Zsófia Virányi

The Evolution of Self-Control

Significance Although scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problem-solving tasks measuring self-control and evaluated the leading hypotheses regarding how and why cognition evolves. Across species, differences in absolute (not relative) brain volume best predicted performance on these tasks. Within primates, dietary breadth also predicted cognitive performance, whereas social group size did not. These results suggest that increases in absolute brain size provided the biological foundation for evolutionary increases in self-control, and implicate species differences in feeding ecology as a potential selective pressure favoring these skills. Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Wolves Are Better Imitators of Conspecifics than Dogs

Domestication is thought to have influenced the cognitive abilities of dogs underlying their communication with humans, but little is known about its effect on their interactions with conspecifics. Since domestication hypotheses offer limited predictions in regard to wolf-wolf compared to dog-dog interactions, we extend the cooperative breeding hypothesis suggesting that the dependency of wolves on close cooperation with conspecifics, including breeding but also territory defense and hunting, has created selection pressures on motivational and cognitive processes enhancing their propensity to pay close attention to conspecifics’ actions. During domestication, dogs’ dependency on conspecifics has been relaxed, leading to reduced motivational and cognitive abilities to interact with conspecifics. Here we show that 6-month-old wolves outperform same aged dogs in a two-action-imitation task following a conspecific demonstration. While the wolves readily opened the apparatus after a demonstration, the dogs failed to solve the problem. This difference could not be explained by differential motivation, better physical insight of wolves, differential developmental pathways of wolves and dogs or a higher dependency of dogs from humans. Our results are best explained by the hypothesis that higher cooperativeness may come together with a higher propensity to pay close attention to detailed actions of others and offer an alternative perspective to domestication by emphasizing the cooperativeness of wolves as a potential source of dog-human cooperation.

Tracking the evolutionary origins of dog-human cooperation: the “Canine Cooperation Hypothesis”

At present, beyond the fact that dogs can be easier socialized with humans than wolves, we know little about the motivational and cognitive effects of domestication. Despite this, it has been suggested that during domestication dogs have become socially more tolerant and attentive than wolves. These two characteristics are crucial for cooperation, and it has been argued that these changes allowed dogs to successfully live and work with humans. However, these domestication hypotheses have been put forward mainly based on dog-wolf differences reported in regard to their interactions with humans. Thus, it is possible that these differences reflect only an improved capability of dogs to accept humans as social partners instead of an increase of their general tolerance, attentiveness and cooperativeness. At the Wolf Science Center, in order to detangle these two explanations, we raise and keep dogs and wolves similarly socializing them with conspecifics and humans and then test them in interactions not just with humans but also conspecifics. When investigating attentiveness toward human and conspecific partners using different paradigms, we found that the wolves were at least as attentive as the dogs to their social partners and their actions. Based on these findings and the social ecology of wolves, we propose the Canine Cooperation Hypothesis suggesting that wolves are characterized with high social attentiveness and tolerance and are highly cooperative. This is in contrast with the implications of most domestication hypotheses about wolves. We argue, however, that these characteristics of wolves likely provided a good basis for the evolution of dog-human cooperation.

Social learning from humans or conspecifics: differences and similarities between wolves and dogs

Most domestication hypotheses propose that dogs have been selected for enhanced communication and interactions with humans, including learning socially from human demonstrators. However, to what extent these skills are newly derived and to what extent they originate from wolf–wolf interactions is unclear. In order to test for the possible origins of dog social cognition, we need to compare the interactions of wolves and dogs with humans and with conspecifics. Here, we tested identically raised and kept juvenile wolves and dogs in a social learning task with human and conspecific demonstrators. Using a local enhancement task, we found that both wolves and dogs benefitted from a demonstration independent of the demonstrator species in comparison to a control, no demonstration condition. Interestingly, if the demonstrator only pretended to hide food at the target location, wolves and dogs reacted differently: while dogs differentiated between this without-food and with-food demonstration independent of the demonstrator species, wolves only did so in case of human demonstrators. We attribute this finding to wolves being more attentive toward behavioral details of the conspecific models than the dogs: although the demonstrator dogs were trained to execute the demonstration, they disliked the food reward, which might have decreased the interest of the wolves in finding the food reward. Overall, these results suggest that dogs but also wolves can use information provided by both human and conspecific demonstrators in a local enhancement task. Therefore we suggest that a more fine-scale analysis of dog and wolf social learning is needed to determine the effects of domestication.

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.

Testing the myth: tolerant dogs and aggressive wolves

Cooperation is thought to be highly dependent on tolerance. For example, it has been suggested that dog–human cooperation has been enabled by selecting dogs for increased tolerance and reduced aggression during the course of domestication (‘emotional reactivity hypothesis’). However, based on observations of social interactions among members of captive packs, a few dog–wolf comparisons found contradictory results. In this study, we compared intraspecies aggression and tolerance of dogs and wolves raised and kept under identical conditions by investigating their agonistic behaviours and cofeeding during pair-wise food competition tests, a situation that has been directly linked to cooperation. We found that in wolves, dominant and subordinate members of the dyads monopolized the food and showed agonistic behaviours to a similar extent, whereas in dogs these behaviours were privileges of the high-ranking individuals. The fact that subordinate dogs rarely challenged their higher-ranking partners suggests a steeper dominance hierarchy in dogs than in wolves. Finally, wolves as well as dogs showed only rare and weak aggression towards each other. Therefore, we suggest that wolves are sufficiently tolerant to enable wolf–wolf cooperation, which in turn might have been the basis for the evolution of dog–human cooperation (canine cooperation hypothesis).

Wolf Howling Is Mediated by Relationship Quality Rather Than Underlying Emotional Stress

Summary While considerable research has addressed the function of animal vocalizations, the proximate mechanisms driving call production remain surprisingly unclear. Vocalizations may be driven by emotions and the physiological state evoked by changes in the social-ecological environment [1, 2], or animals may have more control over their vocalizations, using them in flexible ways mediated by the animal’s understanding of its surrounding social world [3, 4]. While both explanations are plausible and neither excludes the other, to date no study has attempted to experimentally investigate the influence of both emotional and cognitive factors on animal vocal usage. We aimed to disentangle the relative contribution of both mechanisms by examining howling in captive wolves. Using a separation experiment and by measuring cortisol levels, we specifically investigated whether howling is a physiological stress response to group fragmentation [5] and whether it is driven by social factors, particularly relationship quality [6, 7]. Results showed that relationship quality between the howler and the leaving individual better predicted howling than did the current physiological state. Our findings shed important light on the degree to which animal vocal production can be considered as voluntary. Video Abstract

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.

Inhibitory Control, but Not Prolonged Object-Related Experience Appears to Affect Physical Problem-Solving Performance of Pet Dogs.

Human infants develop an understanding of their physical environment through playful interactions with objects. Similar processes may influence also the performance of non-human animals in physical problem-solving tasks, but to date there is little empirical data to evaluate this hypothesis. In addition or alternatively to prior experiences, inhibitory control has been suggested as a factor underlying the considerable individual differences in performance reported for many species. Here we report a study in which we manipulated the extent of object-related experience for a cohort of dogs (Canis familiaris) of the breed Border Collie over a period of 18 months, and assessed their level of inhibitory control, prior to testing them in a series of four physical problem-solving tasks. We found no evidence that differences in object-related experience explain variability in performance in these tasks. It thus appears that dogs do not transfer knowledge about physical rules from one physical problem-solving task to another, but rather approach each task as a novel problem. Our results, however, suggest that individual performance in these tasks is influenced in a complex way by the subject’s level of inhibitory control. Depending on the task, inhibitory control had a positive or a negative effect on performance and different aspects of inhibitory control turned out to be the best predictors of individual performance in the different tasks. Therefore, studying the interplay between inhibitory control and problem-solving performance will make an important contribution to our understanding of individual and species differences in physical problem-solving performance.

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.