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Significant Neuroanatomical Variation Among Domestic Dog Breeds - PubMed

  • ️Tue Jan 01 2019

Comparative Study

Significant Neuroanatomical Variation Among Domestic Dog Breeds

Erin E Hecht et al. J Neurosci. 2019.

Abstract

Humans have bred different lineages of domestic dogs for different tasks such as hunting, herding, guarding, or companionship. These behavioral differences must be the result of underlying neural differences, but surprisingly, this topic has gone largely unexplored. The current study examined whether and how selective breeding by humans has altered the gross organization of the brain in dogs. We assessed regional volumetric variation in MRI studies of 62 male and female dogs of 33 breeds. Neuroanatomical variation is plainly visible across breeds. This variation is distributed nonrandomly across the brain. A whole-brain, data-driven independent components analysis established that specific regional subnetworks covary significantly with each other. Variation in these networks is not simply the result of variation in total brain size, total body size, or skull shape. Furthermore, the anatomy of these networks correlates significantly with different behavioral specialization(s) such as sight hunting, scent hunting, guarding, and companionship. Importantly, a phylogenetic analysis revealed that most change has occurred in the terminal branches of the dog phylogenetic tree, indicating strong, recent selection in individual breeds. Together, these results establish that brain anatomy varies significantly in dogs, likely due to human-applied selection for behavior.SIGNIFICANCE STATEMENT Dog breeds are known to vary in cognition, temperament, and behavior, but the neural origins of this variation are unknown. In an MRI-based analysis, we found that brain anatomy covaries significantly with behavioral specializations such as sight hunting, scent hunting, guarding, and companionship. Neuroanatomical variation is not simply driven by brain size, body size, or skull shape, and is focused in specific networks of regions. Nearly all of the identified variation occurs in the terminal branches of the dog phylogenetic tree, indicating strong, recent selection in individual breeds. These results indicate that through selective breeding, humans have significantly altered the brains of different lineages of domestic dogs in different ways.

Keywords: MRI; canines; dogs; evolution; morphology; selective breeding.

Copyright © 2019 the authors.

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Figures

Figure 1.
Figure 1.

Neuroanatomical variation in domestic dogs. A, MRI images and 3D reconstructions of warped template from 10 selected dogs of different breeds. Images are public-domain photos from Wikimedia Commons. B, Unbiased group-average template for this dataset. See Figure 1-1, and Figure 1-2 for processing schematics. Neuroanatomical labels (based on Palazzi, 2011; Datta et al., 2012, Evans and de Lahunta, 2013) are as follows: (a) olfactory peduncle; (b) orbital (presylvian) gyrus; (c) proreal gyrus; (d) pre cruciate gyrus; (e) postcruciate gyrus; (f) marginal (lateral) gyrus; (g) ectomarginal gyrus; (h) suprasylvian gyrus; (i) ectosylvian gyrus; (j) sylvian gyrus; (k) insular cortex; and (l) piriform lobe. C, Brain-wide morphological variation, regardless of breed, as indexed by the SD of all dogs' Jacobian determinant images. D, A Monte Carlo permutation test on demeaned gray matter Jacobian determinant images revealed that much of gray matter shows significant deviation from group-mean morphology. Colored regions are all p < 0.05 after multiple-comparisons correction; t-statistic values are illustrated.

Figure 2.
Figure 2.

pGLS analyses on gross brain, body, and skull measurements. A, Brain volume versus body mass. B, Neurocephalic index vesus cephalic index. Plotted points represent breed averages, not individuals.

Figure 3.
Figure 3.

Covarying regional networks in dog brain morphology. Independent components analysis revealed six regional networks where morphology covaried significantly across individuals. Red and blue regions are volumetrically anticorrelated: in individuals where red is larger, blue tends to be smaller, and vice versa. Graphs represent volumetric quantification of the top five anatomical constituents of each of the two portions of each component.

Figure 4.
Figure 4.

Relationship between morphologically covarying regional brain networks and phylogenetic tree. Circles indicate factor loading. (Phylogenetic tree is from Parker et al., 2017.)

Figure 5.
Figure 5.

Relationship between morphologically covarying regional brain networks and ostensible behavioral specializations. Colors indicate partial correlation coefficients resulting from multiple regression analysis on source-based morphometry results. Outlined boxes are significant at p < 0.05.

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