Evolutionary Behavioral
Sciences Program, Department
of Social and Behavioral
Sciences, State University of New York
Polytechnic Institute, Utica, NY 13502,
USA
Abstract
While the origin of yawning appears to be
physiologic, yawns may also hold a derived
communicative function in social species. In
particular, the arousal reduction hypothesis
states that yawning signals to others that the
actor is experiencing a down regulation of
arousal and vigilance. If true, seeing another
individual yawn might enhance the vigilance of
observers to compensate for the reduced mental
processing of the yawner. This was tested in
humans by assessing how exposure to yawning
stimuli alters performance on visual search
tasks for detecting snakes (a threatening
stimulus) and frogs (a neu- tral stimulus). In a
repeated-measures design, 38 participants
completed these tasks separately after viewing
yawning and control videos. Eye-tracking was
used to measure detection latency and distractor
fixation frequency. Replicating previous
evolutionary-based research, snakes were
detected more rapidly than frogs across trials.
Moreover, consistent with the view that yawning
holds a distinct signaling function, there were
significant interactions for both detection
latency and distractor fixation frequency
showing that vigilance was selectively enhanced
following exposure to yawns. That is, after
viewing videos of other people yawning,
participants detected snakes more rapidly and
were less likely to fixate on distractor frogs
during trials. These findings provide the first
experimental evidence for a social function to
yawning in any species, and imply the presence
of a previously unidentified psychological
adaptation for preserving group vigilance.
Résumé
A côté des bâillements
physiologiques, certains bâillements
peuvent également avoir une fonction
dérive, par exemple de communication au
sein des espèces à vie sociale. En
particulier, l'hypothèse de
réduction de la vigilance stipule que le
bâillement signale aux autres que
l'effecteur subit une régulation à
la baisse de la vigilance. Si cela est vrai,
voir un autre individu bâiller pourrait
renforcer la vigilance des observateurs pour
compenser l'altération de la vigilance du
bâilleur.
Ceci est ici testé chez l'homme en
évaluant comment l'exposition à
des stimuli de bâillements modifie les
performances au cours de tâches de
détection visuelle de serpents (un
stimulus de menace) et les grenouilles (un
stimulus neutre). Cette conception a
été testée de façons
répétées chez 38
participants après avoir visionné
des vidéos de bâillements et de
contrôle. Le suivi oculaire a
été utilisé pour mesurer la
latence de détection et la
fréquence de fixation du distracteur.
Reproduisant les résultats de recherches
antérieures en lien avec
l'Évolution, les serpents ont
été détectés plus
rapidement que les grenouilles au cours de ces
essais.
De plus, conformément à la
conception selon laquelle le bâillement a
aussi une fonction de signalisation distincte,
il y a eu des modifications significatives
à la fois sur la latence de
détection et sur la fréquence de
fixation du distracteur montrant que la
vigilance était sélectivement
augmentée après l'exposition aux
bâillements. Autrement dit, après
avoir visionné des vidéos d'autres
personnes en train de bâiller, les
participants ont détecté des
serpents plus rapidement et étaient moins
susceptibles de se fixer sur les grenouilles
pendant les essais. Ces résultats
fournissent la première preuve
expérimentale d'une fonction sociale du
bâillement chez n'importe quelle
espèce, et impliquent la présence
d'une adaptation psychologique non
identifiée auparavant pour
préserver la vigilance de groupe.
Andrew
C. Gallup. Yawning and the thermoregulatory
hypothesis
Yawning is characterized by an involuntary
and powerful stretching of the jaw with deep
inspiration, followed by a temporary period of
peak muscular contraction and a passive closure
of the jaw with expiration (Barbizet 1958).
Yawns, or at least similar patterns of
mandibular gaping, have been observed across
vertebrate classes (Baenninger 1987) and emerge
early on during intrauterine development (De
Vries et al. 1982). These phylogenetic and
ontological findings suggest yawning has been
conserved throughout vertebrate evolution.
Moreover, several additional lines of evidence
indicate that yawning is an adaptation rather
than a byproduct. For example, yawning is an
overt response that conflicts with other
movement (Miller et al. 2010) and in rare cases
can entail extreme costs resulting in
subluxation or locking of the jaw (Tesfaye and
Lal 1990). In addition, psychological research
shows hedonic properties to yawning (Provine and
Hamernik 1986) where the inability to achieve
full yawns is often perceived as frustrating
(Walusinski 2018).
Numerous functional hypotheses of yawning
have been developed over the last 80 years, with
most proposing either (1) individual
physiological benefits or (2) communication to
others (Guggisberg et al. 2010; Smith 1999).
Yawns are known to have two distinct causes:
spontaneous yawns appear physiologically driven
(Baenninger 1997), and contagious yawns are
triggered by sensing yawns in others (Provine
1986). Yawning may therefore be multifunctional,
including underlying physiologic actions shared
across vertebrates, and derived communicative
roles among social species (Gallup 2011).
Physiologically, comparative and
neurological research suggests that yawns act to
modify cortical arousal (Baenninger 1997) and
promote state change (Provine and Hamernik 1986;
Provine 2005) through enhanced intracranial
circulation (Walusinski 2014) and brain cooling
(e.g., Gallup et al. 2011; Eldakar et al. 2015;
Ramirez et al. 2019). However, aside from being
contagious among humans (Pro- vine 1986) and
some non-human animals (Anderson et al. 2004;
Palagi et al. 2009; Gallup et al. 2015), direct
tests of any communicative value to yawning are
lacking and no functional outcomes to contagious
yawning have been observed (Massen and Gallup
2017). Observational studies of non-human
primates report that yawns of differing
intensity or morphology (e.g., covered teeth
versus uncovered gum yawns) occur more often
during certain social contexts, but no clear
social functions have been identified for these
yawn-types (see Leone et al. 2014; Zannella et
al. 2017). Although "threat yawns" have been
described as a signal among some primate
species, as first noted by Darwin (1872), these
gaping behaviors represent directed canine
displays with focused visual attention on the
target. Therefore, "threat yawns" differ
fundamentally from the stereotyped motor action
pattern that defines yawning across vertebrate
classes, which includes a distinct
spatiotemporal organization and disparate
physiologic activation with head tilting, eye
closure, tearing, and salivating (Anderson 2010;
Barbizet 1958; Provine 2012).
As a potential signal, one of the most well
documented features of spontaneous yawning
pertains to its circadian pattern; i.e., yawns
are not randomly triggered across the day, but
rather occur with greatest frequency before
sleeping and/or after waking across diverse
species (Ania et al. 1984; Baenninger et al.
1996; Miller et al. 2012a; Provine et al. 1987;
Zilli et al. 2007). As a result, yawn frequency
in humans is positively correlated with
subjective ratings of sleepiness (Giganti et al.
2010). Moreover, yawning occurs naturally among
people during states of diminished mental
processing and boredom (Provine and Hamernik
1986), as well as during reduced awareness from
anesthesia (Kasuya et al. 2005). Due to these
connections, the development of computer vision
systems for detecting yawning, as a primary
indicator of drowsiness and fatigue, has
expanded rapidly within the last decade (for a
partial sampling, see Abtahi et al. 2011; Yang
et al. 2020; Zhang et al. 2015).
Consistent with the view that yawns serve to
communicate one's internal state (Guggisberg et
al. 2010), Dourish and Cooper (1990) proposed
that yawning could signal the end of sustained
concentration or from the experience of a
stressful event. More recently, Liang et al.
(2015) coined this the arousal reduction
hypothesis, proposing that yawns signal to
others that an individual is experiencing a down
regulation of arousal and vigilance. In a study
of stressful encounters in wild Nazca boobies
(Sula granti), these authors showed that,
similar to research on budgerigars
(Melopsittacus undulatus) (Miller et al. 2010,
2012b) and humans (Eldakar et al. 2017), yawning
is absent during exposure to stressors but then
becomes potentiated thereafter. These findings
were interpreted by Liang et al. as support for
the arousal reduction hypothesis, with yawning
"communicating to others the transition from a
state of physiological and/or psychological
arousal (for example, due to action of a
stressor) to a more relaxed state" (p. 38; Liang
et al. 2015).
While the conclusions of Liang et al. (2015)
have been critiqued with regards to the
inference of communication in the context
studied, in particular as it relates to
nocturnal yawning by adult boobies and yawning
by nestlings in the absence of parents or
response from nearby nestlings (see Gallup and
Clark 2015), yawns could still hold a signaling
function in this and other species within social
settings where signals could be readily
detected. Yawning is an overt motor action
pattern that is reliably identified in others.
Recent research shows that even human infants
can discriminate yawning from other types of
mouth movements (as measured by brain activity)
(Tsurumi et al. 2019), suggesting that the
detection of yawns in others is biologically
important.
Here, we propose a novel extension of the
arousal reduction hypothesis termed the group
vigilance hypothesis. In particular, we posit
that the detection of yawns in others functions
to increase vigilance in the observer as a means
of compensating for any reductions in these
processes experienced by the yawner. Consistent
with the view that spontaneous yawns are
triggered during reduced states of vigilance
(Dourish and Cooper 1990; Liang et al. 2015) and
arousal (Baenninger 1997) tied to circadian
fluctuations in sleep ness (Giganti et al. 2010)
and diminished mental processing (Provine and
Hamernik 1986; Gallup and Gallup 2007), yawning
occurs during major shifts in brain and skull
temperature across diverse species (Gallup and
Gallup 2010; Shoup-Knox et al. 2010; Eguibar et
al. 2017; Gallup et al. 2017).
Accordingly, in terms of social
functionality, yawns may not only serve to
signal the internal state of the actor, but the
detection of yawns in others is predicted to
initiate neurophysiological changes to modify
the mental state of observers that would
function to maintain or improve group vigilance.
In support of this hypothesis, imaging studies
on humans show distinct patterns of neural
activation indicative of enhanced vigilance and
threat detection following exposure to yawns.
For example, visual and auditory yawning stimuli
have been shown to activate regions of the
prefrontal cortex (PFC) (Nahab et al. 2009;
Arnott et al. 2009) and the superior temporal
sulcus (STS) (Schu_rmann et al. 2005; Tsurumi et
al. 2019), and these very same brain areas have
been implicated in attentional allocation to
biologically relevant and threatening stimuli
(Mobbs et al. 2007; Dinh et al. 2018), vigilance
(Parasuraman et al. 1998; Nelson et al. 2014),
and visual search tasks (Ellison et al. 2004;
Bichot et al. 2015). Together, this neurological
coupling suggests that merely sensing yawns from
others could enhance processing in these
domains. If true, this would represent the first
evidence for a social function to yawning, which
could provide critical insight into the
evolution of yawn contagion, as the partial
spreading of socially-triggered yawns within a
group would help propagate this signal to nearby
conspecifics.
We tested the group vigilance hypothesis in
an experiment designed to examine how exposure
to video clips of people yawning altered
performance on visual search tasks for detecting
threatening and neutral stimuli (snakes and
frogs). Based on the group vigilance hypothesis,
which extends upon the view that yawns signal a
reduction in vigilance by the actor (i.e., Liang
et al. 2015), we hypothesized that observing
other people yawn would selectively enhance the
detection of snakes. Specifically, we predicted
that participants would (1) detect target snakes
more rapidly, (2) show fewer fixations towards
distractor frogs, and (3) show more fixations
towards distractor snakes after viewing other
people yawn. Snakes represent an ecologically
valid stimulus since they have been a recurring
survival threat to mammals during evolutionary
history (O_hman and Mineka 2003), and estimates
suggest that even now snake bites claim the
lives of approximately 100,000 people each year
(Cheng and Currie 2004). While there is evidence
that a specific fear of snakes is developed
through learning (Mineka et al. 1984), snakes
are nonetheless rapidly prioritized in the
visual system even among children without prior
experience with these dangerous animals (LoBue
and DeLoache 2008). Moreover, research indicates
that both humans and non-human primates possess
neurological adaptations designed for detecting
snakes (i.e., Snake Detection Theory) (e.g.,
Isbell 2006; 2009; O_hman et al. 2001; O_hman,
2009; Shibasaki and Kawai 2009; Van Le et al.
2013), including regions activated when sensing
yawns (Dinh et al. 2018). Therefore, if yawning
serves as a signal that increases an observer's
vigilance to threats, this should be present for
the detection of snakes.
Discussion
Although yawning is widespread across
vertebrate classes (Baenninger 1987), and
contagious yawning has been well-documented in
humans and other group-living species (Massen
and Gallup 2017), a social function to yawning
has not been established. The arousal reduction
hypothesis (Dourish and Cooper 1990; Liang et
al. 2015) states that yawns signal to others
that the individual is experiencing a down
regulation of arousal and vigilance. As an
extension of this hypothesis, we predicted that
viewing other people yawn would improve
vigilance.
In a high-powered repeated-measures design,
we found strong support for the group vigilance
hypothesis, showing that exposure to yawning
stimuli selectively enhanced the detection of
snakes. As predicted, participants detected
snakes more rapidly and showed fewer fixations
on distractor frogs after viewing vid- eos of
people yawning. In addition, the fixation
frequency on snake distractors was higher during
frog-target searches, albeit marginally,
following exposure to yawning stimuli. These
effects occurred independent of whether
participants reported yawning contagiously as a
result of the stimuli, and are consistent with
past research showing that merely sensing yawns
in others activates neural substrates (i.e., PFC
and STS) involved in threat detection, sustained
attention, and visual search (Bichot et al.
2015; Dinh et al. 2018; Ellison et al. 2004;
Mobbs et al., 2007; Nelson et al. 2014;
Parasuraman et al. 1998). The fact that exposure
to people yawning improves the detection of
snakes, but not frogs, implies that the
neurological effects of observing yawns are
domain specific to threaten stimuli.
A similar, yet distinct connection between
yawning and vigilance has previously been
suggested in the literature, though this relied
on the transmission of yawn contagion (Gallup
and Gallup 2007). According to the brain cooling
hypothesis, the physiological consequences of
yawning serve to counteract intermittent rises
in brain temperature and enhance mental
processing, and thus the transmission of yawns
across group members through contagion is
predicted to improve collective vigilance and
facilitate adaptive responses to external
stimuli (Miller et al. 2012b). However,
psychological experiments show that contagious
yawning is highly variable and occurs in less
than 50% of participants even following exposure
to repeated yawning stimuli (Platek et al. 2003;
see Anderson et a, 2004 for similar findings in
chimpanzees), suggesting an even lower rate of
contagion under natural conditions (Anderson
2020; Kapita_ny and Nielsen 2017). In addition,
research measuring brain activity through
electroencephalography has cast doubt on whether
the motor action pattern of yawning alters
vigilance levels (Guggisberg et al. 2007),
though these particular findings may not
generalize to the larger population since the
sample studied experienced excessive daytime
sleepiness (Gal- lup 2011). Conversely, if
merely sensing yawns in others is sufficient to
improve vigilance, as shown here, then even
partial spreading of this response through
contagion could effectively modify the
collective detection of threats among groups in
real-world settings. Research examining the
spatial and temporal factors driving the
acquisition of visual information in human
crowds suggests that signals from just a small
proportion of contagious yawners could propagate
among natural aggregates (Gallup et al. 2012).
Therefore, the current findings are consistent
with the hypothesis that contagious yawning
enhances group vigilance (Gallup and Gallup
2007), but indicate that this follows at least
in part, if not primarily, from a signaling
function of yawning.
These findings offer novel insights into the
multifunctionality of yawning in social species,
and improve our understanding of some previously
documented factors that influence yawn
contagion. In light of the effects observed
here, the high spontaneous yawning frequency
experienced in the evening (e.g., Zilli et al.
2007), for example, appears to not only function
in triggering neurophysiological changes at the
end of the waking hours (Gallup and Gallup 2007;
Provine et al. 1987), but may also serve as a
signal to enhance the detection of threats
during this vulnerable period of the night prior
to sleep onset. For example, previous research
has shown that snake bites are most common in
the evening (Rahman et al. 2010), when the
incidence of contagious yawning is highest
(Giganti and Zilli 2011). From an evolutionary
perspective, the higher rate of contagious
yawning between kin and in-group members
reported in Hominidae (Campbell and De Waal
2011; Norscia and Palagi 2011; Norscia et al.
2020; Palagi and Norscia 2013; Palagi et al.
2014) is consistent with the proposed signaling
function to yawning as this could promote
inclusive fitness.
Some limitations to this study should be
acknowledged. For one, although we demonstrate a
robust effect on vigilance following exposure to
yawning, the video stimuli used as a control did
not include a comparable, non-yawning, gaping of
the jaw. Therefore, in addition to the presence
or absence of yawning, there were differences
between these conditions in terms of a wide
mouth opening. However, there are strong grounds
to expect that the results here are specific to
yawning and not from other gaping movements. In
particular, there is clear neurological evidence
that humans begin to discriminate yawning from
other mouth movements in infancy (Tsurumi et al.
2019). Moreover, studies demonstrating an
enhanced activation of brain regions involved in
threat detection after viewing yawns previously
controlled for gaping and wide mouth openings,
showing that these neurologic effects are tied
to the distinct motor action pattern of yawns
(Nahab et al. 2009; Schu_rmann et al. 2005;
Tsurumi et al. 2019). In other words, simply
viewing non-yawning gaping movements fails to
induce comparable neural changes in the PFC and
STS that are proposed to explain these observed
effects.
Another limitation to this study was the use
of just one type of threatening and neutral
animal within the search tasks, i.e., snakes and
frogs. Although snakes represent a recurrent
survival threat to humans during evolutionary
history, and there is evidence for specialized
neurobiological adaptations in primates for
detecting snakes (Isbell 2006, 2009; O_hman et
al. 2001; O_hman, 2009; Shibasaki and Kawai
2009; Van Le et al. 2013), it remains unknown
whether exposure to yawning would improve the
detection of other types of threatening
stimuli.
Further research should therefore expand
upon these initial findings using a variety of
threatening and non-threatening stimuli. For
example, to assess whether the neurological
effects of observing yawns are specific to
ancestral threats, future research could
investigate whether seeing others yawn similarly
enhances the detection of novel threats that are
learned within modern environments (e.g., guns
and hypodermic needles).
The experimenter presence during testing was
also a limitation to this study, as it likely
reduced the rate of yawn contagion (Gallup et
al. 2016; 2019). While we were able to show that
the enhanced vigilance from viewing yawns was
independent of whether participants reported
yawning contagiously, the small number of
yawning participants did not permit statistical
comparisons to participants that did not yawn.
However, descriptive data in Table 1 indicate a
Data presented as mean ± standard deviation
greater improvement in detection latency during
snake trials for participants that yawned,
suggesting that the combination of visual
exposure to yawns and subsequent yawn contagion
may produce an even greater effect on vigilance
(as suggested by the brain cooling hypothesis,
Gallup and Gallup 2007). Further research is
needed to examine this possibility, as well as
whether merely sensing yawns in others induces
changes in arousal similar to when individuals
experience yawning themselves (Baenninger
1997).
In summary, the findings from this
study provide the first experimental evidence
for a social function to yawning in any species,
and imply the presence of a previously
unidentified psychological adaptation for
preserving group vigilance. We hope this work
spurs future research examining the relationship
between yawning and vigilance in both humans and
non-human animals. In addition to replicating
and extending upon the visual search tasks
performed here in the laboratory, future studies
could test for similar effects using auditory
stimuli (Massen et al., 2015). Moreover,
follow-up studies should investigate how sensing
others yawn alters scanning rates and other
indicators of vigilance under natural
conditions. If attempts to replicate and expand
upon the group vigilance hypothesis are
successful, this theoretical insight into the
signaling function of yawning could provide a
major advance in our understanding of the
evolution and elaboration of yawning via
contagion and distinct yawn- types among social
vertebrates.
