Wednesday, February 12, 2020

Calling into question that contagious yawning is a signal of empathy: No evidence of familiarity, gender or prosociality biases in dogs

Contagious yawning is not a signal of empathy: no evidence of familiarity, gender or prosociality biases in dogs. Patrick Neilands et al. Proceedings of the Royal Society B: Biological Sciences, Volume 287, Issue 1920, February 5 2020.

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–empathy hypothesis. Furthermore, in an experiment testing the prosociality bias, a novel prediction of the contagious yawning–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.

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–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 [35,4951]. 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–empathy hypothesis. This suggests that contagious yawning in dogs is not mediated by an empathy-related perception–action mechanism [5254]. The presence of contagious yawning in non-human animals, therefore, cannot be assumed to be evidence for a perception–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–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–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–empathy hypothesis predicts the presence of all three biases. As such, testing for all three biases represents a powerful test of the contagious yawning–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–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–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–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–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.

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