-
- Abstract
-
- Yawning is a stereotyped action pattern that
is prevalent across vertebrates. While there is
growing consensus on the physiological functions
of spontaneous yawning in neurovascular
circulation and brain cooling, far less is known
about how the act of yawning alters the
cognition and behavior of observers. By bridging
and synthesizing a wide range of literature,
this review attempts to provide a unifying
framework for understanding the evolution and
elaboration of derived features of yawning in
social vertebrates. Recent studies in animal
behavior, psychology and neuroscience now
provide evidence that yawns serve as a cue that
improves the vigilance of observers, and that
contagious yawning functions to synchronize
and/or coordinate group activity patterns. These
social responses to yawning align with research
on the physiological significance of this
behavior, as well as the ubiquitous temporal and
contextual variation in yawn frequency across
mammals and birds. In addition, these changes in
mental processing and behavior resulting from
the detection of yawning in others are
consistent with variability in the expression of
yawn contagion based on affinity and social
status in primates. Topics for further research
in these areas are discussed.
-
- Résumé
-
- Le bâillement est un comportement
stéréotypé chez tous les
vertébrés. Si l'on s'accorde de
plus en plus sur les fonctions physiologiques du
bâillement spontané dans la
circulation neuro-vasculaire et le
refroidissement du cerveau, on en sait beaucoup
moins sur la façon dont l'acte de
bâiller modifie la cognition et le
comportement des observateurs. En reliant et en
synthétisant un large éventail de
littérature, cette revue tente de fournir
un cadre unifié pour comprendre
l'évolution et l'élaboration des
caractéristiques dérivées
du bâillement chez les
vertébrés sociaux. Des
études récentes sur le
comportement animal, la psychologie et les
neurosciences prouvent aujourd'hui que les
bâillements servent d'indice pour
améliorer la vigilance des observateurs,
et que les bâillements contagieux ont pour
fonction de synchroniser et/ou de coordonner les
modèles d'activité de groupe. Ces
réponses sociales au bâillement
s'alignent sur les recherches concernant la
signification physiologique de ce comportement,
ainsi que sur la variation temporelle et
contextuelle omniprésente de la
fréquence des bâillements chez les
mammifères et les oiseaux. En outre, ces
changements dans le traitement mental et le
comportement résultant de la
détection du bâillement chez les
autres sont cohérents avec la
variabilité dans l'expression de la
contagion du bâillement basée sur
l'affinité et le statut social chez les
primates. Des sujets pour des recherches
ultérieures dans ces domaines sont
discutés.
Tous
les articles d'Andrew Gallup
- Tous
les articles sur la contagion du
bâillement
- All
articles about contagious
yawning
-
- Yawning is considered a stereotyped or fixed
action pattern and appears to have similar
within-species duration, interval and
variability (Provine, 1986). Characterized by a
three-phase response, yawns are defined by an
involuntary and powerful gaping of the jaw, a
temporary period of peak muscular contraction
with head titling and eye closure and a passive
closure of the jaw (Barbizet, 1958). Among
terrestrial vertebrates, the first two phases of
this response often include a deep inhalation of
air, while the third phase is accompanied by a
shorter expiration. Yawning and similar
yawn-like gaping behaviors are conspicuous in
nature and have been documented within all
classes of vertebrates (e.g. Baenninger, 1987;
Craemer, 1924; Luttenberger, 1975; Rasa, 1971;
Sauer & Sauer, 1967). The omnipresence of
this behavior across diverse species and
lineages suggests that it is phylogenetically
old and likely evolved with the emergence of
jawed fishes.
-
- The widespread nature of spontaneous, or
nonsocial, yawning suggests it is an adaptation
that holds important functionality. In fact,
Charles Darwin even contemplated the conserved
nature of yawning among humans and nonhuman
animals in formulating his theory of natural
selection (Darwin, 1987). Yet, clearly the mere
pervasiveness of a trait both within and across
species does not imply functional significance,
since it could represent a by-product or
spandrel (Gould & Lewontin, 1979). For
yawning, however, the case for adaptation
becomes stronger when considering its hedonistic
properties (Provine, 1986), the risks for
subluxation of the jaw (Tesfaye & Lal, 1990)
and associated costs of drawing unwanted
attention, momentarily decreasing alertness
and/or conflicting with immediate anti-predatory
behaviors (Miller et al., 2010). Moreover,
recent neurological studies provide further
support for an adaptive significance to this
behavior (Gallup, Church, & Pelegrino,
2016). In particular, recent phylogenetically
controlled analyses from >100 species of
birds and mammals revealed robust positive
correlations between yawn duration and brain
mass and overall and cortical/pallium neuron
totals (Massen et al., 2021). These findings
demonstrate a link between yawn duration and
brain size and complexity that cannot be
explained by allometry alone, indicating yawns
likely serve an important neurophysiologic
function that has been conserved across amniote
evolution.
-
- Studies examining the ultimate mechanisms of
yawning typically focus on roles either in
physiology or in social behavior (Guggisberg et
al., 2010). Instead of one or the other,
however, emerging research indicates that
yawning holds both physiological and social
functionality. That said, the ubiquity of
yawning across lineages, within nonsocial
animals and during periods of seclusion leads to
the conclusion that the primitive feature of
this behavior is physiologic. Accordingly, any
social roles of yawning in gregarious species
would represent a more recently derived feature
of this trait, built upon the original
neurophysiological function(s) shared across
vertebrates (Gallup, 2011). This perspective can
be further
- illustrated when comparing spontaneous
yawns, which are generated by internal changes
in physiology, with contagious yawns, which are
triggered socially by sensing the yawns of
others. By definition, every contagious yawn can
be traced back to an original spontaneous yawn,
and thus contagious yawning must have evolved
more recently in time. Further lines of evidence
also lead to the same conclusion. Spontaneous
yawning is ubiquitous among vertebrates
(Baenninger, 1987; Massen et al., 2021), appears
to be a universal act within a given species
(Walusinski, 2018) and begins early on during
embryological development (de Vries et al.,
1982). These features all indicate that
spontaneous yawning holds basic and important
functionality that is not social. Conversely,
contagious yawning has only been documented in
social species (Massen & Gallup, 2017;
Palagi et al., 2020), shows individual
variability in expression (humans, Homo sapiens:
Provine, 1986; chimpanzees, Pan troglodytes:
Anderson et al., 2004) and does not develop
until after infancy (humans: Cordoni et al.,
2021; Millen & Anderson, 2011; chimpanzees:
Madsen et al., 2013; domesticated dogs, Canis
lupus familiaris: Madsen & Persson, 2013).
Collectively, these lines of evidence suggest a
more recent phylogenetic origin for yawn
contagion.
-
- This review will highlight the current
scientific understanding of the ways in which
yawns alter the cognition of observers and
facilitate changes in group dynamics across
diverse species, as well as offer suggestions
for future investigation in these areas. In
particular, various lines of research will be
presented that reveal adaptive outcomes to (1)
the mere detection of yawns as well as (2)
subsequent yawn contagion. In both cases, it is
essential to understand the underlying
physiological causes and consequences of
spontaneous yawning. First, when it comes to
yawn detection, the internal changes that
initiate this behavior in the actor are what
determines the information that is transmitted
to receivers. In other words, the way yawns
change the behavior of observers hinges upon
what they reveal about the internal state of the
yawner. Second, when it comes to contagious
yawns, an under- standing of the biological
significance of this motor action pattern is
essential to appreciate how its propagation via
contagion may then go on to alter subsequent
behavior of the collective. Not only do
spontaneous and contagious yawns share a similar
morphology (i.e. they appear indistinguishable
from one another), but based on the cumulative
properties of evolution, we should expect that
they also share similar fundamental mechanistic
and perhaps functional properties. Accordingly,
the factors known to trigger spontaneous yawns
should have a similar effect on yawn contagion.
This view is supported by psychological research
showing that the expression of contagious
yawning can be effectively modulated by the same
physiological variables known to modulate
spontaneous yawning. These include circadian
factors (Gallup et al., 2021; Giganti &
Zilli, 2011), cooling and warming of the brain
via temperature manipulations to the neck and
skull (Gallup & Gallup, 2007; Ramirez et
al., 2019), ambient temperature variation (e.g.
Eldakar et al., 2015; Massen et al., 2014) and
stressful situations (Eldakar et al., 2017).
Therefore, prior to focusing on the social
nature of yawning, I discuss the literature on
the physiology, contexts and environ- mental
triggers of spontaneous yawning.
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- FUNCTION(S) OF SPONTANEOUS
YAWNING
- Numerous hypotheses have been proposed to
explain the physiological significance of
yawning (e.g. Smith, 1999), but most lack
empirical support or have been falsified. This
includes the common, but incorrect, assertion
that yawning functions to equilibrate blood
oxygen levels. Through a series of elegant
experiments on human subjects, Provine, Tate, et
al. (1987) demonstrated that yawn frequency is
not altered by breathing enhanced or decreased
levels of O2 or CO2, and physical exercise
sufficient to double breathing rates had no
effect on yawning. It has therefore been
concluded that yawning and breathing are
controlled by different mechanisms, and it is
now widely accepted in the scientific liter-
ature that respiration is not a necessary
component of yawning (Corey et al., 2012;
Guggisberg et al., 2010). These conclusions also
align with recent research showing that
yawn-like behavior of common bottlenose
dolphins, Tursiops truncatus, occurs in the
absence of breathing (Enokizu et al.,
2021).
-
- Instead, studies suggest that yawning
functions to facilitate state change (Provine,
1986, 2005) and increase arousal (Greco &
Baenninger, 1991; Matikainen & Elo, 2008;
Walusinski, 2006). The state change hypothesis
has shown to be a powerful framework for
understanding this behavior, as yawns are by far
most frequent during changes in state associated
with behavioral transitions, such as from
sleeping to waking, from waking to sleeping and
from fluctuations of attentiveness and boredom,
and even sexual arousal (Provine, 2005). Related
to the switching of activity patterns, yawns
commonly occur in anticipation of important
events and tend to be followed by an arousing
effect both behaviorally and physiologically
(reviewed by Baenninger, 1997). In addition,
laboratory studies have shown that electrical
and chemical stimulation of the paraventricular
nucleus of the hypothalamus, the brain area that
controls yawning (Argiolas & Melis, 1998;
Melis et al., 1987), evokes both yawning and
cortical arousal in Wistar rats (Sato-Suzuki et
al., 1998; Seki et al., 2002). Mechanistically,
state change and arousal could be achieved
through the acceleration of heart rate,
intracranial circulation and cerebrospinal fluid
flow produced by the deep inhalation and
powerful stretching of the jaw during yawning
(Askenasy, 1989; Matikainen & Elo, 2008;
Schroth & Klose, 1992; Walusinski,
2014).
-
- Given the rise in yawn frequency prior to
sleep onset (e.g. Provine, Hamernik, et al.,
1987; Zilli et al., 2007), however, it be- comes
clear that not all yawns result in increased
arousal. Although yawning consistently precedes
initial increases in motor activity (Baenninger
et al., 1996) and skin conductance (Greco &
Baenninger, 1991), subsequent changes in arousal
and alertness from this behavior may be governed
by circadian factors. This perspective can
potentially explain differences in the
neurological effects documented after yawns in
humans as measured by elec- tro-encephalography.
For example, during the intravenous induction of
general anaesthesia, which produces a controlled
loss of awareness during an otherwise active
state, yawns are frequently observed and induce
counteracting spikes in arousal (Kasuya et al.,
2005). Among individuals experiencing excessive
sleepiness, however, yawns occur during periods
of progressive drowsiness and sleep pressure but
fail to produce increases in arousal (Guggisberg
et al., 2007). Therefore, while yawning is
consistently triggered during low vigilance, it
may be that increases in arousal from this
action pattern occur primarily during waking and
active states rather than during periods of
sleepiness/fatigue prior to resting or sleep
onset.
-
- More recent research provides evidence for a
thermoregulatory function to yawning in
homeotherms (Gallup & Gallup, 2007, 2008).
This hypothesis proposes that yawns function to
cool the brain, which in turn could improve
alertness and mental processing efficiency of
the yawner. Accordingly, yawns should be
triggered by initial rises in brain temperature
and the action pattern of yawning should
function as a compensatory brain cooling
mechanism by promoting increased cerebral blood
flow, ventilation of the sinus system and
countercurrent heat exchange with the ambient
air (reviewed by Gallup & Eldakar, 2013).
Consistent with these pre- dictions, laboratory
studies on humans, rodents and birds show that
yawns are preceded by rises in brain/skull
temperature and that, following the execution of
this behavior, temperatures
- decrease significantly (Eguibar et al.,
2017; Gallup & Gallup, 2010; Gallup et al.,
2017; Shoup-Knox et al., 2010). Moreover, the
manipulation of brain temperature in humans has
recently been shown to produce predicted changes
in yawn frequency (Ramirez et al., 2019). In
addition, consistent with the view that yawning
evolved a brain cooling function, comparative
studies on humans (Massen et al., 2014),
nonhuman primates (Macaca fascicularis: Deputte,
1994; Cebus capucinus: Campos & Fedigan,
2009), rats (Rattus norvegicus: Gallup et al.,
2011) and birds (Melopsittacus undulatus: Gallup
et al., 2009, 2010) all show that yawn frequency
can be reliably manipulated by changes in
ambient temperature.
-
- CONTEXTS OF SPONTANEOUS YAWNING
- Consistent with the aforementioned
physiological significance of yawning, a large
number of comparative studies have revealed
similar contexts and behavioral changes that
accompany yawns across diverse species that
relate to state change, arousal and
thermoregulation. In particular, this includes
the close temporal connection between sleeping
and waking, activity patterns and stress.
-
- Circadian Variation and Behavioral
Transitions
- The most well-documented feature of yawning
across different species is its link to
circadian changes in sleep and activity. Studies
in humans consistently show a bimodal
distribution in yawn fre- quency during the day,
with an initial rise in the rate of yawning
shortly after waking in the morning and a larger
increase in yawn frequency in the evening prior
to sleep onset (Baenninger et al., 1996; Giganti
et al., 2010; Provine, Hamernik, et al., 1987;
Giganti & Zilli, 2011; Zilli et al., 2007,
2008). Consistent with links to drowsiness,
human yawns are also more common during periods
of boredom and/or low levels of stimulation
(Provine & Hamernik, 1986). In addition to
showing clear connections to state change and
modified arousal, changes in yawn frequency
before and after sleeping correlate strongly
with circadian fluctuations in brain/ body
temperature (Landolt et al., 1995).
-
- Similar temporal patterns of yawning are
observed in wild nonhuman primates, including
grey-cheeked mangabeys, Lophocebus albigena, and
crab-eating macaques, M. fascicularis, where
pre- and post-sleep yawning peaks occur
throughout the day (Deputte, 1994). Analogous
patterns are also observed in Sprague Dawley
rats in the laboratory, whereby yawns occur with
greatest frequency during transitional
sleep/wake phases (Anias et al., 1984). In
captive chimpanzees, one study found that nearly
all in- stances of yawning (98.2%) occurred
during periods of rest while sitting and lying
down (Vick & Paukner, 2010). Yawning also
commonly occurs under similar contexts in sea
lions (Otaria flavescens) (Palagi,
Guille_n-Salazar, et al., 2019) and has been
linked with sleep or recumbency periods in
African elephants, Loxodonta africana (Rossman
et al., 2017).
-
- Yawning appears to be driven by similar
circadian factors in birds as well. In the South
African ostrich, Struthio camelus australis, for
example, it is noted that yawning occurs just
prior to sleeping/ resting and again when a rest
has been interrupted (Sauer & Sauer, 1967).
In captive budgerigars, M. undulatus, the
temporal variation in yawning also varies across
the day and is frequent in the evening prior to
sleep onset (Miller, Gallup, Vogel, Vicario, et
al., 2012).
-
- Based on the circadian factors that
influence yawning and the purported arousing
function of yawns (Baenninger, 1997), this
behavior has also been noted to precede
increases in activity levels across taxa. In
preterm human infants, yawns appear to increase
behavioral arousal and predict higher motoric
activation (Giganti et al., 2002). Similarly,
among young adults (e.g. college students),
instances of yawning seem to be unvaryingly
followed by an increase in activity (as measured
by wrist movement) (Baenninger et al., 1996).
Likewise, an increase in locomotion within the
first few minutes after yawning has been
documented in both captive chimpanzees (Vick
& Paukner, 2010) and bottlenose dolphins
(Enokizu et al., 2021). Yawning is also common
during varied behavioral transitions in wild
populations of ringtailed lemurs, Lemur catta,
and white sifaka, Propithecus verreauxi
(Zannella et al., 2015). Analogously, yawns
occur primarily upon arousal from recumbency in
African elephants (Rossman et al., 2017) and
alongside new phases in activity among South
African ostriches (Sauer & Sauer,
1967).
-
- Stress and Anxiety
- Yawning also tends to increase during and
following periods of stress across diverse
species. Stressful situations naturally elicit
changes in mental state and arousal, and among
varied physio- logical effects, stress produces
rises in bodily temperature (i.e. stress-induced
hyperthermia: Olivier et al., 2003; Zethof et
al., 1994). In humans, increases in yawning have
been observed lead- ing up to stressful and
anxiety-provoking events, such as in para-
troopers prior to their first free-fall,
musicians waiting to perform and Olympic
athletes prior to competition (Provine, 2005).
Among nonhuman primates, yawning and other
self-directed behaviors (e.g. scratching,
self-grooming) are considered an indicator of
psychosocial stress and anxiety (Maestripieri et
al., 1992). In female olive baboons, Papio
anubus, for example, self-directed behaviors
like yawning increase substantially when the
closest neighbour is dominant compared to
subordinate (Castles et al., 1999). For wild
chimpanzees, yawning has been noted to increase
in the presence of humans (Goodall, 1968) as
well as following vocalizations from
neighbouring groups of conspecifics (Baker &
Aureli, 1997). Simi- larly, a positive
correlation has been observed between yawn
frequency and aggressive behavior in Przewalski
horses, Equus ferus przewalskii (Gorecka-Bruzda
et al., 2016). Yawning also increases following
nonsocial stressors. In strepsirrhine primates,
yawns in- crease following alarm calls or after
predator attacks (Zannella et al., 2015), and
fear conditioning trials have been shown to
induce yawning in Wistar rats (Kubota et al.,
2014).
-
- A combination of experimental and
observational studies across a diverse array of
mammals and birds have revealed a distinct
temporal relationship between the onset of
stress and the associ- ated yawning response
(Demuru & Palagi, 2012; Eldakar et al.,
2017; Fenner et al., 2016; Liang et al., 2015;
Miller et al., 2010; Miller, Gallup, Vogel,
& Clark, 2012; Moyaho & Valencia, 2002).
For example, in a study of captive budgerigars,
yawns were measured over a 1 h period following
handling restraint (Miller et al., 2010). In the
first 20 min following this encounter, yawning
was relatively infrequent (~1.5 M yawns/h), but
in the next 20 min, yawn frequency more than
tripled (>5 yawns/h). Moreover, yawn latency
was negatively correlated with body temperature
increases due to handling, i.e. birds that were
more hyperthermic yawned sooner. In a separate
study on wild Nadza boobies, Sula granti,
yawning was measured in adult birds during and
after a comparable human capture-restraint
stressor (Liang et al., 2015). Similar to
budgerigars, booby yawns were absent during the
stressor itself and remained at low frequency
from 0 to 30 min following release (median 1Ú4
0) before increasing significantly 30e60 min
thereafter (median 1Ú4 2). Lastly, in a study on
humans, Eldakar et al. (2017) examined the
impact of an acute physical stressor (cold
pressor test) on contagiously triggered yawning.
Analogous to the avian research, yawns were
infrequent immediately following the stressor,
but 20min thereafter both the overall frequency
of yawning and the number of participants that
yawned at least once during testing doubled.
Taken together, these findings appear to reveal
a homologous temporal effect regarding the
relationship between yawning and acute physical
stress in birds and mammals, whereby yawning is
inhibited during stressors, but then becomes
potentiated thereafter.
-
- THE DETECTION OF YAWNS IN OTHERS
- Atop the physiological significance of
yawning, researchers have long posited
additional social functions to this behavior
(Deputte, 1994; Leone et al., 2014; Moyaho et
al., 2017; Sauer & Sauer, 1967). In
particular, it was initially suggested that,
among primates, yawns preceded by a social
interaction could provide a communicative
function to conspecifics (Bolwig, 1959). In
order to function in this capacity, however,
yawns must be detected and distinguished from
background noise by receivers (Wiley, 2006). In
support of this view, recent neurological
research shows that human infants as young as 5
months old can discriminate yawning from other
types of mouth movements (Tsurumi et al., 2019).
Using functional near- infrared spectroscopy,
the presentation of yawning stimuli produced a
significantly increased haemodynamic response at
the superior temporal sulcus, as measured by the
concentration of oxyhaemoglobin. This work
indicates that the neural mechanism underlying
the processing of yawning movements develops
very early on in humans e at about the same time
infants begin to discriminate emotional facial
expressions (Kotsoni et al., 2001; LaBarbera et
al., 1976) e suggesting that the detection of
yawns in conspecifics is biologically
important.
-
- Given the close relation to sleeping, it has
been proposed that yawns serve as a paralingual
signal for drowsiness in humans (Provine,
Hamernik, et al., 1987). As yawns are also noted
during states of hunger and psychological stress
in nonhuman primates, Deputte (1994) suggested
that yawning could be viewed as an indicator of
'uneasiness' similar to other self-directed
behaviors. More recently, in an attempt to
account for the varied contexts and situations
in which yawning is elicited, Guggisberg et al.
(2010) proposed that yawns function in
communicating mild to moderately unpleasant, but
not immediately threatening, states to other
members of a group. However, this appears overly
general and nonspecific. In order for traits to
evolve a signalling function as stated, the
information transmitted by the sender must be
reliable and easily interpreted (Searcy &
Nowicki, 2010).
-
- One potentially unifying feature of
spontaneous yawns is that they reflect a current
state of low arousal and vigilance and rising
brain temperature. Therefore, the act of yawning
could provide meaningful information to
conspecifics. Recently, following the
observation that yawning is absent during
physical stressors but then potentiated
thereafter in Nazca boobies, Liang et al. (2015)
introduced the arousal reduction hypothesis,
which predicts that yawns signal to others that
the individual is experiencing a down regulation
of arousal and vigilance. This hypothesis is
consistent with psychological studies showing
yawns increase in frequency during sleepiness
and fatigue (Giganti et al., 2010; Provine,
Hamernik, et al., 1987; Zilli et al., 2008) and
periods of boredom (Provine & Hamernik,
1986), as well as neurological studies
demonstrating that brain markers of decreased
vigilance precede the act of yawning (Guggisberg
et al., 2007; Kasuya et al., 2005). However,
this hypothesis falls short in a number of
important areas. At its basis, signals are
traits that evolved to alter the behavior of
another organism (Maynard Smith & Harper,
2003), and the receiver must benefit from the
information being transmitted (Searcy &
Nowicki, 2010). As stated, the arousal reduction
hypothesis is functionally unclear and fails to
stipulate the benefits of yawning and who
receives such benefits. In addition, this
hypothesis is inconsistent with evidence for a
clear arousing effect to some yawns (for a
commentary, see Gallup & Clark, 2015).
-
- To date, the view that yawning evolved as a
signal has not been empirically supported. That
is, there are no studies showing that
spontaneous yawns are elicited in ways or
contexts that serve to intentionally convey
information and alter the behavior and/or mental
processing of recipients. An exception to this
would be a distinct pattern of yawn-like
behaviors within sexually dimorphic nonhuman
primates. In particular, modified mouth-gaping
actions from males, which are referred to as
tension or aggression yawns, are known to play a
role in threat displays (Altmann, 1967;
Bertrand, 1969). This was in fact first
described by Charles Darwin in The Expression of
the Emotions in Man and Animals (Darwin, 1872).
In such cases, a dominant male will gape his
mouth open while fixing his eyes on a target
individual (a subordinate) and displaying his
canines. These yawn-like displays have been
documented dur- ing antagonist interactions and
hostile social situations across different old
world monkeys (Macaca nigra: Hadidian, 1980; M.
fascicularis and Macaca fuscata: Troisi et al.,
1990; Cercocebus albigena and M. fascicularis:
Deputte, 1994; Theropithacus gelada: Leone et
al., 2014). Unlike true yawns (see definition
above), however, which typically include the
tilting of the head and closure of the eyes
(Deputte, 1994), the display yawner fixes their
attention on the target during the episode to
monitor the effect of the threat. These
tension/aggression yawns also vary in other
morphological characteristics, whereby the
yawner uncovers their gums to more clearly
expose their canines (Leone et al., 2014;
Zannella et al., 2017), which is consistent with
the view that these yawns are most common in
species with sexual dimorphism in canine size.
Therefore, while these threat displays indeed
appear to hold a communicative function, they
are distinct from the more ubiquitous forms of
yawning related to sleeping, arousal and thermo-
regulation in other animals.
-
- Yawning as a Cue
- Yawns could still alter the behavior of
conspecifics without evolving a specific
communicative function. Building from ideas
presented in the arousal reduction hypothesis
(Liang et al., 2015), and linking directly to
known physiological function(s) and con- texts
of spontaneous yawns, Gallup and Meyers (2021)
recently proposed specific yawn-induced changes
in mental processing that should follow the
observation of yawns in others. In particular,
it was predicted that seeing others perform this
action pattern would enhance the vigilance of
observers as a means of compensating for the
diminished arousal and vigilance experienced by
the yawner. Independent of the resultant changes
to the mental state of the yawner, which are
likely tied to circadian factors (as discussed
above), yawns are consistently triggered during
states of low arousal and vigilance (Guggisberg
et al., 2007; Kasuya et al., 2005) and rising
brain temperature (Shoup-Knox et al., 2010).
Although initially described as a signal, in
this case yawns likely serve as a cue whereby
the detection of this behavior provides
information about the current (reduced)
alertness of the yawner, which in turn induces
neurological changes to enhance the vigilance of
observers. This was termed the group vigilance
hypothesis.
-
- In support of this hypothesis, neuroimaging
studies on humans show distinct patterns of
brain activation following exposure to yawning
stimuli that are indicative of improved threat
detection. For example, merely seeing and
hearing other people yawn activates regions of
the prefrontal cortex (Arnott et al., 2009;
Nahab et al., 2009) and the superior temporal
sulcus (Schürmann et al., 2005; Tsurumi et
al., 2019). These brain regions are known to be
involved in attentional allocation to visual
search (Bichot et al., 2015; Ellison et al.,
2004), the detection of biologically relevant
and threatening stimuli (Dinh et al., 2018;
Mobbs et al., 2007) and vigilance (Nelson et
al., 2014; Parasuraman et al., 1998).
-
- As a direct test of the group vigilance
hypothesis, Gallup and Meyers (2021) had 38
human subjects complete a series of visual
search tasks for detecting snakes and frogs
(repeated measures design). Snakes represented a
recurrent evolutionary threat to humans
(Headland & Greene, 2011; Isbell, 2006;
Kasturiratne et al., 2008), while frogs served
as a control stimulus. Participants were
displayed eight-image arrays, where a single
snake or single frog was presented among seven
distractor images. During each trial,
participants were tasked with locating the
single target image (a frog or snake) as quickly
as possible. A series of snake-target and
frog-target searches were performed both after
viewing videos of people yawning and after
viewing the same people display neutral behavior
with non-yawning mouth movements. Eye tracking
was used to measure the latency to fixate on
target images across trials. As predicted by the
group vigilance hypothesis, vigilance was
selectively enhanced after viewing videos of
other people yawning. That is, participants
detected snakes more rapidly after seeing other
people yawn, while this manipulation had no
effect on the detection of frogs. The results
from Gallup and Meyers (2021) are consistent
with studies on the physiological significance
and con- texts of spontaneous yawning and
represent the first experimental evidence for
changes in cognitive performance induced merely
by the observation of yawns in others.
-
- CONTAGIOUS YAWNING
- The detection of yawns from conspecifics is
also known to elicit more overt behavioral
changes, such as yawn contagion, whereby the
yawns of others can trigger the reflexive
matching of this action pattern in observers.
Studies show that contagious yawning can be
triggered through visual and/or auditory cues
(Massen et al., 2015; Norscia et al., 2020;
Palagi et al., 2009; Silva et al., 2012), and in
humans can even be induced in solitude by
thinking or reading about the act of yawning
(Greco & Baenninger, 1991; Provine, 1986,
2005). The neural mechanisms governing
contagious yawning are not well known, but
perhaps involve mirror neurons (Haker et al.,
2013). Comparatively, there is a growing number
of species with documented evidence for yawn
contagion, with the phylogeny of this behavior
possibly reflecting the conservation of a
homologous trait in great apes and convergent
evolution in other lineages.
-
- Among the great apes, experimental evidence
for contagious yawning is present in humans
(Platek et al., 2003), chimpanzees (Anderson et
al., 2004; Campbell et al., 2009), bonobos, Pan
paniscus (Tan et al., 2017), and orang-utans,
Pongo pygmaeus (van Berlo et al., 2020).
Chimpanzees also yawn contagiously in response
to human yawners (e.g. Campbell & de Waal,
2014). However, there is no evidence for yawn
contagion among gorillas, Gorilla gorilla (Amici
et al., 2014; Palagi, Norscia, et al., 2019). In
other primates, the evidence for contagious
yawning is limited. However, observations of
gelada baboons indicate yawn contagion in both
captive and wild populations (Gallo et al.,
2021; Palagi et al., 2009). There is also a
report of video-induced yawning in stump-tailed
macaques, Macaca arctoides (Paukner &
Anderson, 2006), but this response has been
interpreted as a sign of stress and anxiety
rather than contagion since the yawning stimuli
also produced an increase in other self-directed
behaviors (i.e. scratching). Other studies show
no evidence for contagious yawning in
crab-eating macaques and grey-cheeked mangabeys
(Deputte, 1978), common marmosets, Callithrix
jacchus (Massen et al., 2016), or in either
ringtailed lemurs, L. catta, or red-ruffed
lemurs, Varecia variegata rubra (Reddy et al.,
2016).
-
- Across other mammals, experimental evidence
for contagious yawning has been documented in
domesticated dogs in response to human yawns
(Joly-Mascheroni et al., 2008; Romero et al.,
2013; Silva et al., 2012) but not in response to
conspecifics (Harr et al., 2009), which could
reflect selection on the emphasis of attending
to human cues during domestication. There is
also experimental evidence for contagious
yawning in a subline of Spraguee Dawley rats
(Moyaho et al., 2015). Observational evidence
for contagious yawning is present in captive
wolves (Canis lupus lupus) (Romero et al.,
2014), and most recently, domesticated pigs, Sus
scrofa (Norscia, Coco, et al., 2021), and
African lions, Pantheo leo (Cassetta et al.,
2021). Other mammalian species with limited
evidence of yawn contagion, thus requiring
further investigation, include sheep, Ovis aries
(Yonezawa et al., 2017), African elephants
(Rossman et al., 2020), and southern elephant
seals, Mirounga leonine (Wojczulanis-Jakubas et
al., 2019). One study on horses, Equus caballus,
provided no evidence for yawn contagion
(Malavasi, 2014).
-
- Only a few studies have investigated
contagious yawning among nonmammalian species.
No formal investigations have been per- formed
on amphibians or fish, although Baenninger
(1987) assessed the temporal expression of
yawn-like behaviors in Sia- mese fighting fish,
Betta splendens, and found no evidence for
contagion. In the only study on reptiles, the
responses of red-footed tortoises, Geochelone
carbonaria, were observed following the
observation of conditioned yawn-like behavior in
a conspecific (Wilkinson et al., 2011). No
increase in tortoise yawning occurred when
compared to control conditions. To date, the
only evidence for yawn contagion in a
nonmammalian species comes from studies on
captive budgerigars, whereby yawns appear
temporally clustered within flocks under
seminatural conditions (Miller, Gallup, Vogel,
Vicario, et al., 2012) and can be experimentally
triggered following exposure to both live and
videorecorded yawns from conspecifics (Gallup et
al., 2015). In the only other study on yawn
contagion among birds, observations of captive
ravens, Corvus corax, found no evidence for this
effect (Gallup et al., 2014).
-
- Comparative studies of contagious yawning
have thus far been relatively limited, so there
are bound to be other species that show this
behavior. However, it is worth noting that there
are a number of methodological challenges to the
study of yawn contagion (Campbell & Cox,
2019; Campbell & de Waal, 2010).
Experimental studies offer the most robust test,
whereby explicit yawn versus control comparisons
can be made, but experiments are often limited
to animals in captivity. In addition, many
experiments designed to elicit yawn contagion
use video stimuli with repeated clips of
yawning, which could inadvertently produce a
supernormal stimulus (Anderson, 2010). Moreover,
video stimuli might not be optimal for all
species (D'Eath, 1998). As an alternative
experimental approach, live animals can be
paired together both with and without visual
and/or auditory access, and the temporal
association of yawning between individuals can
be assessed across conditions (e.g. Gallup et
al., 2015).
-
- Observational studies offer a more
naturalistic depiction of yawn contagion, but
these also present methodological challenges.
Such studies often classify yawns as contagious
when they occur within predetermined time
periods (i.e. 3 min or 5 min) following the
observation of a yawn from another individual
(e.g. Demuru & Palagi, 2012; Palagi et al.,
2009). However, the clustering of yawns within
groups could also result from the individuals
sharing com- mon circadian rhythms or activity
patterns and have nothing to do with contagion.
In addition, the time frames used are often
arbitrary, and different species could have
longer or shorter contagion latencies (Campbell
& Cox, 2019). As a solution to these
problems, observational studies can examine the
temporal distribution of yawning across
recording sessions to rule out circadian effects
(Miller, Gallup, Vogel, Vicario, et al., 2012),
as well as develop response curves, whereby the
rate of yawning significantly above the baseline
would be evidence of yawn contagion (Campbell
& Cox, 2019).
-
- Function(s) of Contagious
Yawning
- While numerous studies have examined
individual differences and social-psychological
correlates of yawn contagion in different
species (reviewed by Massen & Gallup, 2017;
Neilands et al., 2020; Palagi et al., 2020),
only limited research has attempted to uncover
its functional significance. That said, it has
long been speculated that the spreading of yawns
across groups may function to synchronize and/or
coordinate group behavior (e.g. Baenninger et
al., 1996; de Waal & Preston, 2017; Deputte,
1994; Guggisberg et al., 2010; Massen et al.,
2012; Miller, Gallup, Vogel, & Clark, 2012;
Prochazkova & Kret, 2017; Provine, Hamernik,
et al., 1987; Sauer & Sauer, 1967; Vick
& Paukner, 2010), which could provide
survival benefits to group members (Duranton
& Gaunet, 2016). This hy- pothesis is
consistent with the large and aforementioned
literature connecting yawns to circadian rhythms
and behavioral transi- tions. For example, given
that the neurovascular consequences of yawning
produce changes in state (Provine, 1986) and
initiate behavioral transitions and increased
movement (Baenninger et al., 1996; Vick &
Paukner, 2010), contagion could generate
coordinated or synchronized group activity. In
line with this view, ethological studies of wild
animals show that yawns are naturally clustered
within groups during collective transitions in
behavior (Deputte, 1994; Sauer & Sauer,
1967). However, these studies fail to take into
account that the individuals within these groups
are under- going similar circadian and
physiologic changes that may lead to a nonrandom
distribution of yawns and a synchronization of
activity that is independent of social influence
or function (see Campbell & Cox, 2019;
Miller, Gallup, Vogel, Vicario, et al.,
2012).
-
- To date, only one study has systematically
examined the role of contagious yawning on
behavioral synchronization. In an observational
study of wild African lions, Casetta et al.
(2021) marked the occurrence of all yawns from
19 individuals across two social groups in order
to classify the connection between yawn
contagion and motor synchrony. Yawn contagion
was defined by a yawn that followed a yawn from
another lion within a 3 min window when there
were no visual obstructions between the
individuals. Motor synchrony was defined by the
collective switching of behavior status by
either transitioning from moving to resting or
resting to moving, also within a 3 min window.
It was found that motor synchrony between lions
increased by a factor of 11 when one yawned
contagiously in response to the other, which was
significantly higher than situations without
contagion or when there were no yawns observed.
In particular, the results showed that yawn
contagion increased the likelihood that
observers would replicate the motor patterns of
actors. These findings from Casetta et al.
(2021) are notable in providing the first direct
evidence for a potential function to contagious
yawning, which will most surely lead to
follow-up research examining the role of yawn
contagion in motor synchrony across different
species.
-
- A separate, but not mutually exclusive,
adaptive hypothesis for yawn contagion stems
from the purported brain cooling function of
yawning. In particular, Gallup and Gallup (2007)
proposed that contagious yawns may have evolved
to promote overall group vigilance. Accordingly,
if yawns serve to counteract rising brain
temperature and reduced alertness and mental
processing, the transfer of this behavior to
nearby conspecifics could then in- crease their
vigilance as well. This hypothesis is consistent
with interdisciplinary lines of research
suggesting that yawns are trig- gered to
counteract decrements in alertness and arousal
(Baenninger, 1997; Kasuya et al., 2005;
Walusinski, 2006). Yet, to date, the vigilance
hypothesis has not been directly tested. One
study showed that auditory disturbances, which
elicit startle responses and vigilance behavior,
also enhance yawn contagion in budgerigars
(Miller, Gallup, Vogel, & Clark, 2012).
However, this work did not examine whether
contagious yawning produced a change in
vigilance thereafter. As previously discussed,
recent research on humans has also shown that
merely witnessing others yawn improves
individual threat detection (Gallup &
Meyers, 2021). The small number of participants
that yawned contagiously (N 1Ú4 5) in this study
did not permit statistical comparisons, but the
results were highly similar for yawners and
non-yawners. Even if vigilance is not improved
further among contagious yawners e which remains
an empirical question e the spreading of this
cue across the group via contagion should
enhance collective vigilance under natural
conditions.
-
- In addition to extending upon existing
functional hypotheses of spontaneous yawning,
and accounting for the contexts and behavioral
activities in which nonsocial yawns are most
common, the synchronization and vigilance
hypotheses are consistent with studies
documenting how various social factors modulate
yawn contagion among primates: i.e. social
status and affiliation. For example, within
dominance hierarchies, patterns of vigilance
contagion and synchronized movement are most
often initiated by high-ranking individuals (Iki
& Kutsukake, 2021), and research on
chimpanzees and bonobos shows that yawn
contagion most often stems from the yawns of
dominant group members (male chimpanzees: Massen
et al., 2012; female bonobos: Demuru &
Palagi, 2012). Similarly, within freely moving
groups, individuals with greater contact and
affiliation are more likely to display
coordinated movement (Farine et al., 2016), and
a number of studies have reported biases in yawn
contagion based on social closeness or
affiliation. This includes naturalistic
observations of humans, bonobos and gelada
baboons (Demuru & Palagi, 2012; Gallo et
al., 2021; Palagi et al., 2009, 2014; Norscia
& Palagi, 2011; Norscia et al., 2020; but
see Massen et al., 2015) as well as
video-induced experiments on captive chimpanzees
(Campbell & de Waal, 2011; Madsen et al.,
2013). As a general rule, it seems that
attention drives yawn contagion (Gallup, 2021;
Massen & Gallup, 2017). Among chimpanzees
and bonobos, attention is disproportionately
directed towards individuals that are familiar
and of the dominant sex (Lewis et al., 2021).
Biased attention towards higher-ranking
individuals is also present in other primates,
such as Angolan talapoin monkeys, Miopithecus
talapoin (Keverne et al., 1978), and rhesus
macaques, Macaca mulatta (Shepherd et al.,
2006). Similarly, primates tend to stay in close
proximity to genetic relatives and socially
bonded individuals (Macaca maurus: Matsumura
& Okamoto, 1997; C. capucinus: Perry et al.,
2008; chimpanzees: Langergraber et al., 2009),
increasing the chances of detecting and
responding to the yawns from these group members
(Gallo et al., 2021). From an evolutionary
perspective, biases in yawn contagion based on
genetic relatedness (as has been shown in
humans; Norscia & Palagi, 2011; Norscia et
al., 2020) may hold fitness benefits by
facilitating greater social cohesion and
protection among kin. Moreover, these hypotheses
offer further explanatory power for observed
differences in yawn contagion based on
reproductive status in humans. For example,
during pregnancy, women appear more susceptible
to contagious yawning (Norscia, Agostini, et
al., 2021). Given that pregnant women also have
increased reactions to threatening stimuli (Roos
et al., 2012), heightened yawn contagion could
improve vigilance and group synchronization
during a period of increased danger sensitivity.
Therefore, the synchronization and vigilance
hypotheses offer fruitful avenues for further
study.
-
- SUMMARY AND FUTURE DIRECTIONS
- Yawning is a neurophysiological adaptation
that is omnipresent across vertebrates (Massen
et al., 2021), and the detection of this action
pattern in others appears to be biologically
important among social species (Tsurumi et al.,
2019). Moreover, recent studies indicate that
yawning serves as a cue that enhances individual
vigilance and promotes motor synchrony through
contagion (see Fig. 1 for a graphic illustration
of these processes). However, additional
research is needed to replicate and further
examine the nature of these effects, as well as
investigate potential comparative differences in
these responses based by on ecological factors
and evolutionary history. In particular, future
studies could examine how exposure to yawns
alters the detection of threatening stimuli
across different species, as well as how
experimentally induced yawn contagion influences
different patterns of motor synchrony and group
coordination among human and nonhuman animals in
the laboratory. In addition, naturalistic
studies could investigate how the detection of
yawning alters scanning rates and vigilance
monitoring in free-moving groups, as well as how
yawning and other patterns of behavioral
contagion influence collective movement across
different species. For example, among many
species, yawning and stretching tend to
co-occur, and both behaviors have been found to
be contagious in budgerigars (Gallup et al.,
2017; Miller, Gallup, Vogel, Vicario, et al.,
2012). Since yawn and stretch contagion could
have similar functions among animal groups in
initiating collective action, future research
could assess whether behavioral contagion in
general is a key feature in initiating
synchrony.
-
- The current evidence suggests that yawning
serves as a cue rather than as a signal, but
future studies could further examine whether
spontaneous yawns evolved specifically to
communicate internal states and/or alter the
behavior of observers in some species. For
example, studies could investigate whether
yawning occurs more readily in the presence of
others and in contexts in which synchrony and/or
vigilance would be most advantageous to the
group. In addition, researchers could examine
patterns in the variability of yawn expression.
A recent study on macaques (Macaca tonkeana and
M. fuscata) suggests differences in the
morphology and duration of yawning are
predictive of the contexts in which this
behavior arises (Zannella et al., 2021), so
follow-up studies could also assess how
different types of yawns differentially impact
the subsequent vigilance behavior and
synchronization of observers. Similarly,
researchers could assess differences in
yawn-induced changes in behavior based on the
presence or absence of auditory cues. Vocal
components to yawning appear to be common among
humans and non-primates (e.g. Massen et al.,
2015; Palagi et al., 2009), yet seem unnecessary
for the physiological function(s) of this action
pattern. Thus, studies could investigate the
factors that contribute to variation in vocal
yawning and how the social outcomes of yawning
vary based on visual and/or auditory
detection.
- Further examination of yawning in animals
could provide important insights into the social
role of this behavior and its function in
altering group dynamics, which could in turn
offer applications for improving performance in
surveillance settings and organized group
activities in our own species. Based on what is
already known about the social nature of
yawning, it appears time to systemically examine
some of the more overt social features of this
behavior in humans. This includes the
stigmatization of yawning in some cultures
(Schiller, 2002), which leads to the active
concealment (Schino & Aureli, 1989) and/or
inhibition of yawning when in the presence of
others (Gallup, Church, Miller, et al., 2016;
Gallup et al., 2019). For example, further
research is needed to fully understand and
disentangle the potential physiologic and social
causes and consequences of inhibiting
spontaneous and contagious yawning in groups. In
line with the comparative perspective
highlighted throughout this review, the bridging
of both human and nonhuman animal research will
provide the most comprehensive understanding of
this evolutionarily conserved behavior.
-
-
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