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Introduction
Most behavioral and cognitive studies have
used the most sophisticated human abilities
(e.g., theory of mind and language) as the main
ground to make comparative arguments. Yet, this
top-down approach has contributed to drawing the
line between human and other animals' skills.
Indeed, selecting the emotional and cognitive
"pinnacles of mental evolution" the human brain
(sensu de Waal & Ferrari, 2010, p. 201) can
shed light on unique human traits but not on the
common basic mechanisms underlying the more
complex ones (de Waal & Ferrari, 2010; Hecht
et al., 2012). While the hominin fossil record
cannot give us any clues on the social and
emotional abilities that may have paved the way
for the emergence of human empathy, studying
synchronous behaviours and body resonance (e.g.,
laughing, rapid facial mimicry, yawning;
Provine, 2012; Davila-Ross, Menzler &
Zimmermann, 2008; Mancini, Ferrari & Palagi,
2013a) in our closest living relatives may
provide valuable information about how empathy
evolved.
Empathy is a multilayered phenomenon, whose
shared basal forms represent the pre-existing
framework in which more complex emotional and
cognitive processes are nestled (Preston &
de Waal, 2002; de Waal, 2008). Perceiving and
sharing others' emotions, the so called
"affective empathy", is a phylogenetically old
capacity. Affective empathy is an automatic
process and may come about through emotional
contagion (de Waal, 2008). At a higher layer of
the empathic sphere, we find "cognitive empathy"
which requires self-other differentiation,
perspective-taking and mental state attribution,
basic capacities to infer others' emotional
states. Affective and cognitive empathy
dissociate in humans with the former preceding
the latter both ontogenetically and
phylogenetically (Decety, 2010). Humans show the
most complex form of empathy and, therefore, are
commonly deemed as the most empathic species
(Preston & de Waal, 2002; Decety &
Jackson, 2004; Decety & Cowell, 2014).
However, no quantitative, direct
inter-specific comparison has ever been made to
actually demonstrate that this assumption is
true at each floor of the empathic building.
Recent findings endorse that other animals show
affective empathy (Palagi et al., 2009; de Waal,
2012a; Panksepp & Panksepp, 2013). In this
view, cross-species research is needed to
explore empathy capacities as a bottom-up,
emotional and developmental process of the brain
(de Waal, 2012b). According to several
neurobiological (Cooper et al., 2012; Haker et
al., 2013), psychological (Lehmann, 1979; Platek
et al., 2003) and ethological findings (Palagi
et al., 2009; Campbell & de Waal, 2011;
Campbell & de Waal, 2014; Romero, Konno
& Hasegawa, 2013) yawn contagion is an
empathy-related phenomenon. Specifically, yawn
contagion is a form of emotional contagion,
which represents the most basal layer of the
empathic domain (e.g., see the "Russian Doll
Model" in de Waal, 2008; Preston & de Waal,
2002; Hatfield, Rapson & Le, 2009). Several
good reasons make the yawn and its contagion
excellent phenomena to explore the evolutionary
roots of empathy.
Due to its evolutionary antiquity, a yawn
can be easily detected and quantified, appearing
morphologically identical across many different
vertebrate taxa and, consequently, withdrawing
the risk of any subjective interpretation
(Provine, 2005). Therefore, the plesiomorphic
nature of yawning enables cross-species research
(Baenninger, 1987; Baenninger, 1997; Deputte,
1994; Guggisberg et al., 2010). Yawning is
automatic, unstoppable and easily recognisable
also when people try to hide or inhibit it due
to cultural constraints (Lehmann, 1979). These
features make this behaviour an honest signal
and, therefore, highly reliable (Provine,
1986).
Yawn contagion is obvious in human
beings&emdash;about 50 percent respond to video
stimuli of yawning faces (Provine,
1986)&emdash;and seems to be based on a
perception-action mechanism (Preston & de
Waal, 2002; de Waal, 2012c), which consists in
the involuntary re-enactment of an observed
facial expression and creates shared
representations. Neurophysiological evidence of
this coupling has derived from the discovery of
mirror neurons (di Pellegrino et al., 1992),
recently associated with yawn contagion (Cooper
et al., 2012; Haker et al., 2013). Therefore,
yawn contagion provides a "low-tech" but
significant evidence of mirror-like phenomena.
Mirror neurons, firstly described in the
pre-frontal cortex of the rhesus macaque, fires
when the subject either performs a motor action
or observes the same action performed by another
subject (Gallese et al., 1996; Ferrari et al.,
2003). A mirror system, homologous to that of
macaques, has been later discovered in humans
(Rizzolatti & Craighero, 2004). The mirror
mechanism (or motor mimicry), not requiring any
kind of conscious awareness, creates an
emotional bridge and, thanks to it, two
individuals can synchronize their affective
states (Hatfield, Rapson & Le, 2009). This
emotional bridge, in turn, fosters mirroring and
triggers positive feedback which constitutes the
core of social affinity. Such feedback is more
easily activated when subjects sharing a strong
empathic bonding are involved. While a positive
attachment enhances body and emotional resonance
(e.g., emotional reactions, unconscious mimicry,
self-other overlap and shared representations),
a negative attachment or a prejudice can inhibit
or suppress it (Xu et al., 2009; Avenanti,
Sirigu & Aglioti, 2010). In humans, when the
attachment is profoundly negative (as in case of
defectors, enemies, competitors) empathy can
even turn into Schadenfreude that is feeling
pleasure from the sufferings of others (de Waal,
2008; Decety & Cowell, 2014). This emotional
circuitry, in its positive and negative form,
has been found not only in humans (Singer et
al., 2006; Pfeifer et al., 2008) but also in
monkeys (Masserman, Wechkin & Terris, 1964;
Palagi et al., 2009; Mancini, Ferrari &
Palagi, 2013a; Mancini, Ferrari & Palagi,
2013b; Ferrari, Bonini & Fogassi, 2009;
Paukner et al., 2009) and apes (Anderson,
Myowa-Yamakoshi & Matsuzawa, 2004;
Davila-Ross, Menzler & Zimmermann, 2008;
Campbell & de Waal, 2011; Campbell & de
Waal, 2014).
In humans (Homo sapiens) and one of its
closest living phylogenetic relatives, the
bonobo (Pan paniscus), yawn contagion is present
and significantly affected by the emotional
closeness linking the responder to the first
yawner (the trigger). In the two species, the
yawn response is most likely when the yawning
stimulus comes from kin or friends (Norscia
& Palagi, 2011; Demuru & Palagi, 2012).
Since both in humans and bonobos yawn contagion
is a socially modulated phenomenon, these
species are good models to test some hypotheses
on the evolutionary origins of the linkage
between yawn contagion and empathy. The
opportunity provided by yawn contagion to apply
the same unit of measurement and identical
operational definitions permits to directly
compare human empathy with that of other
species. Indeed, most of the studies on empathic
capacities in Homo sapiens have been carried out
through questionnaires used to measure
self-reported scores of empathy. This approach
bears the risk of overestimating the human
empathic potential and leads to the
unfeasibility of comparing it to that of other
species (Lawrence et al., 2004).
As a whole, the possibility of employing a
highly straightforward behaviour, such as
yawning, to explore a highly complex phenomenon,
such as empathy, represents a unique opportunity
to investigate and compare empathy in human and
non-human species (de Waal, 2012b).
Theoretically, humans could appear as the
most empathic species not because they
experience greater emotional contagion
(affective empathy) but because they can better
understand others' perspective and simulate
others' emotional experiences (cognitive
empathy). Indeed, empathy is a construct
comprising dissociable components interacting
and operating in parallel (Decety & Cowell,
2014). Cognitive empathy can be impaired in
autistic subjects (Dziobek et al., 2008; Usui et
al., 2013) whereas emotional empathy can be
dramatically impaired in narcissistic
individuals (Ritter et al., 2011), criminal
psychopaths (Woodworth & Porter, 2002),
rapists (Englander, 2007), and child molesters
(Marshall, Hamilton & Fernandez, 2001). Yet,
both emotional and cognitive empathy contribute
to physiological human empathy (Cox et al.,
2011; Decety & Cowell, 2014). Therefore, if
humans are actually the most empathic species,
they should possess the highest empathic
response starting with emotional contagion, the
ground level of affective empathy.
We tested this hypothesis by comparing our
species with bonobos, which diverged from the
human line about 5-7 mya (Fleagle, 2013). We
expect that the frequency of yawn response is
always higher in humans than in bonobos,
whatever the relationship quality linking the
responder to the trigger. Since the time
elapsing from the yawn stimulus to the response
can be reduced when the social bond is strong
(Norscia & Palagi, 2011), we also expect
that the emotional affinity linking the subjects
affects, more in humans than in bonobos, the
promptness of the yawn response.
The inter-specific analysis of the overall
frequency of yawn contagion did not reveal any
difference between human and bonobo response
susceptibility. The inter-species comparison
revealed a higher promptness in humans than in
bonobos, who showed a longer tail-effect in
their response latency. However, both species
concentrated their responses within the first
minute after perceiving the stimulus yawn (Fig.
1). As yawn contagion is the expression of a
mirror-like phenomenon (Cooper et al., 2012;
Haker et al., 2013), our findings suggest that
not only is yawn contagion well-rooted in the
biology of bonobos and humans but also that the
neural processes underlying and modulating yawn
contagion might have been already present in the
most recent common ancestor of the two species
(5-7 mya, Fleagle, 2013). The similar
sensitivity to others' yawns shown by the two
species is probably due to similar selective
pressures. In fact, both species are
characterized by obligate gregariousness based
on one of the most complex forms of social
structure: the fission-fusion system (Aureli et
al., 2008). Behavioural (Couzin, 2007) and
emotional synchronization (S˙pinka, 2012) has
been playing a pivotal role in favouring and
shaping the evolutionary pathways leading to
social living (Video S1). Synchronizing with
others requires the ability to mirror their
motor actions, to experience their emotional
states and, consequently, to act in the
appropriate manner. In this process familiarity
makes the difference. Our intra-specific
analysis demonstrated that yawn contagion is a
socially modulated phenomenon, with strongly
bonded subjects showing a higher susceptibility
than weakly bonded subjects, thus confirming
previous results (humans, Norscia & Palagi,
2011; bonobos, Demuru & Palagi, 2012). In
this respect, the degree of contagion of around
50% reported by previous studies using videos of
strangers' yawns as stimuli (Provine, 2005) may
be a conservative estimate.
The social modulation of yawn contagion has
been proven also in the congeneric species of
bonobos, the chimpanzee (Pan troglodytes).
Chimpanzees are more susceptible to respond to
videos showing yawns performed by in-group than
by out-group members (Campbell & de Waal,
2011). This result is in line with a great body
of research on human in-group/out-group bias
that affects numerous empathy-driven behavioural
and emotional reactions (Bourgeois & Hess,
2008; Xu et al., 2009; Avenanti, Sirigu &
Aglioti, 2010). Recently, Campbell & de Waal
(2014) also found that the rate of chimpanzee
response to others' yawns was similar when the
stimulus came from an in-group chimpanzee and
from a human subject, thus demonstrating that
the chimpanzee involuntary empathic response
goes beyond the species boundary, as it occurs
in humans (Phillips, 2009). Yet, no evidence of
a social modulation in chimpanzee yawn contagion
emerged as a function of the relationship
quality shared between the responder and the
familiar trigger (Massen, Vermunt & Sterck,
2012). Both neuroanatomical (Rilling et al.,
2012) and behavioral features (Hare, Wobber
& Wrangham, 2012) can account for the
different effect of the relationship quality on
chimpanzee and bonobo yawn contagion. Compared
to chimpanzees, bonobos seem to show a different
emotional and affective sensitivity (Furuichi,
2011; de Waal & Lanting, 1997; Hare et al.,
2007) and a milder competitive propensity (Kano,
1992; Tan & Hare, 2013). Moreover, genetic
findings revealed that a DNA segment regulating
the responses to a hormone involved in social
bonding (vasopressin) is present in humans and
bonobos, but can be absent in chimpanzees
(Hammock & Young, 2005). However, the
different effects of the relationship quality on
yawn contagion in the two Pan species has to be
taken cautiously due to the different
methodological approaches used to verify and
quantify the phenomenon (video
stimulus&emdash;Massen, Vermunt & Sterck,
2012; living stimulus&emdash;Demuru &
Palagi, 2012).
At the inter-specific level, striking
differences emerged in the social modulation of
human and bonobo yawn contagion. While strong
and weak relationships between individuals had
to be assessed according to species-specific
criteria (see Methods section), the previous
works on bonobos (Demuru & Palagi, 2012) and
humans (Norscia & Palagi, 2011) indicate
that the strong-weak categorization produces a
similar effect on yawn contagion in either
species, with yawn contagion being highest
between individuals sharing strong
relationships. This result is confirmed in this
study. Compared to bonobos, the human
susceptibility (Fig. 2) and promptness (Fig. 3)
to others' yawns were significantly more
potentiated when kin and friends were involved.
Humans' responses were more frequent and faster
when the trigger and the responder shared a
strong emotional bond. On the other hand,
susceptibility and promptness incredibly
overlapped between the two species when a strong
emotional involvement between subjects was
lacking, thus indicating that emotional
contagion is not always highest in humans. It is
worth remarking that these findings would have
been impossible to detect if limiting the
analysis to the intra-specific level.
What explains the difference in yawn
contagion between species is the deepness of the
emotional affinity linking the subjects.
Compared to bonobos, humans show a different
degree of sensitivity at the most basal layer of
empathy, but only when they are strongly
emotionally involved. Moreover, the latency of
yawn contagion is socially modulated in humans
(the stronger the emotional involvement, the
faster the response) but not in bonobos.
Therefore, the positive feedback linking
emotional affinity and the mirroring process is
more easily and rapidly activated in humans than
in bonobos. Such over-activation explains not
only the human potentiated yawning response, but
also other kinds of unconscious mimicry
response, such as happy, pain or angry facial
expressions (Chiao et al., 2008). Minagawa-Kawai
and coworkers (2009) investigated the response
latency of smiles in mother-infant pairs and
found neurobiological support for the
"over-activation" hypothesis. The faster
response was associated with an increased
activation in the regions around the
orbitofrontal cortex in mothers while viewing
their own infant's smile compared to an
unfamiliar infant's smile. In these mothers,
specific neuronal regions involved in positive
emotional regulation were activated by both
viewing familiar and unfamiliar infants but the
magnitude of activation was greater when
affective attachment was involved. A similar
neuro-ethological approach has never been
applied to quantify the extent of the neural
activation at the basis of the difference in
yawn contagion latency as a function of the
emotional closeness.
The higher human sensitiveness to yawns
emitted by friends and kin can be explained by
the peculiarity of the emotional attachment
characterizing our species (Bowlby, 1969;
Maestripieri, 2003). Compared to bonobos, the
strong relationships established between humans
are probably qualitatively different, because
they are built upon more complex and
sophisticated emotional foundations linked to
cognition, memory, and memories. This
interpretation is in line with findings
endorsing that affective and cognitive empathy
cooperate in modulating the phenomenon of yawn
contagion in humans as it occurs for other kinds
of unconsciously mimicked behaviours (Van Baaren
et al., 2009). The idea that also the cognitive
component of human empathy explains some
features of yawn contagion is supported by the
ontogenetic co-emergence of yawn contagion and
theory of mind capacities in children (Anderson
& Meno, 2003; Helt et al., 2010; Millen
& Anderson, 2011) and the correlation of
these two phenomena in adults (Platek et al.,
2003). Therefore, it seems that in humans
affective empathy is enhanced by the cognitive
components concurring in awakening and
nourishing the affective involvement
characterizing strong relationships (Van Baaren
et al., 2009).
The most intriguing and original result
emerging from our cross-species analysis is the
strong similarity between human and bonobo
contagion susceptibility when the stimulus comes
from a familiar, but weakly bonded subject. This
finding indicates that the foundations of the
empathic mechanism are alike in the two species.
The absence of a strong emotional involvement
seems to bring to light the most basic component
of yawn contagion by removing the influence of
the higher and more complex layers
characterizing the cognitive sphere of human
empathy (e.g., perspective taking, mental state
attribution, theory of mind). As a whole, our
cross-species approach supports the shared and
multilayered architecture of animal empathy
(Preston & de Waal, 2002; de Waal, 2008).
Therefore, we cannot state that emotional
contagion is always highest in humans, but only
that they are able to create a unique and
extremely intense form of emotional attachment,
thanks to the complexity of the neural circuits
linking social experiences and cognitive
capacities. When such a pervasive attachment is
missing, humans climb down from the highest step
of the empathic podium to return to the
understory layer which our species shares with
other great apes.
