The Evolution of a Cooperative Social Mind
Dorothy L Cheney1 and Robert M. Seyfarth2
1. Department of Biology, University of Pennsylvania, Philadelphia, PA 19104
2. Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104
email: cheney@sas.upenn.edu
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Text: 12,273
Complete MS: 16,814
Oxford Handbook of Comparative Evolutionary Psychology
edited by J. Vonk & T. Shackelford
Keywords: cooperation, contingent cooperation, reproductive success, social relationships, social
cognition
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Abstract
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It has long been hypothesized that the demands of establishing and maintaining social
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relationships in complex societies place strong selective pressures on cognition and intelligence.
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What has been less clear until recently is whether these relationships, and the skills they require,
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confer any reproductive benefits, and whether such benefits vary across individuals. During the
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last few years, much progress has been made in resolving some of these questions. There is now
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evidence from a variety of species that animals are motivated to establish close, long-term bonds
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with specific partners, and that these bonds enhance offspring survival and longevity. The
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cognitive and emotional mechanisms underlying such cooperation, however, are still not
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understood. It remains unclear, for example, whether animals keep track of favors given and
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received, and whether they rely on memory of past cooperative acts when anticipating future
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ones. Although most investigations with captive primates have indicated that cooperation is
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seldom contingency-based, several experiments conducted under more natural conditions suggest
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that animals do take into account recent interactions when supporting others. Moreover, while
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interactions within dyads are often unbalanced over short periods of time, pairs with strong
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bonds have strongly reciprocal interactions over extended time periods. These results suggest
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that the apparent rarity of contingent cooperation in animals may not stem from cognitive
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constraints. Instead, animals may tolerate short-term inequities in favors given and received
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because most cooperation occurs among long-term reciprocating partners.
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h. 1 Introduction
Many species of animals, including in particular many non-human primates, live in large
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social groups composed of both kin and nonkin, with whom they both cooperate and compete. It
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has long been hypothesized (e.g. Jolly 1966; Humphrey 1976; reviewed by Cheney & Seyfarth
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2007) that the demands of establishing and maintaining social relationships in these complex
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societies should place strong selective pressures on cognition and intelligence. What has been
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less clear until recently is whether these relationships, and the skills they require, confer any
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reproductive benefits, and whether such benefits vary across individuals. Indeed, doubts persist
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about whether non-human primates even have the cognitive capacity or motivation to maintain
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long-term relationships.
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During the last few years, much progress has been made in resolving some of these
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questions, although many remain unanswered. In particular, the cognitive and emotional
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mechanisms underlying cooperation are still not understood. It remains unclear, for example,
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whether animals keep track of favors given and received, and whether they rely on memory of
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past cooperative acts when anticipating future ones. Some problems are methodological, arising
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from the difficulties of testing cooperation experimentally under natural conditions. Others stem
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from the different results obtained from observations of wild animals as opposed to those living
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in captivity (see also Boesch, this volume).
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In this chapter, I first briefly summarize recent research on non-human primates’
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knowledge of other individuals’ social relationships, intentions, and motivations. I then describe
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several studies suggesting that the ability to maintain long-term social relationships confers
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significant reproductive benefits. Finally, I discuss some of the many outstanding questions
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regarding the function of cooperation in non-human primates and the cognitive mechanisms that
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may underlie them. I restrict my discussion to species that exhibit relatively low reproductive
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skew, including in particular Old World monkeys and apes. Although many callitrichid species
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exhibit high levels of cooperation, this cooperation is largely obligate and functions primarily to
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aid the reproduction of the breeding pair. My focus here instead is on species where individuals
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vary in the extent of their cooperation and the strength of their social bonds, with the aim of
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examining whether such variation is correlated with some measure of reproductive success.
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h1. The recognition of other individuals’ social relationships
Over the past 30 years considerable progress has been made in the study of social cognition
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in primates and, to a lesser extent, non-primates. A variety of observational and experimental
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studies, conducted primarily on Old World monkeys, have provided evidence that animals
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recognize other individuals’ social relationships and dominance ranks, and that they use this
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knowledge, for example, when reconciling with opponents and their families and when soliciting
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alliance partners.
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h2. The recognition of other individuals’ social relationships
In some species, natural patterns of aggression and reconciliation suggest that monkeys
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have some knowledge of the close relations that exist among matrilineal kin (i.e. close
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associates). For example, an individual who has just been involved in an aggressive interaction
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with another will often redirect aggression by attacking a third, previously uninvolved individual
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(rhesus macaques, Macaca mulatta: Judge 1982, 1991; Japanese macaques, M. fuscata: Aureli et
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al. 1992; vervet monkeys, Chlorocebus aethiops: Cheney and Seyfarth 1986, 1989). Similarly,
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Perry et al. (2004) found that capuchin monkeys (Cebus capuchinus) preferentially solicited
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allies who both out-ranked their opponents and had a social relationship with them that was
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closer than their relationship with the opponent.
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Field playback experiments provide additional evidence that monkeys recognize other
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animals’ kin relations. In one experiment conducted on wild chacma baboons (Papio hamadryus
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ursinus), two unrelated females heard a call sequence that mimicked a fight between two other
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individuals. When the apparent combatants were unrelated to the subjects, they showed little or
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no reaction. However, when each of the two opponents was closely related to the two subjects,
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subjects were significantly likely to look at each other. Furthermore, the dominant subject was
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more likely to seek out the subordinate subject and supplant her in the half hour that followed
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these trials than in the half hour that followed trials that had not involved the two subjects’
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relatives. In other words, the females behaved as if they recognized that a conflict between their
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families had occurred and had temporarily disrupted their relationship (Cheney and Seyfarth
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1999).
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Many primates reconcile with an opponent by touching, hugging, or behaving in a friendly
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way towards the opponent after aggression (Cords 1992; de Waal 1996). In baboons,
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reconciliation often takes the form of a grunt given by the aggressor to her victim (Cheney et al.
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1995b; Silk et al. 1996; Cheney & Seyfarth 1997). The grunts of a close relative of the aggressor
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can also function as a proxy to reconcile opponents. Playback experiments have shown that
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victims of aggression are more likely to tolerate their opponent’s proximity in the hour after the
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dispute if they have heard the grunt of their opponent’s relative than if they have heard the grunt
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of a more dominant individual belonging to a different matriline (Wittig et al. 2007a). Such kin-
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mediated reconciliation can succeed only if the victim recognizes the relationships that exist
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among other group members (see also Das 2000; Judge and Mullen 2005). Conversely, if the
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victim hears the threat-grunt of her opponent’s relative shortly after aggression, she is more
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likely to avoid her opponent and other members of her opponent’s matriline (Cheney and
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Seyfarth 2007; Wittig et al. 2007b).
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The experiments on baboons’ responses to kin-mediated reconciliation and vocal
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alliances support the view that baboons recognize other females’ matrilineal kinship relations.
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This is not, however, to say that baboons treat all the members of a matriline as equivalent.
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Although they recognize that close kin can serve as proxies for each other, they nonetheless
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distinguish among the different members of a matriline. Hearing a ‘reconciliatory’ grunt from an
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opponent’s relative changes females’ disposition toward the opponent and that relative, but less
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so toward other members of the opponent’s matriline (Cheney and Seyfarth 2007; see Rendall et
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al. 1996 for experiments demonstrating the recognition of individuals and of the close relations
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among matrilineal kin in rhesus macaques).
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Similarly, among chimpanzees (Pan troglodytes) uninvolved ‘bystanders’ will sometimes
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direct friendly behavior toward the victim of an aggressive dispute. In one study, the probability
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that a bystander would engage in such behavior depended primarily on the strength of the bond
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between the bystander and the victim: the stronger their bond, the more likely that such
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‘consolation’ would occur (Kutsukake & Castles 2004; see also de Waal & Aureli 1996). In
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another study, however, the bystander was most likely to direct friendly behavior toward the
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victim if the bystander had a close relationship with the aggressor (Wittig 2010). This
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‘consolation’ gesture increased the likelihood that the aggressor and victim would tolerate each
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other’s proximity in the near future. This effect disappeared if the relationship between the
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bystander and the aggressor was relatively weak. Here again, victims acted as if they recognized
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the close bond (or lack of it) between the bystander and the aggressor. As a result, they treated
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the bystander’s friendly behavior as a proxy for reconciliation only if the bystander was a close
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associate of the aggressor.
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The ability to recognize the social relationships that exist among others appears to have
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been favored by natural selection because it allows an individual to predict, for example, who is
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likely to support an opponent in an aggressive alliance. This skill is essential in any species
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where triadic interactions are common (Harcourt 1988). Recognition of other animals’ close
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associates may also help individuals to form and maintain social relationships. While the
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evolutionary benefits of this kind of social knowledge seem clear, however, the underlying
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mechanisms are less well understood. Considered in isolation, the recognition of other animals’
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close kin relations could be accomplished through simple associative mechanisms. The
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recognition of matrilineal kin, however, does not occur in isolation: matrilineal kin relations are
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embedded in a network of short- and long-term bonds that vary among individuals according to
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age, rank, reproductive state, and many other variables. Whether social knowledge under natural
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conditions, in all its simultaneous manifestations, can be explained by simple theories of
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association remains an open issue.
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h2. The recognition of other individuals’ dominance ranks
Like the bonds among matrilineal kin, linear, transitive dominance relations are a
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pervasive feature of behavior in many primate groups. A linear rank hierarchy might emerge
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because individuals simply take note of who is dominant and who is subordinate to themselves –
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an egocentric view of the world, but one that nonetheless would result in a linear, transitive rank
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order. Alternatively, individuals might also distinguish among the relative ranks of others. If rank
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were determined by a physical attribute like size, recognizing other individuals’ ranks would be
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easy. Among most primates, however, there is little relation between rank and size, condition, or
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age. As a result, the problem is considerably more challenging.
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There are hints from their behavior that monkeys do recognize other individuals’ relative
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dominance ranks. In a meta-analysis of 14 different species, including New and Old World
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monkeys, Schino (2001) found consistent evidence that high-ranking females received more
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grooming and were groomed by more different individuals than lower-ranking females. These
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data suggest a general preference for grooming high-ranking individuals, but they fall short of
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showing that each animal recognizes the relative ranks of others. In subsequent papers, Schino et
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al. used a within-subject regression analysis to test the hypothesis that each individual distributed
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grooming among others in direct relation to their relative ranks. They found a significant rank
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effect in Japanese macaques (Schino et al. 2007) but no such effect in capuchins (C. apella;
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Schino et al. 2009).
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Knowledge of other individuals’ rank relations, like the knowledge of other individuals’
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kin relations, is also evident in patterns of recruitment and coalition formation. Female vervets,
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macaques, and baboons, for example, almost always support the higher-ranking of two
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opponents when forming alliances (vervets: Cheney 1983; Seyfarth 1980; rhesus macaques: de
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Waal 1991; Japanese macaques: Chapais 2001). Animals do not simply recruit any higher-
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ranking individual: male bonnet macaques (M. radiata), for example, solicit relatively lower-
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ranking allies when threatening very low-ranking opponents and higher-ranking allies when
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threatening higher-ranking ones. Because rank relations among male bonnet macaques change
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often, males appear to be monitoring carefully the relative ranks of potential opponents (Silk
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1993, 1999).
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These observational studies are supported by field experiments. In one study, female
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chacma baboons heard a sequence of vocalizations mimicking an interaction that violated the
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female dominance hierarchy. The sequence consisted of a series of grunts originally recorded
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from a lower-ranking female combined with a series of fear barks originally recorded from a
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higher-ranking female. As a control stimulus, subjects heard the same anomalous sequence of
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calls but with the inclusion of the grunts of a third female who out-ranked both of the other
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individuals. Supporting the view that baboons recognize other individuals’ dominance ranks,
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subjects looked in the direction of the loudspeaker for significantly longer durations when they
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heard the sequence that violated the dominance hierarchy (Cheney et al. 1995a).
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The recognition of other individuals’ dominance ranks has also been documented among
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adult male chacma baboons, whose aggressive contests often involve loud ‘wahoo’ calls
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(Kitchen et al. 2003; Fischer et al. 2004). In this experiment, subjects heard wahoo sequences
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that mimicked a contest between either adjacently ranked or disparately ranked males. They
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responded significantly more strongly to playback of a wahoo contest between males of disparate
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ranks than to playback of a contest between males of adjacent ranks (Kitchen et al. 2005). The
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result is particularly striking because, like the ranks of male bonnet macaques, the ranks of male
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baboons change often.
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The recognition of other individuals’ rank relations, like the recognition of other animals’
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matrilineal kin relations, requires by itself no special skills in learning and intelligence beyond
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those well-documented in laboratory studies of classical conditioning. In nature, however,
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recognition of other animals’ ranks does not occur on its own – it must necessarily be integrated
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into a complex matrix of other social relations. We are only beginning to understand how this is
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achieved.
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Having found that chacma baboons recognize the close bonds among matrilineal kin and
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individual dominance ranks, Bergman et al. (2003) tested whether individuals integrated their
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knowledge of other individuals’ kinship and rank to recognize that the female dominance
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hierarchy is composed of a hierarchy of families (that is, sub-groups of closely bonded females).
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Rank relations among adult female baboons are generally very stable over time, with few rank
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reversals occurring either within or between families. When rare reversals do occur, however,
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their consequences differ significantly depending on who is involved. If, for example, a female
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rises in rank above her sister, the reversal affects only the two individuals involved; the family’s
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rank relative to other families remains unchanged. However, a rare rank reversal between two
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females from different matrilines is potentially much more momentous, because it can affect
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entire families, with all the members of one matriline rising in rank above all the members of
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another.
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Bergman et al. (2003) played sequences of calls mimicking rank reversals to subjects in
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paired trials. In one set of trials, subjects heard an apparent rank reversal involving two members
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of the same matriline. In the other set, the same subject heard an apparent rank reversal involving
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the members of two different matrilines. As a control, subjects also heard a fight sequence that
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was consistent with the female dominance hierarchy. As before, listeners responded with
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apparent surprise to call sequences that appeared to violate the existing dominance hierarchy.
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Moreover, between-family rank reversals elicited a consistently stronger response than did
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within-family rank reversals (Bergman et al. 2003). Subjects acted as if they were classifying
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individuals simultaneously according to both kinship and rank. The classification of individuals
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simultaneously according to two different criteria has also been documented in an observational
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study of Japanese macaques (Schino et al. 2006).
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h2.Recognition of more transient social relations
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Bonds among matrilineal kin and a linear, transitive female dominance hierarchy are
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components of monkey social structure that typically remain stable for many years. It is not
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surprising, therefore, that primate social cognition has been most well documented in these two
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domains. There is growing evidence, however, that primates also recognize and monitor more
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transient social bonds. Just this kind of monitoring seems to occur in multi-male groups of
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chacma baboons, where males form sexual consortships with adult females during the time when
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they are most likely to ovulate. Sexual consortships constitute a form of mate guarding, and
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typically involve the highest-ranking male. When a consortship has been formed, lower-ranking
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males can only gain mating opportunities by taking advantage of very temporary separations
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between a female and her consort to mate ‘sneakily’.
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To test whether subordinate males monitor sexual consortships for such opportunities,
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Crockford et al. (2007) used a two-speaker playback experiment to simulate a temporary
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separation between the consort pair. One speaker played the consort male’s grunt, to signal his
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location. The other, located approximately 40 meters away, played the female’s copulation call,
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to signal that she was mating with another male and that further mating opportunities might be
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available. Subordinate males responded immediately to the apparent separation between the
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female and her consort by approaching the speaker playing the female’s call. By contrast, when
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the same playback was repeated a few hours after the consortship had ended, subordinate males
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showed no interest. Apparently, they already knew that the consortship had ended and the
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information was therefore redundant. Thus, males appear to monitor the status of these transient
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consort relationships very closely, even though they typically last for only a few days (see Smuts
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1985 for similar data on animals’ recognition of male-female ‘friendships’ in baboons).
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h2. Social cognition in non-primates
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Many non-primate species display examples of social cognition that rival those found in
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monkeys and apes. When competing over access to females, male dolphins (Tursiops truncatus)
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form dyadic and triadic alliances with specific other males, and allies with the greatest degree of
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partner fidelity are most successful in acquiring access to females (Connor et al. 1999, 2001).
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These observations suggest that opponents may recognize the bonds that exist among others and
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selectively retreat when they encounter rivals with a long history of cooperation. Other hints of
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such recognition are seen in spotted hyenas (Crocuta crocuta). Hyenas will often redirect
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aggression toward another, previously uninvolved individual after a fight. Observations suggest
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that these forms of aggression are selectively directed against a relative of the former opponent
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(Engh et al. 2005).
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A variety of species also show evidence of recognizing other individuals’ dominance
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ranks. Like many monkeys, hyenas (Engh et al. 2005), lions (Panthera leo; Packer and Pusey
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1982), horses (Equus equus; Feh 1999), and dolphins (Connor & Mann 2006) intervene
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selectively on behalf of the higher-ranking animal when forming a coalition. Hyenas also seem
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to make transitive inferences about other individuals’ dominance ranks (Engh et al. 2005). The
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ability to engage in transitive inference seems to have evolved independently in several species
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with linear dominance hierarchies. Pinyon jays (Gymnorhinus cyanocephalus) provide a good
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example. These birds live in stable flocks of 50 to 500 individuals, each containing individuals
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that are linked by kinship and arranged in a linear dominance hierarchy. Elegant experiments by
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Paz-y-Miño et al. (2004) have shown that jays use transitive inference to calculate their own
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dominance status relative to that of a stranger they have observed interacting with their group-
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mates.
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Striking examples of social cognition have even been found in monogamous birds (e.g.
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Peake et al. 2002) and fish (Oliveira et al. 1998; Grosenick et al. 2007), where individuals
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‘eavesdrop’ on competitive interactions and remember the identities of winners and losers. These
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data suggest that there is no simple causal relation between large group size and the knowledge
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of other animals’ relations.
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h1. Recognition of intentions and knowledge
Although it now seems clear than many animals recognize other group members’
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relationships and dominance ranks, we still know little about whether they imbue these
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relationships with emotions and motives, as humans do. In the more than 30 years since Premack
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and Woodruff (1978) posed the question “Does the ape have a theory of mind?” much progress
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has been made in the study of mental state attribution in animals. Many questions, however,
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remain unresolved (see Smith et al., this volume).
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h2. The recognition of motives and intent
Several lines of evidence suggest that many animals routinely attribute simple mental
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states, like intentions and motives, to others. This ability is particularly evident in their
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vocalizations, when animals must make inferences about the intended recipient of someone
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else’s calls. Monkey groups are noisy, tumultuous societies, and an individual could not manage
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her social interactions if she interpreted every vocalization she heard as directed at her.
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Inferences about the directedness of vocalizations are probably often mediated by gaze direction
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and relatively simple contingencies. Even in the absence of visual signals, however, monkeys are
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able to make inferences about the intended recipient of a call based on their knowledge of a
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signaler’s identity and the nature of recent interactions. For example, when female chacma
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baboons were played the ‘reconciliatory’ grunt of their aggressor within minutes after being
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threatened, they behaved as if they assumed the call was directed at themselves, as a signal of
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benign intent. As a result, they were more likely to approach their former opponent and to
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tolerate their opponent’s approaches than after hearing either no grunt or the grunt of another
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dominant female unrelated to their opponent (Cheney and Seyfarth 1997). Call type was also
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important, because subjects avoided their recent opponent if they heard her threat-grunt rather
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than her ‘reconciliatory’ grunt (Engh et al. 2006b). By contrast, if subjects heard a female’s
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threat-grunt shortly after grooming with her, they ignored the call and acted as if they assumed
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that the female was threatening another individual. Thus, baboons use their memory of recent
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interactions to make inferences about the caller’s intention to communicate with them.
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In some cases, these inferences are complex and indirect, and call upon baboons’
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knowledge of the kinship relationships of other group members. For example, when female
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baboons were played the threat-grunts of their aggressor’s relative soon after being threatened,
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they avoided members of their aggressor’s matriline. In contrast, when they heard the same
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threat-grunts in the absence of aggression, they ignored the call and acted as if they assumed that
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the call was directed at someone else (Wittig et al. 2007b). Similarly, as already mentioned,
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when subjects heard the ‘reconciliatory’ grunt of their aggressor’s relative after a fight, they were
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more likely to approach both their aggressor and the relative whose grunt they had heard (Wittig
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et al. 2007a). They did not do so, however, if they had heard the ‘reconciliatory’ grunt of
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another, unrelated female. Here again, subjects behaved as if they believed that a grunt from
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their aggressor’s relative must be directed at them, as a consequence of the fight. What is
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especially interesting in these experiments is that subjects inferred that they were the target of the
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vocalization even though they had not recently interacted with the signaler, but with her relative.
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They could only have done so if they recognized that close bond that existed between the two
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females.
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In primates, faces and voices are the primary means of transmitting social signals, and
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monkeys recognize the correspondence between facial and vocal expressions (Ghazanfar &
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Logothetis 2003). Presumably, visual and auditory signals are somehow combined to form a
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unified, multi-modal percept in the mind of a monkey. In a study using positron emission
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tomography (PET), Gil da Costa et al. (2004) showed that when rhesus macaques hear one of
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their own species’ vocalizations, they exhibit neural activity not only in areas associated with
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auditory processing but also in higher-order visual areas, including STS. Auditory and visual
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areas also exhibit significant anatomical connections (Poremba et al. 2003).
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Ghazanfar et al. (2005) explored the neural basis of sensory integration using the coos
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and grunts of rhesus macaques as stimuli. They found clear evidence that cells in certain areas of
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the auditory cortex are more responsive to bi-modal (visual and auditory) presentation of
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species-specific calls than to unimodal presentation. Although significant integration of visual
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and auditory information occurred in trials with both vocalizations, the effect of cross-modal
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presentation was greater with grunts than with coos. The authors speculate that this may occur
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because grunts are usually directed toward a specific individual in dyadic interactions, whereas
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coos tend to be broadcast generally to the group at large. The greater cross-modal integration in
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the processing of grunts may therefore have arisen because, in contrast to listeners who hear a
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coo, listeners who hear a grunt must determine whether or not the call is directed at them.
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In sum, when deciding “Who, me?” upon hearing a vocalization, monkeys must take into
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account the identity of the signaler (who is it?), the type of call given (friendly or aggressive?),
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the nature of their prior interactions with the signaler (were they aggressive, friendly, or
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neutral?), and the correlation between past interactions and future ones (does a recent grooming
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interaction lower or increase the likelihood of aggression?). Learned contingencies doubtless
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play a role in these assessments. But because listeners’ responses depend on simultaneous
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consideration of all of these factors, this learning is likely to be both complex and subtle.
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h2. Inferences about others’ knowledge
Although baboons and other monkeys may be able to recognize other individuals’
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intentions when inferring whether or not they are the target of another individual’s call, there is
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less convincing evidence that they also take into account their audience’s knowledge or beliefs
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when producing or assessing calls. Both monkeys and apes give alarm calls, for example,
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without any apparent recognition of whether listeners are ignorant or already informed about the
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presence of a predator (reviewed by Cheney and Seyfarth 2007). Similarly, although the ‘food
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calls’ of capuchin monkeys (Gros-Louis 2004) and the pant hoots of chimpanzees (Clark &
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Wrangham 1994) attract others to food, signalers show no evidence of recognizing whether their
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audience is already aware of the presence of food. To provide another example, chacma baboons
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often give ‘contact’ barks when separated from others. When several individuals are calling
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simultaneously, it often appears that they are answering each other’s calls in order to inform
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others of the group’s location. Playback experiments suggest, however, that baboons call
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primarily with respect to their own separation from the group, not their audience’s. They
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‘answer’ others when they themselves are separated, and they often fail to respond to the calls of
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even their offspring when they themselves are in close proximity to other group members
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(Cheney et al. 1996; Rendall et al. 2000). In this respect, the vocalizations of monkeys and apes
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are very different from human speech, where we routinely take into account our audience’s
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beliefs and knowledge during conversation.
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The extent to which animals attribute knowledge, ignorance, and beliefs to others is
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controversial. It is now well established that many animals are highly attentive to other
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individuals’ direction of gaze. In particular, domestic dogs (Canis familiaris) are adept at using
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gaze or gestures to determine which of two locations has food. When presented with a human or
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another dog informant, they reliably choose the location where the informant is looking,
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pointing, or orienting (e.g. Hare et al. 1998; Hare & Tomasello 1999; Miklosi & Topal 2004).
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Indeed, in one direct comparative experiment dogs were more accurate than chimpanzees in their
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ability to use communicative cues like pointing, gazing, and reaching to locate food (Brauer et al.
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2006b). In addition to using other individuals’ direction of gaze to gain information, dogs often
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go out of their way to make eye contact with others before attempting to communicate with
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them, and they appear to be sensitive to whether a person is attentive or inattentive (Gacsi et al.
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2004).
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Some investigators have suggested that animals’ attentiveness to gaze direction is an
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indication that animals recognize what other individuals can and cannot see and hence what they
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can and cannot know. Rhesus macaques, for example, are more likely to attempt to steal food
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from a human whose eyes are averted than from one whose eyes are not (Flombaum & Santos
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2005), and captive chimpanzees are more likely to approach food that a competitor cannot see
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than food it can see (Hare et al. 2000). Similarly, when potential competitors are present, ravens
364
(Corvus corax) and scrub jays (Aphelocoma californica) are more likely to cache food in sites
365
that are out of view or hidden behind barriers than in more open sites (reviewed by Clayton this
366
volume; Bugnyar & Heinrich 2005; Bugnyar & Kotrschal 2002; Emery et al. 2004; Dally et al.
367
2005).
368
These results are certainly consistent with the interpretation that animals recognize the
369
relationship between seeing and knowing. However, they are also consistent with a simpler
370
interpretation that posits that animals use gaze direction to assess not other individuals’
371
knowledge, but rather their intentions. As a result, they recognize, for example, that other
372
individuals are motivated to defend food that they are looking at, and less likely to defend food
373
in which they show no interest.
374
Some recent experiments have attempted to avoid this confound by eliminating the
375
possibility that subjects are responding only to their rival’s direction of gaze when choosing
376
among food items. Kaminski et al. (2008) presented chimpanzees with the choice of three
377
buckets, two of which contained food. The first bucket was baited in the presence of both the
378
subject and the rival. The second bucket was baited in the presence only of the subject. In the test
379
condition, the subject’s view of the apparatus was blocked, while the rival was allowed to choose
380
first. In the control condition, the subject chose first. When subjects chose first, they were as
381
likely to choose the bucket that their rival had seen baited as the one he had not. However, when
382
they chose second, they were more likely to choose the bucket that their rival had not seen
383
baited, suggesting they inferred that the rival would have chosen the bucket that he had seen
384
baited. In other words, they acted as if they recognized what their rival knew, based on what he
385
had seen.
18
386
To date, most studies of animals’ ‘theory of mind’ have been conducted on captive
387
animals, using paradigms and rewards determined by human experimenters. It is to be hoped that
388
future investigations will attempt to address these questions under more natural conditions, on
389
the animals’ own terms. Until such experiments are conducted, we can only speculate about the
390
selective forces that might favor the evolution of a theory of mind, and its function in social
391
interactions.
392
393
394
h1. The function of cooperation, social relationships, and a social mind
If knowledge of other individuals’ relationships and mental states is adaptive, it should be
395
possible to identify correlations between social knowledge and reproductive success. Although
396
this has not yet proved impossible, there is growing evidence that animals benefit from social
397
bonds, that they are motivated to form social bonds, and that there is individual variation not
398
only in the strength and consistency of social bonds but also that this variation is correlated with
399
reproductive success.
400
Female monkeys form the strongest and most enduring social bonds with close kin
401
(reviewed by Silk 2007). Among wild female baboons, for example, the strongest bonds are
402
formed between mothers and daughters, the next strongest bonds with maternal sisters, and less
403
close bonds with less closely related individuals (Silk et al. 2006a, b; 2010a). Females form the
404
strongest social bonds with those that groom them most equitably, and those that groom most
405
equitably have the most enduring social bonds (Silk et al. 2006a, 2006b, 2010a). A similar
406
pattern characterizes wild male chimpanzees (Mitani 2009b). Indeed, a number of studies have
407
demonstrated that primates balance grooming exchanges with long-term partners; although
408
grooming within dyads is often unbalanced over short periods of time, pairs with strong bonds
19
409
have strongly reciprocal grooming relations over extended time periods (chimpanzees: Gilby &
410
Wrangham 2008; Gomes et al. 2009; capuchins: Schino et al. 2009, anubis baboons (P.h.
411
anubis): Frank & Silk 2009). Even females who lack close kin form close relationships with a
412
few specific females, though these are often not as enduring as those formed among kin. This is
413
true also of male chimpanzees. Although males form the strongest and enduring bonds with
414
maternal brothers (Langergraber et al. 2007; Mitani 2009b), close bonds are not limited to kin,
415
and even unrelated females chimpanzees often establish and maintain close bonds with specific
416
other females (Langergraber et al. 2009).
417
Close bonds also appear to be correlated with reproductive success. Female yellow
418
baboons (P. h. cynocephalus) that are more socially integrated into their groups experience
419
higher infant survival than females who are less socially integrated (Silk et al. 2003b). Similarly,
420
female chacma baboons who maintain strong bonds with other adult females have higher
421
survivorship among their offspring than females with weaker bonds (Silk et al. 2009).
422
Furthermore, females who maintain the closest and most consistent bonds experience greater
423
longevity (Silk et al. 2010b). These effects are independent of dominance rank, suggesting that
424
strong and consistent bonds may partially offset any fitness loss due to low dominance rank.
425
Importantly, the fact that most females’ partner changes are not due to the death of the partner
426
suggests that some females may be more skilled or more motivated than others in maintaining
427
relationships with preferred partners over time. Positive correlations between sociality and
428
reproductive success have also been documented in unrelated wild female horses (Cameron et al.
429
2009), indicating again that the strength of an individual’s social relationships exerts a stronger
430
effect on reproductive success than the mere presence of kin. These findings also parallel
20
431
evidence from humans showing that social integration enhances longevity and health (e.g.
432
Berkman & Glass 2000; Cacioppo & Hawkley 2003; Smith & Christakis 2008).
433
The factors that underlie the correlation between strong social bonds and fitness are not
434
yet understood, and there is some uncertainty about the direction of the causal links between
435
social bonds and fitness. One causal factor may be related to stress. When rats (Rattus
436
norvegicus) and other rodents are housed in isolation, they become hypervigilant and fearful of
437
new stimuli (Cavigelli & McClintock 2003; Cavigelli et al. 2006; reviewed by Cheney &
438
Seyfarth 2009). Fearfulness early in life is associated with greater reactivity to stressful events
439
later in life and earlier age at death. Socially isolated females have more exaggerated
440
glucocorticoid responses to every day stressors, and are much more likely to develop mammary
441
cancers than group-housed females (McClintock et al. 2005). Similarly, prolonged social stress
442
impairs the immune system of female long-tailed macaques (M. fasicularis; Shively et al. 2005),
443
but affiliative interactions with group members partially offset these deleterious effects (Cohen et
444
al. 1992; Gust et al. 1994).
445
The quality of social relationships may influence females’ ability to cope with the
446
challenges of daily life. For example, female house mice (Mus musculus), which often share
447
nests with other females and rear their pups communally, reproduce more successfully when they
448
are allowed to choose their nestmates than when nestmates are assigned randomly (Weidt et al.
449
2008). Rat sisters with well-balanced affiliative relationships exhibit lower glucocorticoid levels,
450
fewer tumors, and higher survival rates than those with less well-balanced relationships (Yee et
451
al. 2008). Female chacma baboons display marked increases in glucocorticoid levels when a
452
preferred social partner dies (Engh et al. 2006a). In the same population, females experience
453
lower glucocorticoid levels when their grooming networks are more focused, and females with
21
454
more focused grooming networks show less pronounced responses to various stressors, including
455
the immigration of potentially infanticidal males (Crockford et al. 2008; Wittig et al. 2008).
456
Similar effects have been observed in semi-free-ranging rhesus macaque females, who exhibit
457
lower glucocorticoid levels in months when their grooming networks are less diffuse (Brent et al.
458
2010).
459
460
461
h1. The mechanisms underlying cooperative behavior
Despite the reproductive benefits of strong cooperative relationships, the mechanisms
462
that motivate individuals to form such bonds are still far from well understood. Female baboons,
463
for example, do not groom only with close kin and those with whom they share a close social
464
bond; they also groom less regularly with other females. When a close partner dies, they may
465
attempt to establish a close bond with a previously infrequent partner. We hypothesize that
466
knowledge of other individuals’ relationships guides the formation of new relationships, but this
467
hypothesis has not yet been tested. Indeed, we still know little about whether or how animals
468
keep track of their social relationships, of cooperative and non-cooperative interactions, or of
469
favors given and received.
470
471
472
h2. The mechanisms underlying social interactions
There continues to be debate about the psychological mechanisms that underlie animals’
473
social interactions and relationships. Because we have no direct evidence that animals can plan
474
or anticipate the benefits that might derive from a long-term relationship, a number of
475
investigators have argued that animals’ cooperative interactions are motivated only by short-term
476
rewards, such as the opportunity to handle an infant or gain access to food. According to these
22
477
arguments, social interactions are not founded on long-term patterns of affiliation but are based
478
instead on short-term by-product mutualism or biological markets motivated by the likelihood of
479
immediate reward (Noe & Hammerstein 1994). For example, much cooperative behavior in
480
nonhuman primates occurs in the form of low cost services like grooming and alliance support
481
against lower-ranking opponents (Widdig et al. 2000; Watts 2002; Schino 2007). Because these
482
alliances function primarily to reinforce the status quo, it has been suggested that they might
483
more properly be regarded as a form of mutualism. Similarly, when a female grooms another in
484
order to gain access to her infant, she may simply be engaging in a short-term negotiation with a
485
trading partner who controls a desirable commodity (Barrett et al. 1999, 2003; Fruteau et al.
486
2009; Henzi & Barrett 2002).
487
There is no doubt that many social interactions vary with current conditions. Several
488
studies have shown, for example, that female baboons often groom lactating females to obtain
489
immediate access to their infants (Seyfarth 1976; Altmann 1980; Frank and Silk 2009; Henzi &
490
Barrett 2002; Silk et al. 2003a). Female baboons are particularly likely to reconcile after conflicts
491
with mothers of newborns, as reconciliatory behavior facilitates infant handling (Silk et al.
492
1996). Similarly, males groom estrous females at higher rates than pregnant or lactating females,
493
and subordinate individuals groom dominant individuals in apparent exchange for tolerance at
494
food sites (de Waal 1997; Ventura et al. 2006). In an experiment directly testing the hypothesis
495
that grooming in vervet monkeys is motivated in part by the expectation of immediate reward,
496
Fruteau et al. (2009) manipulated a food container in such a way that it could only be opened by
497
one low-ranking female. Consistent with biological market theory, the rate at which the female
498
subsequently received grooming from others increased significantly. This initial gain, however,
23
499
decreased after a second subordinate female was allowed to open the container. Thus, grooming
500
appeared to be adjusted according to the relative value of the provider.
501
The view that many social interactions are based on the current value of commodities and
502
the supply of alternative trading partners is not necessarily inconsistent with evidence indicating
503
that others reflect long-terms patterns of affiliation. Female baboons, for example, form long-
504
term bonds with only a small number of other females; many of their other social interactions
505
may well be initiated or maintained by interactions that depend on the current value of
506
commodities. Nevertheless, their long-term bonds can endure for years despite short-term
507
fluctuations in behavior due, for example, to the birth of infants. Moreover, grooming often
508
occurs in the absence of an immediate reward, and it is seldom evenly balanced between partners
509
within single bouts. Finally, despite short-term asymmetries, non-human primates form the
510
strongest bonds with those individuals with whom they have the most balanced and reciprocal
511
grooming interactions over extended periods of time (see above).
512
513
514
h2. The mechanisms underlying reciprocity and contingent cooperation
During the last decade, there has also been increasing skepticism about the relevance of
515
reciprocity in the social interactions of animals. Because most cooperative interactions like
516
grooming occur between long-term partners (often kin) for whom any single altruistic act may be
517
relatively insignificant, many investigators are now convinced that the sort of reciprocal altruism
518
first proposed by Trivers (1971) may be both rare and fragile in nature (e.g. Hammerstein 2003;
519
Clutton-Brock 2009). Although there is limited experimental and correlational evidence that
520
animals sometimes rely on memory of recent interactions when behaving altruistically toward
521
others, interpretation has been complicated by a paucity of convincing examples, the absence of
24
522
important controls in some early tests, and a number of experimental studies seeming to indicate
523
that animals lack the cognitive or empathetic ability to sustain contingent cooperative exchanges.
524
As originally formulated by Trivers (1971; see also e.g. Stephens 1996; Gurven 2006;
525
West et al. 2007; Schino & Aureli 2009), reciprocal altruism occurs when the donor of an
526
altruistic act incurs an immediate cost but receives delayed benefits when the recipient
527
reciprocates the altruistic act at some future time. For reciprocal altruism to evolve, individuals
528
must have a high probability of meeting again, and they must be able to detect or avoid cheaters.
529
Reciprocal altruism can be distinguished from mutualism, in which both participants receive
530
immediate benefits that are greater than any immediate costs, and from kin selection, in which
531
the donor gains inclusive fitness benefits despite incurring costs. Because the costs and benefits
532
of many altruistic acts are difficult to quantify, I will here use the term ‘contingent cooperation’
533
rather than ‘reciprocal altruism’ to describe altruistic behavior whose occurrence is contingent
534
upon a specific previous altruistic act. This definition is agnostic with respect to the precise costs
535
and benefits of the altruistic behavior; it posits only that a given supportive act by individual A
536
toward B is causally dependent upon a previous supportive act by B toward A.
537
538
h3. Cognitive constraints on contingent cooperation
539
Some of the skepticism about the relevance of contingent cooperation in animals’
540
interactions stems from doubts about whether animals possess the requisite cognitive abilities to
541
sustain such cooperation. These include the ability to remember specific interactions, to delay
542
reward, to track favors given and returned, to plan and anticipate future outcomes, and to
543
distinguish between cooperators and defectors (e.g. Stevens & Hauser 2004; Stevens et al. 2005;
544
Barrett et al. 2007; Henzi & Barrett 2007; Hauser et al. 2009). Many of these objections may not
25
545
be valid. As already described, for example, a number of playback experiments have
546
demonstrated that female baboons’ behavior is influenced by memory of a recent interactions
547
with specific individuals and their relatives (Cheney & Seyfarth 1997; Engh et al. 2006b; Wittig
548
et al. 2007a, b). The extent to which this memory is explicit is as yet unknown.
549
Other purported cognitive limitations can also be questioned. There is now a large
550
literature on animals’ numerical discrimination abilities, suggesting that quantity assessments
551
and counting are widespread across many taxa (reviewed by Shettleworth 2010). Like children,
552
nonhuman primates appear to rely on two distinct core systems for representing quantities: one
553
for identifying small absolute numbers and another for estimating and comparing larger amounts
554
(Feigenson et al. 2005). In macaques, specific neurons in the PFC appear to be tuned to
555
particular small numbers (Nieder et al. 2002). Rhesus macaques are also able to sum the number
556
of sounds they hear and the number of objects they see, indicating that the ability to match and
557
add quantities is cross-modal and extends across different currencies (Jordan et al. 2008).
558
Similarly, although many tests with non-human primates have suggested a general failure to
559
delay rewards beyond very short periods of time (e.g. Evans & Beran 2007; Ramseyer et al.
560
2006), there appears to be considerable inter-individual variation in self-imposed delayed
561
gratification (Beran 2002; Pele et al. 2010). Moreover, the ability of primates and other animals
562
to delay gratification in contexts that do not involve food rewards remains largely untested. Thus,
563
contingent cooperation in animals is not necessarily constrained by the inability to delay reward
564
or to quantify past cooperative acts.
565
It has also been assumed that animals are not capable of contingent cooperation because
566
it demands the ability to anticipate future interactions. Leaving aside for the moment the question
567
of whether mental projections of future outcomes are necessary to sustain contingent
26
568
cooperation, the assumption that animals are unable to anticipate events that have not yet
569
occurred may not be valid. There is a long history in experimental psychology of tests
570
demonstrating that many animals – including pigeons, rats, and nonhuman primates – accurately
571
and predictably anticipate future rewards and outcomes (reviewed by Shettleworth 2010). Both
572
the prefrontal cortex and the amygdala play important roles in delay discounting and reward
573
anticipation in animals (Miller & Wallis 2003; Churchwell et al. 2009; Crystal 2009).
574
Furthermore, although non-human primates may lack the ability to reflect explicitly and
575
consciously about their past and future interactions (reviewed by Cheney & Seyfarth 2007), they
576
do appear to have some mental access to their own experiences (reviewed by Smith et al., this
577
volume). Indeed, the ability to monitor uncertainty and assess knowledge appears to be highly
578
adaptive, especially when an animal finds itself in a novel predicament.
579
It is also doubtful that non-human primates are unable to distinguish cooperators from
580
non-cooperators. In tests conducted in captivity that require two individuals to work together to
581
obtain a food reward, both capuchin monkeys and chimpanzees are more likely to cooperate with
582
partners with whom rewards are shared more equitably (de Waal & Davis 2003; Melis et al.
583
2006b; Melis et al. 2009; reviewed by Silk & House, this volume). Chimpanzees also recognize
584
which partners are most effective (Melis et al. 2006a), and they show a limited ability to increase
585
their rate of cooperation with partners who have cooperated with them in the past (Melis et al.
586
2008). They are also able to some extent to resolve conflicts of interests when working together
587
to achieve a common goal (Melis et al. 2009; see Silk & House for more discussion).
588
589
h3. Emotional constraints on contingent cooperation
27
590
In humans, inequity aversion, social tolerance, and the motivation to engage in joint
591
activities are important catalysts for cooperative behavior. The degree to which non-human
592
primates are motivated by these emotions, however, remains unclear (reviewed by Silk & House,
593
this volume). Some experiments have suggested that capuchins and chimpanzees reject food
594
offered by humans if a rival is receiving a better reward (Brosnan & de Waal 2003; Brosnan et
595
al. 2005; Takimoto et al. 2010). Other experiments, however, have failed to replicate these
596
results, suggesting that the food rejections are due to frustration at seeing, but not obtaining, a
597
preferred food item rather than to perceived inequity. Indeed, in some cases, seeing a rival eating
598
preferred food actually increases the likelihood that subjects will accept less preferred food
599
(Brauer et al. 2006a, 2009; Dubreuil et al. 2006). In captivity, chimpanzees seem generally
600
indifferent to inequitable outcomes to themselves and others. In two experiments in which
601
chimpanzees had the opportunity to deliver food to a partner at no cost to themselves, subjects
602
showed no evidence of other-regarding behavior (Silk et al. 2005; Jensen et al. 2006; but see
603
Lakshminarayanan & Santos 2008). They did not behave spitefully or withhold food from their
604
partner; they simply ignored their partner’s returns. Similarly, in ultimatum games, chimpanzees
605
appear to behave more rationally than humans, accepting inequitable returns to themselves if no
606
alternatives are available (Jensen et al. 2007a).
607
It has also been argued that a lack of social tolerance may contribute to the low levels of
608
cooperation achieved by chimpanzees in many experiments. Bonobos (Pan paniscus) achieve
609
higher levels of success in some cooperative tasks than do chimpanzees, seemingly because their
610
willingness to share rewards with their partners prompts continued cooperation (Hare et al.
611
2007). One explanation for this greater tolerance is that adult bonobos retain the characteristics
612
of juveniles, because juvenile chimpanzees also tend to be more cooperative than adult
28
613
chimpanzees (Wobber et al. 2010). It remains unclear, however, whether bonobos also show
614
higher degrees of cooperation and tolerance for partners under natural conditions, in contexts
615
where the nature of the task and its rewards are not determined by humans. It is not known, for
616
example, whether bonobos show higher levels of cooperation than chimpanzees when hunting, or
617
whether they share their kills more equitably. Similarly, it is not at all apparent whether bonobos
618
ever engage in any behavior that is as cooperative and potentially costly as chimpanzees’
619
patrolling behavior (Watts & Mitani 2001; Mitani et al. 2010; see below), or if they do, whether
620
they are more likely than chimpanzees to share risks equitably.
621
Taken together, the results of these experiments suggest that cooperation in animals may
622
be sustained by qualitatively different mechanisms than it is in humans. Indeed, experiments
623
explicitly designed to compare the behavior of children and young chimpanzees suggest that
624
humans may be uniquely motivated to engage others’ attention, to empathize with others, and to
625
share their intentions, emotions, and knowledge (Tomasello et al. 2005; Warneken & Tomasello
626
2009; Silk & House; this volume). It is also possible, however, that inequity aversion may be less
627
universal in humans than is often supposed. Surveys of people living in societies that lack large-
628
scale religions and economic markets have tended to reveal a general indifference to unfair
629
outcomes (Henrick et al. 2010), suggesting that what is often regarded as a species-specific
630
prosociality in humans is not entirely the result of innate psychological mechanisms (see Boesch,
631
this volume; Silk & House, this volume).
632
633
634
635
h2. How rare, in fact, is contingent cooperation?
Most primates live in groups that include both kin and nonkin, with whom they both
cooperate and compete. Because individuals do not derive inclusive fitness benefits from
29
636
cooperating with nonkin, investigators have typically postulated that any form of cooperation
637
among nonkin must be maintained either by mutualism or by some form of contingent
638
cooperation from which individuals derive long-term benefits while tolerating short-term
639
inequities. For several reasons, however, it has proved difficult to investigate contingent
640
cooperation under natural conditions. First, in the absence of experiments, it is almost impossible
641
to determine whether a given altruistic act is causally dependent upon a specific prior interaction.
642
Second, many altruistic acts occur in different currencies –such as grooming, alliance support, or
643
food sharing – whose relative values are difficult to calibrate or quantify. Moreover, even
644
altruistic acts that occur in the same currency may not carry equal value to each participant. In
645
species that form dominance hierarchies, for example, a low-ranking individual may value
646
alliance support from a more dominant partner more highly than vice versa. As a result, he may
647
willing to provide substantially more alliance support to the dominant partner than he receives in
648
return and still regard the relationship as reciprocal. Given these tautological assumptions, almost
649
any relationship can be termed reciprocal. Finally, the degree to which interactions are regarded
650
as reciprocal may also be a function of the time scale under consideration. As already mentioned,
651
grooming exchanges within single bouts are often unbalanced and asymmetrical. Nonetheless,
652
over longer periods of time partners with close social bonds exhibit a high degree of reciprocity
653
in their grooming interactions.
654
655
h3. Observational evidence
656
Correlations between grooming and alliance support have been documented in a variety
657
of primates (reviewed in Silk 2007). In a meta-analysis involving 14 different primate species,
658
Schino (2007) found a weak but highly significant correlation between grooming and alliances
30
659
among female non-human primates over extended periods, but little evidence that alliance
660
support is motivated specifically by recent grooming bouts (see also Schino et al. 2007). For
661
example, in one year-long study of Japanese macaques, individuals formed most coalitions with
662
preferred grooming partners, but there was no evidence that a recent grooming bout increased the
663
probability of support over the short term (Schino et al. 2007). Monkeys appeared to choose
664
alliance partners on the basis of long-term partner preferences rather than on memory of specific
665
interactions. These observations suggest that grooming and alliance support have evolved as a
666
system of long-term, low-cost reciprocity (Schino & Aureli 2009) rather than one of short-term,
667
contingency-based exchange.
668
In contrast, de Waal (1997) reported that captive chimpanzees were more likely to share
669
food with individuals who had recently groomed them than with those that had not. Here again,
670
however, the effect of prior grooming appeared to be influenced by the nature of the relationship
671
between the two individuals. For pairs that seldom groomed, sharing was contingent upon recent
672
grooming; for pairs that regularly groomed at high rates, sharing was less influenced by recent
673
interactions.
674
Similarly, wild male chimpanzees reciprocate grooming, alliances, and meat-sharing with
675
specific long-term partners. Although exchanges are often asymmetrical within dyads over short
676
time periods, they become more evenly balanced over longer periods of time, and they are not
677
simply a byproduct of association frequency or genetic relatedness (Mitani 2006, 2009a; see
678
Boesch, this volume). Cooperation also involves the exchange of services in different
679
currencies, with males reciprocating grooming for support, and support for meat, for example.
680
The most costly cooperative behavior shown by male chimpanzees occurs in the form of
681
boundary patrols and inter-group aggression. Chimpanzees make sometimes lethal incursions
31
682
into the territories of neighboring communities (Nishida et al. 1985; Watts & Mitani 2001;
683
Wilson & Wrangham 2003; Mitani et al. 2010; Boesch this volume). These incursions are highly
684
risky, because a small party or lone individual is vulnerable to a fatal attack if a larger party is
685
encountered; therefore, they cannot be undertaken alone. Although it remains unclear whether
686
patrols are planned, they do appear to involve some degree of shared intentionality and a high
687
degree of mutual support. Little is known about the mechanisms that motivate chimpanzees to
688
initiate and participate in these highly cooperative and potentially costly activities. It is not
689
known, for example, whether chimpanzees take into consideration memory of another
690
individual’s behavior during previous patrols when deciding whether or not to recruit or join him
691
in a patrol. Whether cooperation in this context is more, or less, contingent upon memory of
692
previous events, remains unclear.
693
In sum, most observational studies suggest that cooperation under natural conditions is
694
generally not contingent upon specific recent events. Instead, reciprocal exchanges tend to
695
emerge gradually among regular partners over repeated interactions and longer time scales,
696
despite not being balanced over short periods of time (Mitani 2006, 2009a; reviewed by Schino
697
& Aureli 2009).
698
699
h3. Experimental evidence
700
It is difficult if not impossible to demonstrate through observation alone that a given
701
cooperative act is contingent upon a specific previous act. Experiments have typically been
702
conducted on captive animals, relying on single food exchanges as evidence for reciprocity.
703
These have usually yielded negative results. For example, in one set of experiment with captive
704
chimpanzees, subjects were given a choice of cooperating with either an individual who had
705
previously helped them or one that had not (Melis et al. 2008). Although there was some
32
706
evidence that subjects increased their cooperation with the more helpful partner, this effect was
707
relatively weak. Similarly, in another experiment explicitly designed to test whether cooperation
708
was contingent upon a specific recent interaction, Brosnan et al. (2009) found no evidence that
709
chimpanzees were more likely to provide food to a partner if that partner had previously
710
provided food to them (see also Yamamoto & Masayuki 2010). Melis et al. (2006b) suggest that
711
chimpanzees may be capable of contingent reciprocity, but that long-term partner preferences
712
that develop over repeated interactions may override the decisions that chimpanzees make on the
713
basis of immediate exchanges and rewards. It is also possible, however, that the lack of
714
convincing evidence for contingent cooperation in tests with captive animals results in part from
715
the stringent standards set by these experiments, which have typically required proof of equal
716
back-and-forth exchanges of single currency food rewards whose amounts and timing are
717
determined by humans. These requirements may have set the bar unrealistically high, leading
718
investigators to underestimate the extent to which a recent cooperative interaction may motivate
719
animals to cooperate again.
720
Several investigations conducted under more natural conditions, and without the distraction
721
of food rewards, provide more positive evidence for the reciprocal exchange of cooperative
722
behavior. Unfortunately, however, interpretation is complicated by the lack of important controls
723
in early experiments and the lack of follow-up studies to correct for these confounds. For
724
example, in the well-known study of vampire bats (Desmodus rotundus: Wilkinson 1984) most
725
reciprocal exchanges of blood occurred among close kin. Furthermore, although some
726
individuals regularly exchanged blood with unrelated partners, it was not clear whether any
727
specific act of regurgitation was contingent upon a specific recent donation. The same was true
728
in Packer’s (1977) classic study of reciprocal alliance formation in wild baboons: although males
33
729
supported those individuals who most supported them, cooperative behavior may have emerged
730
not as a result of memory of specific previous alliances but through bonds that developed
731
gradually over extended periods of time.
732
A recent investigation of mobbing behavior in pied flycatchers (Ficedula hypoleuca)
733
provides more convincing evidence for contingent cooperation (Krams et al. 2008). In this
734
experiment, subjects had the opportunity to help one of two neighbors in mobbing an owl. One
735
of these neighbors had recently helped the subjects to mob an owl at their own nest box, while
736
the other had been prevented from doing so by the experimenters. Subjects were significantly
737
more likely to help previous supporters than apparent defectors, suggesting that cooperative
738
behavior was contingent upon memory of each of the neighbor’s behavior. However, the
739
possibility that the birds’ behavior might have been influenced by any recent interaction with
740
their neighbors – not just a supportive one – was not addressed.
741
This confound was also present in Seyfarth and Cheney’s (1984) playback experiment on
742
wild vervet monkeys. Although subjects were more attentive to the recruitment call of an
743
unrelated female after grooming with her than after no interaction, it remained unclear whether
744
subjects might have been equally responsive after any interaction with her, including even
745
aggression.
746
Subsequently, Hemelrijk (1994) demonstrated that grooming increased the probability of
747
actual alliance support in an imaginative experiment with captive long-tailed macaques. In this
748
experiment, three females were temporarily isolated from the rest of the group, and one of the
749
two higher-ranking females was dabbed with a sticky mixture of seeds and syrup to elicit
750
grooming. After 10 minutes, the experimenters provoked aggression by feeding a desirable tidbit
751
to the lowest-ranking of the three females and then observed whether the bystander supported the
34
752
primary aggressor. Hemelrijk found that bystanders were more likely to provide support after
753
being groomed by the aggressor than after no grooming had occurred, suggesting that support
754
was based on memory of the prior grooming interaction.
755
Recently, we conducted a playback experiment with wild chacma baboons that attempted
756
to control for some of the confounds complicating earlier experiments (Cheney et al. 2010). In
757
the test condition, a subject was played the recruitment call of another female at least 10 minutes
758
after she had groomed with that female and then separated without any further interactions. This
759
playback was designed to mimic a context in which the former grooming partner was threatening
760
another individual and soliciting aid. Each subject’s responses were compared to her responses in
761
two control conditions. The first control was also conducted after the subject and the same
762
female had groomed and then separated for at least 10 minutes. In this case, however, no
763
playback was conducted. This control was designed to test whether a recent friendly interaction
764
might simply motivate the subject to approach her partner again, even in the absence of any
765
solicitation for support. In the second control, the same female’s threat-grunts were played to the
766
same subject at least 10 minutes after the subject had threatened that female. This control was
767
designed to test whether subjects’ responses to a recruitment call were primed by any prior
768
interaction, not just a friendly one. On the assumption that a recent cooperative interaction would
769
exert a stronger influence on females with weaker social bonds than those with stronger social
770
bonds (de Waal 1997; Schino & Aureli 2009), we predicted that nonkin would be more likely
771
than kin to show different responses across conditions. Kin selection theory predicts in any case
772
that contingency-based altruism should be less common among kin than among nonkin. Indeed,
773
in one study of captive Japanese macaques kin were never observed to support each other in the
774
half hour after grooming, even when they had the opportunity to do so (Schino et al. 2007).
35
775
Results provided some support for delayed contingent cooperation among unrelated
776
individuals. Hearing the recruitment call of a recent grooming partner caused subjects to move in
777
the direction of the loudspeaker and approach their former partner. When the subject and her
778
partner were close kin no such effect was observed. Importantly, subjects’ responses were not
779
influenced by any type of recent interaction, because subjects only responded to their former
780
partner’s recruitment call after grooming, and not after aggression. Similarly, their responses
781
were not prompted only by the motivation to resume a friendly interaction, because prior
782
grooming alone did not elicit approach. Instead, subjects were most likely to approach their
783
former grooming partner when they had also heard her recruitment call. Thus, females’
784
willingness to attend to the recruitment calls of other individuals appeared to be motivated at
785
least in part by memory of a specific friendly interaction.
786
In sum, several factors may interact to motivate contingent cooperation in animals under
787
natural conditions: the strength of the partners’ social relationship, the nature of their recent
788
interactions, and the opportunity to reengage in some form of cooperative behavior. Animals
789
appear to possess many of the cognitive abilities thought to be essential for the emergence of
790
contingent cooperation, if only in rudimentary form. Nonetheless, such cooperation appears to be
791
much more rare than the high rates of non-contingent cooperation that develops among kin and
792
long-term partners.
793
794
795
h2. The avoidance of non-cooperators
If cooperation depends on the memory of previous behavior, why do animals seldom
796
avoid or punish cheaters and free-loaders? In captive tests, for example, chimpanzees will
797
continue to work with non-cooperators despite receiving inequitable returns (Melis et al. 2006b,
36
798
2009). And while they retaliate against an individual who steals food from them, but they do not
799
attempt to punish those who obtain disproportionate rewards, and they are not spiteful (Jensen et
800
al. 2007b; Melis et al. 2009).
801
Under natural conditions, too, free-loaders appear to be tolerated. To provide two
802
examples, individual lionesses vary predictably in their participation in territorial conflicts. In
803
playback experiments that simulated the approach of an aggressive intruder, some females
804
consistently advanced toward the source of the calls, while others consistently lagged behind and
805
avoided the potential cost of a conflict (Heinsohn & Packer 1995). Advancers were aware of the
806
laggards’ behavior, because they often looked back at them; nonetheless, they did not avoid or
807
punish them. It is possible that advancers tolerate laggards because they derive inclusive fitness
808
benefits through the laggards’ survival and reproduction. Laggards may also cooperate in other
809
currencies, such as hunting. It is also possible, however, that lions do not have the cognitive
810
ability to recognize laggards as free-loaders, with the result that laggards are able to exploit
811
advancers.
812
Similarly, male chimpanzees do not participate equally in boundary patrols. As with
813
lions, some individuals are allowed to reap the benefits of territorial integrity and even expansion
814
without incurring any costs (Mitani 2006; Mitani et al. 2010). Mitani (2006; 2009a) offers
815
several, as yet untested, explanations for chimpanzees’ tolerance of free-loaders. First, the
816
benefits of patrolling may be greater for some individuals than others. Perhaps, for example,
817
patrolling is a costly signal that enhances an individual’s dominance or access to females.
818
Second, patrolling may yield indirect fitness benefits in the form of enhanced survival and
819
reproduction of close kin. Thus, males with more kin in the community may engage in higher
820
rates of patrolling. Finally, like the lions just mentioned, chimpanzees may lack the cognitive
37
821
capacity to foster or infer deceptive intent. If true, animals may well not be capable of achieving
822
the sort of contingent cooperation manifested by humans, which is sustained in part by inequity
823
aversion and sensitivity to envy, spite, and deception (Jensen et al. 2007b).
824
This last objection, however, only denies the possibility for human-like contingent
825
cooperation in animals; it does not rule it out entirely. The detection of cheaters does not in
826
principle require the ability to impute complex mental states like deception to others. It could
827
arise through relatively simple associative processes, by which animals learn to avoid individuals
828
whose presence is associated with a negative experience. Indeed, mental state attribution may be
829
irrelevant to the emergence of contingent cooperation in animals. Schino and Aureli (2009; see
830
also Schino et al. 2007) have argued that the focus on cognitive constraints in discussions of
831
contingent cooperation is misguided, and confuses proximate and ultimate explanations for
832
behavior. Altruistic behaviors may be favored by natural selection because of the subsequent
833
benefits they confer, but what motivates animals to behave altruistically are the previous benefits
834
they have received. In this view, the accumulation of multiple, altruistic exchanges over time
835
causes animals to form partner-specific emotional bonds that motivate future altruistic behavior.
836
In contrast to cooperation in humans, therefore, contingent cooperation in animals may be
837
mediated by relatively simple proximate mechanisms based on the memory of previous
838
interactions rather than the expectation of future reward. Thus, reciprocity may be maintained by
839
a kind of partner-specific ‘emotional book-keeping’ (de Waal 2000; Schino & Aureli 2009) that
840
permits long-term tracking of multiple partners and facilitates cooperation in different behavioral
841
currencies. The resulting bonds that develop between preferred partners may motivate future
842
positive interactions without the need for explicit tabulation of favors given and returned, or
843
calculations of anticipated benefits (de Waal 2000; Aureli & Schaffner 2002; Aureli & Whiten
38
844
2003). For unrelated females who interact at low rates, a single grooming bout may temporarily
845
elevate a female’s positive emotions toward her partner sufficiently above baseline to influence
846
her immediate interactions with her. In contrast, grooming and support among females with close
847
bonds (who are also usually kin) should be less subject to immediate contingencies and less
848
influenced by single interactions.
849
Finally, it is important to emphasize that while the absence of punishment in animals
850
may derive in part from cognitive constraints, it is likely that a strict accounting of services given
851
and received is maladaptive in stable societies where individuals establish close bonds with
852
others and interact regularly in a variety of contexts. Indeed, although the cognitive constraints
853
that supposedly limit the occurrence of contingent cooperation in animals is often contrasted
854
with humans’ sensitivity to inequitable exchanges, human friendships are rarely contingency-
855
based. Numerous studies have shown that people seldom keep tabs of past costs and benefits in
856
interactions with regular partners (reviewed by Silk 2003). Although people become resentful
857
and dissatisfied when exchanges within a friendship are consistently unbalanced, tallying of
858
favors given and received are typically reserved for strangers and infrequent associates. It seems
859
probable that the relative rarity of contingent cooperation in animals stems less from the inability
860
to remember and keep track of interactions than from a similar tolerance of short-term inequities
861
among long-term partners.
862
863
864
h1. Future directions
We are only beginning to understand the many functions of cooperative behavior in
865
animals and the cognitive and emotional mechanisms that underlie them. There have been only a
866
handful of direct experimental tests of contingent cooperation under natural conditions, and we
39
867
as yet do not understand how supportive, reciprocal relationships emerge from single interactions
868
that are often asymmetrical. Similarly, there have as yet been few attempts to document the
869
reproductive benefits of cooperation and strong social bonds. Here, I highlight three of many
870
possible foci for future research.
871
872
h2 Cognition
873
The recognition of other individuals’ relationships can in principle be achieved through
874
relatively simple associative processes. At the same time, however, there is increasing evidence
875
that animals attribute simple mental states like motives and perspective to others. It therefore
876
seems possible that monkeys and apes – and perhaps also animals – may imbue knowledge of
877
others’ relationships with motives and emotions. In other words, they may not just recognize that
878
A associates with B, but also that A likes B. What, if anything, might this additional layer of
879
social knowledge buy them?
880
I have argued that contingent cooperation does not require complex cognition, such as the
881
ability to detect cheaters or to plan future cooperative acts based on memory of previous ones.
882
Nonetheless, some animals may engage in such mental activities. Non-human primates have
883
some capacity to access their knowledge states and to assess their certainty or uncertainty. Smith
884
et al. (this volume) suggest that metacognition permits animals to weigh alternative strategies in
885
novel contexts, and that it may serve as a precursor to reading others’ minds, as well. Although
886
playback experiments indicate that baboons remember the nature of specific interactions with
887
specific individuals, the extent to which this memory is explicit or episodic remains to be
888
determined. Similarly, some forms of cooperative behavior in animals – the boundary patrols of
889
chimpanzees in particular – are highly suggestive of shared intentionality, planning, and episodic
40
890
memory. To date, however, these cognitive abilities have been examined only under captive
891
conditions, in tests whose rules and constraints are determined by humans. A challenge for future
892
research will be to devise experimental means to examine mental state attribution and
893
metacognition under more natural conditions, in contexts where behavior has the potential to
894
influence reproductive success.
895
896
h2. Personality
897
Recent evidence from baboons has indicated that females vary in the strength and
898
stability of their social relationships, and that this variation contributes significantly to individual
899
variation in reproductive success. The fact that some females fail to maintain the same partners
900
over time also suggests that some individuals may be less skilled or motivated than others at
901
establishing and maintaining bonds. Although the proximate mechanisms underlying these
902
individual differences are not yet understood, they may well be related to personality traits
903
associated with attributes like anxiety, caution, and confidence. For example, in female primates
904
there tends to be no correlation between stress and dominance rank or number of kin. Instead,
905
glucocorticoid levels are more strongly influenced by the size and stability of a female’s social
906
network. Females tend to have lower glucocorticoid levels in months when their grooming
907
network is focused rather than diffuse (reviewed by Cheney &Seyfarth 2009; see also Brent et al.
908
2010).
909
These results emphasize that personality traits may exert a stronger influence on social
910
relationships and reproductive success than more obvious attributes like dominance rank. Some
911
individuals, for example, may be more adept than others at recruiting allies, reconciling with
912
others, and assessing the strength and stability of others’ relationships. Whatever the cause,
41
913
results point to the need for a stronger focus in future research on individual difference in
914
personality traits.
915
Personality traits are influenced not only by genetic factors but also by environmental
916
factors that affect gene expression. In both humans and rhesus macaques, for example, a specific
917
polymorphism in the serotonin transporter gene is associated with deficits in neurobiological
918
functioning and poor control of aggression (Suomi 2007). Monkeys carrying the deleterious
919
‘short’ allele are less willing than monkeys homozygous for the ‘long’ allele to gaze directly at
920
the faces and eyes of conspecifics, and they react more adversely to images of dominant animals
921
(Watson et al. 2009). Similarly, mothers carrying short versions of the allele are more likely to
922
be abusive, and both they and their infants exhibit higher cortisol levels (McCormack et al. 2009;
923
Maestripieri et al. 2009).
924
Indeed, maternal effects have been shown to have a profound impact on offspring
925
growth, dominance, HPA axis, and personality in a variety of species (reviewed by Onyango et
926
al. 2008; Jablonka & Raz 2009). For example, egg composition in birds is strongly influenced by
927
food availability, and these maternal effects can influence phenotypic expression across multiple
928
generations (Lindstrom 1999). Similarly, in female rodents social isolation and low levels of
929
maternal care during infancy reduce the expression of hypothalamic estrogen receptors, which in
930
turn results in decreased maternal behavior in these females as adults. These epigenetic effects
931
may persist across generations (Champagne & Mashmoodh 2009). In baboons, the adolescent
932
sons of dominant mothers exhibit significantly lower glucocorticoid levels than the sons of
933
subordinate mothers (Onyango et al. 2008). This effect persists beyond that age when males have
934
begun to out-rank females and suggests that maternal influences from infancy and perhaps even
935
gestation can have profound effects on the organization of the HPA axis. These influences may
42
936
stem in part from patterns of maternal rejection and protectiveness, which has long been known
937
to have long-term influences on offspring behavior (e.g. Hinde 1974).
938
Thus, genetic variation affecting factors such as serotonin and oxytocin reactivity,
939
anxiety, and social reward may influence the strength and stability of an individual’s social
940
bonds, which in turn exert epigenetic effects in offspring. Differences in personality traits may
941
well explain some of the individual variation in cooperative behavior.
942
943
944
h2. The integration of field and laboratory studies
There is currently some disconnect between results obtained in experiments with captive
945
animals and observations derived from field observations. For example, experiments
946
investigating contingent cooperation in captive animals have consistently yielded negative
947
results, while several conducted under more natural conditions have yielded more positive
948
results. In captivity chimpanzees seem relatively indifferent to inequitable outcomes to others
949
and themselves and fail to reciprocate favors in back-and-forth exchanges (Silk & House, this
950
volume). In the wild, however, chimpanzees exchange grooming, alliances, and meat-sharing
951
with specific long-term partners (Mitani 2006, 2009a). Although exchanges over the short term
952
are often asymmetrical, reciprocity emerges gradually over repeated interactions. In captivity,
953
tasks that require cooperation are easily disrupted by disparities in the participants’ dominance
954
ranks, the size of the rewards, and the degree to which rewards can be monopolized. In contrast,
955
under natural conditions chimpanzees not only share meat (if inequitably) but also regularly
956
participate in risky boundary patrols that are obligately cooperative. These discrepancies point to
957
the need both for more detailed investigations of cooperation in the wild and, in captivity, for
958
experiments that carry ecological and behavioral validity.
43
959
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