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Highly heritable and functionally relevant breed differences in dog behaviour
Open accessPublished version of a preprint
Abstract
Variation across dog breeds presents a unique opportunity to investigate the evolution and biological basis of complex behavioural traits. We integrated behavioural data from more than 14 000 dogs from 101 breeds with breed-averaged genotypic data ( n = 5697 dogs) from over 100 000 loci in the dog genome. We found high levels of among-breed heritability for 14 behavioural traits (the proportion of trait variance attributable to genetic similarity among breeds). We next identified 131 single nucleotide polymorphisms associated with breed differences in behaviour, which were found in genes that are highly expressed in the brain and enriched for neurobiological functions and developmental processes, suggesting that they may be functionally associated with behavioural differences. Our results shed light on the heritability and genetic architecture of complex behavioural traits and identify dogs as a powerful model in which to address these questions.
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“Additionally, studies have shown that certain behaviours, such as trainability, aggression towards strangers, attention seeking, and attachment, may be more heritable than others [165].”
From Ethical Concerns about Fashionable Dog Breeding (2024) · cites this paper as [165]
Citations
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
PLINK: a tool set for whole-genome association and population-based linkage analyses.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., et al. (2007) · The American Journal of Human Genetics · doi:10.1086/519795 · Cited by 34,089
Regularization Paths for Generalized Linear Models via Coordinate Descent
Friedman, J., Hastie, T., & Tibshirani, R. (2010) · Journal of Statistical Software · doi:10.18637/jss.v033.i01 · Cited by 19,927
Tissue-based map of the human proteome
Uhlén, M., Fagerberg, L., Hallström, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å., Kampf, C., Sjöstedt, E., Asplund, A., et al. (2015) · Science · doi:10.1126/science.1260419 · Cited by 15,286
MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package
Hadfield, J. D. (2010) · Journal of Statistical Software · doi:10.18637/jss.v033.i02 · Cited by 4,900
Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt
Durinck, S., Spellman, P. T., Birney, E., & Huber, W. K. (2009) · Nature Protocols · doi:10.1038/nprot.2009.97 · Cited by 4,226
Genome-wide efficient mixed-model analysis for association studies
Zhou, X., & Stephens, M. (2012) · Nature Genetics · doi:10.1038/ng.2310 · Cited by 3,627 · cited 7×
“EMMA models were fit using the EMMREML R package (34).”
MethodInfluentialGenome sequence, comparative analysis and haplotype structure of the domestic dog
members, B. S. P., Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S., Karlsson, E. K., Jaffe, D. B., Kamal, M., Clamp, M., Chang, J. L., Kulbokas, E. J., et al. (2005) · Nature · doi:10.1038/nature04338 · Cited by 2,568
BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis
Durinck, S., Moreau, Y., Kasprzyk, A., Davis, S. R., Moor, B. D., Brāzma, A., & Huber, W. K. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti525 · Cited by 2,327
Heritability in the genomics era — concepts and misconceptions
Visscher, P. M., Hill, W. G., & Wray, N. R. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2322 · Cited by 1,921
Efficient Control of Population Structure in Model Organism Association Mapping
Kang, H. M., Zaitlen, N., Wade, C. M., Kirby, A. W., Heckerman, D. E., Daly, M. J., & Eskin, E. (2008) · Genetics · doi:10.1534/genetics.107.080101 · Cited by 1,869
dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering
Galili, T. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv428 · Cited by 1,826
Neuroendocrine perspectives on social attachment and love
Sue Carter, C. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00055-9 · Cited by 1,425
An ecologist’s guide to the animal model
Wilson, A. J., Réale, D. J. F., Clements, M., Morrissey, M. M., Postma, E., Walling, C. A., Kruuk, L. E. B., & Nussey, D. H. (2009) · Journal of Animal Ecology · doi:10.1111/j.1365-2656.2009.01639.x · Cited by 1,037
Human-like social skills in dogs?
Hare, B., & Tomasello, M. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.07.003 · Cited by 967
Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication
vonHoldt, B. M., Pollinger, J. P., Lohmueller, K. E., Han, E., Parker, H. G., Quignon, P., Degenhardt, J. D., Boyko, A. R., Earl, D. A., Auton, A., et al. (2010) · Nature · doi:10.1038/nature08837 · Cited by 825
Self-citationGenetic Structure of the Purebred Domestic Dog
Parker, H. G., Kim, L. V., Sutter, N. B., Carlson, S., Lorentzen, T. D., Malek, T. B., Johnson, G. S., DeFrance, H. B., Ostrander, E. A., & Kruglyak, L. (2004) · Science · doi:10.1126/science.1097406 · Cited by 753
Oxytocin-gaze positive loop and the coevolution of human-dog bonds
Nagasawa, M., Mitsui, S., En, S., Ohtani, N., Ohta, M., Sakuma, Y., Onaka, T., Mogi, K., & Kikusui, T. (2015) · Science · doi:10.1126/science.1261022 · Cited by 753
Wilkins, A. S., Wrangham, R. W., & Fitch, W. T. (2014) · Genetics · doi:10.1534/genetics.114.165423 · Cited by 751
Hsu, Y., & Serpell, J. A. (2003) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.2003.223.1293 · Cited by 709
Self-citationPitfalls of predicting complex traits from SNPs
Wray, N. R., Yang, J., Hayes, B. J., Price, A. L., Goddard, M. E., & Visscher, P. M. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3457 · Cited by 690
A Single IGF1 Allele Is a Major Determinant of Small Size in Dogs
Sutter, N. B., Bustamante, C. D., Chase, K., GRAY, M. M., Zhao, K., Zhu, L., Padhukasahasram, B., Karlins, E., Davis, S. R., Jones, P. G., et al. (2007) · Science · doi:10.1126/science.1137045 · Cited by 673
Early canid domestication: the farm-fox experiment.
Trut, L. (1999) · American Scientist · doi:10.1511/1999.2.160 · Cited by 626
A neurobiological basis of social attachment.
(1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.6.726 · Cited by 553
A Simple Genetic Architecture Underlies Morphological Variation in Dogs
Boyko, A. R., Quignon, P., Li, L., Schoenebeck, J. J., Degenhardt, J. D., Lohmueller, K. E., Zhao, K., Brisbin, A. G., Parker, H. G., vonHoldt, B. M., et al. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000451 · Cited by 499
Self-citationParker, H. G., Dreger, D. L., Rimbault, M., Davis, B. W., Mullen, A. B., Carpintero-Ramirez, G., & Ostrander, E. A. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.079 · Cited by 455
Survival of the Friendliest: Homo sapiens Evolved via Selection for Prosociality
Hare, B. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-010416-044201 · Cited by 444
QST–FST comparisons: evolutionary and ecological insights from genomic heterogeneity
Leinonen, T., McCairns, R. J. S., O'Hara, R. B., & Merilä, J. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3395 · Cited by 422
Dog behaviour, evolution, and cognition
Miklósi, Á. (2015) · Choice Reviews Online · doi:10.5860/choice.191407 · Cited by 328
The genomics of selection in dogs and the parallel evolution between dogs and humans
Wang, G.-D., Zhai, W., Yang, H.-C., Fan, R.-X., Cao, X., Zhong, L., Wang, L., Liu, F., Wu, H., Cheng, L.-G., et al. (2013) · Nature Communications · doi:10.1038/ncomms2814 · Cited by 323
Oxidative DNA damage, antioxidants, and cancer
Collins, A. R. (1999) · BioEssays · doi:10.1002/(sici)1521-1878(199903)21:3 · Cited by 316
Complex disease and phenotype mapping in the domestic dog
Hayward, J. J., Castelhano, M. G., Oliveira, K. C., Corey, E. E., Balkman, C. E., Baxter, T. L., Casal, M. L., Fang, M., Garrison, S. J., Kalla, S. E., et al. (2016) · Nature Communications · doi:10.1038/ncomms10460 · Cited by 274
A Genomic Background Based Method for Association Analysis in Related Individuals
Amin, N., van Duijn, C. M., & Aulchenko, Y. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001274 · Cited by 262
Dog star rising: the canine genetic system
Sutter, N. B., & Ostrander, E. A. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1492 · Cited by 259
Development and validation of a novel method for evaluating behavior and temperament in guide dogs
Serpell, J. A., & Hsu, Y. (2001) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(00)00210-0 · Cited by 244
Self-citationSvartberg, K. (2005) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2004.08.030 · Cited by 235
Predictive validity of a method for evaluating temperament in young guide and service dogs
Duffy, D. L., & Serpell, J. A. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.02.011 · Cited by 220
Self-citationDog Behavior Co-Varies with Height, Bodyweight and Skull Shape
McGreevy, P. D., Georgevsky, D., Carrasco, J., Valenzuela, M., Duffy, D. L., & Serpell, J. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080529 · Cited by 213
Self-citationGene set analysis of genome-wide association studies: Methodological issues and perspectives
Wang, L., Jia, P., Wolfinger, R. D., Chen, X., & Zhao, Z. (2011) · Genomics · doi:10.1016/j.ygeno.2011.04.006 · Cited by 207
Dog Behaviour, Evolution, and Cognition
Miklósi, Á. (2014) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199646661.001.0001 · Cited by 195
Whither Pst? The approximation of Qst by Pst in evolutionary and conservation biology
BROMMER, J. E. (2011) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2011.02268.x · Cited by 194
vonHoldt, B. M., Shuldiner, E., Koch, I. J., Kartzinel, R. Y., Hogan, A., Brubaker, L., Wanser, S., Stahler, D., Wynne, C. D. L., Ostrander, E. A., et al. (2017) · Science Advances · doi:10.1126/sciadv.1700398 · Cited by 186
Self-citationGenetic mapping of canine fear and aggression
Zapata, I., Serpell, J. A., & Alvarez, C. E. (2016) · BMC Genomics · doi:10.1186/s12864-016-2936-3 · Cited by 168
Self-citationUnleashing the Canine GenomePreprint
Ostrander, E. A., & Kruglyak, L. (2000) · Genome Research · doi:10.1101/gr.155900 · Cited by 165
Single-Nucleotide-Polymorphism-Based Association Mapping of Dog Stereotypes
Jones, P., Chase, K., Martin, A. J., Davern, P., Ostrander, E., & Lark, K. G. (2008) · Genetics · doi:10.1534/genetics.108.087866 · Cited by 159
Pendleton, A. L., Shen, F., Taravella, A. M., Emery, S., Veeramah, K. R., Boyko, A. R., & Kidd, J. M. (2018) · BMC Biology · doi:10.1186/s12915-018-0535-2 · Cited by 156
MacLean, E. L., Herrmann, E., Suchindran, S., & Hare, B. A. (2017) · Animal Behaviour · doi:10.1016/j.anbehav.2017.01.005 · Cited by 128
Self-citationSerpell, J. A., & Duffy, D. L. (2014) · Springer eBooks · doi:10.1007/978-3-642-53994-7_2 · Cited by 124
Self-citationUnraveling the evolution of uniquely human cognition
MacLean, E. L. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521270113 · Cited by 124
Self-citationLequarré, A., Andersson, L., André, C., Fredholm, M., Hitte, C., Leeb, T., Lohi, H., Lindblad‐Toh, K., & Georges, M. (2011) · The Veterinary Journal · doi:10.1016/j.tvjl.2011.06.013 · Cited by 115
Demographically-based evaluation of genomic regions under selection in domestic dogs
Freedman, A. H., Schweizer, R. M., Ortega-Del Vecchyo, D., Han, E., Davis, B. W., Gronau, I., Silva, P. M., Galaverni, M., Fan, Z., Marx, P., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005851 · Cited by 104
Genetic variation in aggression-related traits in Golden Retriever dogs
Liinamo, A.-E., van den Berg, L., Leegwater, P. A. J., Schilder, M. B. H., van Arendonk, J. A. M., & van Oost, B. A. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.04.025 · Cited by 103
Genetic Characterization of Dog Personality Traits
Ilska, J. J., Haskell, M. J., Blott, S. C., Sánchez-Molano, E., Polgár, Z., Lofgren, S. E., Clements, D. N., & Wiener, P. (2017) · Genetics · doi:10.1534/genetics.116.192674 · Cited by 100
NAM: association studies in multiple populations
Xavier, A., Xu, S., Muir, W. M., & Rainey, K. M. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv448 · Cited by 83
Artificial Selection on Brain-Expressed Genes during the Domestication of Dog
Li, Y., vonHoldt, B. M., Reynolds, A., Boyko, A. R., Wayne, R. K., Wu, D., & Zhang, Y. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst088 · Cited by 83
Self-citationThe Social dog: behavior and cognition
(2014) · Choice Reviews Online · doi:10.5860/choice.186934 · Cited by 81
Genetic selection of athletic success in sport-hunting dogs
Kim, J., Williams, F. J., Dreger, D. L., Plassais, J., Davis, B. W., Parker, H. G., & Ostrander, E. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800455115 · Cited by 79
Wei, Q., Khan, I., Ding, Z., Yerneni, S., & Kihara, D. (2017) · BMC Bioinformatics · doi:10.1186/s12859-017-1600-5 · Cited by 73
Big thoughts in small brains? Dogs as a model for understanding human social cognition
Mikl??si, ?., Top??l, J., & Cs??nyi, V. (2007) · Neuroreport · doi:10.1097/wnr.0b013e3280287aae · Cited by 73
Evaluation of the C-BARQ as a measure of stranger-directed aggression in three common dog breeds
van den Berg, S. M., Heuven, H. C. M., van den Berg, L., Duffy, D. L., & Serpell, J. A. (2010) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2010.02.005 · Cited by 70
Self-citationNoh, H. J., Tang, R., Flannick, J. A., O'Dushlaine, C. T., Swofford, R., Howrigan, D. P., Genereux, D. P., Johnson, J., van Grootheest, G., Grünblatt, E., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00831-x · Cited by 69
Destabilizing selection as a factor in domestication
BELYAEV, D. K. (1979) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a109263 · Cited by 57
Marshall-Pescini, S., & Kaminski, J. (2014) · The Social Dog · doi:10.1016/b978-0-12-407818-5.00001-2 · Cited by 55
The Genius of Dogs: How Dogs Are Smarter than You Think
Hare, B. A., & Woods, V. E. (2013) · Medical Entomology and Zoology · Cited by 50
Dogs hijack the human bonding pathway
MacLean, E. L., & Hare, B. A. (2015) · Science · doi:10.1126/science.aab1200 · Cited by 46
Self-citationA Compendium of Canine Normal Tissue Gene Expression
Briggs, J., Paoloni, M. C., Chen, Q., Wen, X., Khan, J. I., & Khanna, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017107 · Cited by 38
Anterior Pituitary Transcriptome Suggests Differences in ACTH Release in Tame and Aggressive Foxes
Hekman, J. P., Johnson, J. L., Edwards, W. D., Vladimirova, A. V., Gulevich, R. G., Ford, A. L., Kharlamova, A. V., Herbeck, Y. E., Acland, G. M., Raetzman, L. T., et al. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.300508 · Cited by 37
Holding back the genes: limitations of research into canine behavioural genetics
van Rooy, D., Arnott, E. R., Early, J. B., McGreevy, P. D., & Wade, C. M. (2014) · Canine Genetics and Epidemiology · doi:10.1186/2052-6687-1-7 · Cited by 36
de Gortari, P., & Mengod, G. (2009) · Brain Research · doi:10.1016/j.brainres.2009.11.009 · Cited by 32
Differences in Evaluation of a Dog’s Temperament by Individual Members of the Same Household
Jakuba, T., Polcová, Z., Fedáková, D., Kottferová, J., Mareková, J., Fejsáková, M., Ondrašovičová, O., & Ondrasovic, M. (2013) · Society and Animals · doi:10.1163/15685306-12341314 · Cited by 20
Pendleton, A. L., Shen, F., Taravella, A. M., Emery, S., Veeramah, K. R., Boyko, A. R., & Kidd, J. M. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/118794 · Cited by 6
Data from: Complex disease and phenotype mapping in the domestic dog
Hayward, J. J., Castelhano, M. G., Oliveira, K. C., Corey, E. E., Balkman, C., Baxter, T. L., Casal, M. L., Center, S. A., Fang, M., Garrison, S. J., et al. (2015) · Data Archiving and Networked Services (DANS) · doi:10.5061/dryad.266k4 · Cited by 5
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Rodriguez, K. E., Herzog, H., & Gee, N. R. (2021) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.619600 · Cited by 213
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Salonen, M., Sulkama, S., Mikkola, S., Puurunen, J., Hakanen, E., Tiira, K., Araujo, C., & Lohi, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-59837-z · Cited by 182
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Hecht, E. E., Smaers, J. B., Dunn, W. D., Kent, M., Preuss, T. M., & Gutman, D. A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0303-19.2019 · Cited by 138
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Metadata
- Authors
- MacLean, E. L., Snyder-Mackler, N., vonHoldt, B. M., & Serpell, J. A.
- Affiliations
- University of Arizona (US)
- Department of Psychology, University of Washington, Seattle, WA, USA
- Princeton University (US)
- University of Pennsylvania (US)
- Corresponding author
- MacLean, Evan L.
- Venue
- Proceedings of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2019-10-02
- Volume
- 286
- Issue
- 1912
- Pages
- 20190716
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC6790757
- OpenAlex
- W2978398499
- Cited by
- 144
- References
- 73
- Citations by year
- 2026: 11 · 2025: 18 · 2024: 35 · 2023: 17 · 2022: 20 · 2021: 24 · 2020: 13 · 2019: 6
- FWCI
- 9.49
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UA Campus Repository (The University of Arizona) (acceptedVersion)
- Funders
- University of Pennsylvania
- National Institute on Aging (R00AG051764)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Human-Animal Interaction Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Keywords
- dog behavior, dog breeds, heritability, breed differences, single nucleotide polymorphisms, genetic architecture, brain gene expression, neurobiology, dog genome
- MeSH terms
- Animals, Behavior, Animal, Breeding, Dogs, Genotype, Species Specificity, Genome, Polymorphism, Single Nucleotide, Heredity
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