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Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
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Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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21 novembre 2017
Scientific Reports
2017;7: n°14733
Bonobos respond prosocially
toward members of other groups
 
Jingzhi Tan, Dan Ariely & Brian Hare

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Abstract
Modern humans live in an "exploded" network with unusually large circles of trust that form due to prosociality toward unfamiliar people (i.e. xenophilia). In a set of experiments we demonstrate that semi-free ranging bonobos (Pan paniscus) &endash; both juveniles and young adults &endash; also show spontaneous responses consistent with xenophilia. Bonobos voluntarily aided an unfamiliar, non-group member in obtaining food even when he/she did not make overt requests for help. Bonobos also showed evidence for involuntary, contagious yawning in response to videos of yawning conspecifics who were complete strangers. These experiments reveal that xenophilia in bonobos can be unselfish, proactive and automatic. They support the first impression hypothesis that suggests xenophilia can evolve through individual selection in social species whenever the benefits of building new bonds outweigh the costs. Xenophilia likely evolved in bonobos as the risk of intergroup aggression dissipated and the benefits of bonding between immigrating members increased. Our findings also mean the human potential for xenophilia is either evolutionarily shared or convergent with bonobos and not unique to our species as previously proposed.
 
Introduction
 
Trust is fundamental to social life. One hallmark of human societies is that they have an unusually wide circle of trust. This includes unfamiliar individuals that can be anything from distant acquaintances to anonymous strangers. Conflicts occur between rival groups, but modern humans manage to live in a global social network connected by trusting relationships between unrelated strangers. Contemporary hunter-gatherers commonly engage in cooperative interactions among unfamiliar individuals, so did early Homo sapiens (e.g. flexible dispersal, high social fluidity, intergroup alliance and long-distance trade). This extensive circle of trust provides enormous benefits by creating an interconnected and ever-growing market for information, goods and support. Such interconnectedness has been suggested to allow for cumulative culture and large-scale cooperation, two cornerstones of humanity.
 
The human potential for xenophilia or prosociality toward unfamiliar individuals seems critical then to our species success in encouraging cooperation and cultural exchange. In absence of past experience with strangers, humans rely on signals of positivity in establishing trust. When encountering a stranger of unknown group membership humans are capable of making these positive signals with a prosocial first move. This is in contrast to a negative or xenophobic response, and it does not require a prosocial preference for the unfamiliar over the familiar, although such a preference can be considered the extreme expression of xenophilia. A pattern of human xenophilia is observed across cultures and early in development. It can occur even when the xenophilic actors obtain no selfish benefits, have limited cognitive control and receive no signals for help from the recipient. This profile suggests that human xenophilia is in part driven by unselfish motivations and automatic processes. However, it remains unclear to what extent this kind of xenophilia evolved once our lineage split with other apes.
 
One hypothesis proposes that human xenophilia was derived in our lineage, which is supported by the larger pattern of xenophobia in most primates &endash; including chimpanzees. It has been suggested that human xenophilia evolved from the conserved fear of strangers seen across primates as a result of unique human bonding mechanisms such as intermarriage and cultural institutions. Others suggest human xenophilia evolved due to ultra-strong prosocial motivation produced by group selection or cooperative breeding.
 
The first impression hypothesis suggests that xenophilia evolves in response to the benefits of new social partners. This hypothesis predicts that prosocial responses to strangers can evolve in any social species where the selfish benefits of bonding with new partners outweigh the costs. For example, xenophilia can be favored when there is limited risk of xenophobic aggression. In this case positive encounters with strangers can develop into repeated interactions. Strangers will become attractive social partners since social networks can be expanded through the formation of low risk and low cost "weak ties". A core prediction of the first impression hypothesis is that social preferences for positive interactions with non-group members (e.g. xenophilia) and cognition should evolve to support the network expansion of individuals when it enhances inclusive fitness49.
 
Bonobos (Pan paniscus) provide a powerful test of this prediction of the first impression hypothesis. Bonobos have been proposed as a product of selection against aggression or "self-domestication" that was driven by reduced feeding competition. Bonobos not only possess a syndrome of morphological and physiological traits associated with domestication, but also show less severe forms of aggression than chimpanzees. Territorial patrols, infanticide, and lethal intergroup aggression have never been observed in bonobos. Tension can rise during intergroup encounters, but escalation into physical aggression with injuries is uncommon. Instead, affiliative behaviors such as grooming, traveling together and socio-sexual behaviors have often been seen during interactions between immigrants or neighboring groups.
 
Unlike chimpanzees in captivity, there are no reports of bonobos killing adults or infants as a result of transfers between groups (although male immigrants without mothers can become targets of female aggression). Most importantly, while both bonobos and chimpanzees are patrilocal, only bonobo immigrants are attractive social partners for resident males and females. Unrelated, immigrating members in bonobo groups even form alliances, gain priority of access to food and achieve high social status
 
Experiments have demonstrated that physical interactions with unfamiliar conspecifics can be rewarding for bonobos. Instead of monopolizing food in their possession, bonobos unlocked a one-way door in order to physically interact and co-feed for the first time with an unfamiliar neighbor (but not with a familiar recipient). They often opened a second door for another non-group member even if it meant being outnumbered by non-group members &endash; something chimpanzees actively avoid68. In another experimental context bonobos also released an unfamiliar conspecific into a room with food that they themselves could not access. This meant bonobos helped non-group members even when they received no social reward.
 
However, it is still unclear how similar the xenophilic tendencies of bonobos are to that seen in humans - which can be unselfish, proactive and automatic toward complete strangers. While proactive or unsolicited prosociality toward group members has been experimentally demonstrated in some contexts in chimpanzees and other primates, proactive food provisioning of unfamiliar individuals from other groups remains little studied. Previous tests with bonobos have demonstrated their tendency to share with unfamiliar recipients from a different social group when using explicit measures of prosociality. This work even suggests the potential for proactive sharing in bonobos since help was not contingent on gestures made by recipients. However, we remain without a strong test of (1) proactive sharing, (2) with completely novel conspecifics and (3) involuntary or implicit measures of social preferences commonly used in human research. We conducted a series of experiments to test the first impression hypothesis that meet these methodological challenges.
 
We first examined whether bonobos voluntarily provisioned an unfamiliar conspecific from a neighboring group who was unable to use overt signals to indicate their desire for help (i.e. since overt requests for help were prevented, aid was considered proactive). We then tested whether bonobos had an involuntary contagious yawning response to complete strangers. Contagious yawning has been used by many as an implicit measure of social preference in various primates and non-primate species since it is under involuntary control, although see. Regardless of its exact proximate mechanism, contagious yawning has been positively associated with social rapport in a variety of animals including humans and bonobos. This includes work showing that yawn contagion in xenophobic chimpanzees is made in response to in-group but not out-group conspecifics. These findings make contagious yawning a useful implicit measure of positive social preference. We therefore tested the first impression hypothesis by examining how bonobos help and contagiously yawn in response to unfamiliar conspecifics. The first impression hypothesis predicts that bonobos will proactively provision food to unfamiliar, non-group members and will contagiously yawn in response to complete strangers.
 
Discussion
 
In strong support of the first impression hypothesis bonobos proactively provisioned out-of-reach food to an unfamiliar non-group member and showed involuntary, contagious responses to the yawns of complete strangers. The aid that bonobos explicitly provided the unfamiliar recipient in obtaining food is consistent with common definitions of proactive prosociality, while contagious yawning suggests their xenophilia is not completely under voluntary control and is present even when there is zero familiarity. This bonobo pattern of xenophilia resembles contagious yawning and unconscious mimicry seen in humans more than chimpanzees, as well as the heuristic-like response that drives human sharing with strangers in controlled experiments. Like humans, bonobos proactively help unfamiliar conspecifics and their positive response is at least in part automatic.
 
Xenophilia in the current experiments was directed to conspecifics with various levels of familiarity, from neighbors with whom the subjects had never shared an enclosure to completely novel individuals. The xenophilia observed in this sanctuary sample is consistent with reports from a wide range of field sites and captive facilities showing that bonobos display affiliative behaviors toward acquaintances and new immigrants. Our findings together with these observations do not support the alternative that our subjects have become xenophilic due to repeated testing, due to their rearing history, or due to the sanctuary environment that allowed visual and vocal contacts across group barriers. Given that sanctuary bonobos are relatively risk-averse and indifferent to novel stimuli in non-social contexts, a general attraction to novelty clearly cannot explain our findings. Finally, the social context at the sanctuary is highly similar to the experience of most wild primates that often see or hear neighboring groups but rarely physically interact with them due to the potential cost of aggression. Despite this, and unlike chimpanzees, bonobos in the wild and in our experiments appear to have evolved a xenophilic preference for this same type of stranger.
 
It is difficult to explain the prosociality observed here as a result of harassment, reciprocity or a lack of inhibition since subjects could not physically interact with recipients, they had never been in the same group and pretests demonstrated subjects understood the experimental set-up (i.e. they passed self-regard pretests). The physical setup and presence of a conspecific in the controls rule out mechanisms such as local enhancement or social facilitation. We are unaware of any evidence that bonobos can solicit the novel form of help tested here through non-gestural cues (e.g. subtle vocalizations, facial expressions or even situational cues1). This might be an interesting topic for future research, given bonobos are relatively sensitive to human social cues. Moreover, based on our control the contagious yawning results cannot be attributed to an inability of subjects to discriminate strangers from groupmates in the videos.
 
According to the first impression hypothesis, xenophilia evolves when the benefits of bonding with new partners outweigh the costs. In the case of bonobos, strong female alliances and sexual selection against male aggression likely removed the threat of lethal intergroup aggression that drives chimpanzee xenophobia44,116. This might have turned a costly interaction into a highly beneficial one. Xenophilia was increasingly favored as strangers became more likely to turn into valuable long-term social partners. It is important for future studies to test other predictions of the first impression hypothesis. Future research will need to examine the role of age and sex as it relates to the strength of xenophilia in bonobos. For example, our subjects were relatively young (4&endash;18 years old), and within the age range (6&endash;14 years old) that bonobos typically leave their natal groups in the wild. Bonobos may show a different preference once they are past this age. Or the preferences of older adults may vary depending on the sex of the stranger. The first impression hypothesis predicts that, unfamiliar adult females will be preferred over adult males and that unfamiliar adult males may illicit xenophobic responses in some contexts (i.e. interactions between two strange adult males). It will be exciting to take this next step and understand which kind of strangers bonobos respond with xenophilia.
 
Another powerful test of this hypothesis will be quantitative comparisons between spontaneous responses toward strangers in bonobos and chimpanzees1. Despite a growing literature documenting bonobo xenophilia and chimpanzee xenophobia, most studies, including the current one, have focused on one species. This creates methodological variations across paradigms that prevent a more precise comparison between the two species. Although in one current experiment (experiment 2) we made the design and the analysis as comparable to the chimpanzee study by Campbell et al. as possible, our comparison is still qualitative. Methods that allow for direct quantitative comparisons of both species are still needed. This comparison would be particularly powerful if it used eye tracking techniques to examine attention as it relates to yawning rates. It might be important to correct for higher levels of attention given to the yawns of strangers than those of groupmates.
 
While there is consensus that contagious yawning is involuntary, the nature of the mechanism driving this automatic response is still unclear. Future research will be needed to understand if bonobo contagious yawning is an expression of some basic form of empathy, a 'social heuristic', or an oxytocin-vasopressin mediated response. Regardless of the exact mechanism, our results suggest that bonobos have an involuntary positive response to complete strangers. As described for humans, bonobos seem predisposed to making a good "first impression" when interacting with a new social partner. For both humans and bonobos, many strong bonds likely start from positive encounters between unfamiliar adults catalyzed by xenophilia. However, our results also suggest how xenophilia is constrained in both species in different ways. For example, the strong xenophobic reaction that humans display toward strangers from different cultural mediated outgroups severely limits human intergroup prosociality. Likewise, while bonobos potentially even prefer an unfamiliar conspecific from another group over their own groupmate, they are probably much less flexible in terms of the contexts and the consistency with which they will provide aid (e.g. food-provisioning to strangers did not occur when the cost became considerably high).
 
The most exciting puzzle for the future will be determining why humans evolved the potential for trusting relationships with strangers in a wider variety of contexts &endash; allowing rapid diffusion of information and reciprocal between-group cooperation. This will require uncovering whether some forms of xenophilia are shared or convergent between humans and bonobos. Regardless of the answer, bonobo networking has much to teach us about the origins of the human network we all rely upon.