The expression of empathy in human's closest relatives, bonobos and chimpanzees: current and future directions.

Empathy is a complex, multi-dimensional capacity that facilitates the sharing and understanding of others' emotions. As our closest living relatives, bonobos (Pan paniscus) and chimpanzees (P. troglodytes) provide an opportunity to explore the origins of hominin social cognition, including empathy. Despite certain assumptions that bonobos and chimpanzees may differ empathically, these species appear to overlap considerably in certain socio-emotional responses related to empathy. However, few studies have systematically tested for species variation in Pan empathic or socio-emotional tendencies. To address this, we synthesise the growing literature on Pan empathy to inform our understanding of the selection pressures that may underlie the evolution of hominin empathy, and its expression in our last common ancestor. As bonobos and chimpanzees show overlaps in their expression of complex socio-emotional phenomena such as empathy, we propose that group comparisons may be as or more meaningful than species comparisons when it comes to understanding the evolutionary pressures for such behaviour. Furthermore, key differences, such as how humans and Pan communicate, appear to distinguish how we experience empathy compared to our closest living relatives.

The naturalistic approach to laughter in humans and other animals: towards a unified theory.

This opinion piece aims to tackle the biological, psychological, neural and cultural underpinnings of laughter from a naturalistic and evolutionary perspective. A naturalistic account of laughter requires the revaluation of two dogmas of a longstanding philosophical tradition, that is, the quintessential link between laughter and humour, and the uniquely human nature of this behaviour. In the spirit of Provine's and Panksepp's seminal studies, who firstly argued against the anti-naturalistic dogmas, here we review compelling evidence that (i) laughter is first and foremost a social behaviour aimed at regulating social relationships, easing social tensions and establishing social bonds, and that (ii) homologue and homoplasic behaviours of laughter exist in primates and rodents, who also share with humans the same underpinning neural circuitry. We make a case for the hypothesis that the contagiousness of laughter and its pervasive social infectiousness in everyday social interactions is mediated by a specific mirror mechanism. Finally, we argue that a naturalistic account of laughter should not be intended as an outright rejection of classic theories; rather, in the last part of the piece we argue that our perspective is potentially able to integrate previous viewpoints-including classic philosophical theories-ultimately providing a unified evolutionary explanation of laughter. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

My Fear Is Not, and Never Will Be, Your Fear: On Emotions and Feelings in Animals.

Do nonhuman animals (henceforth, animals) have emotions, and if so, are these similar to ours? This opinion piece aims to add to the recent debate about this question and provides a critical re-evaluation of what can be concluded about animal and human emotions. Emotions, and their cognitive interpretation, i.e., feelings, serve important survival functions. Emotions, we believe, can exist without feelings and are unconsciously influencing our behavior more than we think, and possibly more so than feelings do. Given that emotions are expressed in body and brain, they can be inferred from these measures. We view feelings primarily as private states, which may be similar across closely related species but remain mostly inaccessible to science. Still, combining data acquired through behavioral observation with data obtained from noninvasive techniques (e.g., eyetracking, thermography, hormonal samples) and from cognitive tasks (e.g., decision-making paradigms, cognitive bias, attentional bias) provides new information about the inner states of animals, and possibly about their feelings as well. Given that many other species show behavioral, neurophysiological, hormonal, and cognitive responses to valenced stimuli equivalent to human responses, it seems logical to speak of animal emotions and sometimes even of animal feelings. At the very least, the contemporary multi-method approach allows us to get closer than ever before. We conclude with recommendations on how the field should move forward.

The question of animal emotions.

Do animals, including invertebrates, have felt emotions and does this morally matter?

Modern theories of human evolution foreshadowed by Darwin's Descent of Man.

Charles Darwin's The Descent of Man, published 150 years ago, laid the grounds for scientific studies into human origins and evolution. Three of his insights have been reinforced by modern science. The first is that we share many characteristics (genetic, developmental, physiological, morphological, cognitive, and psychological) with our closest relatives, the anthropoid apes. The second is that humans have a talent for high-level cooperation reinforced by morality and social norms. The third is that we have greatly expanded the social learning capacity that we see already in other primates. Darwin's emphasis on the role of culture deserves special attention because during an increasingly unstable Pleistocene environment, cultural accumulation allowed changes in life history; increased cognition; and the appearance of language, social norms, and institutions.

How animals do business.

The field of comparative behavioural economics investigates decisions about the acquisition and exchange of goods and services. It does so in both humans and other species on the assumption that the cognition and emotions involved have a shared evolutionary background. This preface roughly defines the field and reviews a few selected early studies and concepts to offer a taste of what economic behaviour means in relation to species other than our own. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Chimpanzees (Pan troglodytes) tolerate some degree of inequity while cooperating but refuse to donate effort for nothing.

In cooperative hunting, a carcass cannot be divided equally, and hunts may be unsuccessful. We studied how chimpanzees respond to these two variables, working for unequal rewards and no rewards, which have been rarely included in experimental cooperative tasks. We presented chimpanzees with a task requiring three chimpanzees to work together and varied the reward structure in two separate experiments. In Experiment 1, two individuals received more rewards than the third, making the outcome unequal. We wanted to know if cooperation would continue or break down, and what mechanisms might maintain performance. Experiment 2 used equal rewards, but this time one or more locations were left unbaited on a proportion of trials. Thus, there was a chance of individuals working to receive nothing. In Experiment 1, the chimpanzees worked at a high rate, tolerating the unequal outcomes, with rank appearing to determine who got access to the higher-value locations. However, equal outcomes (used as a control) enhanced cooperative performance, most likely through motivational processes rather than the absence of inequity aversion. In Experiment 2, performance dropped off dramatically when the chimpanzees were not rewarded on every trial. Their strategy was irrational as donating effort would have led to more rewards in the long run for each individual. Our results lead to a hierarchy of performances by condition with equity > inequity > donating effort. Chimpanzees therefore tolerate mild inequity, but cannot tolerate receiving nothing when others are rewarded.

Do chimpanzees (Pan troglodytes) console a bereaved mother?

Comparative thanatology encompasses the study of death-related responses in non-human animals and aspires to elucidate the evolutionary origins of human behavior in the context of death. Many reports have revealed that humans are not the only species affected by the death of group members. Non-human primates in particular show behaviors such as congregating around the deceased, carrying the corpse for prolonged periods of time (predominantly mothers carrying dead infants), and inspecting the corpse for signs of life. Here, we extend the focus on death-related responses in non-human animals by exploring whether chimpanzees are inclined to console the bereaved: the individual(s) most closely associated with the deceased. We report a case in which a chimpanzee (Pan troglodytes) mother experienced the loss of her fully developed infant (presumed stillborn). Using observational data to compare the group members' behavior before and after the death, we found that a substantial number of group members selectively increased their affiliative expressions toward the bereaved mother. Moreover, on the day of the death, we observed heightened expressions of species-typical reassurance behaviors toward the bereaved mother. After ruling out several alternative explanations, we propose that many of the chimpanzees consoled the bereaved mother by means of affiliative and selective empathetic expressions.

Fish, mirrors, and a gradualist perspective on self-awareness.

The mirror mark test has encouraged a binary view of self-awareness according to which a few species possess this capacity whereas others do not. Given how evolution works, however, we need a more gradualist model of the various ways in which animals construe a self and respond to mirrors. The recent study on cleaner wrasses (Labroides dimidiatus) by Kohda and colleagues highlights this need by presenting results that, due to ambiguous behavior and the use of physically irritating marks, fall short of mirror self-recognition. The study suggests an intermediate level of mirror understanding, closer to that of monkeys than hominids.

Chimpanzees ( Pan troglodytes) Are More Averse to Social Than Nonsocial Risk.

Social risk is a domain of risk in which the costs, benefits, and uncertainty of an action depend on the behavior of another individual. Humans overvalue the costs of a socially risky decision when compared with that of purely economic risk. Here, we played a trust game with 8 female captive chimpanzees ( Pan troglodytes) to determine whether this bias exists in one of our closest living relatives. A correlation between an individual's social- and nonsocial-risk attitudes indicated stable individual variation, yet the chimpanzees were more averse to social than nonsocial risk. This indicates differences between social and economic decision making and emotional factors in social risk taking. In another experiment using the same paradigm, subjects played with several partners with whom they had varying relationships. Preexisting relationships did not impact the subjects' choices. Instead, the apes used a tit-for-tat strategy and were influenced by the outcome of early interactions with a partner.

Ethological observations of social behavior in the operating room.

Operating rooms (ORs) are inhabited by hierarchical, mixed-gender clinical teams that are often prone to conflict. In evolutionary terms, one expects more within- than between-gender rivalries, especially since the OR is a place where all sorts of social interactions occur, not merely technical communications. To document the full range of behavior, the present study used ethological observation techniques, recording live all social behavior by the team. Using an ethogram, 6,348 spontaneous social interactions and nontechnical communications were timestamped during 200 surgical procedures. Cooperation sequences (59.0%) were more frequent than conflict sequences (2.8%), which ranged from constructive differences of opinion to discord and distraction that could jeopardize patient safety. Behavior varied by clinical role and with the gender composition in the OR. Conflict was initiated mostly down the hierarchy between individuals several ranks apart. Cooperation tended to increase with a rising proportion of females in the OR, but the most pronounced effect concerned the interaction between both genders. If the attending surgeon's gender differed from that of the majority of other personnel in the OR, cooperation was significantly more common.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Novice chimpanzees cooperate successfully in the presence of experts, but may have limited understanding of the task.

Despite many observations of cooperation in nature, laboratory studies often fail to find careful coordination between individuals who are solving a cooperative task. Further, individuals tested are often naïve to cooperative tasks and there has been little exploration of partnerships with mixed expertise. In the current study, we examined acquisition of a cooperative pulling task in a group with both expert (N = 4) and novice (N = 11) chimpanzees (Pan troglodytes). We used five measures of competence and understanding: (1) success at the task, (2) latency to succeed, (3) efficiency, (4) uncoordinated pulling, and (5) pulling when a partner was present versus absent. We found that novices showed evidence of trial and error learning and developed competence over time, whereas the behavior of experts did not change throughout the course of the study. In addition to looking at patterns over time, we compared the performance of novices in this mixed-expertise group to an earlier study of novices in a group of all-novices. Novices in the mixed-expertise group pulled the same overall amount but for shorter periods of time, leading to higher pulling rates than individuals in the all-novice group. Taken together, these results suggest that learning in the presence of experts led to rapid and frequent success, although not necessarily careful coordination.

Long-term consistency in chimpanzee consolation behaviour reflects empathetic personalities.

In contrast to a wealth of human studies, little is known about the ontogeny and consistency of empathy-related capacities in other species. Consolation-post-conflict affiliation from uninvolved bystanders to distressed others-is a suggested marker of empathetic concern in non-human animals. Using longitudinal data comprising nearly a decade of observations on over 3000 conflict interactions in 44 chimpanzees (Pan troglodytes), we provide evidence for relatively stable individual differences in consolation behaviour. Across development, individuals consistently differ from one another in this trait, with higher consolatory tendencies predicting better social integration, a sign of social competence. Further, similar to recent results in other ape species, but in contrast to many human self-reported findings, older chimpanzees are less likely to console than are younger individuals. Overall, given the link between consolation and empathy, these findings help elucidate the development of individual socio-cognitive and -emotional abilities in one of our closest relatives.Non-human animals are known to exhibit behaviours suggestive of empathy, but the development and maintenance of these traits is unexplored. Here, Webb and colleagues quantify individual consolation tendencies over 10 years across two chimpanzee groups and show evidence of consistent 'empathetic personalities'.

Mammalian empathy: behavioural manifestations and neural basis.

Recent research on empathy in humans and other mammals seeks to dissociate emotional and cognitive empathy. These forms, however, remain interconnected in evolution, across species and at the level of neural mechanisms. New data have facilitated the development of empathy models such as the perception-action model (PAM) and mirror-neuron theories. According to the PAM, the emotional states of others are understood through personal, embodied representations that allow empathy and accuracy to increase based on the observer's past experiences. In this Review, we discuss the latest evidence from studies carried out across a wide range of species, including studies on yawn contagion, consolation, aid-giving and contagious physiological affect, and we summarize neuroscientific data on representations related to another's state.

Discrimination of emotional facial expressions by tufted capuchin monkeys (Sapajus apella).

Tufted or brown capuchin monkeys (Sapajus apella) have been shown to recognize conspecific faces as well as categorize them according to group membership. Little is known, though, about their capacity to differentiate between emotionally charged facial expressions or whether facial expressions are processed as a collection of features or configurally (i.e., as a whole). In 3 experiments, we examined whether tufted capuchins (a) differentiate photographs of neutral faces from either affiliative or agonistic expressions, (b) use relevant facial features to make such choices or view the expression as a whole, and (c) demonstrate an inversion effect for facial expressions suggestive of configural processing. Using an oddity paradigm presented on a computer touchscreen, we collected data from 9 adult and subadult monkeys. Subjects discriminated between emotional and neutral expressions with an exceptionally high success rate, including differentiating open-mouth threats from neutral expressions even when the latter contained varying degrees of visible teeth and mouth opening. They also showed an inversion effect for facial expressions, results that may indicate that quickly recognizing expressions does not originate solely from feature-based processing but likely a combination of relational processes. (PsycINFO Database Record