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Genetics of canine behavior: A review

Amanda Rigterink, Katherine Houpt

CITATION

Rigterink A, Houpt K. Genetics of canine behavior: A review. World J Med Genet 2014; 4(3): 46-57

URL

http://www.wjgnet.com/2220-3184/full/v4/i3/46.htm

DOI

http://dx.doi.org/10.5496/wjmg.v4.i3.46

OPEN ACCESS

Articles published by this Open-Access journal are distributed under the terms of the Creative Commons Attribution Non-commercial License, which permits use, distribution, and reproduction in any medium, provided the original work is properly cited, the use is non commercial and is otherwise in compliance with the license.

CORE TIP

This review incorporates the latest findings in the rapidly moving field of canine behavioral genetics. The genes involved in tameness of foxes and in domestication of dogs from wolves are discussed. The genes involved in several obsessive compulsive behaviors such as flank sucking and circling are mentioned. The genetic and physiological differences between aggressive and non-aggressive dogs of various breeds are emphasized.

KEY WORDS

Dog; Wolf; Fox; Canine aggression; Dopamine; Serotonin; Canid

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© 2014 Baishideng Publishing Group Inc. All rights reserved.

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NAME OF JOURNAL

World Journal of Medical Genetics

ISSN

2220-3184 ( online)

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Published by Baishideng Publishing Group Inc, 8226 Regency Drive, Pleasanton, CA 94588, USA

WEBSITE

http://www.wjgnet.com



ESPS Manuscript NO: 8375

Columns: REVIEW
Genetics of canine behavior: A review
Amanda Rigterink, Katherine Houpt
Amanda Rigterink, Indiana Veterinary Behavior Services, LLC, West Lafayette, IN 47906, United States

Katherine Houpt, College of Veterinary Medicine, Department of Clinical Sciences Cornell University, CVM Cornell University, Ithaca, NY 14853-6401, United States

Author contributions: Rigterink A reviewed domestication and breed differences in behavior; Houpt K reviewed aggression and other behavior abnormalities.

Correspondence to: Katherine Houpt, Professor, College of Veterinary Medicine, Department of Clinical Sciences Cornell University, CVM Cornell University, 3065 E Dixon Lake Road, Ithaca, NY 14853-6401, United States. kah3@cornell.edu

Telephone: +1-989-4488083 Fax: +1-989-4488083

Received: December 26, 2013 Revised: May 20, 2014 Accepted: June 10, 2014

Published online: August 27, 2014
Abstract

The past decade has seen rapid progress in the field of canid behavioral genetics. The recent advances are summarized in this review. The identification of the genes responsible for tameness in silver foxes is the culmination of a half century of behavioral testing and, more recently, genomic investigation. There is agreement that domestic dogs evolved from wolves, but when and from which population remains controversial. The genetic differences between wolves and dogs identified include those for neurotransmitters and digestion. Breed differences in behavior are well known, but only recently have the genetics underlying these differences been investigated. The genes responsible for flank sucking in Doberman Pinschers and for several other obsessive compulsive problems in other breeds have been identified. Aggression is the least desirable canine trait, and several laboratories have detected differences in neurotransmitters and their receptors between aggressive and non-aggressive dogs. In English Cocker Spaniels, the genes linked to aggressive behavior code for dopamine, serotonin, and glutamate receptors. A dopamine transporter gene has been associated with impulsive behavior in Malinois.
© 2014 Baishideng Publishing Group Inc. All rights reserved.
Key words: Dog; Wolf; Fox; Canine aggression; Dopamine; Serotonin; Canid
Core tip: This review incorporates the latest findings in the rapidly moving field of canine behavioral genetics. The genes involved in tameness of foxes and in domestication of dogs from wolves are discussed. The genes involved in several obsessive compulsive behaviors such as flank sucking and circling are mentioned. The genetic and physiological differences between aggressive and non-aggressive dogs of various breeds are emphasized.
Rigterink A, Houpt K. Genetics of canine behavior: A review. World J Med Genet 2014; 4(3): 46-57 Available from: URL: http://www.wjgnet.com/2220-3184/full/v4/i3/46.htm DOI: http://dx.doi.org/10.5496/wjmg.v4.i3.46
INTRODUCTION

This review is a summary of recent research focusing on the current knowledge of the genetic contribution to behavior in the Canidae family. We first review the farm fox experiment and how this long-term study has led to greater understanding of the process of canine domestication at the phenotypic and molecular levels. We then turn our attention to the relationship between dogs and wolves and canine breed differences in behavior. Finally, we review the current knowledge of the genetic basis of aggressive behavior in dogs.
TAME FOX EXPERIMENT

The farm-fox experiment constitutes a major milestone in canid behavioral genetics, clearly demonstrating the genetic basis of behavior. No discussion of the genetics of canine behavior would be complete without summarizing some of the groundbreaking research performed at the Institute of Cytology and Genetics (ICG) of the Russian Academy of Sciences[1-3]. For more than 50 years, scientists at the ICG in Novosibirsk, Russia have been reconstructing experimentally the domestication process in farm-bred silver foxes (a variant form of the red fox, Vulpes vulpes) as a novel model for studying the genetic basis of canine domestication and behavior. In 1959, scientist Dmitry Belyaev and his team began an intensive selective breeding program of silver farm foxes to isolate the trait of tame behavior towards humans[2,4]. After several generations of selective breeding in a controlled environment, Belyaev succeeded in attaining a subset of tame foxes. During fifty years of continuous selective breeding, the farm-fox experiment has tested over 52000 foxes for tameness, with the resultant tame population of foxes showing friendly dog-like responses to humans as early as one month of age[2,3,5].

The goal of selective breeding of the farm foxes was limited strictly to behavioral criteria related to tameness. However, physical, developmental, physiological, and other behavioral differences also emerged in the tame foxes compared to the original farm-bred foxes. The selection for tameness led to numerous physical changes in the foxes, including piebald coats, floppy ears, and curly tails, despite no selection criteria for these traits[2]. In addition, the socialization period elongated from approximately 45 to 60 d in the selected tame foxes, similar to the socialization period in the domestic dog[1]. Tame foxes also developed a novel repertoire of affiliative vocalizations towards humans to promote interaction[6]. Hare et al[7] found that tame fox kits are as skillful as puppies in using human point and gaze gestures for finding hidden food, demonstrating that domestication has led to improved social cognitive ability. Physiological differences also were found with hormonal assays showing that tame foxes do not experience stress when in contact with humans. A comparative study of hypothalamic-pituitary-adrenal axis (HPA) function in tame vs unselected foxes showed that in tame foxes, basal and stress-induced blood cortisol levels were respectively three- and five-fold lower than in the unselected foxes[2,8].

In the 1970s, a second parallel strain of farm foxes began to be bred selectively at the Institute for Cytology and Genetics-those with aggressive behaviors towards humans. Fifty farm-bred silver foxes with the most aggressive responses towards humans were selected and used as the basis of the aggressive population[9]. Criteria for measuring behavior in the aggressive population were the critical distances between the experimenter and the caged animals at which the animals first demonstrated aggression and the intensity of the aggressive responses[10].

From the evolution of these tame and aggressive populations of foxes, much information has been learned about the changes that can occur with intensive behavior selection pressures. Because the fox-farm domesticated foxes were created in only a few decades through intense selection and by focusing exclusively on certain behavioral traits, it seemed reasonable to assume that a small number of genetic loci determined the behavioral traits[11]. A rudimentary map of the fox genome with karyotype and some linkage groups was available by the late 1990s; however, a meiotic linkage map of the fox was needed to determine which loci were implicated in tame behavior[9]. Fortunately, the fox and the dog share a close evolutionary and genetic relationship, and since the dog genome was sequenced by 2005[12], available canine genomic information then could be utilized to develop the necessary fox meiotic map[3,11]. The availability of high resolution canine genome maps and sequence data aided in the creation of the fox meiotic linkage map, with the high genomic sequence identity between dog and fox permitting the adaptation of canine microsatellites for genotyping and meiotic mapping in foxes. Using 320 such markers, Kukekova et al[3] constructed the first meiotic linkage map of the fox genome. This first mapping covers 16 fox autosomes and the X chromosome. After alignment with a canine genome sequence of similar length, high conservation of marker order between homologous regions of the two species was apparent[11]. Utilizing and adapting scoring systems (for tameness and aggression phenotypes) developed by the fox-farm experiment over the years for the selective breeding process, Kukekova et al[3] created a new principal-component analysis of fox behavior with selected traits. This new scoring system effectively reduced 311 binary scoring behaviors to fifty of the most important traits that would serve as quantitative phenotypes (and continuous variables) to represent heritable differences in behavior among individual foxes and the fox populations and permit quantitative genetic analysis[10]. By interval mapping using fox and canine meiotic maps, a locus for tame behavior on fox chromosome VVU12 was identified. This locus is orthologous to a genomic region implicated in canine domestication[13]. Tameness as the defining trait of domestication is a complex “phenotype” consisting of many behavioral variables. In fact, when genome-wide association studies were performed by Kukekova et al[3], the resulting data suggested that at least two VVU12 loci are associated with tame vs aggressive behavior and active vs passive behavior. Moreover, differing mapping characteristics of specific behavioral traits were found, suggesting different genotype/phenotype relationships; for example, floppy vs erect ears are associated with different regions of VVU12 and vary between tame and aggressive foxes. Expression of the VVU12 loci thus appears to depend on interaction with other parts of the genome and on individual fox parents[13].

At the molecular level, the development of transcriptome sequencing significantly enhances genetic study without the need for a fully sequenced genome. The comparison of transcriptome sequencing from the prefrontal cortices of a tame and an aggressive fox is in the preliminary stages at this time[9]. Thus far, preliminary analysis of “comparison of transcriptome sequences of the same genes between the tame and aggressive fox samples has identified a large set of informative single nucleotide polymorphism (SNP) markers and begun a catalogue of gene-specific sequence variants between the two strains”[13].

The farm-fox experiment demonstrates that over generations, intensive selection for tame behavior in foxes can serve as a reliable model for studying the genetic basis of canine domestication. The identification of genetic loci that both influence tame behavior in foxes and are homologous to regions in the dog genome supports the hypothesis that domesticated behavior in dogs and foxes may have similar genetic bases. These recent advances will help identify more genes implicated in fox behavior that can be correlated to dog domestication.
WOLVES TO DOGS

The complete sequencing of the dog genome has greatly expanded general knowledge of the processes of genome evolution and the genetic basis of phenotypic traits in dogs and other animals. However, the evolutionary path leading from wild ancestor to domesticated dog continues to remain elusive. Comparative genomics utilizing the completed dog genome has confirmed the close relationship of dogs to such other canidae as foxes, coyotes, and wolves. It appears that modern canids share a common ancestor dating back approximately ten million years; the closest relatives to the dog such as the gray wolf and coyote share a common ancestor dating to approximately three to four million years ago[14]. Like the dog, all wolf-like canids have 78 chromosomes and can mate with one another to produce fertile offspring. Thus, wolf-like canid species are among the strongest candidates for the ancestors of today’s dog. Moreover, molecular genetic data from the past two decades[12,15,16] strongly support the origin of the dog from the gray wolf in particular[17]. Molecular evidence also suggests that divergence of dog from wolf and the beginning of the dog’s relationship with humans occurred as recently as 15000 years ago[9,14]. Other studies looking at genomic variation in wolves, Chinese indigenous dogs, and modern breeds point to an even earlier beginning to domestication, possibly about 30000 years ago, prior to the development of an agricultural human society[18,19]. Very early domestication may have involved the intentional taming of small groups of wolves who, less fearful of humans and motivated by hunger, scavenged the camps of Mesolithic human hunters-gatherers[20].

Where canine domestication originated also is debatable. While DNA genomic data suggest a Middle Eastern origin, analyses of mitochondrial DNA and Y-chromosome markers from various dog breeds and from geographically-dispersed wolf populations suggest that canine domestication originated in East Asia[9]. Wang et al[18] used whole-genome sequencing to compare gray wolves, Chinese indigenous dogs, and modern breeds. They found that the genetic variation between the three canid groups generally decreased step-wise from wolf to Chinese dog to modern dog breed. Based on these findings, they speculate that the Chinese indigenous dog may represent the link between wolf and dog and the progenitor of today’s diverse modern dog breeds. They identified 311 genes that appear to have been selected in dogs compared to wolves and that have functions affecting sexual reproduction, digestion/metabolism, neurological processes, and cancer. The fact that these particular genes overlap to a great extent with those also selected in humans suggests a parallel evolutionary process in dogs and humans, especially in the realm of neurological processes. They note that: As domestication is often associated with large increases in population density and crowded living conditions, these “unfavourable” environments might be the selective pressure that drove the rewiring of both species. Positive selection in neurological pathways, in particular the serotonin system, could be associated with constant need for reduced aggression stemming from the crowded living environment[18].

Another study employed mitochondrial DNA sequencing, showing a closer relationship of dogs to gray wolves from East Asia[21]. VonHoldt et al[22] sought to identify the primary source of genetic diversity for domestic dogs and conducted an extensive genome-wide survey of over 48000 SNPs in dogs and gray wolves. Their data, however, showed that dogs share a greater percentage of multi-locus haplotypes unique to gray wolves from the Middle East rather than from East Asia[22].

Although genetic data support the theory that the process of canine domestication began in East Asia over 15000 years ago, a recent study compared the complete mitochondrial genome sequences of 18 European prehistoric canids to a comprehensive panel of modern dogs and wolves. The researchers found phylogenic relatedness between the modern dogs and the ancient canids of Europe dating back to more than 30000 years ago, thus suggesting that canine domestication first may have occurred in Europe rather than in Asia[23].

Behavior differences between dogs and wolves are the most striking result of the domestication process, even more than the marked differences in physical size and shape. In fact, the canine breeds in existence today have diverse physical characteristics that distinguish them from one another just as much as from wolves. However, the fact that all breeds of domestic dog as a group are more similar in behavior when compared to one another than when compared to the wolf suggests that genetic selection for behavior drove the domestication process. It is logical to hypothesize that ancestral wolves initially may have experienced natural selection for tame behavior, permitting coexistence with humans. Based on the findings of the fox-farm experiment where genetic loci influencing tame behavior in foxes are homologous to regions in the dog genome and also related to selection differences between dogs and wolves, it is plausible to suggest that domesticated behavior in dogs and foxes share a similar genomic basis[9].

Several studies before and after the complete sequencing of the dog genome in 2005 have attempted to target, at the molecular level, the genetic basis of behavioral differences between the domestic dog and its wolf progenitor. A study by Saetre et al[24] used microarray technology to evaluate mRNA expression levels of 7762 genes in the post-mortem brains of dogs, wolves, and coyotes. They found markedly altered gene expression of two neuropeptides, CALCB and NPY, in the dogs as compared to the wolves and coyotes. These neuropeptides, present in all mammalian brains, are implicated in energy control and feeding behavior, neuroendocrine stress response via the HPA axis, and possibly play a role in anxiety and depression. The findings of species-specific differences in the elaboration of the neuropeptides suggest that selection for behavior during domestication may have resulted in modification of mRNA expression patterns in genes located in the hypothalamus of the dog[24]. Björnerfeldt et al[25] postulate that domestication of dogs created a new lifestyle that changed selective forces acting on the species, in turn affecting the dog’s genome. Using mitochondrial DNA sequencing in 14 dogs, 6 wolves, and 3 coyotes, they showed that dogs have accumulated into their genome non-synonymous changes in mitochondrial genes at rates faster than in wolves. In turn, this results in elevated levels of protein variations in the dog as compared to the wolf. Björnerfeldt et al[25] conclude that an important consequence of domestication is a “relaxation of selective constraint on dog mitochondrial DNA” that also could have affected other parts of the dog genome to facilitate “the generation of novel functional genetic diversity”[25]. Cruz et al[26] compared the genome of the dog to that of the gray wolf to examine the effect of domestication. Using whole-genome SNP data, they compared the variation in dog and wolf genes. They also found increased frequency in the trend for non-synonymous mutations in dogs as compared to their wild canid counterparts. They concluded that the increase in mutation rate could have myriad effects, some deleterious, and may indicate that the process of domestication in the dog led to an increase in functional genetic variation that has contributed to the markedly diverse physical and behavioral phenotypes characteristic of dog breeds, as well as to the prevalence of pathology in modern breeds[26].

Li et al[27] studied the expression profiles of a specific subset of developmental genes believed to be implicated the evolution of dog domestication. They ran comparative genomic analyses by assaying the SNP genotypes in Chinese native dogs (believed to have the genetic structure most similar to that of ancient dog), German Shepherd (purebred) dogs, and gray wolves to detect a genetic basis for the behavior transformation from wolf to primitive dog to modern purebred dog[27]. Genomic regions that have undergone strong selection in the recent past should show extended haplotype homozygosity[28]. Following this line of reasoning, Li et al[27] detected four regions of high extended haplotype homozygosity that contained only a single highly differentiated SNP located within a single gene. Comparison of candidate genes between the Chinese native dogs and wolves showed a high bias for expression localized in the brain’s prefrontal cortex, the center for complex cognitive-type behaviors. However, candidate genes showing large population differentiation between the Chinese dogs and German Shepherds did not demonstrate significant expression bias. Thus, the finding that wolves and dogs have highly differentiated brain-based genes suggests that behavioral transformation most likely was key to the onset of domestication and that “this rapid evolution likely was driven by artificial selection during the primary transition from wolves to ancient dogs, and was consistent with the evolution of dog-specific characteristics, such as behavior transformation, for thousands of years”[27,28].

Other recent studies have taken a closer look at the genetic processes underlying physiological and behavior differences resulting from dog domestication. Utilizing whole-genome resequencing of wolves and dogs, Axelsson et al[29] identified 36 genomic regions that likely are implicated in selection during the domestication of the dog. It is of interest that more than half of the regions play roles in brain function with 8 regions in particular involved in neurophysiologic pathways that may underlie behavioral changes characteristic of dog domestication. Moreover, they identified 10 genes with selection signals that play key roles in starch digestion and fat metabolism. In terms of starch digestion, three genes (AMY2B, MGAM, and SGLT1) that facilitate the digestion of starches show evidence of being selected for during the process of dog domestication. These findings may indicate that, unlike in carnivorous wolves, genetic mutations found in modern dog facilitate the adaptation to and even thriving on a diet available in cohabitation with humans[29].
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