Contrary to spontaneous yawning&emdash;an
ancient phenomenon common to
vertebrates&emdash;contagious yawning (elicited
by others' yawns) has been found only in highly
social species and may reflect an emotional
inter-individual connection. The authors
investigated yawn contagion in the domestic pig,
Sus scrofa. Owing to the complex socio-emotional
and cognitive abilities of Sus scrofa, they
posited that yawn contagion could be present in
this species (Prediction 1) and influenced by
individual/social factors (Prediction 2).
In June-November 2018, on 104 semi-free
ranging adolescent/adult pigs, 224 videos were
recorded for video analysis on yawning. Kinship
information was refined via genetic analyses.
Statistical elaboration was conducted via GLMMs
and
non-parametric/randomization/cross-tabulation
tests. They found yawn contagion in Sus scrofa,
as it was more likely that pigs yawned when
perceiving rather than not perceiving
(yawning/control condition) others' yawns
(response peak in the first out of three
minutes).
Yawn contagion was more likely: (1) in
response to males' yawns; (2) as the age
increased; (3) within short distance (1 m); (4)
between full siblings, with no significant
association between kinship and distance. The
influence of kinship suggests that&emdash;as
also hypothesized for Homo sapiens&emdash;yawn
contagion might be linked with emotional
communication and possibly contagion.
Résumé
Contrairement au bâillement
spontané, un phénomène
ancien commun aux vertébrés, le
bâillement contagieux (provoqué par
les bâillements d'autrui) n'a
été trouvé que chez des
espèces hautement sociales et peut
refléter une connexion interindividuelle
émotionnelle. Les auteurs ont
étudié la contagion du
bâillement chez le porc domestique, Sus
scrofa. En raison des capacités
socio-émotionnelles et cognitives
complexes de Sus scrofa, ils ont émis
l'hypothèse que la contagion du
bâillement pourrait être
présente chez cette espèce
(Prédiction 1) et influencée par
des facteurs individuels / sociaux
(Prédiction 2).
En juin-novembre 2018, sur 104 porcs
adolescents / adultes en semi-liberté,
224 vidéos ont été
enregistrées pour une analyse
vidéo de leurs bâillements. Les
informations de parenté ont
été affinées via des
analyses génétiques.
L'élaboration statistique a
été menée via des GLMM et
des tests non paramétriques /
randomisation / tabulation croisée. Ils
ont confirmé la réalité
d'une contagion de bâillement chez Sus
scrofa.
Il est plus probable que les porcs
bâillent lorsqu'ils perçoivent
plutôt que de ne pas percevoir (condition
de bâillement / contrôle) les
bâillements des autres (pic de
réponse dans la première des trois
minutes). La contagion du bâillement
était plus probable : (1) en
réponse aux bâillements des
mâles ; (2) à mesure que
l'âge augmenté ; (3) à
courte distance (1 m) ; (4) entre frères
et sœurs, sans association significative
entre parenté et distance. L'influence de
la parenté suggère que, comme
également supposé pour Homo
sapiens, la contagion du bâillement
pourrait être liée à la
communication émotionnelle rendant la
contagion possible.
Introduction
Contrary to spontaneous yawning&emdash;not
elicited by others' yawns&emdash;contagious
yawning takes place when the yawn emitted by a
subject (trigger) induces yawning in another
subject (responder)1. In this respect, yawning
acts as a releasing stimulus (sensu Tinbergen
and Perdeck2). Despite some morphological
variants especially described in primates (e.g.
chimpanzees, Pan troglodytes3; geladas,
Theropithecus gelada4; Tonkean macaques, Macaca
tonkeana and Japanese macaques, M. fuscata5;
humans, Homo sapiens6,7), spontaneous yawning is
considered a plesiomorphic (ancient) trait
because its basic motor pattern has been
observed in a wide array of vertebrates8. On the
other hand, contagious yawning between
conspecifics has been observed so far in a
relatively low number of species, which suggests
that this phenomenon may have appeared more
recently in vertebrate evolution9. In
particular, the presence of yawn contagion has
been found only in highly social species and
seems to be linked to the type of sociality more
than to the phylogenetic closeness9. For
example, in primates yawn contagion seems not to
be expressed in species with relatively low
levels of affiliation or tolerance
(strepsirrhines: ring-tailed lemurs, Lemur
catta, and ruffed lemurs, Varecia
variegata10,11; the cercopithecid, Japanese
macaque12; the hominid, lowland gorilla; Gorilla
gorilla13,14) whereas it is present in other (in
some cases phylogenetically close) species
showing higher levels of social affiliation
(cercopithecids: Tonkean macaque12; geladas4;
hominids: chimpanzees15,16,17; bonobo, Pan
paniscus13,18,19; humans1,6). Yawn contagion has
been also found in non-primate species
characterized by high inter-individual cohesion,
including mammals (wolves, Canis lupus lupus20;
sheep, Ovis aries21; some groups of elephant
seals, Mirounga leonina22), and one social bird
species (budgerigar, Melopsittacus
undulates23).
It has been hypothesized that the emergence
of yawn contagion has been favored by natural
selection in highly social species to enhance
synchronization between individuals (spatial
ranging, coordinated foraging, and sleep/wake
rhythms9). Indeed, in both human and non-human
mammals, spontaneous yawning can be linked to
physiological and behavioral transitions, such
as those occurring over the sleep&endash;wake
cycle or during the transitions around emotional
arousal (humans, Homo sapiens24; South American
sea lions, Otaria flavescens25; Verreaux'
sifaka, Propithecus verreauxi and ring-tailed
lemurs26; rats, Rattus norvegicus27).
In humans and great apes individual features
can influence yawn contagion. These features
include: (1) age (with the yawning response
increasing from the immature period to
adulthood; humans28; chimpanzees29; geladas4);
(2) sex of the trigger (females can elicit more
yawns in bonobos18; males can elicit more yawns
in chimpanzees and in humans for yawns that are
heard but not seen30,31); (3) sex of the
responder (with human females showing highest
frequencies of response at least under certain
conditions32). Moreover, social factors, such as
familiarity between trigger and responder, can
also affect yawn contagion (humans33;
bonobos18,34; chimpanzees17; geladas4;
wolves20). Finally, different levels in the
detectability of the yawning stimulus have been
hypothesized to influence the response9,35.
The species considered in this study is the
domestic pig (Sus scrofa), characterized by
complex cognition, psychology and sociality,
with stable relationships established early in
life and, at least in part, retained in
adulthood36,37,38,39,40,41. Hence, Sus scrofa is
a particularly suitable model to investigate
yawn contagion, addressed here for the first
time in this species. As the phenomenon of yawn
contagion might be related to emotional
communication and/or inter-individual
synchronization in both humans and other
animals9, this study on the domestic pig can be
relevant to both applied research in animal
welfare (especially livestock) and theoretical
studies on the evolutionary convergences
underlying the behavior of both humans and
non-human social species.
Based on the previous framework, we
formulated the following predictions.
Prediction 1: presence of yawn
contagion
Yawning in pigs can express emotional
arousal and chronic stress42. Domestic pigs can
be influenced by the emotional state of
others43,44, and use facial expressions to
communicate emotional states to others (e.g.
aggressive intent) and convey information about
emotional responses39. Hence, we predicted that
domestic pigs could be influenced by others'
yawns and, more specifically, that yawn
contagion could be present in Sus scrofa.
Prediction 2: modulation of yawn
contagion
Although in a variable way depending on the
species, individual, perceptive and social
factors can modulate yawn contagion9. We
therefore predicted the levels of yawn contagion
could vary depending on individual features
(i.e., sex and age) and on the social and
spatial proximity between pigs.
Discussion
Our results show that yawn contagion is
present in the domestic pig. As a matter of
fact, it was significantly more likely that the
pigs yawned after that at least one yawn had
been emitted by another pig within their visual
range (sight condition) rather than when a
physical obstacle prevented the potential
responder to see the yawning stimulus (control
condition; Prediction 1 confirmed; Table 1; Fig.
2). Moreover, similarly as in other mammalian
species21,34, pig yawn contagion was most likely
in the first minute from the emission of the
triggering stimulus (Fig. 4).
Pigs&emdash;as other highly social mammal
species showing yawn contagion (for a
review9)&emdash;can naturally form groups and
engage in stable social relationships40,41.
Immature individuals start to fine tune their
relationship with others via play, first with
littermates and later also with individuals from
other litters37,38,39. As it has been
hypothesized for other species9, it is possible
that yawning has been co-opted during evolution
to become a signal of behavioral/physiological
change that other group mates could catch and
replicate for reciprocal synchronization,
important for social life.
Our results converge in indicating that the
detection of the yawning stimulus has a crucial
role in determining the yawning response, which
is significantly enhanced if more than one
triggering yawn is emitted (Table 1, Fig. 3) and
when the potential responder is in proximity to
the trigger (²_1 m, Table 2; Fig. 5b). This
finding can be explained by the fact that pigs
(which also rely on olfaction, touch, and
hearing to orient themselves in the environment)
possess a broad visual range (owing to
lateralized eyes) but poor visual
acuity56,57,58,59,60. Considering that no yawn
was vocalized, pigs could only rely on vision to
spot mouth opening. In this respect, any element
increasing stimulus detectability (such as more
yawning stimuli or short distances) could
enhance the yawning response.
In humans, yawn contagion significantly
fluctuates during the day, with peacks in the
morning and in the evening, possibly associated
with the wake-sleep cycle61. In chimpanzees,
weak variations in yawn contagion have been
observed16. In pigs, we observed that yawn
contagion was lowest in late morning (Table 1)
probably because the pigs were fed in this time
slot and spent most of the time feeding and,
then, sleeping. This difference is likely to
disappear in the wild, where animals are not
provisioned with food. In our study, the
variation in the occurrence of yawn contagion
was not significant across the other time slots.
Thus, we cannot state that there is an
appreciable variation of the phenomenon across
the whole day, as expected for a species
that&emdash;although preferring crepuscular and
night activity&emdash;can be active over the
24h56.
Our findings indicate that the breed did not
influence contagious yawning (Table 2). To our
knowledge there is no study addressing the
possible effect of breeds on yawn contagion in
mammals. With the present data, it is not
possible to determine whether our results mean
that the yawning response is not affected by
breed or whether the absence of a significant
effect is due to the fact that the breeds of our
study individuals were mixed.
Taken together, our results also show that
while contagious yawning was significantly
influenced by the sex of the trigger (with males
eliciting more yawns than females; Table 2, Fig.
6a) and by the age of the responder (with yawn
contagion increasing as age increased, Table 2,
Fig. 6b), spontaneous yawning was not. Hence,
yawn contagion probably was not enhanced by
trigger males or responder's age as a result of
generally higher yawning levels in males or
older pigs. Inter-sexual biases in the power of
eliciting a yawning response have been found in
bonobos, where yawning in group mates can be
induced most frequently by females18, and in
humans (for vocalized yawns perceived only by
hearing31) and chimpanzees30 where males as
triggers are particularly effective in
triggering others' yawns. In humans, for
vocalized yawns that are heard but not seen, it
is possible that men's vocalizations are better
heard than women's in natural settings, often
characterized by background noises31. In
chimpanzees and bonobos, the sex bias has been
related to the dominance or social relevance of
the triggering subjects, considering that in
chimpanzees males are dominant30 whereas in
bonobos females acquire leadership by forming
coalitions18. Even though castrated males can
still fight for dominance62, it is unlikely that
dominance provides a possible explanation for
enhanced yawning response in Sus scrofa. As a
matter of fact, at the adaptive level the
dominant status of males may be not as much
relevant for yawn contagion in the light of the
species biology. Under natural conditions, in
both feral pigs and wild boars females with
offspring form matrilineal units and join
together in stable groups of variable size
whereas solitary adult males live isolated and
only temporarily join female groups40,63,64.
This social structure can explain why adult
females and not males form a linear hierarchy,
with older sows being dominant over younger
sows65,66,67,68. In this perspective, a possible
explanation for adult males being best triggers
might be the necessity of other pigs to
synchronise with reproductive males when they
temporarily join the social groups composed by
sows and offspring. However, further
investigation on this issue is necessary to
verify this possibility or formulate other
hypotheses.
With respect to age, in pigs we observed a
significant increase of yawn contagion as age
increased (Table 2; Fig. 6b). In some primate
species, yawn contagion is present in adults and
absent in infants (humans28; chimpanzees30;
geladas4). In humans, yawn contagion seems also
to decline with age in adults69 although no
conclusive results are available (e.g. see32).
Our study subjects had passed the age in which
pigs (if reproductive) reach sexual maturity
(around 6 months), but it should be considered
that in pigs body development continues up to 18
months, with the period between 6 and 18 months
sometimes referred to as adolescence70. Pigs and
humans are thought to share similar brain growth
and development patterns, with pig brain
considered closer to the human brain than other
non-human animal models in terms of size,
structure, and composition71,72,73. Ryan et
al.74 found that longitudinal effects in
magnetic resonance spectroscopy (MRS)
measurements in adolescent female pigs (from
pubescent to sexually mature) were similar to
those reported in adolescent humans. Moreover,
the domestic pigs possess complex cognitive and
affective skills, including object
discrimination, spatial learning, understanding
human cues, emotional sharing, and possible
elements of perspective taking43,75,76 (for
review36). Hence, as it has been hypothesized
for other species, the increased rates of yawn
contagion in pigs with age might also suggest
ongoing maturation of socio-cognitive skills
and/or neural networks involved in the
elaboration of social cues, developmental
changes in action-understanding or
identification of others' affective
state4,29.
Finally, in the pigs under study yawn
contagion was highest between full siblings than
in more weakly related individuals (Table 2;
Fig. 5a). Among our study animals, 88% of full
siblings came from the same litter and therefore
they had spent more time than others in close
association. Even though kinship and social
bonding are distinct aspects41,77, the kinship
bias observed in pigs might have a similar
effect on yawn contagion as the relationship
quality bias observed in other species, in which
yawn contagion was highest between strongly
bonded individuals (humans33; bonobos18,34;
chimpanzees17; geladas4; wolves20). Even if the
issue is still under debate78, it has been
hypothesized that the familiarity and/or kinship
bias observed in yawn contagion might reflect a
form of emotional contagion, a basic building
block of empathy (for review9). Indeed, domestic
pigs show emotional contagion potentials and the
ability to convey social information via facial
expressions39,43.
As explained above, in our study we found
that the spatial proximity between pigs also
enhanced yawn contagion (Fig. 5b), probably by
increasing the detection probability of the
yawning stimulus. Social closeness and tight
kinship often go in tandem with spatial
closeness, with physical proximity being
frequently used as a measure of social and
emotional engagement in social animals79. We
found that spatial distance and kinship between
trigger and potential responder were not
significantly associated with one another.
Consistently, a recent study41 found that social
proximity and relatedness were not correlated in
pigs. Thus, the yawn contagion bias observed in
pigs, might be linked to inter-individual
relatedness, and not just proximity. This
possibility can have interesting repercussions
for animal welfare studies investigating
emotional connection between individuals.
However, no conclusion can be drawn at this
stage of knowledge and further investigations,
experimentally disentangling distance, kinship
and social bond, are necessary to determine
whether yawn contagion may be driven by
familiarity per se or not.
