability (with the reverse applying to preparation-b) recently found evidence that bo- chimpanzees for more bonobo-centric paradigms). nobos are able to discriminate between unfamil- Thus, a combination of existing paradigms and new iar social partners based on both their actions and approaches adapted for the unique characteristics intentions. Future research should continue to of each species will be essential to fully capture the examine social cognition in cooperative settings, in- nuanced cognitive and motivational differences cluding perspective-taking abilities, cognitive and between them. affective empathy and shared intentionality. Since motivation and temperament interact Finally, many areas of ToM are understudied in with ToM abilities, many of the most successful general. For example, little is known about apes’ studies of chimpanzee ToM have capitalized on understanding of others’ emotions, and with their competitive settings that maximize chimpanzees’ heightened sensitivity to faces and gaze bonobos may motivation to demonstrate their cognitive skill be likely to excel in this area. Moreover, to-date no (Hare et al., 2000; Hare et al., 2001). However, com- study has provided positive evidence of explicit false petitive contexts may not motivate bonobos in the belief understanding in nonhumans, and researchers same way that they do chimpanzees. Research has are just beginning to investigate implicit understand- shown that whereas male chimpanzees experience ing of false belief. This new direction relies on the a spike in testosterone preceding competition over kinds of spontaneous anticipatory looking or viola- food, male bonobos experience a spike in cortisol tion of expectation measures that have proven fruit- (Wobber et al., 2010a). These differential responses ful in human infants (Baillargeon et al., 2010). For indicate that while chimpanzees are emboldened in example, using an anticipatory looking paradigm, anticipation of conflict, bonobos become stressed Krupenye, Kano and colleagues (2016) recently dis- and are probably motivated to avoid, rather than covered that—just like human infants—bonobos,

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chimpanzees and orangutans successfully predicted Call, J., Hare, B., Carpenter, M., and Tomasello, M. (2004). that an agent would search for a hidden object where ‘Unwilling’ versus ‘unable’: chimpanzees’ understand- he last saw it, even if the object had been moved ing of human intentional action. Developmental Science, while the agent wasn’t looking. While further work 7, 488–98. Call, J. and Tomasello, M. (1998). Distinguishing inten- is necessary to confirm the mechanism underlying tional from accidental actions in orangutans (Pongo these results and identify its limits, Krupenye, Kano pygmaeus), chimpanzees (Pan troglodytes), and human and colleagues (2016) data provide the first evidence children (Homo sapiens). Journal of Comparative Psychol- that great apes may have at least an implicit under- ogy, 112, 192–206. standing of others’ false beliefs. Call, J. and Tomasello, M. (1999). A nonverbal false belief Future research on social cognition in bonobos task: The performance of children and great apes. Child and chimpanzees promises to yield exciting de- Development, 70, 381–95. velopments. Examining these traits will clarify Campbell, M.W. and De Waal, F.B. (2011). Ingroup–out- group bias in contagious yawning by chimpanzees sup- whether social cognition is largely similar between ports link to empathy. PLoS One, 6, e18283. the two species—that is, whether both species have Cieri, R.L., Churchill, S.E., Franciscus, R.G., Tan, J., and a Pan-typical ToM. Alternatively, future work may Hare, B. (2014). Craniofacial feminization, social toler- demonstrate that the species’ independent evolu- ance, and the origins of behavioral modernity. Current tionary histories have produced key differences in Anthropology, 55, 419–43. their social cognitive abilities. In many cases, this Crockford, C., Wittig, R.M., Mundry, R., and Zuberbuh- work will permit more accurate reconstructions of ler, K. (2012). Wild chimpanzees inform ignorant group the cognitive phenotype of the last common an- members of danger. Current Biology, 22, 142–6. cestor by clarifying which social cognitive abilities Demuru, E. and Palagi, E. (2012). In bonobos yawn conta- gion is higher among kin and friends. PLoS One, 7, e49613. are shared by bonobos, chimpanzees and humans. Fraser, O.N., Stahl, D., and Aureli, F. (2008). Stress reduc- Additionally, by identifying cognitive differences tion through consolation in chimpanzees. Proceedings of between the three species, we will gain critical in- the National Academy of Sciences, 105, 8557–62. sights into the selective forces that have shaped cog- Hamlin, J.K. (2013). Failed attempts to help and harm: nitive evolution not only in our closest relatives but intention versus outcome in preverbal infants’ social in humans as well. evaluations. Cognition, 128, 451–74. Hare, B. (2001). Can competitive paradigms increase the validity of experiments on primate social cognition? References Animal Cognition, 4, 269–80. Hare, B. (2011). From hominoid to hominid mind: what Baillargeon, R., Scott, R.M., and He, Z. (2010). False-belief changed and why? Annual Review of Anthropology, 40, understanding in infants. Trends in Cognitive Sciences, 14, 293–309. 110–18. Hare, B., Call, J., Agnetta, B., and Tomasello, M. (2000). Baron-Cohen, S. (2009. Autism: the empathizing–system- Chimpanzees know what conspecifics do and do not izing (E–S) theory. Annals of the New York Academy of Sci- see. Animal Behaviour, 59, 771–85. ence, 1156, 68–80. Hare, B., Call, J., and Tomasello, M. (2001). Do chimpan- Behringer, V., Deschner, T., Murtagh, R., Stevens, J.M., and zees know what conspecifics know? Animal Behaviour, Hohmann, G. (2014). Age-related changes in thyroid 61, 139–51. hormone levels of bonobos and chimpanzees indicate Hare, B., Call, J., and Tomasello, M. (2006). Chimpanzees heterochrony in development. Journal of Human Evolu- deceive a human competitor by hiding. Cognition, 101, tion, 66, 83–8. 495–514. Brauer, J., Call, J., and Tomasello, M. (2005). All great ape Hare, B., Melis, A.P., Woods, V., Hastings, S., and Wrang- species follow gaze to distant locations and around bar- ham, R. (2007). Tolerance allows bonobos to outperform riers. Journal of Comparative Psychology, 119, 145–54. chimpanzees on a cooperative task. Current Biology, 17, Brauer, J., Call, J., and Tomasello, M. (2008). Chimpanzees 619–23. do not take into account what others can hear in a com- Hare, B., Wobber, V., and Wrangham, R. (2012). The self- petitive situation. Animal Cognition, 11, 175–8. domestication hypothesis: evolution of bonobo psy- Buttelmann, D., Schütte, S., Carpenter, M., Call, J., and To- chology is due to selection against aggression. Animal masello, M. (2012). Great apes infer others’ goals based Behaviour, 83, 573–85. on context. Animal Cognition, 15, 1037–53.

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