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Significant Neuroanatomical Variation Among Domestic Dog Breeds

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Significant Neuroanatomical Variation Among Domestic Dog Breeds Research Articles: Behavioral/Cognitive Significant neuroanatomical variation among domestic dog breeds https://doi.org/10.1523/JNEUROSCI.0303-19.2019 Cite as: J. Neurosci 2019; 10.1523/JNEUROSCI.0303-19.2019 Received: 25 February 2019 Revised: 8 August 2019 Accepted: 13 August 2019 This Early Release article has been peer-reviewed and accepted, but has not been through the composition and copyediting processes. The final version may differ slightly in style or formatting and will contain links to any extended data. Alerts: Sign up at www.jneurosci.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Copyright © 2019 the authors 1 Significant neuroanatomical variation among domestic dog breeds 2 Abbreviated title: Neuroanatomical variation in dogs 3 Authors: Erin E. Hecht, Ph.D. 1*, Jeroen B. Smaers, Ph.D.2, William J. Dunn3, Marc Kent, DVM, DACVIM4, 4 Todd M. Preuss, Ph.D.5,6, David A. Gutman, M.D., Ph.D.7 5 Affiliations: 6 1Department of Human Evolutionary Biology, Harvard University, 02138 7 2Department of Anthropology, Stony Brook University, 11794 8 3Department of Psychology and Neuroscience Program, Michigan State University, 48824 9 4Department of Small Animal Medicine and Surgery, The University of Georgia at Athens, 30602 10 5Division of Neuropharmacology and Neurologic Diseases & Center for Translational Social 11 Neuroscience, Yerkes National Primate Research Institute, Emory University, 30329 12 6Department of Pathology and Laboratory Medicine, School of Medicine, Emory University, 30329 13 7Department of Neurology, School of Medicine, Emory University, 30329 14 *Correspondence to: [email protected] 15 16 Pages: 26 17 Figures: 5 18 Tables: 1 19 Multimedia: 0 20 3D models: 0 21 22 Abstract: 193 words 23 Introduction: 590 words 24 Discussion: 1494 words 25 26 Acknowledgments: We appreciate the contributions of the veterinary and imaging staff at the UGA 27 Veterinary Teaching Hospital. Funding: NSF-IOS 1457291. Author contributions: conceptualization: EEH; 28 formal analysis: EEH, JBS, WJD, DAG; investigation and resources: MK; data curation: EEH, DAG; writing – 29 original draft: EEH, JBS, DAG; writing – review & editing: all authors; visualization: EEH, JBS; supervision: 30 TMP, DAG; funding acquisition: EEH, MK, TMP, DAG. 31 Conflict of interest statement: Authors declare no competing financial interests. 32 1 33 Abstract: 34 Humans have bred different lineages of domestic dogs for different tasks, like hunting, herding, 35 guarding, or companionship. These behavioral differences must be the result of underlying neural 36 differences, but surprisingly, this topic has gone largely unexplored. The current study examined 37 whether and how selective breeding by humans has altered the gross organization of the brain in dogs. 38 We assessed regional volumetric variation in MRI studies of 62 male and female dogs of 33 breeds. 39 Notably, neuroanatomical variation is plainly visible across breeds. This variation is distributed non- 40 randomly across the brain. A whole-brain, data-driven independent components analysis established 41 that specific regional sub-networks covary significantly with each other. Variation in these networks is 42 not simply the result of variation in total brain size, total body size, or skull shape. Furthermore, the 43 anatomy of these networks correlates significantly with different behavioral specialization(s) such as 44 sight hunting, scent hunting, guarding, and companionship. Importantly, a phylogenetic analysis 45 revealed that most change has occurred in the terminal branches of the dog phylogenetic tree, 46 indicating strong, recent selection in individual breeds. Together, these results establish that brain 47 anatomy varies significantly in dogs, likely due to human-applied selection for behavior. 48 49 Significance statement: 50 Dog breeds are known to vary in cognition, temperament, and behavior, but the neural origins of this 51 variation are unknown. In an MRI-based analysis, we found that brain anatomy covaries significantly 52 with behavioral specializations like sight hunting, scent hunting, guarding, and companionship. 53 Neuroanatomical variation is not simply driven by brain size, body size, or skull shape, and is focused in 54 specific networks of regions. Nearly all of the identified variation occurs in the terminal branches of the 55 dog phylogenetic tree, indicating strong, recent selection in individual breeds. These results indicate 56 that through selective breeding, humans have significantly altered the brains of different lineages of 57 domestic dogs in different ways. 58 59 2 60 Introduction 61 A major goal of modern neuroscience is to understand how variation in behavior, cognition, and 62 emotion relates to underlying neural mechanisms. A massive “natural experiment” in this arena has 63 been right under our noses: domestic dogs. Humans have selectively bred dogs for different, specialized 64 abilities – herding or protecting livestock; hunting by sight or smell; guarding property or providing 65 companionship. Significant breed differences in temperament, trainability, and social behavior are 66 readily appreciable by the casual observer, and have also been documented quantitatively (e.g., (Serpell 67 and Hsu 2005, Tonoike, Nagasawa et al. 2015)). Furthermore, recent genetic research indicates that this 68 behavioral variation is highly heritable (MacLean, Snyder-Mackler et al. 2019). 69 This panoply of behavioral specializations must rely on underlying neural specializations. A small 70 number of studies have investigated neural variation in dogs, including, for example, the effects of skull 71 shape on brain morphology (e.g., (Carreira and Ferreira 2015, Pilegaard, Berendt et al. 2017) and 72 anatomical correlates of aggression (e.g., (Jacobs, Van Den Broeck et al. 2007, Vage, Bonsdorff et al. 73 2010)). However, the neural underpinnings of behavioral differences between breeds remain largely 74 unknown. 75 Most modern dog breeds were developed in an intentional, goal-driven manner relatively recently in 76 evolutionary time; estimates for the origins of the various modern breeds vary between the past few 77 thousand to the past few hundred years (Larson, Karlsson et al. 2012). This strong selection pressure 78 suggests that brain differences between breeds may be closely tied to behavior. However, selection 79 also occurred for outward physical appearance, including craniofacial morphology. This may have 80 placed constraints on the internal dimensions of the skull, which in turn may have had secondary effects 81 on brain morphology. There is substantial diversification of skull shape across dog breeds, and this has 82 been linked to behavioral differences (Drake and Klingenberg 2010, McGreevy, Georgevsky et al. 2013). 83 Alternatively, neuroanatomical variation may be explained primarily by body size rather than breed 84 membership, with different breeds’ brains representing minor, random, scaled-up or scaled-down 85 variants of a basic species-wide pattern. 86 Any attempt to determine whether breeding for behavior has altered dog brains would have to be able 87 to differentiate between these competing (and potentially interacting) hypotheses. A simple 88 comparison of regional volumes would be insufficient for several reasons. First, a significant difference 89 in the volume of, for example, the amygdala in pit bulls versus golden retrievers might seem intuitively 90 meaningful, but in order to ascertain whether such a difference was truly the result of selection pressure 91 on behavior, the phylogenetic structure of the dog family tree needs to be taken in to account in order 92 to partition variance attributable to inheritance, and equal statistical priority needs to be given to the 93 alternative hypotheses that observed variation in morphology. Second, and perhaps most importantly, 94 a priori comparisons of regional gray matter volumes presuppose that experimenters can identify 95 meaningful borders between regions. For highly conserved structures with clear anatomical boundaries, 96 like the amygdala, this task is surmountable – but very little is known about the organization of higher- 97 order cortical regions in dogs, and some complex behaviors that are the focus of selective breeding, like 3 98 herding or interspecies communication, almost certainly rely on some of these areas. For this reason, 99 even creating the regional outlines for a simple ROI analysis would be problematic. 100 Therefore, the current study took a totally data-driven, whole-brain, agnostic approach to assessing 101 morphological variation across dog brains. Our goal was to (a) determine whether significant non- 102 random variation in brain anatomy exists across dogs, and if so, (b) differentiate between the competing 103 and possibly interacting explanations for this variation. 104 105 Materials and Methods 106 107 Subjects 108 The dataset included T2-weighted MRI scans from 62 purebred dogs of 33 different breeds. These were 109 grouped into 10 different breed groups as defined by American Kennel Club, which ostensibly represent 110 groupings that were developed for similar behavioral specializations, such as herding or hunting. Table 111 1 lists the breed, breed group, and other data for all dogs included in the study. 112 Cephalic Body index Neuro- Brain Age mass (from cephalic volume Ostensible behavioral specialization ID Breed Sex (years) (kg) database) index (mm3) / purpose 1 Basset Male 4.0 28.1
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