Discrete friendship encounters

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Friendship pervades the human social landscape. These bonds are so important that disrupting them le to health problems, and difficulties forming or maintaining friendships attend neuropsychiatric disorders like autism and depression.

Other animals also have friends, suggesting that friendship is not solely a human invention but is instead an evolved trait.

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A neuroethological approach applies behavioral, neurobiological, and molecular techniques to explain friendship in terms of its underlying mechanisms, development, evolutionary origins, and biological function. Recent studies implicate a shared suite of neural circuits and neuromodulatory pathways in the formation, maintenance, and manipulation of friendships across humans and other animals.

Health consequences and reproductive advantages in mammals additionally suggest that friendship has adaptive benefits. We argue that understanding the neuroethology of friendship in humans and other animals brings us closer to knowing fully what it means to be human. Friendship is a hallmark of human behavior.

Friends may promote our financial success, 1 health, 2 and even survival. This may be because friendship has been deemed a human construct outside the realm of biology 7 or as merely an epiphenomenon of pair bonds and parental care. Work in nonhuman animals has perhaps done the most in terms of ushering in this new trend; ground-breaking have linked social bonds with reproductive success in mammals 910 and have shown that common neural and physiological mechanisms underlie social interactions in humans and other animals.

Here we discuss in detail the findings of the most recent research on the neuroethology of friendship. We largely focus on humans and other primates because this is where most research has been concentrated to date, but include substantial nods to other animals. A review of friendship would not be complete without addressing the puzzle posed by the evolution of cooperation and we also examine this complex issue. We end by highlighting some of the most pressing questions that remain unanswered in this burgeoning and important field.

We must begin by defining what we mean by friendshipwhich we use interchangeably with the term social bond throughout. The former is more commonly used in studies on humans and the latter in studies of other animals, yet both refer to the same concept.

Accordingly, we define friends as pairs of individuals that engage in bi-directional affiliative nonaggressive, nonreproductive interactions with such frequency and consistency so as to differentiate them from nonfriends. That is, compared to nonfriends, friends engage in affiliative interactions considerably more often and over greater periods of time. We specify that friendly interactions are nonreproductive so as to include sex that occurs in a non-reproductive context, as in bonobos, 19 although we acknowledge that reproductive and nonreproductive sex between heterosexual partners can be difficult to differentiate in practice.

Interactions should also be consistent over time; males and females that interact when the female is sexually receptive but not otherwise are not friends. But sexual partners that consistently engage in affiliative interactions over time are friends by this definition, married couples are often friends, which fits with folk wisdom that spouses should be best friends In highly social animals like rhesus macaques Macaca mulattaA friends groom each other and B provide each other with support in agonistic encounters against other group mates. C Affiliative behaviors positively predict reproductive output in this species, suggesting that social bonds are adaptive.

Friendship is underpinned by numerous neural and physiological mechanisms, and may require specific cognitive abilities, such as D gaze following, that allow individuals to successfully coordinate their actions with others and navigate a complex social world. Photo credits: Lauren J.

Our definition of friendship is thus one that focuses on the phenotype. Although tempting, we believe it best to steer clear of definitions that assume the involvement of specific proximate mechanisms e. Friendship can be based on different evolutionary strategies depending on the types of interactions involved or the identities of the social partners. Kin Discrete friendship encounters is an obvious potential explanation for affiliative interactions between relatives 71521 but cannot explain Discrete friendship encounters between nonrelatives.

This does not mean we should exclude affiliative relationships between kin from being defined as friends. Indeed, as we shall discuss, determining Discrete friendship encounters mechanism s upon which cooperation between friends operates is a major line of inquiry open to much debate. We also wish to avoid definitions based on emotional engagement e. We suspect some may disagree with our definition and we welcome this debate.

Yet we suggest that disputes over definitions are somewhat moot. The scientific study of friendship is in its infancy, thus limiting this review to strict definitions would be unhelpful and we have not done so. In addition, research need not be focused explicitly on friendship and thus reliant on a specific definition in order to contribute to our understanding of it.

Studies that improve our understanding of affiliative interactions in general, including the biological mechanisms upon which those interactions are based, are necessary components of the study of friendship. For friendships to form, individuals must first have access to others. In primates, Discrete friendship encounters ancestral state is one of solitary living. In a landmark paper, Shultz et al. Primates are unusual in their rarity of pair bonds, which are more common in other animals, particularly birds. Group living in primates is believed to have followed the shift from nocturnal to diurnal living as a means to defend against predators in a more visual world, 2325 whereas other factors, such as cooperative hunting in carnivores and cooperative breeding in birdsare thought to be the selective pressures driving group living in other taxa.

Affiliative tendencies have a heritable basis in humans, 26 marmots Marmota flaviventris27 and rhesus macaques Macaca mulatta 28 Fig. The relationship between genes and social behavior is, of course, mediated by the nervous system. The social brain hypothesis posits that group living created selective pressures for larger and more complex brains.

Social networks in three primate species. Nodes represent individuals; lines represent interactions between pairs of individuals. The thickness of the lines in A increase with the frequency of interaction. Arrows in C indicate whether named friendships were reciprocal. Individuals toward the center are more embedded in their social networks than those toward the periphery. Ties between closely related female rhesus macaques are highlighted in pink and demonstrate maternal kin bias A.

Social network position is heritable in humans 26 and rhesus macaques, 28 and has been associated with reproductive success in rhesus macaques 28 and chimpanzees. In a recent review, Seyfarth and Cheney 14 describe the marked increase in the diversity of taxa in which friendships have been reported in the last decade. As we summarize in Table 1social bonds exist in birds, ungulates, cetaceans, and primates. Many of these relationships are between closely related individuals. Mother—daughter pairs are the most common, followed by siblings.

In these primates, kin-biased affiliative interactions, often measured using grooming and proximity, are common. Even when animals disperse from their natal groups, and are thus less likely to encounter close relatives in their lifetimes, relatives are more likely to form social bonds than nonrelatives chimpanzees Pan troglodytes43 but see Ref. Animals that are close in age are also frequent social partners.

In many species, the highest ranking male s sires the majority of offspring in a given year, and individuals that are close in age are often paternal siblings. Note: Although we intend this table to be comprehensive, species for which social relationships have been documented but little studied may be absent.

Additionally, we expect many species closely related to those represented also exhibit social relationships e. But friends are not always related. Horses Equus caballus live in groups composed of a single stallion and several unrelated females. Discrete friendship encounters, pairs of unrelated females form differentiated affiliative relationships. People may be unique in the extent to which friends are unrelated.

In summary, many animals form friendships with conspecifics. Social bonds are often between related individuals, but bonds between nonrelatives are not uncommon. Further research in a wider variety of taxa is required to determine whether friendship is a feature of all species that form stable social groups.

Questions also remain about the impact of group composition. Apart from some exceptions, are individuals only friends with nonrelatives when kin are unavailable? To answer Discrete friendship encounters question, we need comprehensive data on within-group relatedness across many taxa. To form friendships, animals must recognize the other members of their social group as unique individuals.

Social animals must also keep track of the quality of their relationships with others; that is, are they friends or foes? In order to distinguish each other as unique individuals, animals must learn the unique recognition cues of others and use those cues to identify those individuals in the future. Animals not only recognize their conspecifics, they also remember them. Female vervet monkeys Chlorocebus aethiopsand chacma baboons Papio hamadryas ursinus discriminate the alarm calls of group mates that recently groomed them compared to those that did not.

Humans remember and also maintain friendships despite long periods of separation; young adults living long distances apart remain friends for 8 years or more. These false-positive kin-recognition errors i. To select, acquire, and maintain friends requires information about others.

But what motivates animals to obtain social information, and how do they do it? Many animals attribute reward value to social information.

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Both humans and other primates find social stimuli intrinsically rewarding, and certain types of social stimuli are more interesting and reinforcing than others. Consistent with these observations are findings that social information activates reward-related areas of the brain, including the anterior cingulate cortex ACCthe orbitofrontal cortex OFCthe nucleus accumbens, and the caudate nucleus. For instance, when rhesus macaques were asked to choose between juice rewards and information about others, a small proportion of neurons in the OFC responded to juice rewards, while another, greater, and nonoverlapping proportion responded to social information.

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Outside the laboratory, animals are not conveniently presented with social information, but must go out and get it. Just like an animal foraging for food amongst sparsely distributed patches, 84 an animal searching for social information must weigh the benefits of obtaining such information against the costs, which include missed opportunities to eat, drink, or sleep.

Discrete friendship encounters

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