Prosocial primates: selfish and unselfish motivations

Abstract

Non-human primates are marked by well-developed prosocial and cooperative tendencies as reflected in the way they support each other in fights, hunt together, share food and console victims of aggression. The proximate motivation behind such behaviour is not to be confused with the ultimate reasons for its evolution. Even if a behaviour is ultimately self-serving, the motivation behind it may be genuinely unselfish. A sharp distinction needs to be drawn, therefore, between (i) altruistic and cooperative behaviour with knowable benefits to the actor, which may lead actors aware of these benefits to seek them by acting cooperatively or altruistically and (ii) altruistic behaviour that offers the actor no knowable rewards. The latter is the case if return benefits occur too unpredictably, too distantly in time or are of an indirect nature, such as increased inclusive fitness. The second category of behaviour can be explained only by assuming an altruistic impulse, which-as in humans-may be born from empathy with the recipient's need, pain or distress. Empathy, a proximate mechanism for prosocial behaviour that makes one individual share another's emotional state, is biased the way one would predict from evolutionary theories of cooperation (i.e. by kinship, social closeness and reciprocation). There is increasing evidence in non-human primates (and other mammals) for this proximate mechanism as well as for the unselfish, spontaneous nature of the resulting prosocial tendencies. This paper further reviews observational and experimental evidence for the reciprocity mechanisms that underlie cooperation among non-relatives, for inequity aversion as a constraint on cooperation and on the way defection is dealt with.

Figure 1.

In the cooperative pulling task two capuchin monkeys are situated in adjacent sections of a test chamber, separated by mesh. The apparatus consists of a counter-weighted tray with two pull bars, with each monkey having access to one bar. If both cups are filled, success requires mutualistic cooperation, whereas if only one cup is filled (as shown here) cooperation is sustained by sharing through the mesh by the advantaged individual, who pays for the other's labour (de Waal & Berger 2000). Drawing by Sarah Brosnan.

Figure 2.

Interactions over sharable food are generally tolerant and peaceful, such as here in a cluster of chimpanzees at the Yerkes Field Station. The female in the top-right corner is the possessor of branches with leaves. The female in the lower left corner is tentatively reaching out for the first time. Whether or not she will be able to feed will depend on the possessor's reaction. Photograph by Frans de Waal.

Figure 3.

Consolation behaviour is common in humans and apes, but largely absent in monkeys. A juvenile chimpanzee puts an arm around a screaming adult male, who has been defeated in a fight. Photograph by Frans de Waal.

Figure 4.

One capuchin monkey reaches through an armhole to choose between differently marked pieces of pipe while her partner looks on. The pipe pieces can be exchanged for food. One token feeds both monkeys; the other feeds only the chooser. Capuchins typically prefer the ‘prosocial’ token (de Waal et al. 2008). Drawing from a video still by Frans de Waal.

Figure 5.

Cooperative and prosocial behaviour is enhanced by familiarity and bonding between parties both via the empathy mechanism, thought to regulate the altruistic impulse and by increased social tolerance, which ensures rewards for the subordinate party. Familiarity and bonding also reduce sensitivity to inequity, while sensitivity undermines cooperative and prosocial behaviour if certain individuals gain conspicuously more than others. Finally, whenever cooperation produces knowable return benefits for the actor, there is the potential of learned reciprocity in which individuals cooperate in order to secure future return favours.