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Pawsitive selection: Genetics of dog-human communication
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.ORCID iD: 0000-0002-6115-7517
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: urn:nbn:se:liu:diva-163173DOI: 10.3384/diss.diva-163173ISBN: 9789179299378 (print)OAI: oai:DiVA.org:liu-163173DiVA, id: diva2:1387235
Public defence
2020-02-28, Planck, F Building, Campus Valla, Linköping, 09:15 (English)
Opponent
Supervisors
Available from: 2020-01-21 Created: 2020-01-21 Last updated: 2020-01-21Bibliographically approved
List of papers
1. Human-directed social behaviour in dogs shows significant heritability
Open this publication in new window or tab >>Human-directed social behaviour in dogs shows significant heritability
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2015 (English)In: Genes, Brain and Behavior, ISSN 1601-1848, E-ISSN 1601-183X, Vol. 14, no 4, p. 337-344Article in journal (Refereed) Published
Abstract [en]

Through domestication and co-evolution with humans, dogs have developed abilities to attract human attention, e.g. in a manner of seeking assistance when faced with a problem solving task. The aims of this study were to investigate within breed variation in human-directed contact seeking in dogs and to estimate its genetic basis. To do this, 498 research beagles, bred and kept under standardized conditions, were tested in an unsolvable problem task. Contact seeking behaviours recorded included both eye contact and physical interactions. Behavioural data was summarized through a principal component analysis, resulting in four components: test interactions, social interactions, eye contact and physical contact. Females scored significantly higher on social interactions and physical contact and age had an effect on eye contact scores. Narrow sense heritabilities (h2) of the two largest components were estimated at 0.32 and 0.23 but were not significant for the last two components. These results show that within the studied dog population, behavioural variation in human-directed social behaviours was sex dependent and that the utilization of eye contact seeking increased with age and experience. Hence, heritability estimates indicate a significant genetic contribution to the variation found in human-directed social interactions, suggesting that social skills in dogs have a genetic basis, but can also be shaped and enhanced through individual experiences. This research gives the opportunity to further investigate the genetics behind dogs’ social skills, which could also play a significant part into research on human social disorders such as autism.

Place, publisher, year, edition, pages
John Wiley & Sons, 2015
Keywords
Beagles, canine behaviour, dogs, domestic dog, eye contact, genetics, heritability, human-directed communication, problem-solving, social behaviour
National Category
Human Computer Interaction
Identifiers
urn:nbn:se:liu:diva-117523 (URN)10.1111/gbb.12194 (DOI)000353405000003 ()25703740 (PubMedID)
Funder
EU, European Research Council, 1242001390
Available from: 2015-04-30 Created: 2015-04-30 Last updated: 2020-01-21
2. Genomic Regions Associated With Interspecies Communication in Dogs Contain Genes Related to Human Social Disorders
Open this publication in new window or tab >>Genomic Regions Associated With Interspecies Communication in Dogs Contain Genes Related to Human Social Disorders
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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
National Category
Genetics
Identifiers
urn:nbn:se:liu:diva-131644 (URN)10.1038/srep33439 (DOI)000384172800001 ()27685260 (PubMedID)
Note

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

Available from: 2016-09-30 Created: 2016-09-30 Last updated: 2020-01-21Bibliographically approved
3. Sociality genes are associated with human-directed social behaviour in golden and Labrador retriever dogs
Open this publication in new window or tab >>Sociality genes are associated with human-directed social behaviour in golden and Labrador retriever dogs
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2018 (English)In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359, Vol. 6, article id e5889Article in journal (Refereed) Published
Abstract [en]

Background: Dogs have human-directed social skills that allow them to communicate and cooperate with humans. We have previously identified two loci on chromosome 26 associated with human contact-seeking behaviors during an unsolvable problem task in laboratory beagles (Persson et A, 2016). The aim of the present study was to verify the single nucleotide polymorphisms (SNPs) in additional dog breeds. We also studied how the allele frequencies have changed during domestication and recent selection. Methods: Dogs of two breeds, 61 golden retrievers and 100 Labrador retrievers, were phenotyped and genotyped, and 19 wolves were genotyped. The Labrador retrievers were divided into common and field type by pedigree data to make it possible to study the effects of recent selection. All dogs were tested in an unsolvable problem task where human-directed social behaviors were scored. DNA from dogs (buccal swabs) and wolves (blood or brain tissue) was analyzed for genotype on two of the previously identified SNP markers, BICF2G630798942 (SNP1) and BICF2S23712114 (SNP2), by pyrosequencing. Results: There was genetic variation for SNP1 in both dog breeds whereas the wolves were fixed for this polymorphism, and for SNP2 there was variation in both dogs and wolves. For both SNPs, Labrador retriever types differed significantly in allele frequencies. We found associations between SNPs and human-directed social behavior in both dog breeds. In golden retrievers, SNP I was associated with physical contact variables, for example, with the duration of physical contact with the owner (F-2,F-56 = 4.389, p = 0.017). SNP2 was associated with several behavioral variables in both breeds, among others owner gazing frequency in both golden retrievers (F-2,F-55 = 6.330, p = 0.003) and Labradors (F-1,F-93 = 5.209, p = 0.025). Discussion: Our results verify the association between the previously identified SNPs and human-directed social behavior scored in an unsolvable problem task. Differences in allele frequencies suggest that these loci have been affected by selection. The results indicate that these genomic regions are involved in human-directed social behavior in not only beagles but in other dog breeds as well. We hypothesize that they may have been important during dog domestication.

Place, publisher, year, edition, pages
PEERJ INC, 2018
Keywords
Genetics; Dog genetics; Dog behavior; Human-dog communication; Human-directed social behavior; Golden retrievers; Labrador retrievers; Wolf; Domestication; Behavior genetics
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:liu:diva-153536 (URN)10.7717/peerj.5889 (DOI)000452327000008 ()30416887 (PubMedID)
Note

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

Available from: 2018-12-20 Created: 2018-12-20 Last updated: 2020-01-21
4. Intranasal oxytocin and a polymorphism in the oxytocin receptor gene are associated with human-directed social behavior in golden retriever dogs
Open this publication in new window or tab >>Intranasal oxytocin and a polymorphism in the oxytocin receptor gene are associated with human-directed social behavior in golden retriever dogs
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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
Keywords
Oxytocin; Oxytocin receptor gene; OXTR; Domestic dog; Canine; Wolf; Canis lupus; Behavior genetics; Canine behavior; Social behavior
National Category
Other Biological Topics
Identifiers
urn:nbn:se:liu:diva-142438 (URN)10.1016/j.yhbeh.2017.07.016 (DOI)000412863500010 ()28765081 (PubMedID)
Note

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

Available from: 2017-10-31 Created: 2017-10-31 Last updated: 2020-01-21

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