Long-term social bonds promote cooperation in the iterated Prisoner's Dilemma

Reciprocal altruism, one of the most probable explanations for cooperation among non-kin, has been modelled as a Prisoner''s Dilemma. According to this game, cooperation could evolve when individuals, who expect to play again, use conditional strategies like tit-for-tat or Pavlov. There is evidence that humans use such strategies to achieve mutual cooperation, but most controlled experiments with non-human animals have failed to find cooperation. One reason for this could be that subjects fail to cooperate because they behave as if they were to play only once. To assess this hypothesis, we conducted an experiment with monogamous zebra finches (Taeniopygia guttata) that were tested in a two-choice apparatus, with either their social partner or an experimental opponent of the opposite sex. We found that zebra finches maintained high levels of cooperation in an iterated Prisoner''s Dilemma game only when interacting with their social partner. Although other mechanisms may have contributed to the observed difference between the two treatments, our results support the hypothesis that animals do not systematically give in to the short-term temptation of cheating when long-term benefits exist. Thus, our findings contradict the commonly accepted idea that reciprocal altruism will be rare in non-human animals.     

An Investigation on Social Representations: Inanimate Agent Can Mislead Dogs (Canis familiaris) in a Food Choice Task

The nature of mental representation of others plays a crucial role in social interactions. Dogs present an ideal model species for the investigation of such mental representations because they develop social ties with both conspecifics and heterospecifics. Former studies found that dogs’ preference for larger food quantity could be reversed by humans who indicate the smaller quantity. The question is whether this social bias is restricted to human partners. We suggest that after a short positive social experience, an unfamiliar moving inanimate agent (UMO) can also change dogs’ choice between two food quantities. We tested four groups of dogs with different partners: In the (1) Helper UMO and (2) Helper UMO Control groups the partner was an interactive remote control car that helped the dog to obtain an otherwise unreachable food. In the (3) Non-helper UMO and (4) Human partner groups dogs had restricted interaction with the remote control car and the unfamiliar human partners. In the Human partner, Helper UMO and Helper UMO Control groups the partners were able to revert dogs’ choice for the small amount by indicating the small one, but the Non-helper UMO was not. We suggest that dogs are able to generalize their wide range of experiences with humans to another type of agent as well, based on the recognition of similarities in simple behavioural patterns.     

Calculated reciprocity? A comparative test with six primate species

Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject’s tendency to provide food to a partner was directly affected by the partner’s previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects’ probability to pull was not affected by the previous number of the partner’s pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.     

Food Transfer in Sichuan Snub-nosed Monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

Food transfer behavior provides a way to distribute food resources among individuals. It is not confined to kin, but also occurs among genetically unrelated individuals. Food transfer among nonkin may result from byproduct mutualism, reciprocal altruism (RA), or tolerated scrounging (TS). Sichuan snub-nosed monkeys (Rhinopithecus roxellana) exhibit a high level of social tolerance, and researchers have observed food transfer behavior in the wild. However, little is known about how tolerant social relations influence food transfer in this species. We recorded food-related interactions and social behavior in a group of captive Sichuan snub-nosed monkeys. Our findings suggest that the monkeys develop partner preference in food transfer behaviors. Moreover, individuals rely primarily on nonharassed approaches to claim food, suggesting that the TS model alone cannot explain their food transfer. Food transfer in this species may be a form of mutualism, in which an individual benefits on an immediate basis by fostering a preferred and tolerant relationship. However, we cannot rule out the possibility of reciprocal altruism. Future studies should record the temporal delay of social exchange to distinguish between mutualism and reciprocal altruism.     

Effects of Relatedness,Dominance, Age,and Association on Reciprocal Allogrooming by Captive Impala

Wild impala display a highly reciprocal allogrooming system that, by virtue of its frequency and high degree of reciprocity, is unique among ungulates. A herd of 35 free-ranging captive impala provided opportunity to examine the degree of reciprocity of allogrooming exchanges and the influence of relatedness, dominance, age and association on partner preferences and distribution of grooming between allogrooming partners. As in wild impala, the exchange of allogrooming bouts in the captive impala was highly reciprocal regardless of partners. Kinship and dominance had no influence on partner preference or distribution of grooming between partners. Although mothers showed a significant preference to allogroom with their unweaned offspring, this preference practically disappeared with older offspring. Age-mates (no greater than 6 mo apart) tended to associate with one another and spatial proximity was positively correlated with grooming partner preference. It was not clear whether impala actively sought out age-mates for grooming, or randomly chose grooming partners from nearby age-mates. The failure to find a role for kinship and dominance is counter to what has generally been found in most Old World terrestrial primate studies. The absence of pronounced social influences, coupled with the known effectiveness of grooming in removing ectoparasites, suggest that a utilitarian role, especially removal of ticks, is an important function of the impala reciprocal allogrooming system.     

The development of coordinated singing in cooperatively displaying long-tailed manakins

Long-tailed manakins (Chiroxiphia linearis) have a puzzlingsocial system in which teams of two males display cooperativelyin dispersed lek arenas, but only the alpha partner mates withvisiting females. One benefit of performing as a nonmatingpartner might be to gain experience as an "apprentice" to improvethe performance of the complex duet song and joint dance. Weexamined the relationship between the age of singers and twomeasures of singing performance: song variability and soundfrequency matching. Singing performance improved with age;variability in four song characteristics of males less than3 years old was greater than that in their older partners,and frequency matching increased with the age of the younger partner. Randomization tests of song samples from seven well-establishedteams showed that males did not track the song-to-song variationin their partners' singing. Another randomization test showedthat frequency matching by these teams was higher than thatof randomly paired partners. We considered three alternativehypotheses for the congruent songs: (1) short-term accommodation to the partner's song; (2) active choice of partners with similarintrinsic frequencies; and (3) long-term development of congruentsong through either practice or song copying. Our results andevidence from long-term monitoring of banded birds best supportthe hypothesis that frequency matching develops over severalyears during the complex and protracted process of partner formation. Nonmating males may benefit from increasing theircompetence at display, eventually enjoying increased matingsuccess when they inherit display sites from older males.     

Preferential learning from non-affiliated individuals in jackdaws (Corvus monedula)

It has been suggested that affiliated social relations may facilitate information transfer between individuals. We here tested this rarely examined hypothesis with juvenile and adult jackdaws (Corvus monedula) in three stimulus enhancement tasks, both in a non-food context (experiment 1) and in a food context (experiments 2 and 3). We first show that siblings and pair partners maintain stronger bonded social relations than do non-siblings and non-pair partners. We therefore tested individuals in sibling and non-sibling dyads and, later in ontogeny, in pair and non-pair dyads. Jackdaws either did not learn from any other conspecific (experiment 1), or they learned from non-affiliated individuals (non-siblings, non-pair partners in experiments 2 and 3). This may be related to two main characteristics of jackdaws' affiliated relationships. First, affiliates share food at a high rate and may rely on their knowledgeable partners to secure food rather than learning from them. Second, affiliates spend most time in close spatial proximity to each other which increases the probability that they simultaneously experience occurrences in their environment. Hence, spatially more distant individuals, which are more likely to be non-affiliated, face different foraging situations and may therefore provide more relevant information which may lead to selective social learning.     

Coordinated control of XerC and XerD catalytic activities during Holliday junction resolution

Site-specific recombinases XerC and XerD function in the segregation of circular bacterial replicons. In a recombining nucleoprotein complex containing two molecules each of XerC and XerD, coordinated reciprocal switches in recombinase activity ensure that only XerC or XerD is active at any one time. Mutated recombinases that carry sub?stitutions of a catalytic arginine residue stimulate cleavage and strand exchange mediated by the partner recombinase on DNA substrates that are normally recombined poorly by the partner. This is associated with a reciprocal impairment of the recombinase's own ability to initiate catalysis. The extent of this switch in catalysis is modulated by changes in recombination site sequence and is not a direct consequence of any catalytic defect. We propose that altered interactions between the mutated proteins and their wild-type partners lead to an increased level of an alternative Holliday junction intermediate that has a conformation appropriate for resolution by the partner recombinase. The results indicate how subtle changes in protein-DNA architecture at a Holliday junction can redirect recombination outcome.     

No Short‐Term Contingency Between Grooming and Food Tolerance in Barbary Macaques (Macaca sylvanus)

The exchange of services such as allo‐grooming, allo‐preening, food tolerance and agonistic support has been observed in a range of species. Two proximate mechanisms have been proposed to explain the exchanges of services in animals. First, an animal can give a service to a partner depending on how the partner behaved towards it in the recent past. This mechanism is usually tested by examining the within‐dyad temporal relation between events given and received over short time periods. Second, the partner choice mechanism assumes that animals give favours towards specific partners but not others, by comparing how each partner behaved towards them over longer time frames. As such, the partner choice mechanism does not make specific predictions on a temporal contingency between services received and given over short time frames. While there is evidence for a long‐term positive correlation between services exchanged in animals, results for short‐term contingencies between services given and received are mixed. Our study investigated the exchange of grooming for food tolerance in a partially provisioned group of Barbary macaques, by analysing the short‐term contingency between these events. Tolerance over food was compared immediately after grooming and in control condition, using food of different shareability. We found no evidence that grooming increases food tolerance or decrease aggression around food in the short term. Food tolerance was affected by the shareability of the food and the sex of the partners. The exchanges of grooming and food tolerance in non‐human primates may be little affected by recent single events. We suggest that long‐term exchanges between services given and received and social partner choice may play a more important role in explaining social interactions than short‐term contingent events.     

Emotional Bookkeeping and High Partner Selectivity Are Necessary for the Emergence of Partner-Specific Reciprocal Affiliation in an Agent-Based Model of Primate Groups

Primate affiliative relationships are differentiated, individual-specific and often reciprocal. However, the required cognitive abilities are still under debate. Recently, we introduced the EMO-model, in which two emotional dimensions regulate social behaviour: anxiety-FEAR and satisfaction-LIKE. Emotional bookkeeping is modelled by providing each individual with partner-specific LIKE attitudes in which the emotional experiences of earlier affiliations with others are accumulated. Individuals also possess fixed partner-specific FEAR attitudes, reflecting the stable dominance hierarchy. In this paper, we focus on one key parameter of the model, namely the degree of partner selectivity, i.e. the extent to which individuals rely on their LIKE attitudes when choosing affiliation partners. Studying the effect of partner selectivity on the emergent affiliative relationships, we found that at high selectivity, individuals restricted their affiliative behaviours more to similar-ranking individuals and that reciprocity of affiliation was enhanced. We compared the emotional bookkeeping model with a control model, in which individuals had fixed LIKE attitudes simply based on the (fixed) rank-distance, instead of dynamic LIKE attitudes based on earlier events. Results from the control model were very similar to the emotional bookkeeping model: high selectivity resulted in preference of similar-ranking partners and enhanced reciprocity. However, only in the emotional bookkeeping model did high selectivity result in the emergence of reciprocal affiliative relationships that were highly partner-specific. Moreover, in the emotional bookkeeping model, LIKE attitude predicted affiliative behaviour better than rank-distance, especially at high selectivity. Our model suggests that emotional bookkeeping is a likely candidate mechanism to underlie partner-specific reciprocal affiliation.     

Experiments on respect of possession and property in hamadryas baboons (Papio hamadryas)

The question of how useful concepts of possession and property are in analysing the relationship between baboons and objects was evaluated in five experimental situations. The results of laboratory experiments concerning the possession of a food container and experiments on possession of fruits confirmed the inhibition of the dominant partner to take food away from a lower-ranking companion. This inhibition always appeared in male-male dyads, while in male-female and female-female dyads, the extent of respect depended on the difference in dominance rank and the type of food. However, in a dominance test, where food pieces were thrown between both partners, the dominant did not allow the subordinate to take a single piece. Given the choice, males preferred neutral food-cans over cans previously used by their partner. In experiments in a field enclosure, whole one-male units preferred their own feeding place over that of another unit. The outcome of the two experiments concerning choice does not support the alternative explanation involving ‘familiar’ versus ‘new’, but does support the property hypothesis.     

Intranasal oxytocin increases social grooming and food sharing in the common vampire bat Desmodus rotundus

Intranasal oxytocin (OT) delivery has been used to non-invasively manipulate mammalian cooperative behavior. Such manipulations can potentially provide insight into both shared and species-specific mechanisms underlying cooperation. Vampire bats are remarkable for their high rates of allogrooming and the presence of regurgitated food sharing among adults. We administered intranasal OT to highly familiar captive vampire bats of varying relatedness to test for an effect on allogrooming and food sharing. We found that intranasal OT did not have a detectable effect on food-sharing occurrence, but it did increase the size of regurgitated food donations when controlling for dyad and amount of allogrooming. Intranasal OT in females increased the amount of allogrooming per partner and across all partners per trial, but not the number of partners. We also found that the peak effect of OT treatments occurred 30–50 min after administration, which is consistent with the reported latency for intranasal OT to affect relevant brain areas in rats and mice. Our results suggest that intranasal OT is a potential tool for influencing dyadic cooperative investments, but measuring prior social relationships may be necessary to interpret the results of hormonal manipulations of cooperative behavior and it may be difficult to alter partner choice in vampire bats using intranasal OT alone.     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

The good, the bad, and the rare: memory for partners in social interactions

For cooperation to evolve via direct reciprocity, individuals must track their partners' behavior to avoid exploitation. With increasing size of the interaction group, however, memory becomes error prone. To decrease memory effort, people could categorize partners into types, distinguishing cooperators and cheaters. We explored two ways in which people might preferentially track one partner type: remember cheaters or remember the rare type in the population. We assigned participants to one of three interaction groups which differed in the proportion of computer partners' types (defectors rare, equal proportion, or cooperators rare). We extended research on both hypotheses in two ways. First, participants experienced their partners repeatedly by interacting in Prisoner's Dilemma games. Second, we tested categorization of partners as cooperators or defectors in memory tests after a short and long retention interval (10 min and 1 week). Participants remembered rare partner types better than they remembered common ones at both retention intervals. We propose that the flexibility of responding to the environment suggests an ecologically rational memory strategy in social interactions.     

Same-Sex Gaze Attraction Influences Mate-Choice Copying in Humans

Mate-choice copying occurs when animals rely on the mating choices of others to inform their own mating decisions. The proximate mechanisms underlying mate-choice copying remain unknown. To address this question, we tracked the gaze of men and women as they viewed a series of photographs in which a potential mate was pictured beside an opposite-sex partner; the participants then indicated their willingness to engage in a long-term relationship with each potential mate. We found that both men and women expressed more interest in engaging in a relationship with a potential mate if that mate was paired with an attractive partner. Men and women''s attention to partners varied with partner attractiveness and this gaze attraction influenced their subsequent mate choices. These results highlight the prevalence of non-independent mate choice in humans and implicate social attention and reward circuitry in these decisions.     

Cooperation among Norway Rats: The Importance of Visual Cues for Reciprocal Cooperation,and the Role of Coercion

Some animals reciprocate help, but the underlying proximate mechanisms are largely unclear. Norway rats (Rattus norvegicus) have been shown to cooperate in a variant of the iterated prisoner's dilemma paradigm, yet it is unknown which sensory modalities they use. Visual information is often implicitly assumed to play a major role in social interactions, but primarily nocturnal species such as Norway rats may rely on different cues when deciding to reciprocate received help. We used an instrumental cooperative task to compare the test rats' propensity to reciprocate received help between two experimental conditions, with and without visual information exchange between social partners. Our results show that visual information is not required for reciprocal cooperation among social partners because even when it was lacking, test rats provided food significantly earlier to partners that had helped them to obtain food before than to those that had not done so. The mean decision speed did not differ between the two experimental conditions, with or without visual information. Social partners sometimes showed aggressive behaviour towards focal test individuals. When including this in the analyses to assess the possible role of aggression as a trigger of cooperation, aggression received from cooperators apparently reduced the cooperation propensity, whereas aggression received from defectors increased it. Hence, in addition to reciprocity, coercion seems to provide additional means to generate altruistic help in Norway rats.     

The Time Frame of Partner Choice in the Grooming Reciprocation of Cebus apella

Recent theoretical and experimental studies argued that reciprocity is constrained by the cognitive limitations of most animals and that, when reciprocation occurs, it should necessarily be short term. In this study, we examined the time frame of partner choice in the reciprocal grooming of captive female tufted capuchin monkeys ( Cebus apella ). Female capuchins groomed preferentially those individuals that overall groomed them most. Tufted capuchins did sometimes reciprocate grooming immediately. We quantified the time course and probability of immediate reciprocation, and excluded from the analysis cases of immediate reciprocation. We then showed that, even excluding immediate reciprocation, female capuchins still preferred to groom those individuals that groom them most. Our results show that partner choice is not necessarily based on immediate reciprocation and suggest that capuchins are able to reciprocate over longer time frames. These findings argue against the hypothesis that long-term reciprocation is absent in species lacking sophisticated cognitive abilities. We suggest that reciprocal altruism over long time frames relies on a system of emotional bookkeeping.     

Pair Swimming and Mutual Partner Guarding in Monogamous Butterflyfish (Pisces,Chaetodontidae): a Joint Advertisement for Territory

The ecology and social systems of Red Sea butterflyfish were studied along the Sinai coast. Distribution, population density and sociography indicate a preponderance of monogamy in all species, independent of reef zonation and seasonal or long-term changes of the reef environment. The social and mating systems are mutual monogamy; partners remain together for up to 6 years. Links between the monogamy and benthic habits of these fish are indicated by their feeding ecology and by a comparison with Indopacific plankton-feeding species, which usually occur in groups. Territories are defended pairwise. Pair partners nearly always remain within visual contact, but a species-typical distance apart. Pair swimming is independent of season or time of day. Experimental partner removals led to speedy replacement of mates. Possible causes of high partner permanency with little partner fidelity are discussed. In good habitats, single territorial adults do not occur. They would be unable to defend and maintain a territory over long periods. While cooperating in defence and maintenance of a territory, each individual can exploit the resources of the territory including availability of a mate. Pair swimming with mutual partner guarding is considered a joint territorial advertisement similar to duetting in birds; it minimizes agonistic interactions between territory holders. As butterflyfish have planktonic larvae without any broodcare, monogamy could not have evolved in response to broodcare activities as in many other vertebrate groups.     

Induced cooperation to access a shareable reward increases the hierarchical segregation of wild vervet monkeys

Until now cooperation experiments in primates have paid little attention to how cooperation can emerge and what effects are produced on the structure of a social group in nature. I performed field experiments with three groups of wild vervet monkeys in South Africa. I induced individuals to repeatedly approach and operate food containers. At least two individuals needed to operate the containers in order to get the reward. The recurrent partner associations observed before the experiment only partly predicted the forming of cooperative partnerships during the experiment. While most of the tested subjects cooperated with other partners, they preferred to do so with specific combinations of individuals and they tended not to mix with other group members outside these preferred partnerships. Cooperation therefore caused the relatively homogeneous networks I observed before the experiment to differentiate. Similar to a matching market, the food sharing partners selected each other limiting their choice. Interestingly neither sex nor age classes explained the specific partner matching. Kinship could not explain it either. Rather, higher ranking individuals cooperated with other higher ranking individuals, and lower ranking also matched among the same rank. This study reveals the key role dominance rank plays when food resources are patchy and can only be accessed through sharing with other individuals.     

Social behaviour of dogs encountering AIBO, an animal-like robot in a neutral and in a feeding situation

The use of animal-like autonomous robots might offer new possibilities in the study of animal interactions, if the subject recognises it as a social partner. In this paper we investigate whether AIBO, a dog-like robot of the Sony Corp. can be used for this purpose. Twenty-four adult and sixteen 4-5 months old pet dogs were tested in two situations where subjects encountered one of four different test-partners: (1) a remote controlled car; (2) an AIBO robot; (3) AIBO with a puppy-scented furry cover; and (4) a 2-month-old puppy. In the neutral situation the dog could interact freely with one of the partners for 1 min in a closed arena in the presence of its owner. In the feeding situation the encounters were started while the dog was eating food. Our results show that age and context influence the social behaviour of dogs. Further, we have found that although both age groups differentiated the living and non-living test-partners for some extent, the furry AIBO evoked significantly increased responses in comparison to the car. These experiments show the first steps towards the application of robots in behavioural studies, notwithstanding that at present AIBO's limited ability to move constrains its effectiveness as social partner for dogs.