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Genomic Regions Associated With Interspecies Communication in Dogs Contain Genes Related to Human Social Disorders
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.ORCID iD: 0000-0002-6115-7517
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.ORCID iD: 0000-0003-2329-2635
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.ORCID iD: 0000-0002-3297-1130
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.
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2016 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 6, article id 33439Article in journal (Refereed) Published
Abstract [en]

Unlike their wolf ancestors, dogs have unique social skills for communicating and cooperating with humans. Previously, significant heritabilities for human-directed social behaviors have been found in laboratory beagles. Here, a Genome-Wide Association Study identified two genomic regions associated with dog's human-directed social behaviors. We recorded the propensity of laboratory beagles, bred, kept and handled under standardized conditions, to initiate physical interactions with a human during an unsolvable problem-task, and 190 individuals were genotyped with an HD Canine SNP-chip. One genetic marker on chromosome 26 within the SEZ6L gene was significantly associated with time spent close to, and in physical contact with, the human. Two suggestive markers on chromosome 26, located within the ARVCF gene, were also associated with human contact seeking. Strikingly, four additional genes present in the same linkage blocks affect social abilities in humans, e.g., SEZ6L has been associated with autism and COMT affects aggression in adolescents with ADHD. This is, to our knowledge, the first genome-wide study presenting candidate genomic regions for dog sociability and inter-species communication. These results advance our understanding of dog domestication and raise the use of the dog as a novel model system for human social disorders.

Place, publisher, year, edition, pages
Nature Publishing Group, 2016. Vol. 6, article id 33439
National Category
Genetics
Identifiers
URN: urn:nbn:se:liu:diva-131644DOI: 10.1038/srep33439ISI: 000384172800001PubMedID: 27685260OAI: oai:DiVA.org:liu-131644DiVA, id: diva2:998790
Note

Funding agencies: European Research Council (ERC) [322206]; Formas

Available from: 2016-09-30 Created: 2016-09-30 Last updated: 2020-01-21Bibliographically approved
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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Available from: 2020-01-21 Created: 2020-01-21 Last updated: 2020-01-21Bibliographically approved

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