Abstract
Behavioral traits like aggression, anxiety, and trainability differ significantly across dog breeds and are highly heritable. However, the neural bases of these differences are unknown. Here we analyzed structural MRI scans of 62 dogs in relation to breed-average scores for the 14 major dimensions in the Canine Behavioral Assessment and Research Questionnaire, a well-validated measure of canine temperament. Several behavior categories showed significant relationships with morphologically covarying gray matter networks and regional volume changes. Networks involved in social processing and the flight-or-fight response were associated with stranger-directed fear and aggression, putatively the main behaviors under selection pressure during wolf-to-dog domestication. Trainability was significantly associated with expansion in broad regions of cortex, while fear, aggression, and other “problem” behaviors were associated with expansion in distributed subcortical regions. These results closely overlapped with regional volume changes with total brain size, in striking correspondence with models of developmental constraint on brain evolution. This suggests that the established link between dog body size and behavior is due at least in part to disproportionate enlargement of later-developing regions in larger brained dogs. We discuss how this may explain the known correlation of increasing reactivity with decreasing body size in dogs.
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References
Andics A, Miklosi A (2018) Neural processes of vocal social perception: dog-human comparative fMRI studies. Neurosci Biobehav Rev 85:54–64
Avants B, Tustison N, Song G, Gee J (2009) ANTS: advanced open-source normalization tools for neuroanatomy. Penn Image Computing and Science Laboratory, Philadelphia
Avants BB, Tustison NJ, Wu J, Cook PA, Gee JC (2011) An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics 9:381–400
Barton RA (2007) Evolutionary specialization in mammalian cortical structure. J Evol Biol 20:1504–1511
Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058
Boyko AR et al (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8:e1000451
Canejo-Teixeira R, Almiro PA, Serpell JA, Baptista LV, Niza M (2018) Evaluation of the factor structure of the canine behavioural assessment and research questionnaire (C-BARQ) in European Portuguese. PLoS One 13:e0209852
Charvet CJ, Darlington RB, Finlay BL (2013) Variation in human brains may facilitate evolutionary change toward a limited range of phenotypes. Brain Behav Evol 81:74–85
Coppinger RP, Coppinger L (2001) Dogs: a startling new understanding of canine origin, behavior & evolution. Simon and Schuster, New York
Cuaya LV, Hernandez-Perez R, Concha L (2016) Our faces in the dog’s brain: functional imaging reveals temporal cortex activation during perception of human faces. PLoS One 11:e0149431
Duffy DL, Hsu Y, Serpell JA (2008) Breed differences in canine aggression. Appl Animal Behav Sci 114:441–460
Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578–1584
Finlay BL, Huang K (2020) Developmental duration as an organizer of the evolving mammalian brain: scaling, adaptations, and exceptions. Evol Dev 22:181–195
Finlay BL, Darlington RB, Nicastro N (2001) Developmental structure in brain evolution. Behav Brain Sci 24:263–278 (discussion 278–308)
Hare E, Kelsey KM, Serpell JA, Otto CM (2018) Behavior differences between search-and-rescue and pet dogs. Front Vet Sci 5:118
Hecht EE, Smaers JB, Dunn WD, Kent M, Preuss TM, Gutman DA (2019) Significant neuroanatomical variation among domestic dog breeds. J Neurosci: off J Soc Neurosci 39:7748–7758
Holekamp KE, Sakai ST, Lundrigan BL (2007) Social intelligence in the spotted hyena (Crocuta crocuta). Philos Trans R Soc Lond B Biol Sci 362:523–538
Hsu Y, Serpell JA (2003) Development and validation of a questionnaire for measuring behavior and temperament traits in pet dogs. J Am Vet Med Assoc 223:1293–1300
Hsu Y, Sun L (2010) Factors associated with aggressive responses in pet dogs. Appl Anim Behav Sci 123:108–123
Ilska J, Haskell MJ, Blott SC, Sanchez-Molano E, Polgar Z, Lofgren SE, Clements DN, Wiener P (2017) Genetic characterization of dog personality traits. Genetics 206:1101–1111
Iwaniuk AN, Dean KM, Nelson JE (2004) A mosaic pattern characterizes the evolution of the avian brain. Proc Biol Sci 271(Suppl 4):S148-151
Lampi S, Donner J, Anderson H, Pohjoismaki J (2020) Variation in breeding practices and geographic isolation drive subpopulation differentiation, contributing to the loss of genetic diversity within dog breed lineages. Canine Med Genet 7:5
Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33:402–416
Larson G, Karlsson EK, Perri A, Webster MT, Ho SY, Peters J, Stahl PW, Piper PJ, Lingaas F, Fredholm M, Comstock KE, Modiano JF, Schelling C, Agoulnik AI, Leegwater PA, Dobney K, Vigne JD, Vila C, Andersson L, Lindblad-Toh K (2012) Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proc Natl Acad Sci USA 109:8878–8883
MacLean EL, Snyder-Mackler N, vonHoldt BM, Serpell JA (2019) Highly heritable and functionally relevant breed differences in dog behaviour. Proc Biol Sci 286:20190716
McGrave EA (1991) Diagnostic criteria for separation anxiety in the dog. Vet Clin North Am Small Anim Pract 21:247–255
McGreevy PD, Georgevsky D, Carrasco J, Valenzuela M, Duffy DL, Serpell JA (2013) Dog behavior co-varies with height, bodyweight and skull shape. PLoS One 8:e80529
Nagasawa M, Tsujimura A, Tateishi K, Mogi K, Ohta M, Serpell JA, Kikusui T (2011) Assessment of the factorial structures of the C-BARQ in Japan. J Vet Med Sci 73:869–875
Pagel MD, Harvey PH (1989) Taxonomic differences in the scaling of brain on body weight among mammals. Science 244:1589–1593
Parker HG, Dreger DL, Rimbault M, Davis BW, Mullen AB, Carpintero-Ramirez G, Ostrander EA (2017) Genomic analyses reveal the influence of geographic origin, migration, and hybridization on modern dog breed development. Cell Rep 19:697–708
Podberscek AL, Hsu Y, Serpell JA (1999) Evaluation of clomipramine as an adjunct to behavioural therapy in the treatment of separation-related problems in dogs. Vet Rec 145:365
Radinsky L (1969) Outlines of canid and felid brain evolution. Ann NY Acad Sci 167:277–288
Reep RL, Finlay BL, Darlington RB (2007) The limbic system in Mammalian brain evolution. Brain Behav Evol 70:57–70
Salt C, Morris PJ, German AJ, Wilson D, Lund EM, Cole TJ, Butterwick RF (2017) Growth standard charts for monitoring bodyweight in dogs of different sizes. PLoS One 12:e0182064
Schoenemann PT (2004) Brain size scaling and body composition in mammals. Brain Behav Evol 63:47–60
Serpell JA, Duffy DL (2014) Dog breeds and their behavior. In: Horowitz A (ed) Domestic dog cognition and behavior. Springer-Verlag, Berlin, pp 31–57
Shouldice VL, Edwards AM, Serpell JA, Niel L, Robinson JAB (2019) Expression of behavioural traits in goldendoodles and labradoodles. Animals (basel) 9:1162
Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83–98
Striedter G (2005) Principles of Brain Evolution. Sinauer Associates, Sunderland
Striedter G (2007) A history of ideas in evolutionary neuroscience. In: Kaas J (ed) Evolution of nervous systems. Academic Press, Cambridge
Thompkins AM, Ramaiahgari B, Zhao S, Gotoor SSR, Waggoner P, Denney TS, Deshpande G, Katz JS (2018) Separate brain areas for processing human and dog faces as revealed by awake fMRI in dogs (Canis familiaris). Learn Behav 46:561–573
Tonoike A, Nagasawa M, Mogi K, Serpell JA, Ohtsuki H, Kikusui T (2015) Comparison of owner-reported behavioral characteristics among genetically clustered breeds of dog (Canis familiaris). Sci Rep 5:17710
Trut L, Oskina I, Kharlamova A (2009) Animal evolution during domestication: the domesticated fox as a model. BioEssays 31:349–360
van den Berg L, Schilder MB, de Vries H, Leegwater PA, van Oost BA (2006) Phenotyping of aggressive behavior in golden retriever dogs with a questionnaire. Behav Genet 36:882–902
Wilson B, Serpell J, Herzog H, McGreevy P (2018) Prevailing clusters of canine behavioural traits in historical US demand for dog breeds (1926–2005). Animals 8:197 (an open access journal from MDPI 8)
Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 92:381–397
Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009) Bayesian analysis of neuroimaging data in FSL. Neuroimage 45:S173-186
Xu L, Adali T, Schretlen D, Pearlson G, Calhoun VD (2012) Structural angle and power images reveal interrelated gray and white matter abnormalities in schizophrenia. Neurol Res Int 2012:735249
Yopak KE, Lisney TJ, Darlington RB, Collin SP, Montgomery JC, Finlay BL (2010) A conserved pattern of brain scaling from sharks to primates. Proc Natl Acad Sci USA 107:12946–12951
Zapata I, Serpell JA, Alvarez CE (2016) Genetic mapping of canine fear and aggression. BMC Genomics 17:572
Zapata I, Hecht EE, Serpell JA, Alvarez CE (submitted-a) (2021) Genome scans of dog behavior implicate a gene network underlying psychopathology in mammals, including humans. bioRxiv [Preprint]. https://doi.org/10.1101/2020.07.19.211078v2
Zapata I, Lilly ML, Herron ME, Serpell JA, Alvarez CE (submitted-b) (2020) Genetic testing of dogs predicts problem behaviors in clinical and nonclinical samples. bioRxiv [Preprint]. https://doi.org/10.1101/2020.08.13.249805
Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imag 20:45–57
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We appreciate the contributions of the veterinary and imaging staff at the UGA Veterinary Teaching Hospital. Funding: NSF-IOS 1457291.
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Hecht, E.E., Zapata, I., Alvarez, C.E. et al. Neurodevelopmental scaling is a major driver of brain–behavior differences in temperament across dog breeds. Brain Struct Funct 226, 2725–2739 (2021). https://doi.org/10.1007/s00429-021-02368-8
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DOI: https://doi.org/10.1007/s00429-021-02368-8