Introduction

Empathy, the ability to share the feelings and sensations of others, is essential to engage in successful social interactions, coordinated activity, and cooperation toward shared goals [1]. Current evolutionary evidence suggests that empathy is a phenomenon with many intermediate forms, ranging from mere agitation at the distress of others to complex forms of perspective taking [2]–[6]. The data also suggest that empathy might be phylogenetically ancient [1]. However, evidence remains meagre, especially in non-primate species, and more data are needed from a wider range of taxa to better understand the evolution and complexity of empathic abilities in non-human animals. In this respect, contagious yawning, i.e., yawning after seeing or hearing another individual yawn, is an ideal candidate behavior to explore basic forms of empathy across species and different types of social systems.

Although contagious yawning is not in itself an emotional reaction, its occurrence has been clinically, psychologically, neurobiologically, and behaviorally linked to our capacity for empathy. For instance, in humans, contagious yawning has been reported to occur more frequently in individuals who score higher on questionnaires evaluating empathy [7] and less in clinical populations characterized by impaired empathic abilities such as autistic and schizotypic individuals [7], [8]. Yawning when seeing other people yawn has also been associated with activations in the same neural networks responsible for empathy and social skills, such as the ventromedial prefrontal cortex [9]–[11]. Finally, the mirror neuron system [12], [13] is activated when a person views or hears a yawn [10], [11], [14], though the role this system plays in eliciting the actual contagious event remains unclear.

Humans are not the only species that show contagious yawning. Recent studies in non-human primates have further supported the association between contagious yawning and empathy. Chimpanzees (Pan troglodytes), bonobos (Pan paniscus) and gelada baboons (Theropithecus gelada) have been reported to yawn in response to perceiving a conspecific yawning [15]–[20]. In these primate species, as well as in humans [21], yawn contagion occurs more frequently between individuals with a close social bond. These findings fit the empathy-based hypothesis of contagious yawning since similarity, familiarity, and closeness are known to facilitate empathy in both humans and non-humans [1], [4].

The evidence of contagious yawning, as well as its link to empathy, remains limited outside the primate order. Attempts to test the empathy-based, emotionally connected hypothesis of contagious yawning have only been done in the domestic dog (Canis lupus familiaris). Although initial exploration of this phenomenon yielded contradicting results [22]–[24], more recent findings are consistent with the view that dogs are not only able to yawn contagiously - at least when the stimulus presented is a live human yawn [22], [25], [26] - but also that their susceptibility to yawns is affected by the emotional proximity to the yawner. Two independent studies, one using audio stimuli [27] and another using visual stimuli [25], showed that dogs yawned more frequently after being exposed to familiar than to unfamiliar yawns.

That contagious yawning fits predictions derived from the empathy-based hypothesis in two phylogenetically distant species within the Mammalia class could suggest that the link between contagious yawning and empathy is deeply rooted in the evolutionary history of mammals. Alternatively, this could also be the result of convergent evolution. Unlike non-human primates or other canids, domestic dogs are unusually skilled at reading human social and communicative behaviors [28], [29]. For example, dogs show, to some extent, an understanding of human referential intentions expressed in communicative gestures [30], [31], and they respond to what humans can and cannot see in various situations [32]. Thus, it could be possible that dogs' ability to yawn contagiously evolved with the capacity for reading human communicative signals, representing a case of convergent social evolution between primates and dogs. Intriguingly, no study has demonstrated dog-to-dog contagious yawning [23], [24], suggesting that dogs may be predisposed to respond more intensively, or only, to human social cues rather than to those of conspecifics.

We studied the evolutionary emergence of contagious yawning and its link to empathy in mammals by examining the phenomenon in wolves (Canis lupus lupus). The wolf is an ideal model species to explore this phenomenon because it is the dog's closest phylogenetic relative and a highly social and cooperative species [33]. If contagious yawning is shared by other social mammals, we would expect it to be present in the wolf. In contrast, the absence of contagious yawning, or its link to empathy, in wolves would suggest that dogs' ability is an evolutionary novel skill, providing a case of behavioral convergence with primates. Using a highly standardized observational approach [19], we specifically investigated under naturalistic settings whether yawning is contagious in wolves and whether this response is biased toward close social partners, as the empathy-based hypothesis predicts.

Methods

Results

Occurrence of contagious yawning

Subjects yawned significantly more often during the yawn condition than during the control observation (Wilcoxon signed-rank test: Z  =  −3.059, n  =  12, p  =  0.002, Figure 1, Table S1 in File S1). Furthermore, when analyzing the effect of different factors on the occurrence of contagious yawning, the best-fitting model, which fits significantly better to the data than the null model, included only two uncorrelated variables: the type of observation and the head orientation of the subject (AICc  =  1068.4, χ²  =  204.82, df  =  3, p < 0.001). Yawning occurred significantly more often when the subjects were exposed to the yawn stimuli, compared to when the original yawner did not perform a yawn (yawn vs. control observation: β  =  2.218, SE  =  0.174, z  =  12.735, p < 0.001). Additionally, yawn occurrence was also affected by the head orientation of the subjects: subjects yawned contagiously more often when they were in visual contact with the yawner and less often when the cue was auditory but not visual (facing vs. not within sight: β  =  −1.301, SE  =  0.291, z  =  −4.461, p < 0.001; within sight vs. not within sight: β  =  −0.908, SE  =  0.233, z  =  −3.884, p < 0.001).

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Figure 1. Example of contagious yawning in wolves.

(a) An individual (on the right) yawned during a resting period. (b) Few seconds later, the subject (on the left) yawned contagiously. Photograph by Teresa Romero.

https://doi.org/10.1371/journal.pone.0105963.g001

Factors affecting the frequency of contagious yawning

When analyzing the factors that could explain the variation in the relative frequency of elicited yawns, the best-fitting model included only two predictor variables: social bond and head orientation (AICc  =  760.3, χ²  =  28.68, df  =  3, p < 0.001). Wolves yawned more often in response to yawns performed by close social partners than in response to yawns performed by other group members (β  =  0.375, SE  =  0.108, z  =  3.468, p < 0.001, Figure 2). Also, wolves' susceptibility to yawning was affected by their orientation towards the trigger, with subjects in visual contact yawning more frequently than those which could not see the trigger (facing vs. not within sight: β  =  −0.616, SE  =  0.183, z  =  −3.368, p < 0.001; within sight vs. not within sight: β  =  −0.573, SE  =  0.150, z  =  −3.812, p < 0.001).

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Figure 2. Average frequency of contagious yawning as a function of the social bond between the trigger and the subject.

https://doi.org/10.1371/journal.pone.0105963.g002

Social bond and contagious yawning

Since it is possible that receivers were only aware of the yawners' identity when they were in visual contact with them, we repeated the previous analysis including only bouts where contagious yawning was present, and the subject and the trigger were in visual contact (N  =  242). Again, wolves' susceptibility to yawn contagiously was affected by the strength of the social bond with the initial yawner (best-fitting GLMM: AICc  =  172.1, χ²  =  6.76, df  =  1, p  =  0.009), with wolves yawning more frequently to close social partners' yawns than to other individuals' yawns (β  =  0.277, SE  =  0.099, z  =  2.799, p  =  0.005).

We further investigated the effect of social bond on contagious yawning by exploring its effect on the latency to the first yawn response. Average latency to yawn contagiously was 9.0 seconds (SD  =  4.3). The LMM analysis showed that wolves' reaction time to yawn contagiously was affected by the strength of the social bond with the model. Overall, subjects' response latency increased as social bond closeness decreased (β  =  −0.217, SE  =  0.094, t  =  −2.309, p  =  0.034). This difference held only for females, however, because males' yawn latencies were not affected by the strength of the social bond with the trigger (social bond*subject's sex: β  =  0.116, SE  =  0.043, t  =  2.699, p  =  0.013, Figure 3).

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Figure 3. Average latency to yawn contagion for the interaction of social bond and sex of the subject.

https://doi.org/10.1371/journal.pone.0105963.g003

Discussion

The current study demonstrates that yawning in wolves is contagious and that, according to the empathy-based hypothesis, the strength of the social bond between the model and the subject correlated with the susceptibility to yawn contagiously. Although yawning is a widespread phenomenon among vertebrates, contagious yawning has only been documented in a few species. The communication hypothesis of contagious yawning states that yawn replication aids social animals in synchronizing behavioral and physiological states of the group [36]. For a highly social animal such as the wolf, coordinating activities has obvious adaptive advantages, since it promotes social cohesiveness of the pack. Unfortunately, we cannot directly test the communication hypothesis since yawns from motor-transitional contexts were excluded from the dataset. Studies from other taxa directly testing this hypothesis are also lacking, although indirect evidence has been found for gelada baboons [19] and domestic dogs [26]. There is also evidence that spontaneous yawning in humans and chimpanzees is related to a change in general activity levels [37], [38]. However, it remains to be seen whether yawns have any effect on the activity levels of other group members. Further research, especially in wild populations, should examine the regulating effect of yawning on synchronized group behavior in order to test its communicative function.

The present study is the first to demonstrate intraspecific contagious yawning in a carnivore species, suggesting that such ability might be deeply rooted in the Mammalia class. Although domestic dogs seem to yawn contagiously in response to human yawners [22], [25]–[27], no study has been able to demonstrate intraspecific (dog-to-dog) contagious yawning. Our finding of yawn contagion in wolves supports the notion that this ability is an adaptation for within-species social communication, which was later transferred to dog-human interactions. Furthermore, that phylogenetically distant species within the Mammalia class, i.e., primates and carnivores, are able to respond to conspecifics' yawns suggests that this response is a common ancestral trait shared by other mammalian social taxa.

Yawning has different communicative modalities (i.e., visual and audio), and although it is known that in some species yawning can be elicited via both cues [8], [10], [19], [27], [39] the exact prevalence of each modality is not clear. We found that yawn contagion occurred more frequently when the subjects were in visual contact with the initial yawner than when the trigger's yawns were out of sight. This result seems to emphasize the greater importance of visual than other sensory cues in wolves. An alternative explanation, however, is that individuals out of sight from the initial yawner were not exposed to any yawn-related stimulus. Although a yawn vocalization was sometimes audible to human observers, due to environmental constrains we were only able to reliably code visual cues as factors in affecting yawn contagion. However, the fact that significantly more yawns occurred even when the yawner was completely out of sight from the subject suggests that auditory cues might have been present and affected subjects' responses. This last result seems to indicate that contagious yawning in wolves may be elicited via auditory cues, which is in line with the idea that motor facilitation in human and non-human animals can be activated by a variety of sensory modes [36], [40], [41]. For instance, even reading about or thinking about yawns trigger yawns in humans [36].

The present study supports an empathy-based explanation of contagious yawning in wolves, as yawns occurred disproportionately when the stimulus was produced by parties socially close to the observer. These differences hold after statistically controlling for time spent in close spatial proximity and attention to the initial yawner. These last results indicate that contagious yawning in wolves is not mediated by the mere opportunity of observing the yawns of others, but rather underscored by affective components of the behavior. In both human and other animals, empathy is not equally aroused by the emotional signals of any individual, but rather is facilitated by similarity, familiarity, and social closeness [1], [4], [42], [43].

According to the Perception-Action model [4], the observation of another's emotional states automatically and unconsciously activates neural representations of similar states in the observer. The more similar and socially close two individuals are, the easier the identification with the partner [1]. In line with this hypothesis, several brain regions linked to contagious yawning are implicated in the simulation of actions, social behavior, and empathy [10], [11]. That the social closeness predicts the infectiousness of yawning in wolves is consistent with the hypothesis that this phenomenon is mediated by empathy. Thus, our results trace back to carnivores the link between contagious yawning and empathy, supporting the idea that basic building blocks of empathy might be present in a wide range of species.

Another point in favor of the empathy hypothesis is the observed sex differences in reaction time. Overall, female wolves responded quicker than males when the initial yawner was a close associate, suggesting that females were particularly responsive. Furthermore, the sex pattern observed in this study did not reflect simply sex differences in sociability, because in wolf society in general, as well as in our study in particular, females are not more affiliative than males (mean ±SD percentage of scan samples individuals affiliated with any group members: females, 6.72±3.31%; males, 7.23±3.26%; Mann-Whitney U-test, N_f  =  6, N_m  =  6, U  =  17, z  =  −0.0801, p  =  0.532). Although sexual dimorphism of yawning frequency has not been observed in humans [36], [44], our finding paralleled results from gelada baboons, where females, but not males, tend to match the type of yawn they observed [19]. Although our results should be taken with caution due to our small sample size, the observed sex difference in reaction time probably reflects the higher ability of female wolves to react to the emotional stimulus of their close associates.

In conclusion, this study provides the first evidence of intra-specific contagious yawning in a carnivore species, the wolf, which suggests that such ability may be widespread among mammals. In addition, our findings show that this phenomenon is modulated by the degree of bonding between individuals. In humans, conscious or unconscious matching of behaviors and facial expressions of others has been theorized to be central in emotionally connecting two individuals [45], [46]. Recently, this idea has received support from behavioral studies in monkeys [47], [48]. Therefore, to yawn when a social partner yawns could be advantageous to promote social connections and affiliative behaviors among individuals.

While an observational study cannot determine the exact cause-effect relationship, our results indicate that contagious yawning is modulated by emotional components of the behavior. These results paralleled previous observations in primates and domestic dogs, and are consistent with the claim that the mechanism underlying contagious yawning relates to the capacity for empathy, an ability that humans probably share with other species beyond primates. By demonstrating the occurrence of contagious yawning in a phylogenetically distant taxon and providing insights into the mechanism underlying this phenomenon, this study broadens our understanding of the evolutionary history of empathy.

Supporting Information

Acknowledgments

We thank the directors and employees of Tama Zoological Park for allowing us to run observations in their installations. We are also grateful to Matthew Campbell, Joshua M. Plotnik, and Sophie Wasserman for useful comments on a previous version of the manuscript.