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15 novembre 2009
 
Proc Natl Acad Sci USA
2009;106(46):19262-19267
Contagious yawning in gelada baboons
as a possible expression of empathy
Palagi E, Leone A, Mancini G, Ferrari PF.
Centro Interdipartimentale Museo di Storia Naturale e del Territorio
Università di Pisa Italy.

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Yawn contagion in humans has been proposed to be related to our capacity for empathy. It is presently unclear whether this capacity is uniquely human or shared with other primates, especially monkeys. Here, we show that in gelada baboons (Theropithecus gelada) yawning is contagious between individuals, especially those that are socially close, i.e., the contagiousness of yawning correlated with the level of grooming contact between individuals. This correlation persisted after controlling for the effect of spatial association. Thus, emotional proximity rather than spatial proximity best predicts yawn contagion. Adult females showed precise matching of different yawning types, which suggests a mirroring mechanism that activates shared representations. The present study also suggests that females have an enhanced sensitivity and emotional tuning toward companions. These findings are consistent with the view that contagious yawning reveals an emotional connection between individuals. This phenomenon, here demonstrated in monkeys, could be a building block for full-blown empathy.
 
-Demuru E, Palagi E. In Bonobos Yawn Contagion Is Higher among Kin and Friends. PLoS One. 2012; 7(11): e49613
-Leone A, Mignini M, Mancini G, Palagi E. Aggression does not increase friendly contacts among bystanders in geladas (Theropithecus gelada) Primates. 2010;51(4):299-305
-Leone A, Ferrari PF, Palagi E. Different yawns, different functions? Testing social hypotheses on spontaneous yawning in Theropithecus gelada. Scientific Reports 2014;4;4010
-Norscia I, Palagi E. Yawn Contagion and Empathy in Homo sapiens. PLoS ONE. 2011;6(12): e28472
-Norscia I, Demuru E, Palagi E. She more than he: gender bias supports the empathic nature of yawn contagion in Homo sapiens. R. Soc. open sci. 2016:3:150459. http://dx.doi.org/10.1098/rsos.150459
-Palagi E, Leone A, Mancini G, Ferrari PF. Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci USA. 2009;106(46):19262-19267
-Palagi E, Norscia I, Demuru E. Yawn contagion in humans and bonobos: emotional affinity matters more than species PeerJ 2:e519
-Zannella A, Stanyon R, Palagi E. Yawning and Social Styles: Different Functions in Tolerant and Despotic Macaques (Macaca tonkeana and Macaca fuscata). J Comp Psychol. 2017
-Zannella A, Norscia I, Stanyon R, Palagi E. Testing Yawning Hypotheses in Wild Populations of Two Strepsirrhine Species: Propithecus Verreauxi and Lemur Catta. Am J Primatol. 2015;77(11):1207-1215
 
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Yawning is a common phenomenon in vertebrates, and in primates it is present since birth (1). From an ethological point of view, yawning is one of the best examples of a fixed action pattern. Once started, a yawn is unstoppable and uncontainable. Motor patterns of yawning are stereotyped and occur in essentially the same form in different contexts, from resting to social interactions (2, 3). Yawning may also be a stress indicator and a sign of neurological pathologies (4). From a physiological perspective, it has been proposed that yawning maintains mental efficiency by regulating brain temperature through a cooling mechanism (5, 6).
 
There are several theories about the possible function of yawning (7, 8). Communication theories propose yawning as a way animals synchronize group behaviors during rest&endash;activity cycles or communicate drowsiness or stress. Arousal theories propose, instead, that yawning should help subjects maintain their attention levels and that it may have evolved to promote maintenance of vigilance and/or shared alertness (2, 9). In humans yawning is demonstrably contagious as it is easily triggered by seeing, hearing, reading, or simply thinking about another individual yawning (3, 10). More than 50% of human subjects yawned within a few minutes after having watched a video of a yawning person (10). The power of contagious yawning is suggested by interspecific effects (11), even though this phenomenon is still under debate (12). In chimpanzees (Pan troglodytes), yawning can be induced by observing a video of a conspecific yawn (13), even though in that study the contagious response was limited to a few of the tested individuals. Recently, however, Campbell et al. (14) demonstrated at the population level that chimpanzees show contagious yawning in response to 3D-animated chimpanzee yawns, thus confirming the results obtained in previous studies. In macaques (Macaca spp.), yawning responses elicited by the video of unfamiliar monkeys yawning were accompanied by selfscratching, perhaps indicative of increased anxiety (15). Although those are the first attempts to investigate the phenomenon of contagious yawning in nonhuman primates, the evidence remains meager, at least in monkeys, and more data are needed to better understand the natural or naturalistic conditions under which yawning can be elicited and the possible social functions of yawn contagion.
 
The infectiousness of yawning and the difficulty to suppress it when we observe someone else yawning are clear signs of a connection present between two or more individuals and suggest that this phenomenon might involve not only purely motor aspects of the behavior but also more subtle emotional channels. These observations have led some researchers to hypothesize a link between contagious yawning and empathy (16&endash;19). In humans, it has been reported that subjects showing higher levels of contagion to yawn stimuli also score higher in questionnaires evaluating empathy and mental state attribution (18). Although debated, there is no consensus about the possibility that nonhuman primates are capable of empathizing with others. However, there is a range of phenomena, from sensitivity to others' distress to reassuring behaviors from both experimental and observational studies, which suggest some level of empathy in nonhuman primates (20&endash;23). Moreover, in both humans and animals empathy is biased toward individuals who are more similar, familiar, or socially closer (24). It is assumed that shared representations are more easily activated the more two individuals have in common. Because empathy is biased toward such individuals, we expect that contagious yawning, if empathybased, should be similarly biased. Although the hypothetical link between contagious yawning and empathy is appealing, it has never been empirically tested in any species, including humans. Here, we report that yawning is contagious in a nonhuman primate, the gelada baboon, and that this response seems unrelated to external stressful events. Moreover, our data demonstrate that yawn contagion is more common between individuals with higher levels of affiliation, thus suggesting that the roots of empathy could may be present in nonhuman primates.
 
 
Discussion
 
The present findings indicate that yawning in gelada baboons is contagious and can be elicited via both visual and acoustic modalities. This latter result is in line with previous data (4) on contagious yawning by blind human subjects, thus suggesting the importance of multimodal perception in yawn triggering. Furthermore, activation of matched motor programs via different sensory modalities has been shown in monkeys. For example, pig-tailed macaques (Macaca nemestrina) increased feeding behavior, even though they were fully satiated, after just hearing another monkey eat without visual input (26). Motor facilitation to specific acoustic stimuli has also been demonstrated in the macaque motor cortex, suggesting that motor output may be facilitated by multiple sensory modalities (27). The contagion effect of yawning may be interpreted as a type of response occurring in highly social animals that need to synchronize behavioral activities (20). Coordinating activities among group members has an undoubted advantage because it promotes social cohesiveness. In fact, we observed such coordination in the social context of our baboons, when they were awake and relaxed, often coinciding with grooming sessions or with transitions from rest to activity, or vice versa. Yawn contagion was present only in adults. The absence in infants and juveniles has also been reported for humans, in which children aged younger than 5 years do not show this contagion (28). The relative insensitivity of immature subjects to yawning may reflect a developmental immaturity of their social cognitive skills and/or brain structures involved in processing social information. In most social animals, including primates, adults have the main role in group decision-making and regulating the group daily activities, whereas the young tend to passively follow adults, especially the mother (29). Thus, synchronizing and coordinating one's own behavior with that of conspecifics could be less relevant for young individuals, which are rather more sensitive to maintain proximity with their mothers in their first years of life before weaning (30).
 
The criteria we adopted for the analysis of contagion allowed us to exclude that yawning responses were elicited by any kind of stressful event. In fact, we excluded all yawning events associated with behavior indicative of stressful conditions (e.g., raised eye browse, self-scratching, self-grooming, body shaking, lip flip, urination, defecation, gravel digging, etc.). Even though yawn contagion requires the reenactment of a behavior, it cannot be considered an imitative or mimicry process because of the reflexive and stereotypical nature of this chain reaction. However, this phenomenon could be compatible with the idea of a common mechanism active during the perception and reenactment of yawning. The discovery of mirror neurons in macaques has prompted the idea that an action&endash; perception mechanism could be responsible for important cognitive functions such as action understanding, response facilitation, and other behavioral matching (31, 32). A human mirror mechanism for action understanding and imitation homologous to that of the macaque has been supported by several neurophysiological and brain imaging studies (33).
 
Only recently, however, has the hypothesis that a similar mechanism may account for contagious yawning been empirically investigated in humans. The findings obtained so far failed to find activation in the traditional parietal-premotor areas populated by mirror neurons. However, a more recent study (34) found that the observation of yawning in humans activates these specific areas. More data are clearly needed, but overall it seems imitation and contagion are different types of phenomena, even though they may share some neural mechanisms (34&endash;36). In the gelada baboons, yawn contagion was particularly evident when the analysis was limited to adult females, which also showed an additional feature: they tended to match the type of yawn. This finding further supports the notion that a neural mechanism involved in behavioral matching is probably involved in this phenomenon. If mirror neurons are involved in contagion they very likely can act, through an indirect pathway (32), on limbic structures and subcortical areas that are involved in the generation and control of the yawning motor patterns. From a social perspective, the matching responsiveness shown by gelada females may be interpreted in light of the female social network characteristic of this species. The relationships within the typical gelada one-male unit (OMU) revolve around adult females, who form the core of the cohesion and stability typical of OMUs (37). In some cases, the strength of female bonds suffices to maintain OMU integrity despite the absence of the male (25). Thus, the matching response recorded between females probably reflects the need and ability of females to stay in tune with each others' behavioral activities and to form coalitions and alliances based on a precise reading of others' behavior. An important implication of the present findings is that the contagion effect triggered by yawning has not only a main consequence to synchronize two individuals but it seems also to influence affective components of the behavior. Through the involuntary reenactment of an observed behavior, emotional states related to the behavior may be arise in the observer. This idea has been theorized by Preston and de Waal (24) and likely involves neural mechanisms that, during the perception of an action or of a facial expression, activate shared representations (31, 38).
 
Recently, this hypothesis has been tested in tufted capuchin monkeys (Cebus apella). When monkeys were being imitated by a human experimenter they increased their liking and interactions toward the imitator compared with a nonimitator (39). It has been proposed that in a highly social species, such as the capuchin monkey, activities are highly synchronized and this might provide a sufficient degree of behavioral matching to promote affiliative behaviors between individuals. Similar effects may be produced by yawn contagion. Even though our study could not disentangle the cause&endash;effect relationship between yawn contagion and affiliation, the correlation between the level of contagion and the rate of grooming suggests that yawn contagion is facilitated by an emotional connection between stimulus animals and receivers.
 
An alternative explanation, however, is that individuals who often groom each other have more opportunities to observe and catch the yawns of the other. However, reduced interindividual distances (measured by proximity and contact sitting) did not correlate with yawn contagion and the correlation between grooming and yawn contagiousness persisted after statistically controlling for spatial association. Thus, social closeness seems to predict yawn contagiousness, which is consistent with the idea that yawn contagion is mediated by empathy (24).
 
Another hypothesis, not necessarily mutually exclusive with the emotional connection hypothesis, is that yawn contagion in geladas can be a sign of mood convergence. Because gelada baboons are highly social animals, which behave in a highly synchronized and cohesive way, the capacity to communicate a sleepy mood may result in a better coordinated group activity for sleeping or waking. However, this hypothesis cannot explain the results presented here because the data were cleaned from the resting&endash;activity transition phases (mainly morning and evening) and included events that did not necessarily follow sleep-resting activities.
 
Yawning has been conserved in its stereotypic forms throughout mammals and other vertebrate taxa, demonstrating its important basic physiological function. In primates, its function has been extended to the social domain. The demand for synchronizing activities in highly social species requires that individuals read each others' behaviors and match it accurately. Matching one's own behavior with that of others, independently on whether this occurs consciously or not, has recently been shown to promote affiliation between individuals through an empathic connection (39). The presence of yawn contagion in gelada baboons and its relation with the degree of bonding between individuals suggests that in this species are probably present the basic components of the multilayered empathy well known of humans and, at least in part, of the great apes.