Sarah Marshall-Pescini

The effect of domestication on inhibitory control: wolves and dogs compared.

Inhibitory control i.e. blocking an impulsive or prepotent response in favour of a more appropriate alternative, has been suggested to play an important role in cooperative behaviour. Interestingly, while dogs and wolves show a similar social organization, they differ in their intraspecific cooperation tendencies in that wolves rely more heavily on group coordination in regard to hunting and pup-rearing compared to dogs. Hence, based on the ‘canine cooperation’ hypothesis wolves should show better inhibitory control than dogs. On the other hand, through the domestication process, dogs may have been selected for cooperative tendencies towards humans and/or a less reactive temperament, which may in turn have affected their inhibitory control abilities. Hence, based on the latter hypothesis, we would expect dogs to show a higher performance in tasks requiring inhibitory control. To test the predictive value of these alternative hypotheses, in the current study two tasks; the ‘cylinder task’ and the ‘detour task’, which are designed to assess inhibitory control, were used to evaluate the performance of identically raised pack dogs and wolves. Results from the cylinder task showed a significantly poorer performance in wolves than identically-raised pack dogs (and showed that pack-dogs performed similarly to pet dogs with different training experiences), however contrary results emerged in the detour task, with wolves showing a shorter latency to success and less perseverative behaviour at the fence. Results are discussed in relation to previous studies using these paradigms and in terms of the validity of these two methods in assessing inhibitory control.

The effect of training and breed group on problem-solving behaviours in dogs

Dogs have become the focus of cognitive studies looking at both their physical and social problem-solving abilities (Bensky et al. in Adv Stud Behav, 45:209–387, 2013), but very little is known about the environmental and inherited factors that may affect these abilities. In the current study, we presented a manipulation task (a puzzle box) and a spatial task (the detour) to 128 dogs belonging to four different breed groups: Herding, Mastiff-like, Working and Retrievers (von Holdt et al. in Nature 464:898–902, 2010). Within each group, we tested highly trained and non-trained dogs. Results showed that trained dogs were faster at obtaining the reward in the detour task. In the manipulation task, trained dogs approached the apparatus sooner in the first familiarization trial, but no effect of breed emerged on this variable. Furthermore, regardless of breed, dogs in the trained group spent proportionally more time interacting with the apparatus and were more likely to succeed in the test trial than dogs in the non-trained group, whereas regardless of training, dogs in the working breed group were more likely to succeed than dogs in the retriever and herding breed groups (but not the mastiff-like group). Finally, trained dogs were less likely to look at a person than non-trained dogs during testing, but dogs in the herding group more likely to do so than dogs in the retriever and working but not the mastiff-like breed groups. Overall, results reveal a strong influence of training experience but less consistent differences between breed groups on different components thought to affect problem solving.

Integrating social ecology in explanations of wolf–dog behavioral differences

Whereas studies in comparative cognition normally invoke ecology and social organization to account for differences in social behaviour and cognition across species, dog–wolf differences have so far been explained mostly as a result of direct human selection for desirable traits ( e.g. , tameness, attention to humans, sociability). Yet, as will be reviewed in this paper, dogs and wolves also differ considerably in both their feeding niche and social organization (which together we refer to as ‘social ecology’). We suggest that observed wolf–dog differences especially in their interaction with the environment ( e.g. , neophobia, persistence, risk taking) and conspecifics ( e.g. , tolerance, cooperation, communication) need to be considered also in regard to their social ecology. We propose that social ecology alongside human selection should be recognized as a potentially important factor affecting dogs’ behaviour, and suggest a number of potential avenues for future research, which can more directly test the relative importance of these selection forces.

Critical issues in experimental studies of prosociality in non-human species

Prosociality and acts of altruism are defined as behaviours which benefit another with either no gain or some immediate cost to the self. To understand the evolutionary origins of these behaviours, in recent years, studies have extended to primate species; however, studies on non-primates are still scarce. In light of the fact that phylogenetic closeness to humans does not appear to correlate with prosocial tendencies, but rather differences in the propensity towards prosociality may be linked to allomaternal care or collaborative foraging, it appears that convergent selection pressures may be at work in the evolution of prosociality. It would hence seem particularly important to extend such studies to species outside the primate clade, to allow for comparative hypothesis testing of the factors affecting the evolution of prosocial behaviours. In the current review, we focus on the experimental paradigms which have been used so far (i.e. the prosocial choice task, helping paradigms and food-sharing tests) and highlight the strengths and weaknesses of each method. In line with the aim of encouraging a broader comparative approach to the topic of prosociality, particular emphasis is placed on the methodological issues that need to be taken into account. We conclude that although a number of the paradigms used so far may be successfully applied to non-primate species, there is a need to simplify the cognitive demands of the tasks and ensure task comprehension to allow for a ‘fair’ comparative approach of prosocial tendencies across species.

Importance of a species’ socioecology: Wolves outperform dogs in a conspecific cooperation task

Significance A popular hypothesis is that during the course of domestication, dogs acquired a tamer temperament, showing increased tolerance and cooperative inclinations compared with their wolf relatives. This “domestication effect” is suggested to mirror how humans evolved a more tolerant and cooperative nature compared with chimpanzees. However, whereas wolves rely heavily on cooperation for hunting, pup-rearing, and territorial defense, dogs’ reliance on cooperation is much reduced. Here we compared similarly raised and kept wolves and dogs on a cooperative string-pulling task and found that, in line with the different socioecology of the two species, wolves better cooperate with their conspecifics than dogs. Furthermore, cooperation in wolves was more successful among partners of similar rank and with a close social bond. A number of domestication hypotheses suggest that dogs have acquired a more tolerant temperament than wolves, promoting cooperative interactions with humans and conspecifics. This selection process has been proposed to resemble the one responsible for our own greater cooperative inclinations in comparison with our closest living relatives. However, the socioecology of wolves and dogs, with the former relying more heavily on cooperative activities, predicts that at least with conspecifics, wolves should cooperate better than dogs. Here we tested similarly raised wolves and dogs in a cooperative string-pulling task with conspecifics and found that wolves outperformed dogs, despite comparable levels of interest in the task. Whereas wolves coordinated their actions so as to simultaneously pull the rope ends, leading to success, dogs pulled the ropes in alternate moments, thereby never succeeding. Indeed in dog dyads it was also less likely that both members simultaneously engaged in other manipulative behaviors on the apparatus. Different conflict-management strategies are likely responsible for these results, with dogs’ avoidance of potential competition over the apparatus constraining their capacity to coordinate actions. Wolves, in contrast, did not hesitate to manipulate the ropes simultaneously, and once cooperation was initiated, rapidly learned to coordinate in more complex conditions as well. Social dynamics (rank and affiliation) played a key role in success rates. Results call those domestication hypotheses that suggest dogs evolved greater cooperative inclinations into question, and rather support the idea that dogs’ and wolves’ different social ecologies played a role in affecting their capacity for conspecific cooperation and communication.

Inequity Aversion Negatively Affects Tolerance and Contact-Seeking Behaviours towards Partner and Experimenter

Inequity aversion has been proposed to act as a limiting factor for cooperation, thus preventing subjects from disadvantageous cooperative interactions. While a recent study revealed that also dogs show some sensitivity to inequity, the underlying mechanisms of this behaviour are still unclear. The aim of the current study was threefold: 1) to replicate the study by Range et al. (2009, PNAS, 106, 340–345); 2) to investigate the emotional mechanisms involved in the inequity response by measuring the heart rate and 3) to explore the link between inequity aversion and cooperation in terms of behaviours shown towards the partner dog and towards the experimenter who caused the inequity. Dog tested in dyads were alternately asked to give their paw and were either equally or unequally rewarded by the experimenter. After each social test condition, we conducted food tolerance tests and free interaction tests in which the subjects’ social behaviour towards the partner and the experimenter were observed. As in the previous study, subjects refused to continue giving their paw when only the partner was rewarded, but not when both dogs were rewarded with rewards of different quality. Although subjects did not react to this quality inequity during the test, we did find reduced durations of food sharing in the subsequent tolerance test, indicating that dogs perceived the inequity but were not able to react to it in the test context. Moreover, subjects avoided their partner and the experimenter more during the free interaction time following unequal compared to equal treatment. Despite the clear behavioural reactions to inequity, we could not detect any changes in heart rate. Results suggest that inequity aversion might in fact be mediated by simple emotional mechanisms: sharing a negative experience, like inequity, might reduce future cooperation by decreasing the likelihood of proximity being maintained between partners.

Investigating Empathy-Like Responding to Conspecifics' Distress in Pet Dogs.

Empathy covers a wide range of phenomena varying according to the degree of cognitive complexity involved; ranging from emotional contagion, defined as the sharing of others’ emotional states, to sympathetic concern requiring animals to have an appraisal of the others’ situation and showing concern-like behaviors. While most studies have investigated how animals reacted in response to conspecifics’ distress, dogs so far have mainly been targeted to examine cross-species empathic responses. To investigate whether dogs would respond with empathy-like behavior also to conspecifics, we adopted a playback method using conspecifics’ vocalizations (whines) recorded during a distressful event as well as control sounds. Our subjects were first exposed to a playback phase where they were subjected either to a control sound, a familiar whine (from their familiar partner) or a stranger whine stimulus (from a stranger dog), and then a reunion phase where the familiar partner entered the room. When exposed to whines, dogs showed a higher behavioral alertness and exhibited more stress-related behaviors compared to when exposed to acoustically similar control sounds. Moreover, they demonstrated more comfort-offering behaviors toward their familiar partners following whine playbacks than after control stimuli. Furthermore, when looking at the first session, this comfort offering was biased towards the familiar partner when subjects were previously exposed to the familiar compared to the stranger whines. Finally, familiar whine stimuli tended to maintain higher cortisol levels while stranger whines did not. To our knowledge, these results are the first to suggest that dogs can experience and demonstrate “empathic-like” responses to conspecifics’ distress-calls.

Does Subjective Rating Reflect Behavioural Coding? Personality in 2 Month-Old Dog Puppies: An Open-Field Test and Adjective-Based Questionnaire

A number of studies have recently investigated personality traits in non-human species, with the dog gaining popularity as a subject species for research in this area. Recent research has shown the consistency of personality traits across both context and time for adult dogs, both when using questionnaire based methods of investigation and behavioural analyses of the dogs’ behaviour. However, only a few studies have assessed the correspondence between these two methods, with results varying considerably across studies. Furthermore, most studies have focused on adult dogs, despite the fact that an understanding of personality traits in young puppies may be important for research focusing on the genetic basis of personality traits. In the current study, we sought to evaluate the correspondence between a questionnaire based method and the in depth analyses of the behaviour of 2-month old puppies in an open-field test in which a number of both social and non-social stimuli were presented to the subjects. We further evaluated consistency of traits over time by re-testing a subset of puppies. The correspondence between methods was high and test- retest consistency (for the main trait) was also good using both evaluation methods. Results showed clear factors referring to the two main personality traits ‘extroversion,’ (i.e. the enthusiastic, exuberant approach to the stimuli) and ‘neuroticism,’ (i.e. the more cautious and fearful approach to the stimuli), potentially similar to the shyness-boldness dimension found in previous studies. Furthermore, both methods identified an ‘amicability’ dimension, expressing the positive interactions the pups directed at the humans stranger, and a ‘reservedness’ dimension which identified pups who largely chose not to interact with the stimuli, and were defined as quiet and not nosey in the questionnaire.

Social Looking in the Domestic Dog

The study of dog social cognition is relatively recent and is rapidly developing, providing an interesting and multi-faceted picture of our “best friend’s” sociocognitive abilities. In particular, since Miklosi et al.s (2003) seminal work “A simple reason for a big difference: wolves do not look back at humans, but dogs do”, there has been a surge of interest in the area of dog–human communication. In the current chapter we focus on dogs’ comprehension of the human gaze and their ability to use human-directed-gazing as a communicative tool. We first review studies on the social significance of human eye contact for dogs, their understanding of eyes as indicators of attention, and their ability to take another’s visual perspective into account. We also consider dogs’ understanding of human eye-gaze as a communicative act, in terms of its potentially referential nature and as an ostensive cue signalling the communicative intent of the actor. We then move on to review studies on dogs’ human-directed gazing behaviour, discussing whether it may be considered part of an intentional and referential communicative act, what the underlying motivations and contexts in which this behaviour is exhibited may be, and what variables affect its occurrence. Where open questions remains, we outline current debates and highlight potential directions for future research.

The influence of social relationship on food tolerance in wolves and dogs

Food sharing is relatively widespread across the animal kingdom, but research into the socio-ecological factors affecting this activity has predominantly focused on primates. These studies do suggest though that food tolerance is linked to the social relationship with potential partners. Therefore, the current study aimed to assess the social factors which influence food tolerance in two canids: wolves and dogs. We presented wolves and dogs with two paradigms: dyadic tolerance tests and group carcass feedings. In the dyadic setting, the affiliative relationship with a partner was the most important factor, with a strong bond promoting more sharing in both species. In the group setting, however, rank was the primary factor determining feeding behavior. Although the dominant individuals of both species defended the carcass more than subordinates, in the dogs, the subordinates mostly stayed away from the resource and the most dominant individual monopolized the food. In the wolves, the subordinates spent as much time as dominant individuals in proximity to, and feeding from, the carcass. Furthermore, subordinate wolves were more able to use persistence strategies than the dogs were. Feeding interactions in the wolves, but not dogs, were also modulated by whether the carcass was on the ground or hanging from a tree. Overall, the social relationship with a partner is important in food distribution in wolves and dogs, but the precise effects are dependent on species and feeding context. We consider how the different socio-ecologies of the two species may be linked to these findings.Significance statementDespite the fact that food sharing is relatively widespread in the animal kingdom, the specific factors underlying whether an animal will share with a specific individual are little understood. When it comes to decisions about food sharing in wolves and dogs, friendship is the deciding factor if it is just two of you, but in a bigger group rank position decides your access to the spoils. What is more, it seems that rank positioning is even more important in dogs than wolves as dominant dogs keep the food for themselves while each wolf pack member has a chance to eat. This is the first evidence that the importance of the social relationship in food sharing is dependent on the feeding context in canids.