In humans, the distribution of yawn
contagion is shaped by social closeness with
strongly bonded pairs showing higher levels of
contagion than weakly bonded pairs. This
ethological finding led the authors to
hypothesize that the phenomenon of yawn
contagion may be the result of certain empathic
abilities, although in their most basal form.
Here, for the first time, we show the capacity
of bonobos (Pan paniscus) to respond to yawns of
conspecifics. Bonobos spontaneously yawned more
frequently during resting/relaxing compared to
social tension periods.
The results show that yawn contagion was
context independent suggesting that the
probability of yawning after observing others'
yawns is not affected by the propensity to
engage in spontaneous yawns. As it occurs in
humans, in bonobos the yawing response mostly
occurred within the first minute after the
perception of the stimulus. Finally, via a
Linear Mixed Model we tested the effect of
different variables (e.g., sex, rank,
relationship quality) on yawn contagion, which
increased when subjects were strongly bonded and
when the triggering subject was a female. The
importance of social bonding in shaping yawn
contagion in bonobos, as it occurs in humans, is
consistent with the hypothesis that empathy may
play a role in the modulation of this phenomenon
in both species.
The higher frequency of yawn contagion in
presence of a female as a triggering subject
supports the hypothesis that adult females not
only represent the relational and decisional
nucleus of the bonobo society, but also that
they play a key role in affecting the emotional
states of others.
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Palagi E. In Bonobos Yawn Contagion Is
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A, Mignini M, Mancini G, Palagi E.
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among bystanders in geladas (Theropithecus
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A, Ferrari PF, Palagi E. Different yawns,
different functions? Testing social hypotheses
on spontaneous yawning in Theropithecus gelada.
Scientific Reports 2014;4;4010
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Palagi E. Yawn Contagion and Empathy in Homo
sapiens. PLoS ONE. 2011;6(12): e28472
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I, Demuru E, Palagi E. She more than he:
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http://dx.doi.org/10.1098/rsos.150459
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J, Ariely D, Hare B. Bonobos respond
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A, Stanyon R, Palagi E. Yawning and Social
Styles: Different Functions in Tolerant and
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2015;77(11):1207-1215
Introduction
In humans (Homo sapiens), seeing, hearing,
reading, or simply thinking about another
individual yawning stimulates a similar response
in the observer [1]. About 50% of human
subjects yawn within a few minutes after
watching a video of a yawning person
[2]. Yawning can be induced in
chimpanzees (Pan troglodytes) by observing a
video of a conspecific yawning [3,4],
even when the ''conspecific'' is a 3D-animated
chimpanzee [5]. As for monkeys, yawn
contagion has been demonstrated via an
observational, highly standardized approach in
gelada baboons (Theropithecus gelada) living
under natural conditions [6]. Outside
the Primate Order, there have been some attempts
to investigate this phenomenon also in dogs
(Canis familiaris). The different authors, who
approached the topic in this species, gained
contrasting findings even on its mere presence
[7-10]. Hence, if yawn contagion is
present in dogs is still an open argument. Since
most yawn events occur in social contexts, it
has been hypothesized that the infectiousness of
yawning may be linked to emotional arousal
[11] and may have a communicative
function (the hypothesis states that yawn
contagion is a non-verbal form of communication
that synchronizes the behavior of a group, for
an extensive review see [12].
The ability to share emotional states, a
phenomenon known as empathy, relies on a
perception-action mechanism and is essential for
successful social interactions [13].
During the observation of a facial expression,
the observer involuntary re-enacts the same
motor pattern by recruiting neural mechanisms
that concurrently activate the same affective
state associated with that specific facial
expression [13-15]. Some recent studies
suggest that yawn contagion is based on a
similar mechanism and could reflect a basic form
of empathy, which can be tentatively defined as
the capacity to catch and feel in an unconscious
and automatic way an emotional state expressed
by another individual [6,16,17]. The
linkage between yawn contagion and empathy in
humans is supported by clinical, psychological,
neurobiological, and ethological clues. Subjects
suffering from empathy-related disorders, such
as autism or schizophrenia, show lower levels of
yawn contagion [18-21]; whereas,
subjects obtaining higher scores in
questionnaires evaluating empathy and mental
state attribution show higher rates of yawn
contagion [22]. From a neurobiological
perspective, several neuroimaging studies
support the empathic basis of yawn contagion
[23-25]. Viewing someone yawning
activates the posterior cingulate and precuneus,
areas known to be part of empathy networks
[23]. The relationship between yawn
contagion and emotional involvement is also
underlined by the activation of the ventromedial
prefrontal cortex, a region involved in the
empathic processes [26-28] and also
associated with the propensity to respond to a
yawn stimulus [25]. Therefore, although
evidence is still under debate [24],
mirror neurons [28,29] might be
recruited for yawn contagion. Mirror neurons
fire when an animal performs an action, as well
as when it perceives another animal performing
the same action [30,31]. Accordingly,
the mirror neuron system is important for
actionIntroduction In humans (Homo sapiens),
seeing, hearing, reading, or simply thinking
about another individual yawning stimulates a
similar response in the observer [1].
About 50% of human subjects yawn within a few
minutes after watching a video of a yawning
person [2]. Yawning can be induced in
chimpanzees (Pan troglodytes) by observing a
video of a conspecific yawning [3,4],
even when the ''conspecific'' is a 3D-animated
chimpanzee [5]. As for monkeys, yawn
contagion has been demonstrated via an
observational, highly standardized approach in
gelada baboons (Theropithecus gelada) living
under natural conditions [6]. Outside
the Primate Order, there have been some attempts
to investigate this phenomenon also in dogs
(Canis familiaris). The different authors, who
approached the topic in this species, gained
contrasting findings even on its mere presence
[7-10]. Hence, if yawn contagion is
present in dogs is still an open argument. Since
most yawn events occur in social contexts, it
has been hypothesized that the infectiousness of
yawning may be linked to emotional arousal
[11] and may have a communicative
function (the hypothesis states that yawn
contagion is a non-verbal form of communication
that synchronizes the behavior of a group, for
an extensive review see [12]).
The ability to share emotional states, a
phenomenon known as empathy, relies on a
perception-action mechanism and is essential for
successful social interactions [13].
During the observation of a facial expression,
the observer involuntary re-enacts the same
motor pattern by recruiting neural mechanisms
that concurrently activate the same affective
state associated with that specific facial
expression [13-15]. Some recent studies
suggest that yawn contagion is based on a
similar mechanism and could reflect a basic form
of empathy, which can be tentatively defined as
the capacity to catch and feel in an unconscious
and automatic way an emotional state expressed
by another individual [6,16,17]. The
linkage between yawn contagion and empathy in
humans is supported by clinical, psychological,
neurobiological, and ethological clues. Subjects
suffering from empathy-related disorders, such
as autism or schizophrenia, show lower levels of
yawn contagion [18-21]; whereas,
subjects obtaining higher scores in
questionnaires evaluating empathy and mental
state attribution show higher rates of yawn
contagion [22]. From a neurobiological
perspective, several neuroimaging studies
support the empathic basis of yawn contagion
[23-25]. Viewing someone yawning
activates the posterior cingulate and precuneus,
areas known to be part of empathy networks
[23]. The relationship between yawn
contagion and emotional involvement is also
underlined by the activation of the ventromedial
prefrontal cortex, a region involved in the
empathic processes [26-28] and also
associated with the propensity to respond to a
yawn stimulus [25]. Therefore, although
evidence is still under debate [24],
mirror neurons [28,29] might be
recruited for yawn contagion. Mirror neurons
fire when an animal performs an action, as well
as when it perceives another animal performing
the same action [30,31]. Accordingly,
the mirror neuron system is important for action
understanding, a prerequisite for empathy
[30-32], and may be part of the neural
network underlying imitative actions
[33-35]. From a behavioral point of
view, the positive correlation between yawn
contagion and social bonding, already
demonstrated in geladas [6] and humans
[16], fits the hypothesis that a link
between yawn contagion and empathy may exist.
The perceptionaction model predicts that in
social species, empathy is biased toward
individuals who are more similar, familiar, or
socially closer [13]. In our species,
yawn contagion and the degree of emotional
closeness are positively correlated such that
occurrence, frequency, and latency of the
response are distributed according to an
empathic gradient [13], which follows
the scheme: kin.close
friends.acquaintances.strangers
[16].
The only study on the frequency of yawn
contagion in nonhuman apes, although based on an
A then B design, indicates that it differs
between familiar and unfamiliar subjects
[36]. Even though they attended more to
the videos of unfamiliar subjects, chimpanzees
yawned more when watching yawns performed by
familiar than unfamiliar individuals, suggesting
an ingroup-outgroup bias in contagious yawning.
The authors discussed the finding as further
empirical evidence about contagious yawning as a
measure of empathy. However, to our knowledge,
no behavioral systematic study investigated the
linkage of yawn contagion and social closeness
among apes living in the same group and tested
under natural conditions.
Via a standardized observational approach we
investigated yawn contagion and its distribution
in a captive group of bonobos (Pan paniscus).
Bonobos are defined by the majority of the
authors [37-42] as a highly prosocial
and tolerant species, characterized by strong
affinitive relationships even among unrelated
subjects [37-39]. They show a vast
repertoire of social behaviors such as play
[40], socio-sexual interactions
[38], and consolation [37],
aimed at increasing the cohesiveness among group
members, especially among females (female bonded
society) [41,42]. Moreover, in a recent
study comparing the neural circuitry implicated
in social cognition in the two Pan species,
Rilling et al. [43] found that bonobos,
compared to chimpanzees, have more developed
cortical brain areas involved in perceiving
distress in both oneself and others, an
emotional state underpinning empathic abilities.
Compared to chimpanzees, bonobos also have a
larger pathway linking the amygdala with the
ventral anterior cingulate cortex, a pathway
implicated in both top-down control of
aggressive impulses, as well as bottom-up biases
against harming others [43]. As a whole,
such neurobiological findings strongly support
bonobos' empathic sensitivity and propensity to
prosociality. For all these reasons, the bonobo
is a good model species to test some hypotheses
about the possible linkage between yawn
contagion and certain empathic abilities,
although in their most basal form.
Here, we report that yawning is contagious
in Pan paniscus and that yawn contagion is
independent from the social context and from the
amount of spontaneous yawns performed. Moreover,
we found that contagion was higher when the
triggering subject was a female, as predicted
for a female bonded society. Finally, our data
show that in bonobos yawn contagion distribution
reflects what has been found in humans
[16], with kin and friend dyads showing
the highest level of yawn contagion.
Discussion
Our data show, for the first time, that
contagious yawning is also present in another
great ape species, Pan paniscus. The study,
conducted within a naturalistic framework,
permitted us to shed light on some interesting
aspects of the yawn contagion modality in this
species.
In bonobos the yawing response mostly
occurred within the first minute after the
perception of the yawn stimulus. This response
latency is similar to that observed in humans
[16] but differs from that of gelada
baboons, in which the yawn contagion typically
peaked in the second minute after the triggering
stimulus [6]. As a result of
phylogenetic inertia, the brain of non-human
apes shows more elements of similarity with that
of humans than with that of cercopithecoids
[46]. Even though the interpretation of
this finding has to be taken with caution, the
similarity of bonobo and human yawn response
latency might reflect the similarity of the
neural pathways underpinning yawn contagion in
the two species.
Spontaneous yawns were more frequent when
bonobos were free from environmental and social
stressors (relax context), but yawn contagion
was context independent, thus suggesting that
the probability of yawning after observing
others' yawns is not affected by the propensity
to engage in spontaneous yawns. Both in humans
and other animals, spontaneous and contagious
yawning may be driven by different mechanisms
[47]. Spontaneous yawning may be more
strictly linked to physiological factors such as
respiratory activity [48,49],
thermoregulation [50], changes in
vigilance/arousal levels [51- 53], and
sleep/wake transitions [54-56]. When a
triggering stimulus is present, the yawn
response seems to be disentangled from
physiological/contextual conditions (social
tension vs relax). This finding supports the
communicative hypothesis of yawn contagion
[6,12,16,36].
In bonobos, yawn contagion increased with
social closeness, thus mirroring what found in
Homo sapiens, in which emotional bonding and
kinship modulate yawn contagion as well
[16]. From an adaptive point of view,
yawn contagion (as other forms of unconscious
mimicry, see [17] for an extensive
review) can aid social groups to synchronize
their activities (communicative hypothesis of
yawn contagion) [2]. Yet, yawn
contagion, compared to other forms of
unconscious mimicry, seems to be enriched by an
emotional component [17], as it is
suggested by its higher frequency between
emotionally bonded subjects.
Although the argument is still under debate
[57], bonobos are generally recognized
by a wide array of authors as one of the most
prosocial and tolerant non-human primates
[39,42,58-62]. Roberts and Strayer
[63] found that emotional expressiveness
and anger are important predictors of empathy
for school-age children, and that empathy
strongly predicted prosocial behaviors
aggregated across methods and sources. As it has
been done for humans, a further hint supporting
a possible link between yawn contagion and
empathy in apes could arise from studies
(through both naturalistic and experimental
approaches) that correlate yawn contagion to
prosocial behaviours, which are hypothesized to
be empathy-related (e.g. consolation
[37,64,65] and targeted helping
[66,67]). Moreover, some authors
[68,69] demonstrated that in humans the
same mechanisms that cause empathy to enhance
prosocial behaviors should also cause it to
inhibit aggression and the expression of anger.
In this perspective, it would be interesting to
verify if, in the great apes, the subjects more
inclined to be infected by others' yawns are
also more inhibited to engage in aggressive
behavior.
Some authors suggested that an attention
bias (with observers paying closer attention to
familiar subjects rather than to unfamiliar
ones) could affect the yawning response
distribution [70]. Since it is extremely
difficult to quantify the attention level of a
subject under both experimental and naturalistic
conditions, we cannot exclude that an attention
bias might affect the studies on yawn contagion.
The only variable that can be controlled is the
unambiguous possibility to perceive the
stimulus, for that reason in this kind of
research the analysis has to be strictly limited
only to those events that are surely perceived.
Yet, some clues indicate that heightened arousal
(degree of physiological responsivity relative
to a baseline) is normally detected in response
to novelty, whereas diminished arousal is
observed in response to perceived familiarity
(habituation process), an evolutionary
adaptation, which has been interpreted by some
authors as a mechanism to avoid the overloading
of the attentional system [71].
Moreover, it has been recently demonstrated that
in patients with unilateral destruction of the
visual cortex (cortical blindness), ''a passive
exposure to unseen expressions evoked faster
facial reactions and higher arousal compared
with seen stimuli, therefore indicating that
emotional contagion occurs also when the
triggering stimulus cannot be consciously
perceived'' [72, p. 17661].
The evidence that yawn contagion is shaped
by social closeness is consistent with the
hypothesis that this phenomenon is a form of
emotional contagion relying on a basic form of
empathy. This association, already hypothesized
for geladas [6] and humans [16],
two phylogenetically distant species within the
Primate Order, suggests that it could be either
deeply rooted in the evolutionary history of the
taxon or the outcome of convergence. Our finding
on a non-human ape, the bonobo, supports the
idea that the link between yawn contagion and a
basic from of empathy is not due to evolutionary
convergence but it is, instead, a common
ancestral trait shared by monkeys and apes,
including humans.
The higher frequency of yawn contagion
between individuals belonging to different
genders and in presence of a female as a
triggering subject suggests that bonobo males
are more affectively reactive towards females,
who constitute the core of social groups
[73]. Massen and co-workers [4]
recently demonstrated that, in chimpanzees, male
yawns were far more contagious than those of
females. In addition, individuals of the
dominant and bonded sex (i.e. males in Pan
troglodytes, [74]) infected each other
at the highest levels. Even though our findings
have to be taken with caution due to the small
sample size of adult males, in bonobos yawn
contagion appears to support the hypothesis that
adult females not only represent the relational
and decisional nucleus of the society
[38], but also that they play a key role
in affecting the emotional states of
others.
In conclusion, even though we are
still far from a clear demonstration of a
linkage between yawn contagion and empathy, the
importance of social bonds in shaping bonobo
yawn contagion seems to support the hypothesis
that a basic form of empathy can play a role in
the modulation of this phenomenon. As for Homo
sapiens, yawn contagion in Pan paniscus is
amplified when an emotional involvement is
present, as it occurs among kin and
friends.
