Genetics and epigenetics of wolf and dog social behavior

An increasing number of human, primate and rodent studies report epigenetic effects of early social environment. However, there is no published data in connection to dogs which live in the actual social environment of humans. Based on former results, the dog model is suitable for studying genetic factors of certain human traits, such as impulsivity, but environmental effects on epigenetic (DNA methylation pattern) modifications have not been studied in canines. The proposed project aims at understanding the interaction between genetic factors and environmental effects on the social behavior of dogs and wolves kept in different social conditions. We will compare dogs living in captive packs with or without human leading or as only pets with owners who control their dogs with different strength. Dogs and wolves raised by humans but living in packs under identical condition will be also involved in order to investigate the evolutionary origins of dog-human relationship. We plan to identify genetic and epigenetic markers associated with the animals` social behavior recorded in standardized test situations. The proposed interdisciplinary project relies on a close collaboration between the ethologists of the Messerli Research Institute, University of Veterinary Medicine Vienna and the Wolf Science Center in Austria and the molecular geneticists at the Laboratory of Molecular Genetics, Institute of Medical Chemistry, Molecular Biology and Pathobiochemistry, Semmelweis University in Budapest, Hungary. One of our aims is to create the Canine Social Behavioural (CSB) Biobank which we plan to use in further international collaborations. The biobank will contain DNA samples as well as detailed behavioral, hormonal, genetic and epigenetic data of about 300 dogs and wolves kept is different social environments. This project will give a unique possibility to test an animal model of social environmental effects. Since dogs live in a social environment shared by humans and they show social behaviors analogous with human patterns, the social behavior of human-kept dogs is most probably more relevant to human social behavior phenotypes compared to that of monkeys kept in captivity or of rodents kept in laboratory settings. If we can detect similar epigenetic changes in the DNA methylation levels of selected gene regions as a consequence of adverse environment in dogs and humans, it will mean a break-through in modeling impairment of human social behavior, which is important in a range of mental health disorders, such as autism. The closer relationship of dogs and humans will enable us to model delicate changes in the social environment, and it will also represent a less expensive model compared to primate models.

There is a great variation across individuals in how they behave when meeting an unfamiliar person or what kind of relationship they build up with their closest partner. To what extent this individual variation in social behaviour results from genetic differences and to what extent it can be attributed to effects of different environments the individuals have grown up and live in belong to the most intriguing questions. Domestic dogs have been living in social environments shared with humans for more than 10.000 years and show social behaviours analogous to human patterns. Therefore, it has been suggested that pet dogs can be a better model of how genes and environment interact to form human social behaviour, as compared to laboratory rodents or primates.In this project we developed methods to record individual variation in the social behaviour of pet dogs, and focused on two behavioural domains essential for the social life of both dogs and humans: relationships with one's closest social partners and encounters with an unfamiliar human in different contexts. Regarding the later domain, we collected behavioural data and DNA samples from 220 pet dogs. We found that how the dogs behaved upon social encounters (e.g. passive, friendly, or aggressive) was associated both with variation in their oxytocin receptor gene (OXTR) and with its methylation level. Oxytocin is an ancient hormone that regulates social fear as well as bonding in mammalian species. Methylation of the DNA is a mechanism through which environmental effects can influence the expression of a gene, thereby modulating genetic effects on behaviour. Accordingly, in a smaller study we measured different levels of OXTR methylation in 2 groups of dogs that were born in the same litters at the Wolf Science Center but then either continued to live in captive packs or were moved to human families as pets. We found no evidence, however, that methylation of pet dogs' OXTR gene would be influenced by the interaction style of their owners.Analyzing the behaviour of 220 owners, we determined that owner warmth, social support and control are the 3 components that constitute dog owners' interaction styles. Importantly, these components are comparable to those of human parenting. This suggests that owners use the same behavioural repertoire when interacting with dogs and children, which makes environmental influences on dogs' and humans' social behaviour even more comparable.Our findings are highly relevant also for dog keeping practices. The link between owners' interaction styles and their dogs' reaction to a social threat calls attention that educating dogs is more than dog training. The behaviour of dogs, similarly to that of children, is crucially influenced by the spontaneous, everyday behaviour of their owners. Not all dog-owner dyads are able to form a close, well-functioning relationship, which can fundamentally affect the well- being of both parties.