A.V. Kharlamova’s research while affiliated with Institute of Cytology and Genetics, Russian Academy of Sciences and other places

In foxes selectively bred by ICG SB RAS for domestication or aggressive behavior toward humans, the behavior was analyzed. We have used the foxes not selected for behavior features as a control. Control foxes also were bred on experimental farm of ICG SB RAS. The peculiarities of explorative activities of foxes toward new objects, introduced inside the domestic cage, as well as behavioral features during attenuation of focused attention on the object of food reinforcement are discussed in the paper. Domesticated foxes demonstrated less neofobia during experiments then aggressive and unselected ones. On the other hand, the explorative behavior of tame foxes was characterized by a greater variability of motor reactions compared to aggressive and unselected ones. In the test for attenuation of focused attention, tame foxes used a greater number of different actions compared to other studied groups. Fox cubs from the domesticated population, placed in a new environment for the first time, found various ways go through obstacles when following a person. Based on these results we discuss the peculiarities of the decision-making in foxes.

The hippocampus plays the key role in stress response regulation, and stress response appears to be weakened in domesticated animals compared to their wild relatives. The hippocampus is functionally heterogeneous along its dorsoventral axis, with its ventral compartment being more closely involved in stress regulation. An earlier series of experiments was conducted with a unique breeding model of animal domestication, the farm silver fox (Vulpes vulpes), which included tame, aggressive, and unselected animals. A decrease in many indices of the hypothalamic–pituitary–adrenal activity was observed in tame animals. Also, adult hippocampal neurogenesis was more intense in tame foxes, and this fact may relate to reduced stress levels in this experimental population of foxes. Nevertheless, the molecular mechanisms responsible for the reduced stress response in tame animals remain obscure. In this study, serum cortisol levels and the mRNA levels of 13 genes in the dorsal and ventral hippocampus have been measured and compared in tame, aggressive, and unselected foxes. At the current stage of domestication, stress-induced cortisol levels in tame, aggressive, and unselected animals differ significantly from each other: tame foxes show the lowest levels, and aggressive ones, the highest. Twelve genes tested demonstrate significant gene expression differences between the dorsal and ventral hippocampi. These differences are mainly consistent with those found in rodents and humans. In tame foxes, significantly elevated mRNA levels were recorded for several genes: CYP26B1 for cytochrome P450 26B1 and ADRA1A for α 1A adrenergic receptor in the dorsal hippocampus, whereas the level of NR3C2 mRNA for mineralocorticoid receptor was higher in the ventral. It is presumed that these genes constitute an important part of the mechanism reducing stress induced by contacts with humans and contribute to linking stress regulation with adult neurogenesis in tame foxes and domesticated animals in general.

Skull morphology was studied in three populations of red foxes (Vulpes vulpes): tame, which was produced by long-term selection for friendly behavior to humans; aggressive, which was produced by long-term selection for aggressive behavior to humans; and conventional farm-bred, which was not deliberately selected for behavior. We have collected skulls measurements from two sets of foxes: (1) 140 backcross foxes produced by breeding of tame and aggressive foxes to each other and then crossing F1 foxes to tame strain, and (2) 150 foxes from original populations (50 tame, 50 aggressive and 50 conventional farm-bred). The backcross foxes have been genotyped with 350 microsatellite markers and analyzed using 2B-PLS analysis. A significant correlation between microsatellite genotypes and skull shape was identified for three microsatellite markers on 10-th fox chromosome: FH2535, RVC1, REN193M22. The second set of foxes (tame, aggressive and conventional) was genotyped for these three markers and also analysed with 2B_PLS. Significant correlation was identified between genotypes and skull size for males, but not for females. The genomic region identified in this study contains IGF-1 gene, which is responsible for 15% of body size variation in dogs. Our findings suggest that IGF-1 gene is also involved in skull size regulation in red foxes.

Full-text: https://rdcu.be/cpN2R Animal and plant domestication is one of the most remarkable cultural achievements in human evolution. The first animal to have been domesticated was the dog. Although related studies are many, little is known about the earliest times of its domestication. This review emphasizes that there are parallels in behavior change and its molecular genetic basis between domesticated foxes and dogs, with a special focus on the so-called “ancient” breeds. Three approaches to the study of the molecular genetic mechanisms of domestication are described and some of their results obtained with modern methods, including highthroughput sequencing, are given. One involves the experimental modeling of early domestication stages in the fox, a farmed animal; another, a comparative analysis of modern dogs and wolves; and yet another, a paleogenetic analysis of ancient dogs and wolves, with an account of their archaeological context. Phylogenetic and phylogeographical approaches to the study of dog domestication and their role in a comprehensive reconstruction of domestication mechanisms are discussed. Difficulties with timing estimates, the geographic position and the reconstruction of molecular mechanisms for dog domestication are considered in the context of sampling strategies for genomic analysis. Genes encoding the signaling system of glutamate receptors and neural crest cells, with their broad pleiotropic effect, are discussed as being the most important targets of selection in experimental and historical domestication. In conclusion, the need of supplementing the studies of domestication mechanisms with analyses of various developmental stages at the molecular and organismal levels is highlighted.

This paper systematizes and generalizes a research cycle devoted to studying the acoustics and vocal behaviour of silver foxes that differ in their tolerance to humans. The research revealed that 50-year selection for tameness toward people resulted in selective use by Tame foxes toward humans of two call types, pant and cackle. At the same time, the selected for aggression toward people Aggressive foxes and the non-selected for behaviour Control foxes, selectively use toward humans cough and snort. Thus, call types representing vocal indicators of friendly and aggressive behaviour of foxes toward humans have been revealed by the research. Nevertheless, experimental domestication did not change vocal behaviour of foxes toward conspecifics; all three strains did not differ by their vocal behaviour toward same-strain silver foxes. Relationship has been investigated between vocal behaviour and degree of tolerance toward people for hybrids between Tame and Aggressive foxes and for backcrosses to Tame and Aggressive foxes. Effect was estimated between fox sex and the degree of human impact on focal fox for variables of fox vocal behaviour. The research revealed the universal for mammals vocal indicators of emotional arousal that are independent of the emotional valence. Characteristics of vocal behaviour that are related with positive and negative emotional valence have been revealed. A simple and effective method for estimating animal discomfort based on "joint calls" that takes into account the characteristics of all calls irrespective of their acoustic structure has been revealed. The obtained results provide a basis for further comparative studies of the acoustic structure and vocal behaviour for other taxa of the genus Vulpes and the related canid genera (Canis, Cuon, Lycaon).

The results of a 35-year selection of foxes for aggressive response to humans are reported. Averaged estimates of the phenotypic manifestation of aggressiveness in all selection generations are presented. The dynamics of these estimates shows that the phenotypic response to the selection was obvious only in the first 12 generations. Subsequent selection did not alter the mean aggressiveness score. Analysis of variance was performed for the intergroup variability (among descendants of different mothers) and intragroup variability (among the offspring within a family). The intragroup variability was constantly low. Most likely, the trait is stabilized by maternal prenatal and early neonatal factors. The general tendency in the dynamics of intergroup variability is that it does not decrease over time during selection, no matter how long the population has been under it. It follows from the statistical indices of the phenotypic similarity between parents and offspring that additive interactions are insufficient for the explanation of the persisting variability. The contribution of epistatic interactions is not ruled out, though. Emphasis is laid on the correlated consequences of the selection for aggressiveness and their coordination with the consequences of the selection in the opposite direction, for elimination of aggressive response to humans, or for tameness. The parallelism of correlated changes in the selection in contrasting directions is illustrated by the examples of some physiological and morphological traits. The phenomenon is discussed in the light of classical notions of the resource of cryptic genetic variation and the role of selection in its phenotypic manifestation. Its interpretation also invokes molecular data pointing that some genetic pathways may regulate parameters of both aggression and tameness and that the selection processes in both directions may have some genetic targets in common.

Foxes long time selected for tame and aggressive behavior were compared on ability to focus attention on the object of food reinforcement. Attenuation of this behavior and rate of training for motor skills also has been examined. Maximal duration of eye focusing was significantly higher in aggressive foxes, in comparison with tame ones. Our experiments allowed divide the group of tame foxes into two subgroups "calm" and "emotional", on the base of emotionality and motor activity during tests. Features of behavior of these two subgroups steadily differed in all tests. "Calm" tame foxes at the extinction test continued the trained skill longer than "emotional" and aggressive ones. Tame foxes were more successful than aggressive in the training for motor skills. The possible reasons of the data obtained are discussed.

The red fox (Vulpes vulpes) demonstrates a variety of coat colors including platinum, a common phenotype maintained in farm-bred fox populations. Foxes heterozygous for the platinum allele have a light silver coat and extensive white spotting, whereas homozygosity is embryonic lethal. Two KIT transcripts were identified in skin cDNA from platinum foxes. The long transcript was identical to the KIT transcript of silver foxes, whereas the short transcript, which lacks exon 17, was specific to platinum. The KIT gene has several copies in the fox genome: an autosomal copy on chromosome 2 and additional copies on the B chromosomes. To identify the platinum-specific KIT sequence, the genomes of one platinum and one silver fox were sequenced. A single nucleotide polymorphism (SNP) was identified at the first nucleotide of KIT intron 17 in the platinum fox. In platinum foxes, the A allele of the SNP disrupts the donor splice site and causes exon 17, which is part of a segment that encodes a conserved tyrosine kinase domain, to be skipped. Complete cosegregation of the A allele with the platinum phenotype was confirmed by linkage mapping (LOD 25.59). All genotyped farm-bred platinum foxes from Russia and the US were heterozygous for the SNP (A/G), whereas foxes with different coat colors were homozygous for the G allele. Identification of the platinum mutation suggests that other fox white-spotting phenotypes, which are allelic to platinum, would also be caused by mutations in the KIT gene. © 2015 Stichting International Foundation for Animal Genetics.