Contrary to spontaneous yawning, which is
widespread in vertebrates and probably
evolutionary ancient, contagious yawning-yawning
triggered by others' yawns-is considered an
evolutionarily recent phenomenon, found in
species characterized by complex sociality.
Whether the social asymmetry observed in the
occurrence of contagious yawning is related to
social and emotional attachment and may
therefore reflect emotional contagion is a
subject of debate. In this study the authors
assessed whether yawn contagion was enhanced in
pregnant women, a cohort of subjects who develop
prenatal emotional attachment in preparation for
parental care, via hormonal and neurobiological
changes. They predicted that if yawn contagion
underlies social and emotional attachment,
pregnant women would be more likely to
contagiously yawn than nonpregnant, nulliparous
women of reproductive age. They gathered data in
two different settings.
In the experimental setting, 49 women were
exposed to video stimuli of newborns either
yawning or moving their mouth (control) and we
video-recorded the women during repeated trials
to measure their yawning response. In the
naturalistic setting, 131 women were observed in
a social environment and their yawning response
was recorded. They tested the factors
influencing the yawning response, including the
reproductive status (pregnant vs. not pregnant).
In both settings, yawn contagion occurred
significantly more in pregnant than nonpregnant
women. By showing that pregnant women were most
likely to respond to others' yawns, these
results support the hypothesis that the social
variation observed in yawn contagion may be
influenced by emotional attachment and that
yawning in highly social species might have been
coopted for emotional contagion during
evolution.
Résumé
Contrairement au bâillement
spontané, qui est répandu chez
tous les vertébrés donc
probablement ancien, le bâillement
contagieux - le bâillement
déclenché par les
bâillements des autres - est
considéré comme un
phénomène évolutif
récent, trouvé chez les
espèces caractérisées par
une socialité complexe. La question de
savoir si l'asymétrie sociale
observée dans la survenue du
bâillement contagieux est liée
à l'attachement social et
émotionnel et peut donc refléter
une contagion émotionnelle est un sujet
de débat. Dans cette étude, les
auteurs ont évalué si la contagion
du bâillement était
augmentée chez les femmes enceintes,
c'est à dire des sujets qui
développent un attachement
émotionnel prénatal en
préparation aux soins parentaux, via des
changements hormonaux et neurobiologiques.
Ils ont prédit que si la contagion du
bâillement sous-tend l'attachement social
et émotionnel, les femmes enceintes
seraient plus susceptibles de bâiller de
manière contagieuse que les femmes
nullipares non enceintes et en âge de
procréer. Ils ont collecté des
données dans deux contextes
différents. Dans le cadre
expérimental, 49 femmes ont
été exposées à des
stimuli vidéo de nouveau-nés
bâillant ou bougeant la bouche
(témoin) et ils ont enregistré les
femmes lors d'essais
répétés pour mesurer leur
réponse au bâillement. Dans le
cadre naturaliste, 131 femmes ont
été observées dans un
environnement social et leur réponse de
bâillement a été
enregistrée. Nous avons testé les
facteurs influençant la réponse au
bâillement, y compris le statut
reproducteur (enceinte vs non enceinte). Dans
les deux cas, la contagion du bâillement
s'est produite significativement plus chez les
femmes enceintes que chez les femmes non
enceintes. En montrant que les femmes enceintes
étaient les plus susceptibles de
réagir aux bâillements des autres,
nos résultats soutiennent
l'hypothèse que la variation sociale
observée dans la contagion du
bâillement peut être
influencée par l'attachement
émotionnel et que le bâillement
chez les espèces hautement sociales
pourrait avoir favorisé la contagion
émotionnelle au cours de
l'évolution.
Whereas spontaneous yawning is independent
from the perception of others' yawns, contagious
yawning occurs when the yawn emitted by a
subject (trigger) acts as a releasing stimulus
(sensu Tinbergen and Perdeck 1951) and elicits
yawning in another subject (responder) (Provine
1989). Although morphological variants are
present in yawns, especially in primates (e.g.,
chimpanzees, Pan troglodytes, Vick and Paukner
2010; geladas, Theropithecus gelada, Palagi et
al. 2009; Tonkean macaques, Macaca tonkeana, and
Japanese macaque, M. fuscata, Zannella et al.
2017; humans, Homo sapiens, Provine 1986, 2012),
spontaneous yawning is probably a plesiomorphic
(ancestral) trait because it has been recorded
in a wide array of vertebrates (Baenninger
1987).
To the contrary, contagious yawning between
conspecifics has been observed thus far in a
relatively small number of species (Palagi et
al. 2020) and may be an apomorphic trait, which
appeared more recently in vertebrate evolution.
With one exception (Pongo pygmaeus; van Berlo et
al. 2020), the species exhibiting yawn contagion
between conspecifics usually live in highly
social groups: namely, all the extant hominine
species (chimpanzees: Anderson et al. 2004;
Campbell and Cox 2019; Campbell and de Waal
2011; bonobo, Pan paniscus: Demuru and Palagi
2012; Tan et al. 2017; but see Amici et al. 2014
on a very small sample size; humans: Provine
1986, 1989), two species of cercopithecines
(geladas and Tonkean macaques; Palagi et al.
2009; Palagi and Norscia 2019), non primate
mammals (lions, Panthera leo: Casetta et al.
2021; wolves, Canis lupus lupus: Romero et al.
2014; sheep, Ovis aries: Yonezawa et al. 2017;
elephant seals, Mirounga leonina:
Wojczulanis-Jakubas et al. 2019; domestic pigs,
Sus scrofa: Norscia et al. 2021), and one social
bird species (budgerigar, Melopsittacus
undulates: Gallup et al. 2015).
One of the most remarkable aspects of
intra-specific yawn contagion is that it shows
social asymmetry in all the species where this
aspect has been investigated (Campbell and de
Waal 2011, 2014; Demuru and Palagi 2012; Massen
et al. 2012; Norscia and Palagi 2011; Palagi et
al. 2009; Romero et al. 2014). The yawning
response is most likely or precisely triggered
by yawns coming from individuals that are
"socially relevant" to the potential responders,
even though the communicative value of the
triggering yawns (e.g., threat, tiredness) can
vary. For example, in humans the yawning
response is highest between familiar subjects
(Norscia and Palagi 2011). In chimpanzees,
living in social groups characterized by male
dominance, males seem to respond more when the
triggering yawn comes from the dominant males
(Massen et al. 2012), whereas in bonobos, living
in groups with female dominance, females seem to
be more effective in eliciting others' yawns
(Demuru and Palagi 2012). Indeed, bonobos and
chimpanzees preferentially attend familiar
subjects of the dominant sex (Lewis et al.
2021). In geladas, the female dyads, which are
responsible for maintaining group cohesion,
showed the most precise matching of different
yawning types (Palagi et al. 2009).
The social attachment between individuals
seems also to affect the rates of yawn
contagion. In dogs (Canis lupus familiaris), the
evidence of interspecific yawn contagion
(dog/human) and its modulation is mixed (for
review: Neilands et al. 2020; Palagi and Cordoni
2020); in wolves, top rates of intraspecific
yawn contagion were found between strongly
bonded subjects (with bonding being measured by
assessing the level of affinitive behavior;
Romero et al. 2014). Adult chimpanzees (but not
immature chimpanzees, Madsen and Persson 2013)
yawn more in response to the yawns of ingroup
than outgroup members (Campbell and de Waal
2011). Bonobos (in vivo but not when exposed to
video stimuli; cf. Tan et al. 2017) show the
highest yawning response between closely bonded
individuals (Demuru and Palagi 2012; Palagi et
al. 2014). A similar situation occurs in
geladas, with yawn contagion being greatest
between individuals that affiliate the most
(Palagi et al. 2009). In humans, yawn contagion
is higher in kin and friends than in
acquaintances and strangers (Norscia and Palagi
2011; Norscia et al. 2016), and the familiarity
bias remains when the yawns are heard but not
seen (Norscia et al. 2020).
Based on neuroethological evidence, it has
been hypothesized that in highly social species
yawning may have been coopted during evolution
for emotional contagion, a basic building block
of empathy (de Waal and Preston 2017; Palagi et
al. 2020). However, at present, it is highly
debated for both human and nonhuman animals
whether the social asymmetry observed in yawn
contagion depends on interindividual bonding,
possibly reflecting emotional attachment, as
postulated by the Emotional Bias Hypothesis
(EBH), and/or on other factors, such as
attentional levels, social dominance, or as-yet
undefined aspects of the social setting
(Adriaense et al. 2020; Kapita_ny and Nielsen
2017; Massen and Gallup 2017; Palagi et al.
2020).
Emotional contagion and empathic processes
are assumed to have evolved from
mother&endash;offspring bond (for review:
Preston 2013). Pregnant women are particularly
suitable to investigate the link between yawn
contagion and bonding because they undergo heavy
psychological, physiological, and
neurobiological changes leading to the
development of maternal attachment and
caregiving (Barba-Mu_ller et al. 2019; Napso et
al. 2018; Tichelman et al. 2019). These changes
often alter body systems so that pregnant women
perform and act differently (e.g., with respect
to dietary choice, motor activity, sensitivity
to emotional stimuli) than nonpregnant women in
the general population (Crozier et al. 2009;
Gradmark et al. 2011; Moya et al. 2014; Oso_rio
et al. 2018).
Although proposing different underlying
mechanisms, definitions, and measures, (Brandon
et al. 2009), the psychological literature
addressing attachment theory (originally
introduced for the postpartum period; Bowlby
1969) converges in indicating that mother-infant
bonding starts long before birth, during
pregnancy (Ferrari et al. 2016; Sadeghi and
Mazaheri 2007; Salehi and Kohan 2017; Sedgmen et
al. 2006). During gestation, women develop what
Rubin (1975:149) called a sense of "we-ness,"
later defined as prenatal attachment, the
emotional and psychological bond between the
mother and her unborn child (Brandon et al.
2009; Rossen et al. 2017). The mother-infant
bonding quality developed in pregnancy is
important because it is positively associated
with the mother-infant bonding quality after
birth (Tichelman et al. 2019).
Psychobiological changes during pregnancy,
involving hormonal and maternal brain
adaptations, occur in both human and nonhuman
mammalian females to support the transition to
parenthood (Kim 2016; Lonstein et al. 2015). In
women, the establishment of prenatal attachment
is sustained by recent neurobiological evidence.
Via magnetic resonance imaging (MRI), Hoekzema
et al., (2017) found that during pregnancy
women's brains undergo dramatic, long-lasting
changes in areas that significantly overlap with
areas involved in the Theory of Mind (ToM)
(i.e., anterior and posterior cortical midline
and specific sections of the bilateral lateral
prefrontal and temporal cortex; Hoekzema et al.
2017). ToM, among other aspects, is related to
the ability to read others' emotions (affective
ToM; Abu-Akel and Shamay-Tsoory 2011). Brain
changes are also linked to the development of
maternal attachment and can significantly
predict the quality of future mother-infant
attach- ment (Hoekzema et al. 2017).
Psychological and neurobiological changes
are interconnected with the massive hormonal
variations that occur in women during gestation
(Barba-Mu_ller et al. 2019; Glynn and Sandman
2011). Changes in the so-called maternal brain
(including areas especially involved in maternal
caregiving) are mediated by glucocorticoids,
prolactin, and oxytocin, whose levels increase
across pregnancy (Kim and Strathearn 2016; Napso
et al. 2018; Prevost et al. 2014; Slattery and
Hillerer 2016). Moreover,
prolactin&endash;Growth Hormone (GH) family and
neuroactive hormones, including melatonin and
its precursor serotonin, prepare pregnant women
to adequately care for their offspring by
impacting on different physiological functions
(Le_vy 2016; Napso et al. 2018). Oxytocin is the
neuroactive hormone that is thought to play a
major role in the development of maternal
attachment and, more generally, social bonding
in humans and other animals (Decety et al.
2016). Although contextual and interindividual
factors can mitigate or even reverse the effects
of oxytocin (Beery 2015; Olff et al. 2013),
during pregnancy oxytocin is involved in the
emergence of mother-infant emotional bonding
and, in humans, also in the mental
representations typical of such bonding (Decety
et al. 2016; Feldman et al. 2007).
In summary, yawn contagion may be related to
emotional attachment (as predicted by EBH), and
pregnant women represent a cohort of subjects
that is bio- logically and psychologically
"equipped" for mother-infant emotional
attachment (Barba-Mu_ller et al. 2019; Brandon
et al. 2009; Palagi et al. 2020; Tichelman et
al. 2019). Hence, to check for further evidence
of the association between yawn contagion and
social attachment, possibly reflecting emotional
attachment (de Waal and Preston 2017), we
focused on the yawning response in pregnant
women. In particular, we predicted that if
social asymmetry in contagious yawning is also
driven by interindividual attachment, a proxy of
emotional attachment, contagious yawning would
occur at higher rates in pregnant compared to
nulliparous women.
Discussion
The results from both the experimental and
the naturalistic data converge in indicating
that women's reproductive status had an effect
on contagious yawning, which was more likely to
occur in pregnant than in nulliparous women
(here defined as women who were not pregnant and
had no children). As a matter of fact, pregnant
women were more likely to respond than
nulliparous women to both video yawns of unknown
infants in the experimental trials and live
yawns from adults in the naturalistic setting
(Tables 2 and 3; Figs. 3 and 5). This finding,
presented for the first time with this study,
provides support to the Emotional Bias
Hypothesis (EBH) because yawn contagion was
highest in the category of women characterized
by enhanced social attachment predisposition,
owing to the biological and psychological
changes typical of the gestation period
(Barba-Mu_ller et al. 2019; Brandon et al. 2009;
Tichelman et al. 2019).
Since yawn contagion has been found to vary
across the day (Giganti and Zilli 2011), we
checked whether our yawning response sampling
could be biased by the time periods during which
the data were collected, depending on the
availability of the study subjects. In neither
setting did we find a significant effect (Tables
1 and 3), probably because the majority of the
data was collected in the morning and in the
afternoon (with little data collected at the
very extremes of the day).
The use of a twofold approach, involving
both experimental and naturalistic data
collection, allowed the verification of the
possible effect of different variables on yawn
contagion. The results of the experimental
trials show that the yawning response was
significantly higher in the yawning than in the
control video condi- tion (Table 1; Fig. 2).
This finding confirms that yawn contagion was
present in the cohort of human subjects
considered in this study (nulliparous and
pregnant women) since it has been found in other
segments of the population (Arnott et al. 2009;
Pro- vine 1989, 2005).
Yawn contagion may be affected by selective,
top-down attentional biases (Massen and Gallup
2017), in addition to bottom-up, stimulus-driven
attention (Attentional Bias Hypothesis, ABH;
Palagi et al. 2020). Therefore, in the
experimental setting we checked for selective
attention to the stimulus and we found no
significant influence of the time of attention
to the stimulus source (video screen) on yawning
(Table 1), which was high overall in both
yawning and control video conditions, as well as
in pregnant and nulliparous women. This finding
reduces the probability that in our sample a
selective attention bias may have accounted for
the differences between stimulus
(yawning/control) and reproductive status
(pregnant/nulliparous) conditions. This is line
with evidence indicating, directly or
indirectly, that contagious yawning in humans
may depend on bottom-up more than top-down
selective attention (Norscia et al. 2020; for a
review see Palagi et al. 2020). Age is another
variable known to possibly affect yawn contagion
rates (Bartholomew and Cirulli 2014). In our
case, in the experimental setting there was a
nonsignificant trend of the influence of age in
the yawning response, possibly because the women
under study fell within the relatively short
reproductive age.
In the naturalistic setting we could verify
the effect of a social bond between the trigger
and the potential responder on the yawning
response. Although the bond was restricted to
two categories (strangers and acquaintances)
owing to data constraints, and despite showing
an inverse correlation with reproductive status,
the bond had a significant effect on yawn
contagion, which was more likely between
subjects who knew each other than between
strangers. This finding is in agreement with
previous literature showing that relationship
quality has an influence on yawn contagion,
whose likelihood increases as the strength of
the social bond increases (from strangers to
acquaintances, friends, and lastly to family
members; Norscia and Palagi 2011; Norscia et al.
2016). Norscia et al., (2020) found no
difference between strangers and acquaintances
when the yawns were heard but not seen, although
friends and family responded at significantly
higher rates than did those in the other
categories. In the absence of the visual cue, it
is probably more difficult for the potential
responders to discern between subjects with whom
they have reduced or no familiarity.
Importantly, our results from the
experimental trials show that reproductive
status (pregnant/nulliparous) had a significant
effect on the yawning response in the yawning
video condition but not in the control video
condition (cf. Tables 2 and 3). Therefore, only
yawning resulting from contagion, and not
spontaneous yawning, was affected by pregnancy
in our sample. Historical accounts report an
increase of spontaneous yawning in the case of
certain diseases (e.g., puerperal fever or
hemorrhage; Walusinski 2010), and excessive
yawning has indeed been indicated as a possible
marker of disease in humans (Thompson and
Simonsen 2015). Progesterone increases daytime
drowsiness and sleeping time (Won 2015) and so
it may increase spontaneous yawning rate during
pregnancy. In this respect, we cannot exclude
that the yawning stimulus might have
preferentially primed the yawning motor response
in pregnant women also because they experienced
increased fatigue (despite showing similar
levels of sleep to those of nulliparous women).
An investigation on how spontaneous rates vary
within subjects across pregnancy, possibly in
relation to fatigue and tiredness, and how
contagious yawning varies depending on the
stimulus (e.g., babies/adults), with hormonal
and neurobiological correlates, could better
clarify the above issues.
Overall, the different yawning response of
pregnant women relative to women with no
children can fall within the broad range of the
behavioral changes that start occurring during
pregnancy, such as motor activity and dietary
choice variations (Crozier et al. 2009; Gradmark
et al. 2011). Compared with childless women,
pregnant women show increased sensitivity to
emotional signals and facial expressions. For
example, pregnant women were found to perceive
infant cries in more differentiated ways than
women with no offspring (Bleichfeld and Moely
1984; Yoshiaki 1985). As gestation progresses,
pregnant women also show enhanced ability to
encode and process emotional faces, especially
related to distress (an emotional state; Keltner
et al. 2019) as an evolutionary adaptation to
motherhood, which requires hypersensitivity to
emotional threat signals and contagion (Oso_rio
et al. 2018; Pearson et al. 2009). Our results
fit with this scenario because they indicate
enhanced responsiveness of pregnant women to
yawning, which has been linked (with various
degrees of evidence) to anxiety and distress in
human and nonhuman primates (from lemurs to
apes: e.g., Baker and Aureli 1997; Coleman and
Pierre 2014; Leone et al. 2014; Palagi et al.
2019; Thompson 2014, 2017; Thompson and Bishop
2012; Zannella et al. 2015). Thompson (2014) has
posited that cortisol (involved in the stress
response) may be involved in yawn contagion, at
least under certain situations. Another
hypothesis, not mutually exclusive to the
cortisol hypothesis, may be that yawn contagion
is, to a certain extent, under the influence of
oxytocin, considering that enhanced emotional
recognition is one of the effects of oxytocin,
whose levels largely increase during pregnancy
(Domes et al. 2007; Preston 2013). In
particular, oxytocin appears to increase the
accuracy of the recognition of faces displaying
angry and happy emotions, especially in women
(Yue et al. 2018). Mariscal et al., (2019) found
that yawn contagion in autism spectrum disorder
(ASD) children was positively related to the
blood concentration of oxytocin. The possible
relationship between oxytocin and yawn contagion
is supported by evidence that yawn contagion in
humans follows the empathic gradient (sensu
Preston and de Waal 2002), being highest between
closely bonded subjects (Norscia and Palagi
2011; Norscia et al. 2020). Some features
typical of mother-infant attachment, such as
social recognition, bonding, and affiliation,
are maintained in adult- hood and promoted by
oxytocin, which has been found to increase trust
(Kosfeld et al. 2005), generosity (Zak et al.
2007), altruism (de Dreu et al. 2010), and both
cognitive and affective empathy (Rodrigues et
al. 2009; Shamay-Tsoory et al. 2013; Smith et
al. 2014; Uzefovsky et al. 2015). One of the
future steps is to evaluate the possible
covariation between oxytocin and yawn contagion
in both pregnant and nulliparous women. Beyond
incorporating hormones, further studies could
involve postmenopausal versus pregnant women and
check how mothers react when they see their own
fetus yawning on the echograph screen.
The possible connection between yawn
contagion and increased social and emotional
bonding is also suggested by the fact that some
of the areas that seem to be involved in yawn
contagion (such as the ventromedial-prefrontal
cortex, superior temporal sulcus, amygdala,
insula, posterior cingulate, and precuneus;
Nahab et al. 2009; Platek et al. 2005;
Schu_rmann et al. 2005) are also involved in
mother-infant care, in mother's enhanced
sensitivity to the baby, and maternal brain
changes occurring during pregnancy
(Barba-Mu_ller et al. 2019; Hoekzema et al.
2017; Kikuchi and Noriuchi 2015; Preston 2013;
Rifkin-Graboi et al. 2015).
In summary, by showing increased occurrence
of yawn contagion in pregnant women, a cohort of
subjects that is specifically "programmed" to
recognize and respond to others' emotions, this
study provides support for the hypothesis that
yawn contagion may, at least under certain
circumstances, underlie emotional contagion
(EBH; Palagi et al. 2020). This process is
considered by some scholars a basic form of
empathy and occurs when an emotion is
transferred from one individual to another,
possibly via a motor perception&endash;action
mechanism, involving the matching of facial
expressions and the resonance of the emotions
that underlie such expressions (de Waal and
Preston 2017).
The perception&endash;action and the
offspring care model both predict that subjects
can preferentially attend the stimuli coming
from closely bonded others, particularly car-
egiving individuals such as pregnant women
toward babies (Preston 2013; Preston and de Waal
2002). Visual, top-down attention has limited
effect on yawn contagion and does not follow a
consistent familiarity trend in hominines
because other fac- tors, such as dominance, can
come into play (Lewis et al. 2021; Norscia et
al. 2020; Palagi et al. 2020). Hence, a possible
bonding hypothesis between EBH and ABH is that
yawn contagion can be influenced by emotional
bonding and attention, mainly directed through
bottom-up mechanisms.
Importantly, not all contagious yawning is
triggered by emotional resonance, and that is
not the point in question here. Contagious
yawning also occurs between strangers (Norscia
and Palagi 2011), and some people are
consistently not susceptible to others' yawns
(Bartholomew and Cirulli 2014; Platek et al.
2003; Provine 1986, 1989). Contagious yawning is
a form of yawning and, as such, can be related
to non-emotional, individual and/or
environmental factors, such as time of the day
(Giganti and Zilli 2011), age (Bartholomew and
Cirulli 2014), and possibly temperature (Gallup
and Eldakar 2011). The perception&endash;action
mechanism itself is based on a theory in motor
control that assumes that our physical motor
acts are primed in the brain by observation of
those in others, even if they do not bear
emotional cues (Preston and de Waal 2002). Thus,
contagious yawning can also be a non-emotional
motoric response. The pivot around which this
study revolves is the possible mechanism leading
to the social variations observed in the
occurrence of contagious yawning. Although still
under debate (Adriaense et al. 2020; Massen and
Gallup 2017), various physiological,
neuroethological, and psychological studies
sustain the possible connection between the
social asymmetry of yawn contagion and emotional
bonding. Some of the brain areas that appear to
be involved in yawn contagion (Nahab et al.
2009; Platek et al. 2005; Schu_rmann et al.
2005) seem to overlap with those involved in
emotional processing of internal and external
stimuli and empathy (Palagi et al. 2020) and,
importantly, with the maternal brain
(Barba-Mu_ller et al. 2019; Hoekzema et al.
2017; Kikuchi and Noriuchi 2015; Rifkin-Graboi
et al. 2015). Highest levels of yawn contagion
are associated with increased oxytocin lev- els
(i.e., ASD children; Mariscal et al. 2019),
enhanced social bonding (i.e., between friends
and family; Norscia and Palagi 2011), and
maternal prenatal bonding (i.e., in pregnant
women; present study). Lower yawn contagion
rates in association with levels of autistic
traits were found to be related to attentive
rather than background emotional empathy
deficits (Helt et al. 2021). Finally, another
study found that sub- jects who yawned in
response to observing others' yawns exhibited
significantly higher empathy scores (Franzen et
al. 2018).
Hence, although we cannot discard the
possibility that other priming and motor
mechanisms may also underlie the social
asymmetry of yawn contagion, the hypothesis that
this behavior has been coopted during evolution
for emotional contagion still stands and gains
further support.
