Dogs have the potential to be an exceptional resource for studying ecological, behavioural and evolutionary processes. However, several widespread misconceptions limit our understanding of dog behaviour and inhibit the use of dogs as model systems in diverse areas of biological science. These include extensive anthropomorphization of dog behaviour, a profound bias towards almost exclusively studying pet dogs, a widespread belief that dog domestication was human-driven, and that the majority of dogs are not subjects of natural selection. Here we argue that dogs should be studied using species-general fundamental principles of ecology and evolution, and that the focus in dog research should shift towards free-ranging dogs, which comprise ca. 80% of the global dog population. By reviewing the available literature on free-ranging dog behavioural ecology we place the dog within an objective biological framework. We find that free-ranging dog populations express substantial variation in their behavioural ecology across their global range and propose that this variation is key to understanding dogs' great success in the rapidly developing anthropogenic niche. Since free-ranging dogs have a global distribution across various environmental gradients, including urbanization, climate and social structures, they provide an ideal opportunity to collect comparable, large-scale data across populations. Combined with in-depth knowledge of dog evolutionary history and the advanced genetic tools specifically developed using this species, dogs can be an outstanding model for the study of behavioural ecology and evolution.

Domesticated animals are generally assumed to display increased sociability toward humans compared to their wild ancestors. Dogs (Canis familiaris) have a remarkable ability to form social relationships with humans, including lasting attachment, a bond based on emotional dependency. Since it has been specifically suggested that the ability to form attachment with humans evolved post-domestication in dogs, attempts to quantify attachment behavior in wolves (Canis lupus) have subsequently been performed. However, while these rare wolf studies do highlight the potential for wolves to express human-directed attachment, the varied methods used and the contrasting results emphasize the need for further, standardized testing of wolves. Here, we used the standardized Strange Situation Test to investigate attachment behavior expressed in wolves and dogs hand-raised and socialized under standardized and identical conditions up until the age of testing. We found that 23-week-old wolves and dogs equally discriminated between a stranger and a familiar person, and expressed similar attachment behaviors toward a familiar person. Additionally, wolves, but not dogs, expressed significantly elevated stress-related behavior during the test, but this stress response was buffered by the presence of a familiar person. Together, our results suggest that wolves can show attachment behaviors toward humans comparable to those of dogs. Importantly, our findings demonstrate that the ability to form attachment with humans exists in relatives of the wild ancestor of dogs, thereby refuting claims that this phenotype evolved after dog domestication was initiated.

Domestication dramatically alters phenotypes across animal species. Standing variation among ancestral populations often drives phenotypic change during domestication, but some changes are caused by novel mutations. In dogs (Canis familiaris) specifically, it has been suggested that the ability to interpret social-communicative behavior expressed by humans originated post-domestication and this behavior is thus not expected to occur in wolves (Canis lupus). Here we report the observation of three 8-week-old wolf puppies spontaneously responding to social-communicative behaviors from an unfamiliar person by retrieving a ball. This behavioral expression in wolves has significant implications for our understanding and expectations of the genetic foundations of dog behavior. Importantly, our observations indicate that behavioral responses to human social-communicative cues are not unique to dogs. This suggests that, although probably rare, standing variation in the expression of human-directed behavior in ancestral populations could have been an important target for early selective pressures exerted during dog domestication.

Domesticated animals display suites of altered morphological, behavioral, and physiological traits compared to their wild ancestors, a phenomenon known as the domestication syndrome (DS). Because these alterations are observed to co-occur across a wide range of present day domesticates, the traits within the DS are assumed to covary within species and a single developmental mechanism has been hypothesized to cause the observed co-occurrence. However, due to the lack of formal testing it is currently not well-resolved if the traits within DS actually covary. Here, we test the hypothesis that the presence of the classic morphological domestication traits white pigmentation, floppy ears, and curly tails predict the strength of behavioral correlations in support of the DS in 78 dog breeds. Contrary to the expectations of covariation among DS traits, we found that morphological traits did not covary among themselves, nor did they predict the strength of behavioral correlations among dog breeds. Further, the number of morphological traits in a breed did not predict the strength of behavioral correlations. Our results thus contrast with the hypothesis that the DS arises due to a shared underlying mechanism, but more importantly, questions if the morphological traits embedded in the DS are actual domestication traits or postdomestication improvement traits. For dogs, it seems highly likely that strong selection for breed specific morphological traits only happened recently and in relation to breed formation. Present day dogs therefore have limited bearing of the initial selection pressures applied during domestication and we should reevaluate our expectations of the DS accordingly.

Domestication is hypothesized to drive correlated responses in animal morphology, physiology and behaviour, a phenomenon known as the domestication syndrome. However, we currently lack quantitative confirmation that suites of behaviours are correlated during domestication. Here we evaluate the strength and direction of behavioural correlations among key prosocial (sociability, playfulness) and reactive (fearfulness, aggression) behaviours implicated in the domestication syndrome in 76,158 dogs representing 78 registered breeds. Consistent with the domestication syndrome hypothesis, behavioural correlations within prosocial and reactive categories demonstrated the expected direction-specificity across dogs. However, correlational strength varied between dog breeds representing early (ancient) and late (modern) stages of domestication, with ancient breeds exhibiting exaggerated correlations compared to modern breeds across prosocial and reactive behaviours. Our results suggest that suites of correlated behaviours have been temporally decoupled during dog domestication and that recent shifts in selection pressures in modern dog breeds affect the expression of domestication-related behaviours independently.

Biologists since Darwin have recognized that domestication, where species are selected to live in human-controlled environments, exerts strong selection on organisms and dramatically impacts their evolutionary trajectories. Across domesticated mammal species, characteristic morphological, physiological and behavioural changes occur simultaneously, as correlated traits, a phenomenon known as the domestication syndrome. Key behavioural alterations are connected with the domestication syndrome, in which domesticated animals express decreased aggression and fearfulness alongside increased sociability and playfulness compared to their wild counterparts. To investigate various aspects of the behavioural implications of domestication, we used the dog (Canis familiaris) and its extant ancestor, the grey wolf (Canis lupus), as our study species. Since we currently lack quantitative confirmation that correlated changes in behaviours follow domestication, we evaluated correlations among sociability, aggression, fearfulness and playfulness in more than 90,000 dogs in Paper I. Contrary to expectations, we found weak support for behavioural correlations in modern dog breeds, but observed exaggerated effect sizes of correlations in ancient breeds. We suggest that while selection on suites of behaviour have been relevant during early dog domestication, a recent shift in selection pressures in modern dog breeds affects the expression of domestication-related behaviours independently. In Paper II we therefore contrasted the expression of sociability, aggression, fearfulness and playfulness during domestication in wolf hybrids and dogs, and found that while wolf hybrids were less playful and overall more fearful than dogs, they were not less social or more aggressive than dogs. Our results suggest that behavioral alterations during domestication do not necessarily occur in concert as predicted by the domestication syndrome and point to an important, but previously overlooked, role of selection on playfulness during the domestication of dogs. Finally, while it has been established that behavioural responses in adult domesticated animals are altered compared to ancestral species, we know little about when such species differences occur. We therefore conducted two studies addressing the effects of domestication on behavioural ontogeny. First, we examined the ontogeny of sociability, playfulness, aggression and fearfulness in wolves and dogs in Paper III and found that while wolves became less social and less playful than dogs at 12 and 16 weeks of age, we found no species differences in the development of fear. Our results suggest that the alteration of behaviours in the domestication syndrome do not develop simultaneously, and that species differences in fear might not occur until later in ontogeny. Then, in Paper IV we present the first extended examination of the development of fear behaviour in wolves and dogs throughout their first 26 weeks of life. We found that while dogs, but not wolves, expressed decreased fear towards novelty with age, this did not result in a species difference in fear response until 26 weeks of age. Our results suggest that differences in fear expression between wolves and dogs occur late during juvenile development and are caused by a loss of sensitivity towards novelty with age in dogs. Together, the four papers in this thesis highlight the need for a re-evaluation of the behaviours hypothesized to be shaped by domestication.