Prosociality and inequity aversion as proximate mechanisms of cooperation in bonobos

Cooperation is a key component of social life. Although it is common among the animal kingdom, cooperative interactions seem an evolutionary puzzle as they involve behaviours that benefit others, but that also seem to conflict with the theory of natural selection, which emphasizes competition and predicts that individuals should act in their own interest. Studies of cooperation in animals, try to understand in which ways human cooperation is unique, how cooperation in humans has evolved, what factors explain between-individual variation in cooperative behaviour and what selective pressures acted upon the evolution of cooperation in animals. Because cooperative behaviours involve an immediate cost to the actor, natural selection must have produced mechanisms to regulate cooperation to overcome any adverse effects of these costs. The two main proximate mechanisms that regulate cooperation are prosociality and inequity aversion, which are considered to be the promotor and stabiliser of cooperation, respectively. In this thesis, I study a social group of bonobos (Pan paniscus) in Zoo Planckendael, using a combination of behavioural and physiological measures in different experimental paradigms to explain the variability in these proximate mechanisms of cooperation in bonobos. Bonobos have been suggested to be an ideal species to study prosociality and IA. First, because they are one of our closest living relatives and studying prosociality and IA in bonobos would increase our knowledge on how unique the level of prosociality and IA in humans is. Second, because bonobos have been described as ‘hippies of the primate world’, who are highly tolerant, prosocial, empathic and cooperative, but prosociality and inequity aversion as drivers of cooperation have not been extensively studied in this species. In order to obtain results that would allow for intra- and inter-species comparisons, I implemented three methodological studies before focusing on prosociality and inequity aversion. First, to decide which food items to use in the experimental paradigms of my PhD, I determined the bonobos’ food preference on ten novel food items and all food items of their weekly diet. Using paired-choice tests, I demonstrated that bonobos preferred fruits over vegetables. I also linked the nutritional content of each food item with the bonobos’ preference which led to the conclusion that bonobos prefer foods that are high in total energy and carbohydrate content but low in water and micronutrient content. Although my study only included commercially available food items, which complicates comparisons with food preference in the wild, the results do inform us about which food items to select for the experimental paradigms: grapes as a highly preferred food item in the prosociality experiments (chapter 6) and the inequity aversion token exchange task (chapter 7) and parsnip as less preferred food item in the inequity aversion exchange task (chapter 7). To be able to use salivary cortisol as a physiological measure of arousal in the experimental paradigms of my PhD, a profound validation of the time-lag between the stimulus and the increase and peak in salivary cortisol was needed. Therefore, using a biological validation, I investigated the timelag between an acute stressor and the urinary and salivary cortisol response in bonobos. Surprisingly, I found that the time-lag between the stressor and the maximal cortisol level was similar in urine and saliva. I did show a faster and steeper increase in salivary cortisol than urinary cortisol after the stressor. In addition, I also demonstrated inter-individual variation in the baseline and stress levels of cortisol. Altogether, these results highlight the importance of appropriate validation studies to confirm the relevant sampling window and to be aware of inter-individual differences in the physiological response to stimuli. Based on these results, I concluded that saliva should be samples 15 to 40 minutes after the stressful event to detect a change in the salivary cortisol levels. In the third methodological chapter, I demonstrated the repeatability of the composite measure of relationship quality and investigated whether bonobos, like many species, prefer to bond with similar others. The preference for similarity has been suggested to be an important aspect of cooperation, because more similar individuals are expected to form strong and reliable social interactions in which emotionally mediated reciprocity may lead to high levels of successful cooperation. Besides relatedness and the sex combination of the dyad, I showed that bonobos that are more similar in the personality trait Sociability form relationships of higher qualities. Dyads with high quality relationships were predicted to show higher levels of prosociality and lower levels of inequity aversion. To study prosociality, I first used a novel provisioning experiment that had previously been used to measure prosociality in chimpanzees. In this experiment, bonobos could push a button to provide juice from a distant fountain to benefit group members (chapter 5). All three experiments were conducted in a group setting but differed in the payoff distribution between the actor and receiver. Second, to allow for inter-species comparisons, I also implemented two validated food provisioning prosociality paradigms, the prosocial choice task (PCT) and the group service paradigm (GSP) (chapter 6). To study inequity aversion in bonobos, I used the standard token exchange task. To complement the standard behavioural measures with the emotional component of inequity aversion, I also investigated a behavioural, rough self-scratching, and a physiological measure, salivary cortisol, of arousal. Interestingly, the results of all prosociality experiments showed that the Zoo Planckendael bonobos mainly behaved out of self-interest: in more than half of the juice-provisioning acts, the subject also obtained juice; bonobos did not prefer the prosocial above the selfish option in the PCT and adult bonobos did not provision group members in the GSP. These findings showed that bonobos, like chimpanzees, behaved indifferently to the welfare of others, which contrasts with the popular image of the prosocial and food sharing bonobo, who is often portrayed as a “hippie of the primate world”. I concluded that this popular image is mainly the result of an age bias in previous experimental studies that looked for evidence of prosociality in bonobos in order to confirm the predictions of the self-domestication hypothesis. I also demonstrated that bonobos reacted to receiving less than a partner by refusing trials and moving away from the experimenter while they never refused trials when receiving more than a partner. The level of inequity aversion was influenced by the relationship quality between individuals. I showed that stronger bonded individuals were more tolerant towards inequity. Further, subjects were more aroused when receiving a better reward than a partner, suggesting that bonobos do notice when being favoured but do not respond to it behaviourally. Altogether, the results of this thesis highlight the importance of validated methodologies and provide supporting evidence for the nuanced view of the prosocial, food-sharing and tolerant hippie ape. I demonstrated that adult bonobos do not behave prosocially in food-related paradigms, which can be explained by the competitive nature around the highly preferred food items, and which corresponds to the food-related behaviour of bonobos in the wild. I also showed that in bonobos, like chimpanzees, the tolerance to inequity is limited to a certain level and linked to specific partners. Although the results contribute to the existing knowledge on the proximate mechanisms of bonobos, I also provide a critical view on the artificial contexts of the implemented experimental paradigms. To fully understand how the proximate mechanisms, prosociality and inequity aversion, interact to result in successful cooperative relationships, more research on diverse social bonobo groups is crucial.

Jaar van publicatie:2022

Trefwoorden:Doctoral thesis

Toegankelijkheid:Open