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- mise à jour
du
- 10 avril
2025
- Commun
Biology
- 2025;8(1):580
|
- Diving
back two hundred million years:
- yawn
contagion in fish
- Galotti A, Manduca G, Digregorio M,
Ambrosini S,
- Romano D, Andreazzoli M, Palagi E.
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- Tous
les articles sur la contagion du
bâillement
- All
articles about contagious
yawning
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- Abstract
- Yawning is a widespread and automatic
behavior in vertebrates. Yawn contagion,
responding with a yawn to others' yawns, helps
synchronize motor activities, particularly in
social animals, promoting coordination within
groups. While primarily observed in social,
endothermic species, yawn contagion remains
unconfirmed in ectotherms. We discovered yawn
contagion in zebrafish (Danio rerio). Using a
deep learning model to distinguish yawning from
breathing, we found that fish not only yawn but
also "catch" yawns from others. The presence of
yawn contagion in fish raises important
evolutionary questions, particularly regarding
its origin. According to evolutionary biology
theories, on one hand, it could be a shared
trait among vertebrates, with the secondary loss
of this phenomenon in some taxa. On the other
hand, it may be a result of convergent
evolution, emerging independently in different
evolutionary lineages as a response to the need
for synchronization of motor actions within
social groups.
-
- Résumé
- Le bâillement est un comportement
très répandu et automatique chez
les vertébrés. La contagion du
bâillement, qui consiste à
répondre par un bâillement aux
bâillements des autres, contribue à
synchroniser les activités motrices, en
particulier chez les animaux sociaux, ce qui
favorise la coordination au sein des groupes.
Bien qu'elle soit principalement observée
chez les espèces endothermiques sociales,
la contagion du bâillement n'a pas encore
été confirmée chez les
ectothermes. Nous avons découvert la
contagion du bâillement chez le poisson
zèbre (Danio rerio). En utilisant un
modèle d'apprentissage profond pour
distinguer le bâillement de la
respiration, nous avons constaté que les
poissons non seulement bâillent mais aussi
« attrapent » les bâillements
des autres. La présence de la contagion
du bâillement chez les poissons
soulève d'importantes questions
évolutives, notamment en ce qui concerne
son origine. Selon les théories de la
biologie de l'évolution, il pourrait
s'agir d'un trait commun aux
vertébrés, avec la perte
secondaire de ce phénomène chez
certains taxons. D'autre part, elle pourrait
être le résultat d'une
évolution convergente, émergeant
indépendamment dans différentes
lignées évolutives en
réponse au besoin de synchronisation des
actions motrices au sein des groupes
sociaux
-
- Introduction
- Yawning is a fixed action pattern widespread
across vertebrate taxa including fish
(Salvelinus leucomaenis)1, amphibians
(Pheognathus hubrichti)?, reptiles (Geochelone
carbonaria) 3, birds (Melopsittacus undulatus)*,
and mammals (Homo sapiens", Pan
troglodytes®, Mandrillus leucophaeus,
Panthera leo®). The evolutionary conserved
trait of yawning and its presence at an early
ontogenetic stage2,9 suggest the importance of
this behavior in physiological regulation
processes. In endothermic species, three
different phases have been operationally
identified during a yawning event i) slow mouth
opening and air inhalation, ii) maximum jaw
stretching for a short period (acme), and iii)
rapid mouth closing and air exhalation5,8,11,
although some emerging data are indicating a
certain degree of variability in the yawning
execution 12,13,14. Despite its apparent
simplicity and automaticity, one of the most
challenging aspects in the study of yawning in
species living in different environments
(terrestrial vs aquatic) 15 and phylogenetically
distant to humans is the unbiased detection of
the behavior.
-
- Yawning seems to be involved in the
regulation of various physiological functions.
It is suggested to have originally evolved as a
thermoregulatory mechanism, particularly in
endotherm vertebrates like mammals and birds
16,17,18, Moreover, the behavior has been linked
to physiological arousal, increasing heart rate
and intracranial circulation through deep
inhalation and jaw stretching 9,20 and to brain
cooling promoting wakefulness and cognitive
performance 6,21. Although most of the research
on yawning has focused on endotherms, there is
increasing evidence that yawning in ectotherms
may also play a role in physiological state
regulation such as thermoregulatory functions22.
For instance, studies on ectotherm species have
shown that yawning often occurs before a shift
in behavioral states, suggesting a role in
preparing for increased activity (fish1,23,24;
amphibians2,25 and reptiles22). In endotherms,
the state-change hypothesis posits that yawning
functions as a mechanism to induce a behavioral
transition from resting to activity, thus
increasing physiological arousal (macaques 12;
drills 7; chimpanzees 13, lions 8).
-
- If yawning is widely observed across
vertebrates, yawn contagion, the phenomenon of
responding to others' yawns with a yawn, has
frequently been reported in endothermic social
species5,20,26,22. To our knowledge, the only
study focusing on yawn contagion in an ectotherm
species (red footed tortoise, Geochelone
carbonaria?) failed to find the phenomenon. One
of the most parsimonious explanations for yawn
contagion is the
- 'chameleon effect, which posits that
perceiving a behavior leads the observer to
unconsciously imitate the gesture, aligning
individuals' activities26,27,28. Recent studies
also indicate that yawn contagion may play a
role in synchronizing group behavior. In lions
(Panthera leo), yawn contagion among group
members facilitates behavioral alignment,
ensuring synchronized activity®. Such
behavioral synchronization is vital for
maintaining social cohesion and plays a key role
in the cooperative dynamics of social species
21,28. Despite being the subject of intense and
lively scientific debate29,30,31, yawn contagion
seems also to be involved in some empathic
processes, being considered a phenomenon driven
by emotional contagion, a building block of
empathy32,33
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- To understand the evolutionary roots of yawn
contagion, we explored these phenomena in the
zebrafish (Danio rerio), a freshwater fish, that
are a valuable model in behavioral neuroscience
research, complementing mammalian systems34,35,
also considering that they share over 70% of
genes with humans36. Due to its social habits
and ability to transmit emotions to group
members37,38, the species is highly suitable for
studying yawn contagion, which has never been
demonstrated in any ectothermic species?.
- Spontaneous yawning has been already
qualitatively described in fishes1,39. However,
since clearly identifying yawning from simply
breathing actions in aquatic vertebrates is
challenging, some authors refer to the behavior
as "mouth gaping" or "yawn-like"
pattern40,41.
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- Here, we employed a deep learning approach
to objectively distinguish yawning from
breathing events in zebrafish. After clearly
identifying yawning using a convolutional neural
network (CNN), we experimentally tested for the
presence of yawn contagion by using the
previously deep learning-based classification of
yawning and breathing events to create video
stimuli.
-
- Discussion
- The CNN has intercepted with a high level of
accuracy the differences between yawning and
breathing events in zebrafish thus confirming
that the yawning event is present as a distinct
pattern in this species. Moreover, a yawn
differed from a breathing event in the duration
of the motor execution implying a profound
mandibular stretching accompanied by the
protrusion of oral bones. Such motor patterns
are strongly similar to those recorded during
yawning in other vertebrates10. Additionally,
further motor bodily components involving fin
stretching and tail lowering were present in
more than half of yawning events (55%) (Fig. 1e,
Supplementary Movie 1 and Supplementary Movie 2)
and always started after the onset of the
mandibular stretching (Fig. 2a). Moreover, those
yawns including fin and tail stretching lasted
longer than those without such bodily motor
activation (Fig. 2b). Stretching different body
districts while yawning is a phenomenon known as
pandiculation or stretch-yawning syndrome, well
reported in many mammals3º and birds41. In
terrestrial vertebrates, pandiculation has a
role in re-activating the central nervous system
after resting periods thus preparing organisms
to properly and rapidly react to environmental
stimuli. Such re-activation seems to be present
also in zebrafish. The analysis of the behavior
state change after a simple yawn and after a
yawn accompanied by body stretching revealed
that the probability of a behavioral shift was
higher in the latter than the former situation
(Fig. 5). It is difficult to say if yawning and
pandiculation are homologous traits across
vertebrate taxa, however, the evidence of these
phenomena in zebrafish suggests possible
convergences in their functions?. A further
interesting issue regarding spontaneous yawning
in ectotherms is its covariation with
temperature and physiological arousal, as
recently demonstrated in reptiles??. This
finding appears to align with the data already
available for endotherms.
-
- Our data indicate that yawn contagion is
present in zebrafish that were more than twice
as likely to yawn while visually detecting
others' yawns. An incidence which is very
similar to that reported for humans. We found
not only that the yawning responses were
significantly higher during Yawningvideo
compared to Breathingvideo, but also that the
latency of responses were shorter in the former
than in the latter condition (Supplementary
Table 4, Fig. 4). The deep learning analysis
made us confident that the Yawningvideo and
Breathingvideo provided to the tested fish
actually included the yawning and breathing
stimuli, respectively. Moreover, the
environmental conditions (e.g., temperature,
light-dark yawn contagion, pH, manipulative
phases, tank uniformly illuminated) were kept
constant across all stages of the experiment,
and the experiments were conducted away from
feeding phases. Therefore, the differences in
the number of yawns emitted in the yawning and
breathing conditions can be ascribed to the
different visual dynamic components of the
stimulus administered and not to other
environmental stimuli. The ability to visually
perceive the yawns of others aligns with the
zebrafish visual perception capabilities, which
are, from a neural perspective, particularly
sophisticated and complex
-
- The presence of yawn contagion in fish
raises thought-provoking evolutionary questions,
thus inviting deeper reflection particularly
regarding the origin of the phenomenon.
According to evolutionary biology theories, yawn
contagion may have two possible origins. On one
hand, its demonstration could trace the origins
of this motor resonance phenomenon back in
evolutionary history, at least coinciding with
the emergence of modern teleosts (200-250
million years ago), followed by the secondary
loss of this trait in certain taxa (absence of
yawn contagion: Geochelone carbonaria? , Corvus
coraxA3, Gorilla gorilla44; presence of yawn
contagion: Melopsittacus undulatus45, Pan
paniscus46). On the other hand, it may represent
a result of convergent evolution, with yawn
contagion emerging independently in different
evolutionary lineages as a response to the need
for synchronization of motor actions within
social groups. Further studies on other
vertebrate taxa (e.g., amphibians) could help
address the intricate issue on the evolution of
contagious yawning.
-
- Yawn contagion in zebrafish can be
interpreted in light of both proximate (e.g.,
social cognitive abilities) and ultimate factors
(e.g., evolutionary advantages) (sensu
Tinbergen42). Recent studies on this species'
ability to share others' emotional states,
whether positive or negative *9 , reveal
intriguing parallels with mammalian neural
systems involved in emotional contagion, which
is well-documented in humans50. Zebrafish can
share the fear or distress of others both
behaviorally and physiologically. They are more
likely to engage with distressed individuals
than with those in neutral states, even though
the distress may signal potential risks51. The
approaches of zebrafish towards distressed
individuals can provide various tangible
benefits to the interacting agents such as
stress buffering?, enhanced vigilance, attack
mitigation, and antipredator advantages 2.
- The presence of yawn contagion in zebrafish
may also be explained by its potential
evolutionary advantages. Yawning serves as a
dependable predictor of upcoming behavioral
state changes52,53 and there are empirical data
showing that yawn contagion between two agents
facilitates their subsequent behavioral
alignment and vigilance state54.
-
- Synchronization at a group-level derives
from synchronization at the dyadic level32. . In
line with the concept of perception-action
coupling proposed by de Waal and Preston 33 -,
the ability to mirror the behaviors of others
becomes exceptionally beneficial for animals
whose survival and reproductive success depend
on qualities like unity and social connection.
Synchronization makes the school formation and
maintenance possible in fish. Schooling acts as
a vital cohesive social system offering numerous
advantages, such as decreased risk of predation
(e.g., vigilance, dilution effect) and enhanced
efficiency in food searching54.
-
- Although it remains uncertain whether yawn
contagion enhances spatial and social alignment,
its presence in zebrafish hints at potential
implications for their social behavior. It would
be interesting to investigate whether yawn
contagion occurs in solitary fish species that
do not engage in schooling or shoaling. This
could help determine if and to what extent
social synchronization plays a role in the
emergence of this motor resonance
phenomenon.
-
- In sum, here we overcame the challenges of
detecting and classifying yawns in fish using a
deep learning model thus underlining the
importance of artificial intelligence in
comparative studies. Then, we obtained robust
results, consistent across diverse experimental
conditions in highly controlled environments,
demonstrating that yawn contagion in zebrafish
is not a mere coincidence but a genuine motor
resonance phenomenon. Our findings challenge the
prevailing assumption that yawn contagion is
confined to mammal and bird species thus opening
new avenues for exploring the neurobiological
mechanisms underlying this phenomenon and its
potential functions from an evolutionary
perspective.
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