Romero T, Konno
A, Hasegawa T. Familiarity Bias and
Physiological Responses in Contagious Yawning by
Dogs Support Link to Empathy. PLoS ONE
2013;8(8):e71365
Abstract
On the basis of observational and
experimental evidence, several authors have
proposed that contagious yawn is linked to our
capacity for empathy, thus presenting a powerful
tool to explore the root of empathy in animal
evolution. The evidence for the occurrence of
contagious yawning and its link to empathy,
however, is meagre outside primates and only
recently domestic dogs have demonstrated this
ability when exposed to human yawns. Since dogs
are unusually skilful at reading human
communicative behaviors, it is unclear whether
this phenomenon is deeply rooted in the
evolutionary history of mammals or evolved de
novo in dogs as a result of domestication. Here
we show that wolves are capable of yawn
contagion, suggesting that such ability is a
common ancestral trait shared by other mammalian
taxa. Furthermore, the strength of the social
bond between the model and the subject
positively affected the frequency of contagious
yawning, suggesting that in wolves the
susceptibility of yawn contagion correlates with
the level of emotional proximity. Moreover,
female wolves showed a shorter reaction time
than males when observing yawns of close
associates, suggesting that females are more
responsive to their social stimuli. These
results are consistent with the claim that the
mechanism underlying contagious yawning relates
to the capacity for empathy and suggests that
basic building blocks of empathy might be
present in a wide range of species.
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.
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.
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 6SD percentage of
scan samples individuals affiliated with any
group members: females, 6.7263.31%; males,
7.2363.26%; Mann-Whitney U-test, Nf = 6, Nm = 6,
U = 17, z = 20.0801, 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 intraspecific 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 causeeffect 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.
