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
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
19 mai 2020
Proceedings of the Royal Society B
2020;287(120)
 Contagious yawning is not a signal of empathy:
no evidence of familiarity, gender
or prosociality biases in dogs
 Neilands P, Claessens S, Ren I, Hassall R, Bastaos A, Taylor A
 

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 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
 
Abstract
Contagious yawning has been suggested to be a potential signal of empathy in non-human animals. However, few studies have been able to robustly test this claim. Here, we ran a Bayesian multilevel reanalysis of six studies of contagious yawning in dogs. This provided robust support for claims that contagious yawning is present in dogs, but found no evidence that dogs display either a familiarity or gender bias in contagious yawning, two predictions made by the contagious yawning&endash;empathy hypothesis. Furthermore, in an experiment testing the prosociality bias, a novel prediction of the contagious yawning&endash;empathy hypothesis, dogs did not yawn more in response to a prosocial demonstrator than to an antisocial demonstrator. As such, these strands of evidence suggest that contagious yawning, although present in dogs, is not mediated by empathetic mechanisms. This calls into question claims that contagious yawning is a signal of empathy in mammals.
 
Résumé
Le bâillement contagieux a été suggéré comme un signe potentiel d'empathie chez les animaux non humains. Cependant, peu d'études ont été en mesure de tester de manière robuste cette affirmation. Les auteurs ont effectué une réanalyse bayésienne à plusieurs niveaux de six études sur le bâillement contagieux chez le chien. Cela a fourni un solide argument aux affirmations selon lesquelles le bâillement contagieux est présent chez les chiens, mais n'a trouvé aucune preuve que les chiens affichent une familiarité ou un parti préférence liée au sexe concernant l'hypothèse du bâillement contagieux et de l'empathie. De plus, dans une expérience testant le biais de prosocialité, une nouvelle prédiction de l'hypothèse contagieuse du bâillement et de l'empathie, les chiens n'ont pas bâillé plus en réponse à un manifestant d'un congénère familier qu'à un étranger. Ceci suggère que le bâillement contagieux, bien que présent chez les chiens, n'est pas médié par des mécanismes empathiques. Cela remet en cause les affirmations selon lesquelles le bâillement contagieux est un signe d'empathie chez les mammifères.
1. Introduction
Empathy, broadly defined as emotional and mental sensitivity to another's state [1], appears to play a key role in humans' prosocial and cooperative behaviour [2&endash;4]. While there are many aspects of empathy, all empathetic responses are ultimately predicated upon an observer having some form of access to another individual's emotional state [1]. Perception&endash;action mechanism accounts argue that this access is granted by state-matching: when an observer perceives a particular state in another individual, neural representations of that state are activated in the observer, resulting in the experience of a similar state [1,5,6]. It has been suggested that this perception&endash;action mechanism evolved early in mammals [1,5,6] and underpins the helping behaviour seen in many non-human mammals [7&endash;14]. However, it is difficult to rule out simpler explanations for helping behaviour that do not require empathy, such as associative learning [12,15] or alternative motivations such as a desire to seek social contact [16&endash;18] or explore novel objects [19].
 
Contagious yawning has emerged as a potentially powerful tool to help resolve this impasse. Contagious yawning occurs when observing another individual yawn induces yawning in the observer [20]. The contagious yawning&endash;empathy hypothesis posits that both contagious yawning and empathy are mediated by the same perception&endash;action mechanism [1,6,21&endash;23]. This hypothesis makes several testable predictions about the propensity of individuals to engage in contagious yawning. First, individuals who report lower levels of empathy should be less likely to engage in contagious yawning. Second, as people show greater empathy for kin and friends, they should be more likely to yawn when exposed to yawning from familiar yawners compared to unfamiliar yawners [21,24]. Finally, it has been hypothesized that, due to more direct involvement in offspring care, female mammals may experience a greater level of empathy than males [25&endash;28] and thus it has been predicted that female mammals should be more likely to engage in contagious yawning [29].
 
Evidence of each of these predictions has been found in humans. Firstly, subpopulations reporting lower levels of empathy, such as children with autism spectrum disorder (ASD) [30] or adults who score highly in psychopathic traits [31], are less likely to engage in contagious yawning. Secondly, both empathy and contagious yawning appear to share a familiarity bias: people experience more empathy for friends and family than strangers and are more likely to contagiously yawn when familiar people yawn [21,24] (but see [32]). Finally, although both men and women are equally likely to engage in contagious yawning, women who do engage in contagious yawning yawn more frequently than men who engage in contagious yawning [29]. While this provides some evidence of a gender bias in human contagious yawning, there is currently much debate surrounding this finding [33,34].
 
Based on this evidence from humans, it has been suggested that the widespread presence of contagious yawning across mammals demonstrates that the perception&endash;action mechanism underpinning empathy is phylogenetically ancient and thus that the helping behaviours seen in mammals are driven by at least a rudimentary form of empathy [1,35,36]. This conclusion rests on two key premises. First, it assumes that contagious yawning is indeed widespread across mammals. Second, it assumes that contagious yawning in animals is underpinned by the same perception&endash;action mechanism mediating empathy. However, there is currently a lack of robust evidence for either of these assumptions [37].
 
Firstly, there is a lack of conclusive evidence that contagious yawning is widespread across mammals. A comprehensive review of the contagious yawning literature by Massen & Gallup [37] demonstrates that the majority of studies on contagious yawning are focused on non-human primates, particularly chimpanzees, with few studies looking at contagious yawning in non-primates. Furthermore, research into contagious yawning in other species has mostly been restricted to a single study. Chimpanzees are the only non-human species of mammal to have consistently shown contagious yawning across multiple studies [38&endash;45]. There is no evidence of contagious yawning in gorillas [44,46] and for both bonobos [24,36,44,47,48] and dogs [35,49&endash;54], the evidence is mixed: some studies have shown evidence for contagious yawning while other studies have found no effect. As well as making it difficult to draw conclusions regarding the presence of contagious yawning in these species, this lack of consistency in replication brings into question claims for contagious yawning in other species that are based on a single study [24,35,36,44,47,49&endash;64]. Given the small sample sizes used in many of these studies [65], their findings may simply reflect either false positives or negatives rather than the true presence or absence of contagious yawning. Such issues are particularly compounded by the variation in study design across different species [66]. In particular, relying on observational rather than experimental methodologies can be problematic due to the influence of synchronized circadian rhythms making it more likely that animals in a group may spontaneously yawn at the same time [37]. As such, it is difficult to say with certainty that there is evidence for contagious yawning in non-human mammals outside of chimpanzees, let alone discern the phylogenetic pattern of contagious yawning across all mammals.
Secondly, contagious yawning in non-human animals may not be mediated by empathetic mechanisms.
 
Contagious yawning in animals may be the result of stress [54,57], an affiliation strategy [67], a means of communication [61], or a mechanism to improve collective vigilance within groups [37,68,69] rather than being related to empathy via a perception&endash;action mechanism. A powerful way to test between these hypotheses is to examine if the patterns of behaviours predicted by the contagious yawning&endash;empathy hypothesis, such as the familiarity bias and the gender bias, are also seen in animals. Such biases can be thought of as cognitive signatures; a particular suite of behaviours that should be seen if contagious yawning is mediated by a perception&endash;action mechanism but not if it is mediated by another cognitive mechanism [70]. Evidence for the familiarity bias has been found in studies on chimpanzees [40,41], dogs [50,64], bonobos [36], gelada baboons [58], and wolves [64], but other studies on chimpanzees [42,43] and dogs [51,53] have not found evidence for this bias, and one study on rats has even found the opposite pattern [61]. In terms of the gender bias, there is currently no consistent support for the prediction that females are more likely to contagiously yawn than males across mammals [37]. Instead of females being more likely to engage in contagious yawning, there appears to be some evidence of an interaction between the gender of the observed yawner and the subject, but this pattern is not consistent. Bonobos yawn more when an individual of the opposite gender yawns and yawn more in general when the observed yawner is female [36]. Female geladas are also more likely to engage in contagious yawning than males but only when the observed yawner is female [58]. By contrast, in chimpanzees, male yawning is more contagious for other males than female yawning is for other females [42], while there is no evidence of any gender bias in dogs [35]. As such, there is currently no conclusive evidence for either signature across mammals, which brings into question whether contagious yawning is mediated by a perception&endash;action mechanism shared with empathetic processes.
 
Here, we tested the contagious yawning&endash;empathy hypothesis in dogs by reanalysing past data and also employing a novel experimental paradigm. First, we established that there is robust evidence for contagious yawning outside of chimpanzees and humans by conducting a Bayesian multilevel reanalysis of a combined dataset from six studies of contagious yawning in dogs. We then examined our combined dataset for evidence of the familiarity bias and the gender bias. Finally, we ran a study to search for a novel signature predicted by the contagious yawning&endash;empathy hypothesis: the prosociality bias. In humans, empathy is modulated by social experience: people experience greater empathy for people who interact with them in a fair or prosocial manner [71,72]. Similarly, dogs show a preference for those who interact with them in a positive manner rather than a negative manner [73]. Therefore, we carried out an experiment to test whether dogs show a prosociality bias (i.e. yawn more contagiously when in the presence of a human who has been nice to them rather than one who has ignored them). We predicted that, if contagious yawning is mediated by empathic processes in dogs, we would find evidence for the familiarity, gender, and prosociality biases in our study.
 
4. Discussion
By combining the data from six different studies, the resulting dataset is the largest used to date to examine the presence of contagious yawning in a non-human mammal. This allowed us to draw conclusions about the presence and absence of contagious yawning and the signatures predicted by the contagious yawning&endash;empathy hypothesis with a greater level of certainty than by relying on individual studies alone. Our reanalysis shows that dogs do exhibit contagious yawning, showing higher probabilities and rates of yawning for yawning demonstrators compared to control demonstrators. This provides robust support for the claims that contagious yawning is present in dogs [35,49&endash;51]. In order to test whether this contagious yawning is related to mechanisms underpinning empathy, we examined this dataset for evidence of the familiarity bias and gender bias. However, dogs in our reanalysis showed no evidence of either of these biases. Similarly, when we ran a novel experiment to look for a prosociality bias, we found that the dogs in our experiment were no more likely to yawn for prosocial demonstrators than antisocial demonstrators. Dogs, therefore, show no evidence for any of the familiarity, gender, or prosociality biases predicted by the contagious yawning&endash;empathy hypothesis. This suggests that contagious yawning in dogs is not mediated by an empathy-related perception&endash;action mechanism [52&endash;54]. The presence of contagious yawning in non-human animals, therefore, cannot be assumed to be evidence for a perception&endash;action mechanism shared between humans and other mammals, as has been previously proposed [1,35,41,58]. That is not to say that some non-human animals do not necessarily experience some form of empathy but that contagious yawning cannot be taken as a diagnostic signal for the presence of these empathetic processes. Furthermore, these results, alongside the arguments put forward by Massen & Gallup in their recent review [37], bring into question the validity of the contagious yawning&endash;empathy hypothesis more broadly.
 
It is important to acknowledge several caveats to our conclusions. Firstly, in both our reanalysis and experiment, the subjects were primarily responding to interspecific yawns from human demonstrators. While it is possible that dogs would respond differently to conspecific and interspecific yawning, there are several reasons to believe that this is not the case. Research in other species such as chimpanzees suggests that they respond similarly to conspecific and interspecific yawns [41], and, in our reanalysis, controlling for demonstrator type did not improve model fit. Nevertheless, more rigorous comparisons between how dogs respond to conspecific and interspecific yawning would be a useful future line of research. Secondly, it is important to note that the familiarity, gender, and prosociality biases are indirect measures of empathy [37]. As such, care needs to be taken in interpreting these biases and there remains substantial debate over how to do so. For example, it has been argued that both the tendency for children with ASD to be less prone to contagious yawning [83] and the familiarity bias [37,84,85] can be explained in terms of differences in attending to yawners rather than differences in empathetic response. Similarly, the gender bias reported in humans [29] is not straightforward to interpret and there is debate over whether it simply reflects a false positive in the literature [33,34]. By contrast, proponents of the contagious yawning&endash;empathy hypothesis argue that the familiarity bias continues to be found even when controlling for differences in subjects' attention [40,41] and that the negative results for the gender bias in previous studies reflects methodological issues with prior experiments [34]. Furthermore, although alternative hypotheses such as the attentional hypothesis could explain the presence of a single bias such as the familiarity bias, only the contagious yawning&endash;empathy hypothesis predicts the presence of all three biases. As such, testing for all three biases represents a powerful test of the contagious yawning&endash;empathy hypothesis. Finally, searching for a novel signature, the prosociality bias, required a novel experimental methodology where dogs were exposed to a prosocial experimenter that interacted with them and an antisocial experimenter that ignored them. Previous work which used a similar methodology demonstrated that dogs do show a preference for the prosocial demonstrator [73], and so if the contagious yawning&endash;empathy hypothesis is correct, dogs should have reacted with increased yawning to the prosocial demonstrator. However, further work would be useful in confirming the presence or absence of the prosociality bias in dogs and other species such as humans.
 
Research into contagious yawning has been dominated by the contagious yawning&endash;empathy debate [37]. However, contagious yawning is an interesting phenomenon in its own right as its evolutionary roots and ultimate function remain a mystery [20]. Contagious yawning in animals may be the result of stress [54,57], an affiliation strategy [67], a means of communication [61], or a mechanism to improve collective vigilance within groups [37,68,69] rather than being related to empathy via a perception&endash;action mechanism. Future research into contagious yawning should include a greater focus on testing between these and other hypotheses. For example, the affiliation hypothesis might predict that contagious yawning should be seen more frequently during reconciliation periods after conflict while the collective vigilance hypothesis posits that contagious yawning should increase in response to external disturbances [37,86]. However, it is important to note that these theories are not necessarily mutually exclusive [87] and that factors such as stress appear to influence yawning propensity in complex ways [88,89]. Additionally, an important next step is to consider evidence of contagious yawning outside of mammals. While there has been some work looking at contagious yawning in budgerigars [86,90] and tortoises [91], research has otherwise been sparse outside of the mammalian class.
 
Future research would benefit from systematically testing contagious yawning across multiple species. One barrier to such projects is that studying a range of different species often requires different experimental set-ups to make such testing feasible. There is a concern that such a range of methodological approaches may make cross-species and cross-study comparisons difficult, if not impossible [35,66]. However, our finding that the effect of treatment on yawning probabilities and rates remains stable when controlling for various aspects of study design suggests that the presence of contagious yawning is relatively robust to differences in experimental design. As such, while it is important to use broadly similar designs (for instance, comparing animals' yawning rates when exposed to either a yawning demonstrator or control demonstrator), there could be considerable flexibility in other aspects of study design. For example, our results suggest that animals' yawning probabilities and rates to either live demonstrators or recorded demonstrators are comparable. Therefore, our findings suggest that more ambitious cross-species work can be carried out with confidence in the validity of the subsequent comparisons.
 
To conclude, our results provide robust support for the hypothesis that contagious yawning is found in dogs, the first non-human species of mammal where it has been clearly shown outside of chimpanzees. However, we found no evidence that dogs yawn more in response to either familiar human yawners compared to unfamiliar human yawners, or to prosocial human yawners compared to antisocial human yawners. Additionally, we found no evidence that female dogs were more likely to yawn in response to a yawning demonstrator than male dogs. As such, these findings cast doubt on the widespread assertion that contagious yawning is mediated by the same perception&endash;action mechanism as empathy [1,6,35,41,58]. Instead, they support recent claims that there is no link between contagious yawning and empathetic processes [37,67] and underline the importance of developing more direct measures of empathy in non-human animals [37,92]. However, while our results suggest that researchers cannot rely on contagious yawning as a diagnostic signal of empathy, our additional findings that the effect of contagious yawning appears to be robust to variations in experimental methods suggest that cross-species comparisons may be a powerful way to disentangle the evolutionary roots of this behaviour.