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Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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mystery of yawning 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

mise à jour du
23 mars 2021
Sci Rep
2021;11:1851
 Yawn contagion in domestic pigs (Sus scrofa) 
Norscia, I., Coco, E., Robino, C.
Chierto E, Cordoni G

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Abstract
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 (_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.