Most mammalian species produce facial expressions, which form meaningful and adaptive components of the animal’s behavioural repertoire. The facial architecture underlying such facial expressions is highly conserved among mammals1, suggesting that human facial expression is based on evolutionarily ancient systems. Therefore, it would seem reasonable to debate the extent to which such facial expressions are underpinned by sophisticated cognitive processes. Historically, animal facial expressions (including human, to an extent) have been considered inflexible and involuntary displays e.g.2,3, reflecting an individual’s emotional state rather than active attempts to communicate with others. There is some evidence that non-human primate facial expressions can be mediated by the presence of an audience, suggesting that the sender has some understanding of whether the expressions can be seen by others4,5,6,7,8. Waller et al. (2015) showed that the production of facial expressions in orangutans is more intense and more complex during play when a recipient is directed towards them suggesting that the production of these expressions is not necessarily an automated response and subject to audience effects6. Similarly, Scheider et al. (2016) showed that Gibbons presented their facial expressions more often and over a longer duration when facing other individuals compared to non-facing situation7.

To date there is no systematic experimental evidence, however, that facial expressions in species other than primates, are produced with similar sensitivity to the attention of the audience.

With the current study, we aimed to test whether domestic dog facial expressions change in response to an highly arousing but non-social stimulus (food) and/or the changing attentional state of their human audience. Domestic dogs are a potentially interesting model for this kind of research as they have a unique history. Dogs have been living with humans for about 30,000 years9, during which time selection pressures seem to have acted on dogs’ ability to communicate with humans. [see for a review10 and11,12 for a recent discussion].

There is broad evidence that domestic dogs attend to a human’s attentional state13,14,15, which is one indicator of intentionality16. After being told not to take a piece of food, dogs steal the food more often when the human’s eyes are closed compared to situations during which the human’s eyes are open, the human has her back turned to the dog or she is distracted13,15. Dogs are also sensitive to the human’s attentional state during communicative interactions with humans. Dogs follow communicative gestures more once the humans eyes are visible and the gesture is clearly directed at them16. Dogs also follow the gaze of a human to a target only if eye contact had been established prior to the gaze shift17.

Waller et al. (2013) analysed the facial expressions of dogs waiting to be rehomed in shelters, and found a negative correlation between the frequency of facial movements the dogs produced when interacting with a stranger, and the rate at which they were re-homed. The more often dogs produced a specific facial movement, Action Unit 101 (which raises the inner eyebrow) the quicker they were re-homed18. Raising the inner eyebrow changes the visual appearance of the eyes and makes them look bigger, a key feature of paedomorphism (juvenile features present in the adult). One hypothesis is therefore that by picking dogs that raise their inner eye brow more, humans simply follow their preference for paedomorphic facial characteristics, a preference which might have acted as a selection pressure during dog domestication18,19.

It is possible, therefore, that dogs have also evolved the ability to use these facial expressions differentially depending on their audience. In which case, during domestication dogs may have gained additional cognitive control of their facial expressions.

The current study investigated whether dog facial expressions can be subject to so called audience effects, and can therefore be tailored to the human’s attentional state, which might suggest some social communicative function and possible voluntary control. The alternative is that dog facial expressions are a simple emotional display based on the dog’s state of arousal. In order to try and discriminate between these two possible explanations, the human, depending on the condition, presented a piece of food, as a non-social and arousing stimulus (a recent study, using thermal imaging, shows that food seems to be more arousing for dogs than social contact with a human as long as the human remains silent20).

Therefore, if dogs produce facial expressions merely as an emotional display, we would expect them to not necessarily differentiate between the social (human attention) and the non social (food) conditions. However, if the dogs behave in different ways in responds to the social and the non-social stimuli, this would provide some evidence that dogs discriminate between the conditions based on social context and one possible explanation for such discrimination that dogs exercise some voluntary control.