Fox Domestication Research Articles

The Fox Domestication Experiment and Dog Evolution: A View Based on Modern Molecular, Genetic, and Archaeological Data

The Fox Domestication Experiment and Dog Evolution: A View Based on Modern Molecular, Genetic, and Archaeological Data

The Silver Fox Domestication Experiment

For the last sixty years, a team of Russian geneticists have been running one of the most important biology experiments of the 20th, and now 21st, century. Each year they have selected the calmest foxes—foxes that are most prosocial to humans—to mimic the early stages of domestication. After providing an overview of how the silver fox domestication study began, I will discuss: 1) work on social cognition in the domesticated silver foxes, 2) work on the molecular genetics of domestication in the silver foxes, including work on changes in allele frequencies and changes in gene expression patterns, 3) a new hypothesis for how selection on tameness leads to the domestication syndrome via changes in the number and migration patterns of neural crest cells very early on in development, and 4) how the silver fox domestication experiment has led to new hypotheses about self-domestication in primates, including humans.

The Effect of Behavioral Selection on the Dentition of Russian Silver Foxes and its Implications for Human Dental Evolution

Animal domestication models have long emphasized that the behavioral transition from ‘wild’ (aggressive) to ‘domestic’ (tame) facilitates the emergence of some un‐selected phenotypic traits like floppy ears, curly tails, and, importantly, dental size reduction. A similar pattern of dental size diminution exists in human evolution. Reduced canine crown dimensions in humans are linked with greater male cooperative behavior compared to primates that exhibit high inter‐male aggression. Moreover, arguments for behavioral evolution toward reduced aggression among humans and bonobos are based, in part, on empirical patterns of dental size reduction from ancestral forms. The Russian fox domestication experiment provides an untapped source for studying this evolutionary dynamic because it provides a controlled, long term study of selection for non‐aggressive behavior and attendant morphological consequences. The objective of this study is to measure dental size variation among these experimental foxes. We employed univariate and multivariate comparisons of maxillary premolar (P4), molar (M1), and canine mesiodistal length, buccolingual breadth, and crown height of the canine, as well as mandibular molar (M1) mesiodistal length and buccolingual breadth. These data were collected in sex‐balanced samples of unselected (n=50), tame (n=49), and aggressive (n=50) experimental strains. Consistent with expectations, tame fox skulls exhibited statistically significantly reduced tooth dimensions in virtually all comparisons relative to both unselected and aggressive strain individuals. This result was most pronounced for the canine tooth measurements. These results in domesticated foxes parallel trends in dental size reduction in humans and bonobos, suggesting that behavioral evolution may play an important role in dental size across mammalian species. Accordingly, these results appear to further support the hypothesis that behavioral evolution influences dental size and highlight the utility of dental evidence as a morphological indicator of reduced aggression.Support or Funding InformationUniversity of Iowa College of Dentistry; University of Missouri; University of North Texas Health Science CenterThis abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours

Strains of red fox (Vulpes vulpes) with markedly different behavioural phenotypes have been developed in the famous long-term selective breeding programme known as the Russian farm-fox experiment. Here we sequenced and assembled the red fox genome and re-sequenced a subset of foxes from the tame, aggressive and conventional farm-bred populations to identify genomic regions associated with the response to selection for behaviour. Analysis of the re-sequenced genomes identified 103 regions with either significantly decreased heterozygosity in one of the three populations or increased divergence between the populations. A strong positional candidate gene for tame behaviour was highlighted: SorCS1, which encodes the main trafficking protein for AMPA glutamate receptors and neurexins and suggests a role for synaptic plasticity in fox domestication. Other regions identified as likely to have been under selection in foxes include genes implicated in human neurological disorders, mouse behaviour and dog domestication. The fox represents a powerful model for the genetic analysis of affiliative and aggressive behaviours that can benefit genetic studies of behaviour in dogs and other mammals, including humans.

Expression of the DNA methyltransferase genes in silver foxes experimentally selected for domestication

Animal domestication is a model of a rapid evolutionary process. In experimental fox domestication, the time required for the emergence and fixation of specific evolutionary changes was reduced from thousands to tens of years, compared to historical domestication. Tame foxes were obtained by extreme selective breeding for emotionally positive response toward humans. Unselected foxes, as well as foxes bred for enhanced aggressiveness to humans were used as control. Epigenetic regulation of gene expression is considered as one of the possible mechanisms of rapid evolution. In this study, expression of DNA methyltransferase genes, DNMT1 and DNMT3A, was investigated. It was demonstrated that, in tame foxes, the level of DNMT3A gene expression in the prefrontal cortex, hippocampus, and spleen was increased by more than 2 times in comparison with aggressive and unselected foxes. At the same time, the DNMT1 expression level did not differ among the studied groups of animals. A possible reason for the differences found in the DNMT3A expression could be the changes in the level and metabolism of methionine, which serves as a donor of methyl groups during DNA methylation. However, this study showed that there were no differences in the serum methionine levels between tame, unselected, and aggressive foxes. Thus, the data support the hypothesis that selection for positive emotional response toward humans affected the DNA methylation machinery.

Fox domestication: Molecular mechanisms involved in selection for behavior

Although animal domestication has enjoyed the attention of geneticists and evolutionary biologists since Darwin’s times, the focal question about the genetic basis of this process has not been duly considered. We present some results of experimental modeling of historical domestication in silver foxes (Vulpes vulpes), an object of commercial breeding. Attention is focused on the role of artificial selection in the transformation of the behavior of these animals, which has brought about unique populations of tame and aggressive foxes. Additional resources were developed to analyze the molecular nature of differences in the behavior of these unique foxes: the meiotic map of the fox genome was constructed, informative segregating subpopulations were obtained by crosses of tame and aggressive animals, and the formerly applied method of behavioral phenotype quantification was improved. The integrated behavioral phenotypes (principal components PC1 and PC2) used in the study were obtained by analysis of ethological parameters recorded with a camcorder. The most important result is that the region most closely associated with tame behavior was identified on fox chromosome 12 by QTL interval mapping. The principle significance of this result is strengthened by the fact that the region is similar to the region on dog chromosome 5, presumed to be responsible for the early domestication of wolves and their evolutionary transformation to primitive dogs.

Molecular identification of a Fuegian dog belonging to the Fagnano Regional Museum ethnographic collection, Tierra del Fuego

Native-European contact in Tierra del Fuego was a rapid process, for which little ethnographic information has been produced. Although the Fuegian dog seemed to have been important to Selk'nam people's life, the taxonomic status of this extinct animal is still uncertain. The aim of the present work was to determine the zoological identity of a taxidermized canid belonging to a Fagnano Regional Museum collection, Río Grande, Tierra del Fuego. For this purpose, DNA from Fuegian dog and patagonian wild canids (Lycalopex culpaeus, Lycalopex griseus and Lycalopex gymnocercus) hairs was extracted. An mtDNA Region Control fragment was amplified by PCR and sequenced. Sequence alignment was performed among the sequences that were obtained in this research and the Canis lupus familiaris sequence from GenBank. Pairwise analysis showed a higher identity between the Fuegian dog and the culpeo fox (97.57%), with greater divergence with the current domestic dog (88.93%). These results were supported by the molecular phylogenetic analysis, suggesting atypical fox domestication by hunter-gatherers.

Island fur farming as the first stage of commercial fox domestication

The mastering of the Aleutian Islands and Alaska by the Russian fur hunters led to semi-free island fur farming. A great contribution to the development of the technology of fur farming on Commander Island in the 20th century was made by a matriarch of domestic fur farming, E.D. Ilyina, and her followers, such as S.V. Marakov. Work modeling the very beginning of the historical domestication of the Commander fox in the form of an economic organization resembling “island fur farming” was started in 2009 to ensure the employment of the Aleutian community. The first observations of the domestication behavior of the Commander blue fox are presented.

Mapping Loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype.

During the second part of the twentieth century, Belyaev selected tame and aggressive foxes (Vulpes vulpes), in an effort known as the "farm-fox experiment", to recapitulate the process of animal domestication. Using these tame and aggressive foxes as founders of segregant backcross and intercross populations we have employed interval mapping to identify a locus for tame behavior on fox chromosome VVU12. This locus is orthologous to, and therefore validates, a genomic region recently implicated in canine domestication. The tame versus aggressive behavioral phenotype was characterized as the first principal component (PC) of a PC matrix made up of many distinct behavioral traits (e.g. wags tail; comes to the front of the cage; allows head to be touched; holds observer's hand with its mouth; etc.). Mean values of this PC for F1, backcross and intercross populations defined a linear gradient of heritable behavior ranging from tame to aggressive. The second PC did not follow such a gradient, but also mapped to VVU12, and distinguished between active and passive behaviors. These data suggest that (1) there are at least two VVU12 loci associated with behavior; (2) expression of these loci is dependent on interactions with other parts of the genome (the genome context) and therefore varies from one crossbred population to another depending on the individual parents that participated in the cross.

An Experiment on Fox Domestication and Debatable Issues of Evolution of the Dog

This paper is a review of the results of the authors obtained in a long-term experiment on fox domestication. Debatable issues of dog evolution are discussed in light of these results. It is demonstrated that genetic physiological mechanisms of the behavior transformation during selection and the nature of the arising phenotypic changes are associated with retarded development of corresponding ontogenetic processes. As a result of this retardation, the adult animals retain juvenile traits of behavior and morphology (the phenomenon of neoteny). The role of hormonal changes caused by domestication in the evolutionary origin of neoteny is discussed.

Reproductive and pituitary-adrenal axis parameters in normal and prenatally stressed prepubertal blue foxes (Alopex lagopus)

AbstractMan-animal relationships are involved in the process of fox domestication. Handling being an important part of man-animal contacts, causes stress responses in farm-bred blue foxes. The purpose of this study was to determine how prenatal stress induced by handling pregnant vixens influences certain morphometric and hormonal parameters of adrenocortical and gonadal function in the prepubertal offspring. Blue fox females were subjected to daily handling sessions, each of 1 min, in the last trimester of pregnancy (term = 52 days). Plasma concentrations of ACTH, cortisol, progesterone, oestradiol and testosterone, as well as the in vitro adrenal and gonadal production of steroids were measured by radio-immunoassay in control (C, no. = 56) and prenatally stressed (PS, no. = 56) blue fox cubs of both sexes at the age of 6 to 7 months. Prenatal stress decreased plasma concentration of cortisol (C: 31·0 (s.e. 4·3) v. PS: 22·7(s.e. 1·6) ng/ml, P < 0·05) as well as progesterone (C: 1·00(s.e. 0·10) v. PS: 0·65(s.e. 0·05) ng/ml, P < 0·05) in female cubs. Prenatal stress did not cause any changes in adrenal or gonadal weights, plasma concentrations of testosterone or oestradiol, or in vitro adrenal or gonadal steroid production, in either sex. It is concluded that persistent handling of pregnant blue foxes did not affect the prepubertal development of the reproductive system but resulted in disregulation in the hypothalamic-pituitary-adrenal axis in the female offspring.

The effect of genetic selection for lack of aggression towards humans on male reproductive physiology in the silver fox

Most of silver foxes bred in captivity show predominantly defensive responses to human contact. Since early captive breeding humans have unconsciously carried out selection for tameness. Thus, artificial selection for the absence of aggressive and fearful responses to humans most likely played a key role in domestication process. To establish the genetic and physiological mechanisms of the early evolution of domestic animals, a model of silver fox domestication was developed at the Institute of Cytology and Genetics (Novosibirsk, Russia). A population of silver foxes has been produced in long-term selection for lack of aggression and fear towards humans (domestic behaviour). The method of selection and the behavioural changes in the course of selection have been described (Belyaev, 1979; Trut, 1995). Selected animals show no aggressiveness to humans and they are better adapted to captive conditions than their wild counterparts. The purpose of this study was to determine how behaviour selection influences testicular function in silver fox males. Plasma concentrations and testicular production of testosterone were determined in selected and control males in different parts of the reproductive cycle and prenatal life. In addition, reproductive behaviour and hormonal responses to opposite sex were estimated in the males of both behaviour groups. Sperm production and sexual activity were also compared between selected and control males.