The Russian Farm-Fox Experiment is the best known experimental study in animal domestication. By subjecting a population of foxes to selection for tameness alone, Dimitry Belyaev generated foxes that possessed a suite of characteristics that mimicked those found across domesticated species. This 'domestication syndrome' has been a central focus of research into the biological pathways modified during domestication. Here, we chart the origins of Belyaev's foxes in eastern Canada and critically assess the appearance of domestication syndrome traits across animal domesticates. Our results suggest that both the conclusions of the Farm-Fox Experiment and the ubiquity of domestication syndrome have been overstated. To understand the process of domestication requires a more comprehensive approach focused on essential adaptations to human-modified environments.
The Origins of Domestication SyndromeThe domestication syndrome describes a suite of behavioral and morphological characteristics consistently observed in domesticated populations. It was first described in animals (although not named as such) by Charles Darwin [1]. The term itself, coined by botanists in the early 1900s [2,3], was applied to animals in the 1980s [3]. Usage has risen dramatically since the mid-1990s, by more than 20-fold (see the supplemental information online) [4].The concept of a domestication syndrome is appealing. The grouping of a collection of traits allows easier identification and facilitates the definition of domesticated taxa. It also inspires a search for causal mechanisms, whether genetic or environmental, responsible for their collective appearance. Characteristics attributed to domestication syndrome vary, but include tamability (see Glossary), loss of reproductive seasonality, and changes in coat color, ear form, tail form, and craniofacial morphology (Figure 1) [1,[5][6][7][8][9][10][11][12][13].
Behavioral genetics in dogs has focused on modern breeds, which are isolated subgroups with distinctive physical and, purportedly, behavioral characteristics. We interrogated breed stereotypes by surveying owners of 18,385 purebred and mixed-breed dogs and genotyping 2155 dogs. Most behavioral traits are heritable [heritability (
h
2
) > 25%], and admixture patterns in mixed-breed dogs reveal breed propensities. Breed explains just 9% of behavioral variation in individuals. Genome-wide association analyses identify 11 loci that are significantly associated with behavior, and characteristic breed behaviors exhibit genetic complexity. Behavioral loci are not unusually differentiated in breeds, but breed propensities align, albeit weakly, with ancestral function. We propose that behaviors perceived as characteristic of modern breeds derive from thousands of years of polygenic adaptation that predates breed formation, with modern breeds distinguished primarily by aesthetic traits.
Little is known about the development of the sensory systems of wolves. The timing of sensory development in wolves is usually extrapolated from studies on dogs, since they are members of the same species. However, early developmental differences between these two subspecies have already been identified. For example, wolves tend to approach and investigate objects in their environment 2 wk before dogs. These changes in developmental timing may play an important role in the behavioral differences between adult wolves and dogs. The purpose of this study is to compare the development of the sensory systems in wolves and dogs.
Responses of seven wolf pups and 43 dog pups to familiar and novel olfactory, auditory, and visual stimuli were tested weekly from 2–7 wk of age. Eleven wolf pups were also observed for orientation towards auditory and visual stimuli during 2‐h sessions, 5 d a week, from 2–8 wk of age. These observations were supplemented by the daily records of caretakers.
The results suggest that wolves and dogs both develop olfaction by 2 wk, audition by 4 wk, and vision by 6 wk on average, despite the 2‐wk shift in their ability to explore. This means that when wolves begin to explore at 2 wk, they are blind and deaf, and must rely primarily on their sense of smell. Thus, there is a significant alteration of how these subspecies experience their environment during the critical period of socialization. These findings lead to an alternative explanation for the difference in dogs' and wolves' abilities to form interspecies social attachments, such as those with humans.
19Previous research suggested that 16--week old dog pups, but not wolf pups, 20show attachment behaviour to a human caregiver. Attachment to a caregiver in dog 21 pups has been demonstrated by differential responding to a caregiver compared to 22 a stranger in the Ainsworth Strange Situation Test. We show here that 3--7 week old 23 wolf pups also show attachment--like behaviour to a human caregiver as measured 24 by preferential proximity seeking, preferential contact, and preferential greeting to 25 a human caregiver over a human stranger in a modified and counterbalanced 26 version of the Ainsworth Strange Situation Test. In addition, our results show that 27 preferential responding to a caregiver over a stranger is only apparent following 28 brief isolation. In initial episodes, wolf pups show no differentiation between the 29 caregiver and the stranger; however, following a 2--min separation, the pups show 30 proximity seeking, more contact, and more greeting to the caregiver than the 31 stranger. These results suggest intensive human socialization of a wolf can lead to 32 attachment--like responding to a human caregiver during the first two months of a 33 wolf pup's life. 34
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