Yawn contagion (YC) is, compared to
spontaneous yawning, an evolutionary recent
phenomenon probably linked to behavioral
synchronization in highly social species that is
more likely when it involves familiar subjects.
Here, we investigate for the first time in
monkeys which factors modulate intra- and
interspecific YC. Through an experimental
approach, we exposed 17 red-capped mangabeys to
video stimuli (Yawn vs Control) depicting
familiar/unfamiliar red-capped mangabeys and
humans, and unfamiliar hamadryas. We found that
mangabeys yawned more often in response to Yawn
than Control videos independently from the
species depicted, demonstrating both intra- and
interspecific YC in the tested species.
Moreover, both mangabey and human familiar
yawning stimuli evoked a stronger yawning
response in the subjects compared to the
unfamiliar counterparts. Neither the amount of
time spent looking frontally at the screen
(probability of stimulus perception) nor the
levels of self-directed behaviors (a proxy of
anxiety) accounted for the results. In
conclusion, we provide the first evidence that
in non-human primate familiarity modulates both
intra- and inter-specific YC. Stimuli emitted by
familiar faces somehow ease the mechanisms
underlying YC, and this modulation can also
apply to heterospecific subjects when previous
shared experiences provide the prerequisites for
the development of social bonds.
La contagion du bâillement (YC) est,
par rapport au bâillement spontané,
un phénomène récent dans
l'évolution, probablement lié
à la synchronisation comportementale chez
les espèces hautement sociales, qui est
plus probable lorsqu'elle implique des sujets
familiers.
Ici, les auteurs étudient pour la
première fois chez le singe les facteurs
qui modulent la YC intra et
interspécifique. Grâce à une
approche expérimentale, ils ont
exposé 17 mangabeys à tête
rouge à des stimuli vidéo (Yawn vs
Control) représentant des mangabeys
à tête rouge et des humains
familiers/non familiers, et des hamadryas non
familiers. Ils ont constaté que les
mangabeys bâillaient plus souvent en
réponse aux vidéos de
bâillements que le contrôle,
indépendamment de l'espèce
représentée, ce qui prouve
l'existence d'une YC intra- et
interspécifique chez les espèces
testées.
De plus, les stimuli de bâillements
familiers au mangabey et à l'homme ont
provoqué une réponse plus forte
chez les sujets que les stimuli non familiers.
Ni le temps passé à regarder
l'écran de face (probabilité de
perception du stimulus), ni les niveaux de
comportements autodirigés (un indicateur
d'anxiété) n'expliquent les
résultats.
En conclusion, ces auteurs fournissent la
première preuve que, chez les primates
non humains, la familiarité module les YC
intra et interspécifiques. Les stimuli
émis par des visages familiers facilitent
d'une certaine manière les
mécanismes sous-jacents au YC, et cette
modulation peut également s'appliquer
à des sujets
hétérospécifiques lorsque
des expériences partagées
antérieures fournissent les conditions
préalables au développement de
liens sociaux.
Introduction
Spontaneous yawning is an evolutionary
ancient trait that is consistent in its presence
and expression across several groups of
vertebrates1,2. Yawning is a multi-functional
phenomenon whose functions are probably
context-dependent and linked to both
physiological as well as behavioral aspects of
life3. Yawn contagion (YC), the ability to
respond with a yawn to others' yawns, is instead
an evolutionary more recent phenomenon4,5.
Recent findings suggest that YC can have an
adaptive social role in bodily coordination,
mood alignment and alertness increase6,7. Both
experimental and observational evidence indicate
sociality and cooperation as triggering factors
for YC to evolve in different
taxa6,8,9,10,11,12,13,14,15. YC can also be
present between subjects belonging to different
species (i.e., interspecific YC16,17,18) thus
indicating a certain level of flexibility of its
underlying mechanisms.
Familiarity shared between the interacting
subjects seems to play a role in the modulation
of stimuli contagiousness, and an animated
debate exists on the proximate causes at the
basis of such modulation (emotional closeness vs
attentional bias, 19,20). Relevant clues
supporting the linkage between yawn and
emotional contagion (a building-block of
empathy, 21) come from psychological studies.
People showing higher susceptibility to
contagious yawning do better at making
inferences about mental states22 and exhibit
fewer schizotypal traits23. Moreover, when
exposed to yawn vs control stimuli, higher
activity in empathy-related neuronal areas was
recorded in people scoring highly on empathy (24
but note that the authors did not measure the
contagion itself25). The emotional bias
hypothesis predicts that the degree of emotional
involvement with a first yawner reflects the
observer's susceptibility to respond with a
yawn4,21. Instead, the attentional bias
hypothesis predicts that YC is merely linked to
the higher levels of social attention that
observers devote to more relevant subjects
(i.e., familiar or dominant)25. More recently,
Gallup et al.26 found that those people scoring
high levels of psychopathic traits, which are
associated with reduced affective empathy, also
showed low levels of YC, with the yawn response
not depending on the attentional level. Although
this dualistic conceptual approach is present in
literature, the two aspects are difficult to
disentangle since probably both attentional and
affective processes play a role in the
modulation of YC20. Whatever the proximate
factors at the basis of YC modulation, several
studies show how affiliation and kinship
increase the susceptibility to respond to
others' yawns in several
species10,11,12,14,16,18,27. Concurrently, the
available data do not always go in the same
direction, with different examples of social
closeness not influencing YC28,29,30,31, thus
challenging the view about the positive effect
of familiarity on the phenomenon. Species
scoring low affiliation and/or high degrees of
ingroup competition do not seem to show YC32,33
and, moreover, while xenophilic species show
similar levels of YC towards known and unknown
individuals34, species classified as xenophobic
show contagion strictly towards ingroup
subjects18. Another factor that has been found
to influence the YC distribution is the sex of
the interacting subjects, especially in those
species where bonding is sex-biased (e.g.,
bonobos, 10; wolves12). Specifically, wolf
females showed a faster yawning response when
sharing a strong bond with the first yawner,
such difference was not found in males12.
Here, we aim at testing the effect of
familiarity on both intra- and interspecific YC
in monkeys due to the absence of data covering
these intermingled aspects in non-ape species.
Filling the gap is necessary if we want to
properly understand the evolutionary aspects of
the phenomenon. Our model is the red-capped
mangabey (Cercocebus torquatus), a highly
sexually dimorphic species living in multi-male
multi-female groups variable in size and
characterized by fission&endash;fusion
dynamics35. Although clear hierarchies exist in
social groups, the dominance relationships are
generally relaxed thus predicting a certain
level of tolerance36. C. torquatus further
possesses a rich repertoire of visual signals
with a large variety of yawning types37. The
peculiarity of their social life and the
variability of yawn performance make the species
a valuable candidate to test hypotheses on the
proximate factors leading to YC. To accomplish
the goal, we showed red-capped mangabeys video
stimuli from familiar and unfamiliar individuals
belonging to three species (Cercocebus
torquatus, Papio hamadryas, Homo sapiens). In
our protocol, we also took into consideration
the probability of stimulus perception (i.e.,
how long the subjects were frontally looking at
the screen) as well as the anxiety level of the
subjects when exposed to the different stimuli
(i.e., self-directed behaviours38), as both
factors can act as confounding factors for YC
and its modulation25,39.
If YC is sensitive to the phylogenetic
closeness between the interacting subjects
(hypothesis 1), we expect red-capped mangabeys
to be more susceptible to yawns produced by
conspecifics and hamadryas baboons than to yawns
produced by humans (prediction 1).
If YC is modulated by previous experiences
(i.e., familiarity) between the interacting
subjects (hypothesis 2), we expect red-capped
mangabeys to be more susceptible to yawns
produced by familiar red-capped mangabeys and
humans than to those produced by the unfamiliar
counterparts (prediction 2).
Discussion
Here, we found that red-capped mangabeys
yawned more often to videos depicting yawning
individuals than to control videos, thus
demonstrating yawn contagion (YC) in this
species. Since self-directed behaviors (SDB, a
proxy of anxiety) were not affected by neither
of the factors considered, this rules out the
possibility that yawning response (YR) was a
by-product of anxiety. This result contrasts
with those from other studies where the
perception of yawn stimuli produced an increase
of both YR and SDB39,41. Our finding also seems
to suggest that mangabeys do not perceive
yawning behavior as a negative stimulus,
differently from what has been found in
humans42.
The YR was not affected by the amount of
frontal looking (FL), thus suggesting that in
the species the probability of responding to a
yawn cannot be merely explained by the
quantitative perception of the stimulus (e.g.,
for how long you perceive it). Male YR was
higher than female YR independently from the
species depicted and from the condition of the
video stimulus. The higher male tendency to
spontaneously yawn is not surprising in those
primate species showing remarkable sexual
dimorphism in canine size37,43. Here, males
yawned more often than females both when exposed
to Control and Yawn stimuli; importantly, the
effect of the Yawn condition in increasing the
likelihood of yawning did not differ between the
two sexes (i.e., the interaction term
Sex*Condition was not significant in the
models), with yawn stimuli producing a
comparable YC effect in both males and females.
Our animals showed similar levels of
susceptibility to yawns emitted by conspecific
and heterospecific subjects thus demonstrating
both intra- and inter-specific YC (prediction 1
not supported). Mangabeys frontally looked for
longer the videos depicting conspecific than
heterospecific subjects, probably related to the
greater socio-ecological relevance for
mother-reared primates to strictly monitor
members of their own species42,44,45. A possible
limit of the study is that we could not use
eye-tracking techniques, preventing us from
actually making conclusions on the attentional
state of the subjects. However, we can
confidently assume that the longer the animals
looked with their head frontally towards the
screen, the higher the probability for them
actually looking at the individual depicted in
the video (which occupied a good portion of the
screen and was easily visible). Moreover, since
YC does not require an active and conscious
attentional and perceptive state of the yawn
stimulus46, we can affirm that when the mangabey
looked frontally at the screen the stimulus was
at least passively perceived.
The literature does not provide data on
inter-specific YC deriving exclusively in
response to unfamiliar subjects/species.
Although direct comparisons are difficult, our
data are consistent with the at least partial
automaticity of motor mimicry phenomena4,47,
which allows a basal likelihood of contagion
independently from the identity and the social
features of the trigger subject. Our data can be
discussed by two not mutually exclusive
interpretations. The consistency of yawning
motor patterns (i.e., stereotypy) across
different primate species48 might explain the
similar efficacy in stimulating a yawning
response in the receiver. It is also possible
that monkeys, as it occurs in humans8, might be
able to automatically generalize the yawning
stimulus whatever its origins.
Our second set of data adds an important
piece of information about the phenomenon in
mangabeys. When familiarity comes into play, it
scores the highest YC rates (prediction 2
supported). Indeed, compared to the unfamiliar
counterparts, both familiar mangabey and human
yawning stimuli evoked a higher YR in the tested
subjects and this held for both males and
females. This higher susceptibility towards
familiar yawns was not clearly due to a higher
probability of familiar stimulus perception,
because mangabeys spent more time frontally
looking unfamiliar rather than familiar
individuals, possibly due to the potential
adaptive implications involved when facing novel
stimuli18,49,50. Similar results have been
recently found in great apes, with chimpanzees
and gorillas being more attracted by novel than
familiar human faces51. The familiarity bias in
FL that we found is not in contrast with the
higher level of FL devoted to conspecific than
to heterospecific subjects; indeed, competition
for resources is expected to be higher between
subjects belonging to the same species (complete
ecological niche overlap) but belonging to
different social groups, and thus stimuli from
unfamiliar conspecifics should be more
attentively monitored. During YC, one can share
the state of the other based on a perceived
motor pattern, through an automatic distributive
associative process, which may get easier when
the stimuli come from familiar faces52. Hence
familiarity with the yawner, independently from
the species it belongs to, may potentiate the
Perception Action Mechanism at the basis of
motor resonance phenomena21.
In chimpanzees, Campbell and de Waal18
reported a familiarity-biased contagiousness
only towards conspecifics, but not towards
humans, a species to which chimpanzees were well
habituated. Conversely, in our study, not only
were red-capped mangabeys susceptible to yawns
produced by conspecifics and humans, but they
also showed a comparable familiarity bias
towards both species. Similar hypotheses have
been so far rarely tested in primates18 and a
modulation in the contagiousness of
heterospecific yawns was only found in
domesticated dogs (16, but see also 28) where,
on the other hand, no study investigated
intraspecific YC. Our data thus represent the
first evidence in mammals of familiar modulation
on YC operating at both intra- and interspecific
level. Unfamiliar humans seem to be perceived by
mangabeys as something equivalent to the
'outgroup' conspecifics, both in terms of
frontal looking at the screen (FL) and
contagiousness (YR). Conversely, since
caretakers daily spend a considerable amount of
time with animals, their faces and yawns are
probably processed as those of 'ingroup'
companions. Stimuli produced by extensively
known humans might be easier to be processed and
thus might be more contagious than those emitted
by stranger faces. Our results also highlight
the ability of mangabeys to discriminate between
familiar and unfamiliar human faces. Although
the capacity to process universal face
prototypes is thought to be present at birth, it
is highly adaptive that face recognition
abilities narrow in the course of ontogeny and
reach a high specificity later in life53. This
can lead to a scarce competence in
discriminating familiar vs unfamiliar
heterospecific faces. Yet, early experience can
maintain a certain degree of plasticity in the
primate face recognition system54. The daily
experience that our mangabeys have with
caretakers are probably at the basis of their
ability to properly process human faces.
Recent data suggests that the propensity to
mimic ingroup subjects has been favored by
natural selection to increase behavioral
synchronization, fundamental for survivorship
and improvement of individual fitness55. For
example, YC in lions translates into a higher
probability to align social activities that are
at the basis of cooperative hunting, offspring
care, and territorial defense6. Other forms of
behavioral synchronization have been reported to
be extremely adaptive (vigilance against
predators56). It is possible that the natural
propensity to be behaviorally infected by group
mates could expand to familiar subjects of
different species under contexts allowing
interspecies interactions (e.g., captivity).
Experimental data demonstrate that capuchin
monkeys preferentially engaged in objects
sharing with experimenters who previously
imitated them compared to experimenters who
performed non-imitative gestures57. This finding
is in line with our results on the importance of
familiarity in modulating YC despite the
inter-specific context. Here, the adaptive value
might reside in the possible linkage between
motor resonance phenomena (YC) and the resource
benefits (e.g., food provisioning) gathered by
monkeys from their caretakers.
In conclusion, in mangabeys YC is
socially modulated not only at intra- but also
at interspecific level, suggesting that the
phylogenetic closeness of the interacting
subjects is not enough to explain the
phenomenon. Other factors such as the social
feature of a species (e.g., social system,
preferential relationships, ingroup competition)
and the ontogenetic pathways of each individual
(e.g., rearing conditions, more or less
opportunities of early experiences, degree of
plasticity in forming bonds) should be taken
into account to fully explain the propensity to
YC and its modulation from an adaptive
perspective.
