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Intranasal oxytocin and a polymorphism in the oxytocin receptor gene are associated with human-directed social behavior in golden retriever dogs
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering. (AVIAN Behaviour Genomics and Physiology Group)ORCID iD: 0000-0002-6115-7517
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering. (AVIAN Behaviour Genomics and Physiology Group)
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering. (AVIAN Behaviour Genomics and Physiology Group)ORCID iD: 0000-0001-5508-4465
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering. (AVIAN Behaviour Genomics and Physiology Group)ORCID iD: 0000-0002-3297-1130
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2017 (English)In: Hormones and Behavior, ISSN 0018-506X, E-ISSN 1095-6867, Vol. 95, p. 85-93Article in journal (Refereed) Published
Abstract [en]

The oxytocin system may play an important role in dog domestication from the wolf. Dogs have evolved unique human analogue social skills enabling them to communicate and cooperate efficiently with people. Genomic differences in the region surrounding the oxytocin receptor (OXTR) gene have previously been associated with variation in doge communicative skills. Here we have utilized the unsolvable problem paradigm to investigate the effects of oxytocin and OXTR polymorphisms on human-directed contact seeking behavior in 60 golden retriever dogs. Human-oriented behavior was quantified employing a previously defined unsolvable problem paradigm. Behaviors were tested twice in a repeated, counterbalanced design, where dogs received a nasal dose of either oxytocin or saline 45 min before each test occasion. Buccal DNA was analysed for genotype on three previously identified SNP-markers associated with OXTR. The same polymorphisms were also geno-typed in 21 wolf blood samples to explore potential genomic differences between the species. Results showed that oxytocin treatment decreased physical contact seeking with the experimenter and one of the three polymorphisms was associated with degree of physical contact seeking with the owner. Dogs with the AA-genotype at this locus increased owner physical contact seeking in response to oxytocin while the opposite effect was found in GG-genotype individuals. Hence, intranasal oxytocin treatment, an OXTR polymorphism and their interaction are associated with doge human-directed social skills, which can explain previously described breed differences in oxytocin response. Genotypic variation at the studied locus was also found in wolves indicating that it was present even at the start of dog domestication.

Place, publisher, year, edition, pages
ACADEMIC PRESS INC ELSEVIER SCIENCE , 2017. Vol. 95, p. 85-93
Keywords [en]
Oxytocin; Oxytocin receptor gene; OXTR; Domestic dog; Canine; Wolf; Canis lupus; Behavior genetics; Canine behavior; Social behavior
National Category
Other Biological Topics
Identifiers
URN: urn:nbn:se:liu:diva-142438DOI: 10.1016/j.yhbeh.2017.07.016ISI: 000412863500010PubMedID: 28765081OAI: oai:DiVA.org:liu-142438DiVA, id: diva2:1153651
Note

Funding Agencies|European Research Council (ERC) [322206]

Available from: 2017-10-31 Created: 2017-10-31 Last updated: 2020-01-21
In thesis
1. Pawsitive selection: Genetics of dog-human communication
Open this publication in new window or tab >>Pawsitive selection: Genetics of dog-human communication
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Through domestication and recent selection, dogs have evolved a unique set of communicative skills to attract and redirect human attention. These social skills have not been seen to the same extent in socialised wolves and are therefore believed to have a significant genetic basis. The process of domestication and breed formation has also had effects on the structure of the dog genome that are favourable for genetic mapping. With a high amount of linkage and long haplotype blocks, fewer genetic markers are needed to find gene-trait associations in dogs than in humans. Dogs serve as an important research model for us since humans and dogs share several diseases, psychiatric disorders and behavioural traits.

In Paper I, I recorded human-directed social behaviours during a two-minute unsolvable problem task in 500 laboratory beagles. The dogs were living at a breeding facility and had been bred, kept and handled under standardised conditions. Behaviours related to task solving and human-directed contact seeking were separated in a principal component analysis, indicating that the behavioural test can be used to study dog-human interaction. Narrowsense heritability (h2) of the largest principal component related to contact seeking behaviours was estimated to 0.23. This study found a significant genetic basis to the variation seen in human-directed contact seeking behaviours recorded in this population.

Next, in Paper II, we collected and genotyped the DNA of 190 of the previously tested beagles with an HD Canine SNP-chip. To find genes associated with human-directed contact seeking I performed a genome-wide association study (GWAS), showing one significant and two suggestive single nucleotide polymorphism (SNP) markers on chromosome 26. The significant SNP is located within a gene named SEZ6L, previously associated with autism in human studies. Two adjacent SNPs with suggestive association were found within a gene called ARVCF, which has been associated with schizophrenia. To our knowledge, this was the first genome-wide study to present regions within the dog genome associated with inter-species communication in dogs.

However, these results could have been unique to this beagle population, so Paper III aimed to verify our previous findings in additional dog breeds. We tested 100 Labrador retrievers and 61 golden retrievers with the same unsolvable problem-task used in Paper I. Their DNA was collected and each individual was genotyped by pyrosequencing on two of the previously identified SNPs. To study the effects of recent selection, the Labrador retrievers were divided into two types. The common type is mainly bred and used for dog shows and as a pet, while the field type is mainly bred and used for hunting purposes. In this study, we found that both markers varied in both dog breeds and was significantly associated with human-directed contact-seeking behaviours. Allele frequencies differed significantly between Labrador retriever types, suggesting that these loci have been affected by recent selection. In conclusion, Paper III verifies the results found in Paper II.

Finally, in Paper IV we investigated the association between dogs’ human-directed social skills and previously known SNP markers in the oxytocin receptor (OXTR) region. The oxytocin system plays an important role in the formation of social bonds and may therefore also be important in the bond between dogs and humans. Here, we hypothesized that dogs receiving intranasal oxytocin respond differently to the hormone, depending on the receptor type. To investigate this, 60 golden retrievers were genotyped for SNP markers in the OXTR region and tested with the unsolvable problem task used in Paper I and III. An association was found between genotype and social behaviour in response to oxytocin administration. Dogs responded differently to oxytocin treatment, depending on OXTR genotype. In summary, this thesis contributes to the knowledge on genetic influence of interspecies communication in dogs.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2020. p. 35
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 2038
National Category
Genetics
Identifiers
urn:nbn:se:liu:diva-163173 (URN)10.3384/diss.diva-163173 (DOI)9789179299378 (ISBN)
Public defence
2020-02-28, Planck, F Building, Campus Valla, Linköping, 09:15 (English)
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Supervisors
Available from: 2020-01-21 Created: 2020-01-21 Last updated: 2020-01-21Bibliographically approved

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