Attachment to humans: a comparative study on hand-reared wolves and differently socialized dog puppies

Attachment Theory, Hand-Reared Wolves

József Topál, Márta Gácsi, Ádám Miklósi, Zsófia Virányi, Enikő Kubinyi, Vilmos Csányi

Attachment to humans: a comparative study on hand-reared wolves and differently socialized dog puppies

Animal Behaviour, Volume 70, Issue 6, December 2005, Pages 1367–1375

Using the Strange Situation Test originally developed for testing the mother–infant relationship in humans, we compared the attachment behaviour of extensively socialized (hand-reared) dog, Canis familiaris, and wolf, Canis lupus, puppies towards their human caregiver with that of pet dog puppies of the same age. The experiment was designed to study whether (1) dog puppies as young as 16 weeks show attachment to a human caregiver, (2) extensive socialization by human caregivers affects attachment behaviour of dog puppies and (3) evolutionary changes (in the form of species-specific differences between wolf and dog pups) affect the emergence of dog–human attachment. We found a characteristic selective responsiveness to the owner in young dogs, similar to that observed in adults. This finding supports the view that puppies show patterns of attachment towards their owners. Extensive socialization had only a minor effect on the attachment behaviour in dog puppies, as the behaviour of pet dogs and hand-reared dogs was basically similar. However, we found a significant species-specific difference between wolves and dogs: both extensively socialized and pet dog puppies were more responsive to the owner than to an unfamiliar human participant, whereas extensively socialized wolves were not. Behavioural differences could be best explained by assuming that selective processes took place in the course of domestication (genetic changes) that are related to the attachment system of the dog.

Domestication is generally viewed as an evolutionary process controlled by human influence (Price 1984). The symbiotic relationship between humans and nonhuman animals entails adaptational demands, which create new conditions of selection for the species to be domesticated and thus might result in a wide range of genetic modifications. The dog has a long history of adaptation to the human environment ( [Vilá et al., 1997] and [Savolainen et al., 2002]), and it is widely assumed that the selection process during domestication may have altered not only their morphological traits but also their behaviour and behaviour control systems ( [Belyaev, 1979] and [Coppinger and Coppinger, 2002]).

Recent studies have suggested an unusual competence of dogs in social interactions with humans (cooperation: [Topál et al., 1997], [Naderi et al., 2001] and [Naderi et al., 2002]; social learning: [Kubinyi et al., 2003], [Pongrácz et al., 2003a] and [Pongrácz et al., 2003b]; communication: [Miklósi et al., 1998], [Miklósi et al., 2000], [Agnetta et al., 2001], [Soproni et al., 2001] and [Soproni et al., 2002]). However, to understand the significance of domestication-related changes in the behaviour of dogs, we need to compare dogs with wolves (Miklósi et al. 2004). In line with this, recent comparisons of the social cognitive skills in dogs and socialized wolves within the context of the interspecific relationship with humans have shed light on some genetic divergences at the behavioural level ( [Hare et al., 2002] and [Miklósi et al., 2003]). Compared with wolves, the dogs' preferential looking at the human in problem-solving situations and their superior performance in using human directional gestures support the existence of genetic predispositions related to the domestication process in the emergence of social cognitive abilities in dogs.

In general, it is widely accepted that the evolutionary emergence of social cognition is closely related to the ‘social field’ (Kummer 1982), which often presents more complex adaptational demands for the animal than do physical characteristics of the environment (Tomasello & Call 1997). One of the basic behavioural phenomena of social relationships is attachment. The evolutionary approach to function and mechanism suggests that attachment is one of the main behaviour organizing systems in parent–offspring relationships, and it is also claimed to be the basic organizational factor for any species' social structure leading to group formation (Bowlby 1958). Attachment is an asymmetrical social relationship between two individuals, which can be tested experimentally in choice situations such as the Strange Situation Test (SST) originally developed to study the mother–infant relationship in humans (Ainsworth & Wittig 1969). The paradigmatic element of this procedure is that separation from the caregiver in an unfamiliar environment evokes anxiety (which is manifested behaviourally in proximity seeking), while the activated attachment system upon reunion with the caregiver manifests in different forms of contact-seeking behaviours. Importantly, attachment behaviour is oriented mainly towards the caregiver, in the sense that there is a significant difference in the level of proximity and contact seeking, and in the effort made to maintain contact, between the caregiver and an unfamiliar person in the same novel situation. Adult dogs show specific patterns of attachment behaviour towards their owner in the SST ( [Topál et al., 1998] and [Prato-Previde et al., 2003]), suggesting a case of functional analogy (evolutionary convergence) to the human infant–parent attachment. Gácsi et al. (2001) reported that attachment develops rapidly: a short period of interaction with humans evoked attachment behaviour towards the handler in adult dogs that had been deprived of human contact (shelter dogs) and the dogs differentiated between their handler and a stranger in the same way as adult pet dogs did.

We designed a comparative experiment to investigate the attachment behaviour of hand-reared and extensively socialized wolf and dog puppies and pet dog puppies that had received a normal socialization regimen from their owners. We investigated whether (1) pet dogs' attachment to humans is observable in the SST as early as 16 weeks of age, (2) extensive socialization by human caregivers causes any change in attachment behaviour of dog puppies and (3) there are species-specific differences between wolves and dogs in their attachment behaviour to humans.

Although one might assume that the ability to show attachment behaviour to individuals of another species (humans) in adulthood is a unique feature of the domestic dog, despite much interest ( [Scott, 1963], [Scott, 1992] and [Ginsburg and Hiestand, 1992]), there has been no clear theory explaining the emergence of the phenomenon. By comparing the emergence of attachment behaviour to humans in dogs and socialized wolves tested by the same experimental method we can examine whether inheritance (genetic background) or environmental effects (rearing history) are more important.

Two hypotheses can be formulated. The socialization hypothesis suggests that attachment could develop mainly as a result of extensive hand rearing and individual socialization to the human social environment (i.e. enculturation) during the ‘critical period’ of socialization (Freedman et al. 1961). The domestication hypothesis, however, claims that there could have been specific genetic changes (in the attachment behaviour organizing system) that have emerged as the result of selective breeding for dependency and attachment to humans (see also [Hare et al., 2002] and [Miklósi et al., 2003] for similar explanations regarding communicative abilities in dogs). The socialization hypothesis predicts that hand-reared wolf and dog puppies will show similar forms of attachment behaviour to their human caregivers, whereas pet dog puppies, being less extensively socialized, will show less attachment to their owners. In contrast, the domestication hypothesis predicts species-specific differences in attachment behaviour to humans between wolves and dogs reared in the same way (i.e. dogs should show more specific attachment behaviour than wolves towards humans). These explanations are not mutually exclusive, however, and both of the hypothesized mechanisms could affect the behaviour phenotype.