The History of Fox Domestication at the Institute of Cytology and Genetics of the Russian Academy of Science Experimental Fox Farm

Since 1959, the Institute of Cytology and Genetics of the Russian Academy of Science in Novisibirsk, Russia has been attempting to domesticate the red fox, Vulpes vulpes, on their experimental fox farm, a project now known as the “Farm-Fox Experiment” (Kukekova et al. 2011; Spady and Ostrander 2007; Trut 1999). Currently led by head of the research group, Dr. Lyudmila N. Trut, the experiment was initiated by the late evolutionary geneticist and Director of the Institute of Cytology and Genetics, Dr. Dimitry K. Belyaev. In 1948, a time when Soviet genetics was beginning to recover from the anti-Darwinian ideology of Trofim Lysenko, Belyaev lost his position as Head of the Department of Fur Animal Breeding at the Central Research Laboratory of Fur Breeding in Moscow. His commitment to genetics led him to conduct genetic research under the guise of studying animal physiology. Under his leadership, the Institute of Cytology and Genetics was founded and became a center of basic and applied research in both classical and modern molecular genetics (Trut 1999). Belyaev mainly worked in genetics and animal breeding and was heavily influenced by the work of Charles Darwin (Belyaev 1979). “Animal domestication was his lifelong project, and fur bearers were his favorite subjects” recalls Dr. Trut (1999, p.162).

Charles Darwin focused much of his research on the domestication and variation of animals and sought to explain why domestic animals are so variable, with variations in body size, pigmentation, relative skeletal proportions, and even reproductive cycles (Belyaev 1979; Price 1984; Trut 1999, 2001; Trut et al. 2009). Domestication has brought about dwarf and giant breeds, wavy and curly coats, and long, Angora type coats and short, Rex type coats. Many domesticated animals are piebald, completely lacking pigmentation in specific body areas (Trut, 1999). “No one doubts that domesticated productions are more variable than organic beings which have never been removed from their natural conditions,” Darwin wrote in 1875 (p. 241). He admitted that the capacity to become more variable under domestication is common to all species and the “tendency to general variability is unlimited” (1875, p. 411).

Darwin also noticed the similarities of changes observed in different domestic animals and even noted features found in domesticated animals that were not found in their wild counterparts. In Chapter XXIV of The Variation of Animals and Plants Under Domestication, Darwin noted that there are no wild species with drooping ears and curled tails, although domesticated animals can acquire these traits (Darwin 1875). Many breeds of dogs and pigs carry their tails curled up in a circle or semicircle. Some domesticated animals even have shorter tails resulting from a decrease in the number of tail vertebrae. (Trut 1999). “This deformity, therefore, appears to be the result of domestication,” Darwin concluded (1875, p.179).

“Different animals, domesticated by different people at different times in different parts of the world, appear to have passed through the same morphological and physiological evolutionary pathways. How can that be?” questioned Trut (1999, p. 166).

Belyaev determined that the main result of domestication has been an enormous increase in the rate and range of variability of the animals. “Domestic animals differ from their wild ancestors, and from each other, much more than do some species and even genera,” he remarked (1979, p. 301). Yet, the most striking feature of changes in separate domesticated species wasn’t how different and varied they were from each other, but the similarities they shared despite these changes. Belyaev believed that the patterns of changes observed in domesticated animals resulted from genetic changes that occurred in the course of selection and that the key factor selected was not a quantitative trait, but a behavioral one, specifically, tameability, an animal’s amenability to domestication and unique ability to interact with humans in a positive way (Hare 2002, 2005; Price 2002; Trut 1999). Following this hypothesis, different animals would respond in similar ways when subjected to the same kinds of selective pressures and extreme stressors of domestication (Trut 1999). Because mammals from widely different taxonomic groups share similar regulatory mechanisms, Belyaev believed that he could replicate common hormonal and neurochemical changes resulting from domestication in a previously-undomesticated species simply by selecting for an animal’s tameness toward humans (Trut 1999).

Belyaev decided to conduct an experiment attempting to replicate the domestication of the dog through the domestication of the silver fox, a color variant of the red fox, Vulpes vulpes. He intended to resolve questions surrounding early domestication and expand understanding of the suite of genes underlying complex behavior and domestication by reconstituting not only the behavioral, but the physiological phenotypic changes associated with domestication by selecting solely for behavior (Spady and Ostrander 2007). In his own words, Belyaev explained the purpose of his Farm-Fox Experiment: “The purpose of the present study was to produce, in the course of systematic selection for behavior, a type of domestic fox in some measure resembling the domesticated dog in its behavior” (Belyaev and Trut 1975/2009, p. 417).

The silver fox is a melanistic variant of the red fox, Vulpes vulpes, rarely found in nature, but commonly maintained on fox farms (Johnson et al. 2015; Westwood 1989). In silver foxes, black color replaces the red color of the guard hairs and the white areas of the wild red fox. Silvering, a sprinkling of white guard hairs throughout the colored pelage, is also present. These foxes were originally called black foxes, until the term “silver” was adopted among fur bearers due to the exclusiveness of the silvering characteristic of the fox. The value of fur bearing animals raised in captivity is considerably influenced by color phase, with mutant colors in foxes having been in great demand since 1940 (Cole and Shackelford 1943; Shackelford 1948). In the beginning stages of Belyaev’s experiment, the silver-colored fox yielded the greatest economic return of all fox colors and was bred for fur quality, body size, and litter size. (Gogoleva et al. 2010a; Westwood 1989).

Silver-Colored Red Fox

Silver-Colored Red Fox

Methodology

Belyaev chose the silver variant of the red fox as his experimental model for several reasons. First, the red fox shares a close taxonomic relationship with the dog and is a member of a sister lineage to dogs, representing a temporal phylogenetic separation of 10 million years (Bardeleben et al. 2003; Kukekova et al. 2008a, 2008b; Trut 1999; Trut et al. 2006; Wayne et al. 1997). This could mean that the fox holds the same genetic potential for domestication as the dog. Secondly, the silver fox’s elite fur-bearing status and importance in the fur industry benefitted Belyaev and fur farmers. Fur farmers have attempted to breed foxes that were no longer restricted by mono-estrousness, the strict seasonal rhythm of reproduction and that would breed multiple times in a year, but all attempts had failed (Belyaev 1979; Trut 1999). Fur farmers were especially interested in foxes that reached sexual maturity more quickly, mated outside of the strict breeding season, became less stressed in the confinements of captivity, and were tamer with handlers and easier to handle in general (Faith 2007; Kukekova et al. 2012). Belyaev was able to begin his experiment with foxes that had already been selectively bred to some degree. The earliest steps of domestication: capture, caging, and isolation from other wild animals, had already taken place in foxes bred for their fur. These animals had been bred on fur farms in Russia since the early 20^th century and were already tamer than their wild relatives as they’d been subjected to rigorous selection for adaption to a new social environment. This helped to reduce the duration of the Farm-Fox Experiment (Statham et al. 2011; Trut 1999; Trut et al. 2009).

Despite captive breeding for over a century, farm-bred foxes still retain characteristic fear-aggressive responses toward humans, such as growling, biting, and avoidance response and have not become domesticated. These behaviors can be defined through the distance between the animal and the human as more fearful foxes will try to increase their distance from an approaching human (Faith 2007; Kukekova et al. 2008a, 2012; Gogoleva et al. 2010a; Trut 1999). Because these foxes were bred for fur quality, body size, and litter size and not for positive attitudes toward people, they have remained fearful of humans and have retained a standard morphological phenotype and seasonal pattern of breeding specific to foxes of natural populations (Faith 2007; Gogoleva et al. 2010a; Kukekova et al. 2008a, 2012; Scientific Committee on Animal Health and Animal Welfare 2001; Statham et al. 2011; Trut et al. 2009). As a result of fur farm keepers not establishing personal relationships with the animals, these foxes can experience short-term and long-term welfare problems in proximity of humans and can display non-vocal behavioral indicators such as: elevated psychological stress, hyperthermia, adrenal responses, changes in blood parameters (Moe and Bakken 1997), peaks of stress-related hormones, such as cortisol and AKTG, latencies to touch novel objects, inability to move, hesitations to defecate (Gogoleva et al. 2010b), restraining from eating in the presence of humans (Rekilä et al. 1997), erected ears (Moe et al. 2006), extent of abnormal behaviors, such as tail biting and reproductive failure (Braastad 1987), infanticide (Bakken 1998), synchrony of activity of family members, and aggressive acts (Ahola and Mononen 2002). Farmed silver foxes also exhibit high vocal activity toward humans, a sign of negative emotional states and psychological discomfort (Jürgens 2009), producing up to a few calls per minute in response to human approach (Gogoleva et al. 2008). When in the presence of humans, these foxes remain in the back portion of their cages, do not approach breeders, move back when the breeder approaches the cage, and move to the back part of the cage when the doors of their cages are opened (Gogoleva et al. 2010b). Out of fear, these animals will sniff the front portion of the cage, demonstrate rear attacking, and express aggressive sounds (Kukekova et al. 2008b). Captive breeding has also been accompanied by frequent reproduction problems brought about by the breeding system and the physical and social environment (Scientific Committee on Animal Health and Animal Welfare 2001). Due to the stress put on silver foxes by selective breeding for fur quality, fur farmers were interested in the possibility of a tame silver fox that was easy to handle. The lowered stress levels in the fox would reflect in larger litters, better fur quality, and longer lifespans of the foxes.

Belyaev (1979) visited multiple fur farms to identify a subset of commercial foxes that showed less fearful and aggressive responses to humans. Several thousand foxes were tested on the basis of contacts with man, which were graded in time, as an experimenter approached the animal’s cage, tried to open it, and monitored the expression of the response. Foxes were also assessed quantitatively by the acceptance of food from the hand of man and response to fondling, handling, and to call (Belyaev and Trut 1975/2009; Faith 2007). About 30% of the foxes he tested were extremely aggressive towards man, 20% were fearful, 40% were aggressively fearful, and only 10% displayed a quiet exploratory reaction without either fear or aggression (Belyaev, 1979). “Even the nonaggressive foxes could not be handled without special precautions against bites,” he writes. “They, too, were virtually wild animals” (Belyaev, 1979, p. 301). From the 10% of curious silver foxes, Belyaev chose 100 vixens, female foxes, and 30 tods, male foxes to foster the new generations of experimentally-bred foxes selected for tameness (Belyaev 1979; Trut 1999; Trut et al. 2009).

Because early exposure to humans can affect the further reactions of foxes to people, the Institute of Cytology and Genetics forbids anyone, including the researchers, to pet or establish personal contacts with any particular fox on the experimental farm outside of time dosage contacts. The institute has maintained a standardized holding regime uniform for all foxes since 1960 and continues to maintain it presently. All foxes experience consistent farm conditions and have similar interactions with people in order to ensure that tameness results from genetic selection. The foxes are not trained and are only allowed brief contact with human beings under uniform conditions. This helps to exclude the influence of new factors on the behavior of the animals and minimizes environmental influences on the fox behavioral phenotypes (Gogoleva et al. 2010a, 2010b; Kukekova et al. 2007, 2008a, 2008b; Trut 1999).

Foxes are bred once per year in January and February and pups are generally born in March-May. Littermates are housed together with their mothers until weaning at the age of 1.5 months, when the mother is removed and the littermates continue to live together without her. At the age of 2-3 months, each fox pup is separated from his littermates and placed into individual, outdoor cages 70 x 85 x 90 cm. with a wire mesh floor. The cages are arranged in batteries of 50 cages per row, with two rows opposite each other and 1.7-meter-wide passageway between them. This close proximity allows the foxes to remain in visual, olfactory, and auditory contact with foxes in neighboring and opposing cages. The cages are covered with a slate roof with two sloping surfaces that provide protection from wind, rain, and sun. The foxes are fed a diet of beef, meat by-products, minced chicken, cereals, vitamins, and minerals twice a day and water is available ad libitum (Gogoleva et al. 2010a, 2010b, 2011; Kukekova et al. 2008b; Trut 1999).

The testing of fox behavior to evaluate fox responses to humans in situations with different levels of interaction between the experimenter and tested animal has also been standardized at the ICG. The early testing process has since been improved upon to create “the standard test.” In the early stages of the experiment, an experimenter would offer food from his hand to a one-month-old pup and try to stroke and handle the pup. The fox cubs were tested twice, once confined in a cage and once allowed to roam freely in an enclosure with other fox pups where the animals could choose to make contact with the experimenter or with another pup. In each test, the reactions of the animal to the experimenter and the fox’s disposition to approach the experimenter were recorded. The test was repeated monthly until the pups were 6-7 months old. At 7-8 months old, when the foxes reached sexual maturity, they were scored for tameness and assigned to one of three classes. Pups that continued to show aggressive-avoidance responses to humans were discarded from the experimental population. The least domesticated foxes, those that showed fear or aggression, such as fleeing from experimenters or biting when stroked or handled, were assigned to Class III. Even still, these Class III foxes were tamer than wild foxes or even foxes bred at fur farms and could be hand-fed at times. Foxes that allowed themselves to be petted and handled but showed no emotionally friendly response to experimenters were assigned to Class II. Class I was reserved for foxes that were friendly toward experimenters and would show positive reactions to humans such as wagging of the tail or whining for attention. By the 6^th generation of breeding, the foxes had become so tame that a fourth class was added, Class IE, the domesticated elite. These foxes were eager to establish human contact and would whimper to attract attention and sniff and lick experimenters like dogs (Belyaev 1979; Abumrad 2009; Trut 1999; Trut et al. 2009; Hare et al. 2002, 2005).

As a result of the vigorous selection process, offspring exhibiting aggressive and fear avoidance responses were no longer present in the experimental population by the 3^rd generation of selective breeding. In the 4^th generation, some pups began to respond to humans by wagging their tails like dogs. Within the 6^th generation, fox cubs eagerly sought contact with humans by wagging their tails, whining and whimpering for attention, and licking, thus inspiring the newly-added Class IE. At this time, 1.8% of the foxes were classified in the IE class. By the 10^th generation, 17.9% of fox pups were classified as domesticated elite, by the 20^th generation, 35% had achieved the status, and in the 30^th generation, 49% were in Class IE. By the 35^th generation, a majority of the foxes in the experimental population, at 70%-80% were ranked as Class IE, showing no aggression, but submissive behavior toward humans upon first behavioral assessment without any prior training. Today, almost all of the foxes are domesticated elite, making up a new breed of genetically tame foxes (Huang et al. 2015; Trut 1999; Trut et al. 2004, 2009).

The fox behavior test has since been modified to create “the standard test” which can measure quantitative differences between the behaviors of the foxes (Trut 1999, 2001; Trut et al. 2009). During “the standard test,” each fox is tested in his home cage at least twice at 4-6 months of age, when the behavioral reaction toward humans is permanently formed, and a subset of foxes is tested three times. No more than one test is given to any individual animal on the same day and, in most cases, the period between tests is one day. All tests are performed between 10:30am and 5:00pm, but no earlier than 30 minutes after feeding. An interval of at least 30 minutes separates testing of animals in neighboring cages. All tests for a particular animal are conducted by the same experimenter and are videotaped and maintained on permanent record. The test is composed of five steps, each one minute long, except the first step (Gogoleva 2010b; Huang et al. 2015; Kukekova et al. 2008a, 2008b, 2011).

The Standard ICG Fox Behavior Test Steps

Note. The test was composed of five steps, each one minute long, except the first step. Adopted from Kukekova et al. 2011, 2008a, 2008b.

After being tested, foxes are rated for tameness. Two scoring systems were developed to measure a fox’s behavioral phenotype: one for tameness and one for aggressiveness. The major criterion for measuring behavior was the critical distance between the experimenter and the caged animal when the animal first demonstrates a reaction and the intensity of that reaction viewed from the video record using a DVD player or WinDVD software. The Class I, II, III, and IE system was replaced by a quantitative system that rates a fox’s response to an experimenter for tameness and aggression on a scale of -0.5 to +4.0. The most aggressive foxes are given a score of -3.5 to -4.0 on the scoring system. These animals show teeth, snarl, and growl at the first sight of a human. When an experimenter is near the fox’s closed cage, the fox attacks the experimenter with bared teeth and fixed dilated pupils. Foxes assigned a score of -3.0 are slightly less aggressive. These foxes show teeth, snarl, growl, and attack the experimenter with bared teeth and fixed dilated pupils when the cage is opened, but not closed. -2.5 foxes growl at an experimenter near their open cages, but do not attack. Foxes assigned the -2.0 score only growl and bite when the experimenter moves an arm towards the fox. The least aggressive, but not tame, foxes are scored a -1.5. These creatures are calm when an experimenter opens the cage, but attempts to touch the fox provoke it to show teeth and snarl. Animals that display neutral behavior, an absence of both actively aggressive and actively tame responses directed toward the observer, are assigned a score of 0. The least tame foxes that do not show aggressive tendencies are assigned a score of +0.5 to +1.0 and show the passive-protection response. These foxes avoid the experimenter and bite if stroked or handled, but draw near if food is offered. Foxes assigned a score of +1.5 to +2.0 let themselves be petted and handled, but show no emotionally friendly response to the experimenter. Foxes given a score between +2.5 to +3.0 show emotionally positive and friendly responses to the experimenter and wag their tails and whine for attention. The tamest foxes score between +3.5 to +4.0 and are eager to establish human contact. These foxes whimper to attract attention and sniff and lick experimenters like dogs (Gulevich et al. 2004; Huang et al. 2015; Kukekvoa et al. 2008b, 2012; Trut 1999, 2001).

A comprehensive set of 50 binary (present/absent or yes/no) objective observations that non-redundantly and accurately measures behaviors is used to clearly distinguish tame foxes from aggressive and wild foxes. Objective observations such as a fox’s location in the cage, amount of time spent in a location in the cage, body posture, position of particular parts of the body, willingness and desire to be touched, eagerness to attack and bite, and even the noises and sounds made by the fox were used to measure behavior. Subjective assessments of fox actions were avoided. To evaluate the location of the fox in the cage while being tested, the space in each cage was partitioned into six different zones, Zones 1-6. Zones 1 and 2 are located at the front of the cage with Zone 2 being closest to the experimenter. Zones 3 and 4 are in the middle of the cage and Zones 5 and 6 are in the back. The systems for measuring behavior yield objective and reproducible behavioral assessments of individuals from the tame and aggressive strains and were used to select the animals exhibiting the tamest and the most aggressive behaviors for breeding the next generations. (Gulevich et al. 2004; Huang et al. 2015; Kukekvoa et al. 2008b, 2011, 2012).

The Standard ICG Fox Behavior Test 50 Behavioral Assignment Traits

Note. Adopted from Kukekova et al. 2011, 2008a, 2008b.

Belyaev (1979) explained that the criteria for breeding foxes began by selecting foxes that consistently displayed tame behavior with respect to people. As the foxes began to show more tame behavior, the selection was restricted to animals that were actively willing to contact the experimenter. Finally, the selection became so strict that in recent years, less than 10% of the most tame individuals of every generation, 5% of breeding males and 20% breeding females, were allowed to breed and parent the next generation (Belyaev 1979; Trut 1999, 2001; Trut et al. 2009).

The selected population was maintained by outbreeding in order to minimize homozygosity due to inbreeding. From time to time, foxes selected for behavior from different fur farms and not related to each other were introduced into the experimental breeding pool. Through outbreeding with foxes from commercial fox farms and other standard methods, the inbreeding coefficients of the experimental fox population was kept between 0.02 and 0.07. This means that the probability of acquired traits are inherited through inbreeding is between 2% and 7% (Belyaev 1979; Trut 1999, 2001; Trut et al. 2004). Kukekova et al. (2004) has confirmed this low level of inbreeding in an analysis using microsatellite markers.

The heritability of domesticated traits, as opposed to a significant epigenetic or maternal environmental influence, was established in studies in the early 1960s involving cross-upbringing of domesticated pups by non-domesticated mothers and vice versa; cross breeding of tame, unselected, and highly aggressive animals; and cross-transplantation of blastocysts and embryos followed by behavioral and genetic investigations (Belyaev 1979; Kukekova et al. 2004, 2008b, 2011; Trut 1999, 2001; Trut et al. 2004, 2009). “We did an experiment with cross-fostering where we gave aggressive cubs to tame mothers and vice-versa,” explained Dr. Trut. “We found out that the mother’s behavior does not influence that of the cub” (Child 2011). Whether a fox was raised by a tame mother or an aggressive mother, it was always the birth mother’s nature and not the foster mother’s nurturing that determined the cub’s behavior. “We even took the experiment one stage further and transplanted embryos from aggressive mothers into tame mothers but the results were the same,” says Trut, explaining the embryo transplantation experiments (Child 2011). Trut (1999) reported that about 35% of the variations in the foxes’ defense response to humans were genetically determined. Despite how the kit was raised or nurtured, only genetics could tell if the animal would be a tame or aggressive individual. These experiments confirmed the genetic basis of the domesticated behavior, demonstrating that behavioral differences between tame and aggressive foxes were genetically, not behaviorally, determined.

After establishing a selectively bred tame strain of foxes, the Institute of Cytology and Genetics began to develop varied populations of foxes. Five populations of foxes are currently maintained on the fox farm: the selectively bred tame strain, a selectively bred aggressive strain, an unselectively bred farm-raised strain, an F1 generation, and a backcross population. (Kukekova et al. 2008; Statham et al. 2011).

In the 1970s, the Institute of Cytology and Genetics started a new population of aggressive foxes at the experimental fox farm. This deliberate selection for animals that show aggressive responses to humans would parallel the tame population of foxes and help reveal similarities and differences between the two strains. This comparison was intended to expand our knowledge and understanding of domestication and how it effects animals. Fifty farm-bred silver foxes with the most aggressive responses to humans were selected from several fox farms and used to found the selectively bred aggressive strain (Kukekova, 2008b; Trut et al. 2009). Aggressive foxes are difficult to handle as they hiss and scream in response to people and growl toward conspecifics (Gogoleva et al. 2010b; Trut 1999, 2001). “It just bit my hand. I didn’t even open the cage. I just put my hand out and it managed to bite me through the bars,” remarked Dr. Lyudmila Trut in the documentary Dogs Decoded after she had brushed her hand across an aggressive fox’s cage. “This isn’t a fox, it’s a dragon” (Child 2011).

An unselected population is also kept at the ICG in order to act as a control group. These foxes originate from several commercial fox farms, are unselected for behavior, and are meant to replicate farm-raised foxes bred for their fur (Abumrad 2009; Kukekova et al. 2008; Statham et al. 2011).

All animal experiments conducted at the Institute of Cytology and Genetics follow the international guiding principles for biomedical research involving animals developed by the Council for International Organizations of Medical Sciences (CIOMS) and are in compliance with the laws, regulations, and policies of the “Animal welfare assurance for humane care and use of laboratory animals,” permit number A5761-01, approved by the Office of Laboratory Animal Welfare (OLAW) of the National Institutes of Health, USA (Huang et al. 2015; Statham et al. 2011). The “Guidelines for the treatment of animals in behavioral research and teaching” are also followed (Gogoleva et al. 2011).

Although the original farm-bred fox population showed a continuous variation in aggressive and fearful behavior, the phenotypes in the newly selected tame and aggressive populations no longer overlap. Belyaev (1979) defined domestication as “the ability of animals to have direct contact with man, not to be afraid of man, to obey him, and to reproduce under the conditions created by him” (p. 301). By this definition, the Farm-Fox Experiment has succeeded in domesticated the red fox. In the process of domesticating these foxes, profound and complex changes occurred in behavior and in the organismic neuroendocrine state (Belyaev and Trut 1975/2009).

Results

Behavior

The foxes from the selected population are not afraid of people and display an active positive reaction to human contact as they seek contact with people (Belyaev 1979). These selectively bred foxes differ remarkably from their wild or farmed counterparts in distinct and specific behavioral traits: their positions within their cages when a human approaches; the positions of their tails and ears; the noises that they make; and their willingness and desire to be touched as opposed to their eagerness to attack and bite (Kukekova et al. 2011). Domestic foxes respond when called, answer to nicknames, come up to man, and permit themselves to be petted and picked up. The most domesticated animals wag their tails in greeting (Abumrad 2009; Belyaev 1979; Belyaev and Trut 1975/2009; Faith 2007). Through experimental testing, Gogoleva et al. (2010b) found that tactile contacts, caressing, and handling were most stimulating for tame foxes because of their desire for human attention. These foxes are eager to establish human contact and approach humans willingly; move on half-bent paws; hold their mouths ajar as they pant with excitement; hold ears horizontally or down; sniff and lick; nip or poke with the nose; roll on the side, back, or even belly up during contact; and try to hold a human’s hand weakly in the mouth by the teeth, all signs of trustfulness shown by domesticated dogs (Belyaev 1979; Kukekova et al 2008a, 2008b, 2012; Trut 1999; Trut et al. 2009). Play activity, which is normally only seen in infantile, wild foxes is more common among foxes of the tame population and persists into adulthood as they actively seek attention from conspecifics and humans in a playful, friendly, and communicative manner (Faith 2007; Kukekova et al. 2008a; Spady and Ostrander 2007; Trut 2001). “They are unusual animals, docile, eager to please, and unmistakably domesticated,” concludes Dr. Trut (1999, p. 163).

These traits have never been observed in the unselected or aggressive populations of foxes. Further, aggressive behaviors, such as attacking, pinned ears, and aggressive sounds are frequently documented in the aggressive population, but have never been observed in the tame population (Kukekova et al 2008a, 2008b). The foxes actively selected for behavior are tame, not as a result of training or taming, but due to prolonged selection for a tame genotype. “There is something moving in the emotions of these foxes,” remarked Belyaev (1979, p. 303). “At the sight of even a strange person, they try actively to attract attention with their whining, wagging of tails, and specific movements.”

Communication

It has been suggested that domesticated animals are able to receive and discern communicative signals from humans, evolving this ability as an adaptation to the tight coexistence and interaction with people (Trut et al. 2009). Gogoleva et al. (2011) even suggests that domesticated animals can provide humans with information, thus involving in inter-species communication. In the presence of humans and conspecifics, tame foxes show emotionally positive responses and communicate in a positive manner (Gogoleva et al. 2011; Trut 1999). Domesticated foxes show explosive behavioral and vocal responses at the appearance of humans before them, even unfamiliar humans (Trut 1999; Trut et al. 2009). Gogoleva et al. (2011) suggests that this high calling rate in response to human appearance may act as a behavioral mechanism for attraction of human attention that is directed to prolonging the contact and involvement of animal-human interaction. These domesticated foxes have been observed producing tonal cackles and noisy pants, but never coughs or snorts, two vocalizations commonly created by aggressive and unselected foxes (Gogoleva et al. 2008, 2010b). They breathe loudly with excitement when in contact with humans, panting similarly to domesticated dogs when interacting with people in a positive manner and offering an invitation to play (Cohen and Fox 1976; Kukekova et al 2008a, 2008b). Domesticated foxes also have a habit of emitting typical barks, resembling those made by domesticated dogs, at the sight of man and whimpering and whining for human attention (Abumrad 2009; Belyaev and Trut 1975/2009; Trut 1999). Gogoleva et al. (2011) reported that domesticated foxes will pant upon human interaction and will increase the proportion of whines to pants when contact is refused by the human. This suggests that human appearance before a tame fox provokes high levels of emotional arousal which entices the fox to react with vocal and non-vocal displays that suggest the desire to interact with humans. In contrast, aggressive and unselectively bred silver foxes respond emotionally negatively to all humans, displaying permanent vocal activity for the duration of human interaction (Gogoleva et al. 2008, 2010b, 2011; Trut 1999; Trut et al. 2009).

In 2006, Hare et al. conducted experiments to test the abilities of domesticated fox pups to understand and utilize human pointing gestures. The domesticated silver fox pups were found to perform the task of finding hidden food items with the assistance of human pointing gestures as skillfully as dog puppies while undomesticated silver foxes, not bred for behavior, failed to perform the task. Domesticated dog pups instinctually use human pointing gestures as guidance as early as 6-9 weeks of age. Interestingly, after weeks of exposure to humans, even the undomesticated control foxes were capable of using human communicative gestures to find the hidden food, yet still not as skillfully as the domesticated foxes with less human exposure (Hare et al. 2006). In comparison, undomesticated timber wolves and chimpanzees are unable to resolve this task without special training (Hare and Tomasello 2005; Hare et al. 2006). These results show that experimentally domesticated foxes with almost no experience with humans and not trained to use human gestures, are as skilled as domestic dogs at using communicative gestures, and are therefore more skilled at understanding human communication than chimpanzees and wolves. Trut et al. (2009) has confirmed the use of human cues for coping with a man-made environment within experimental tests, selection procedures, and even daily routine care in the ICG experimental population of foxes. Domestication in foxes has led to an improved ability to use human communicative gestures and glances and an evolved social cognitive mechanism that more closely resembles social cognitive skills than do those of other animals.

Development

A close relationship has been found between the nervous system and endocrine system. Selection for behavior can intrinsically change the hormonal status of a breed, thus affecting the ontogenetic development of the animal (Belyaev 1979). Tecumseh Fitch, an evolutionary biologist at the University of St. Andrews in Scotland, hypothesizes that neural crest cells contribute to the development of an embryo. In foxes, the migration from the neural crest contributes to the development of the skin, ear cartilage, jaw, tissues, teeth, tail, nervous system, brain, and adrenal glands. When selecting animals for positive responses to humans, the migration from the neural crest is slowed in order to produce foxes with adrenal glands that don’t mature (Abumrad 2009). Because so many quantitative traits in animals are genetic and tend to be controlled by complex systems of genes and polygenes, anything that tampers with these genes changes a multitude of parts within an animal’s genetic makeup (Trut 1999). When a fox’s neural crests do not fully migrate to the adrenal glands to produce less aggressive behavior, they also do not fully migrate to other areas, such as the fox’s ears, and when a section of the ear does not receive as many cells needed to remain straight and stable, it becomes flopped over (Abumrad 2009).

Delay in the developmental rates of the foxes selected for tame behavior has been observed as early as during embryonic morphogenesis. In these foxes, opening of the eyelids and external auditory canal was accelerated while the onset of the fear response was delayed (Trut et al. 2009). On average, domesticated fox pups respond to sounds two days earlier and open their eyes a day earlier than non-domesticated foxes (Trut 1999). The sensitive period for socialization, in which mammals explore their environments, adapt to social factors, learn about their surroundings, and form attachments through the use of sense and locomotion (Scott 1958), persisted past 60 days of age in domesticated foxes, compared to less than 45 days in unselected foxes (Belyaev et al. 1985; Kukekova et al. 2008a; Trut 1999; Trut and Oskina 2004; Trut et al. 2009). Because the type of defense behavior towards man is formed and preserved as a permanent individual characteristic in most animals during the first few months of life when the neurophysiological substrate of the fear response matures, foxes with extended socialization periods don’t show the fear response until later than tame foxes and have more time to become incorporated into a human social environment. Thus, they are more likely to form positive response behaviors toward humans (Belyaev 1979; Trut 1999; Trut et al. 2009). Belyaev (1979) has found that variability in the defense behavior has a hereditary basis, thus selection is possible and repeatability is very high. Foxes can be selected for positive response behaviors toward humans and pass their positive responses to their offspring.

Physiology

Hormonal responses suggest that domesticated foxes do not experience stress when in contact with humans, unlike aggressive foxes, foxes unselected for behavior, and even farm-bred foxes (Gogoleva et al. 2011). The domestication of foxes has effected the hypothalamic-pituitary-adrenal (HPA) system, the main hormonal system which plays an important role in the process of adaptation to captivity, a challenging stressing factor upon animals. The responsiveness of the pituitary-adrenal system not only determines the initial level of plasma hormones, but may also influence the reactivity to psychological stress and ACTH, an adrenocorticotrophic hormone. The HPA axis of domesticated foxes has reduced steadily at all levels from the central regulation of the pituitary to peripheral blood levels of glucocorticoids, and the hypothalamo-pituitary-adrenal system is activated to a higher degree (Belyaev 1979; Belyaev and Trut 1975/2009; Gulevich et al. 2004; Trut 1999; Trut et al. 2009). Because the function of this system helps an animal respond to stress, domesticated animals experience a decrease in the stress response (Trut et al. 2009). Tame and unselected foxes differ in the functional state of the adrenal cortex, as well, as the adrenal cortex responds less sharply in domesticated foxes when the foxes are subjected to emotional stress (Belyaev and Trut 1975/2009; Trut 1999).

After 12 generations of selecting foxes for tame behavior in response to handling and blood sampling, it was found that plasma glucocorticoid levels, produced in relation to stress, were significantly lower in tame animals than unselected animals; the higher the domestic behavior of the animal, the lower the plasma glucocorticoid levels (Belyaev and Trut 1975/2009; Gulevich et al. 2004; Trut 1999; Trut et al. 2009). Trut (1999) identified a correlation between the delayed development of the fear response in domesticated foxes and changes in plasma levels of corticosteroids: the more advanced the animal’s selection for domesticated behavior was, the later it showed the fear response and the later came the surge in its plasma corticosteroids. Foxes selected for tame behavior also demonstrated lower in vitro glucocorticoid production by the adrenals and plasma ACTH levels in response to handling and blood sampling in comparison to unselected animals and those selected for aggressive behavior (Gulevich et al. 2004). ACTH response was about 2-4 times more intense in domestic females than in wild females, showing that domestic and wild foxes differ in the degree to which they respond to the same dose of ACTH (Belyaev and Trut 1975/2009). Tame foxes also had significantly lowered basal and stress-induced blood plasma cortisol levels in response to ACTH stimulation and stress than aggressive and unselected individuals and experienced 30% lower stress levels (Gulevich et al. 2004; Oskina and Tinnikov 1992; Trut et al. 2009).

Studies of the brain’s serotonin system in tame foxes and foxes unselected for behavior have found changes in the neurochemistry of domesticated foxes. Tame foxes possessed lower density of 5-HT1A serotonin receptors, in the hypothalamus. Higher levels of serotonin, its main metabolite 5-hydroxyindol acetic acid, and tryptophan hydroxylase, the key enzyme of serotonin synthesis, were found in the midbrain and hypothalamus (Belyaev 1979; Gulevich et al. 2004; Trut 1999; Trut et al. 2009). The hypothalamus is a biologically important, evolutionary conserved brain structure and modulator of behavioral and neuroendocrine responses to environmental agents (Trut et al. 2009). Serotonin is a neurotransmitter that inhibits aggression and centrally regulates the hypothalamic-hypophyseal-adrenal-sexual system, thus selection for tame behavior is associated with changes in both the central and the peripheral mechanisms of the neuro-endocrine control of ontogeny (Belyaev 1979; Popova 2006; Trut 1999).

In all foxes, both absolute and relative adult hippocampal neurogenesis (AHN) have been found to be markedly higher in the temporal hippocampus, associated with odor memory and social behavior (Kesner et al. 2011; Kjelstrup et al. 2002). Behavioral neoteny is regulated differently from physiological neoteny and might be associated with higher AHN in the hippocampus of the fox (Huang et al. 2015).

Reproduction

The selection for tame behavior in foxes has also resulted in a change in the level of steroid sex hormones, estradiol and progesterone, hormones responsible for implantation and embryonic mortality, thus accounting for higher fertility of domesticated foxes as compared to wild foxes. Female foxes selected for positive responses to humans show increased levels of estradiol and progesterone during the first days of pregnancy than foxes unselected for behavior (Belyaev 1979). Belyaev (1979) identified a phenotypic and a genotypic correlation between the type of defensive behavior of females and the time of onset of their reproductive activity within the breeding season.

Foxes which do not show aggressive and fear responses when coming into contact with man mated earlier during the breeding season, had larger litters, and experienced longer moulting times than foxes with aggressive defense behaviors toward humans. On average, these foxes reached sexual maturity one month earlier then farm-bred foxes, mating anywhere from November to May, rather than the usual fox mating period of late January to late March in Siberia (Belyaev 1979; Oskina 1995; Trut 1999). They also gave birth to litters that were one pup larger than wild fox litters, ranging from two to fourteen pups with an average of five or six (Trut 1999). Some foxes even mated twice in one year. (Belyaev 1979; Trut 1999). These results agreed with Darwin’s observation in 1876, “With our domesticated animals, the various races when crossed together are quite fertile” (p. 304). Domestication of the fox, just as domestication of all other species, has increased the duration and success of its reproduction.

In 1962, 6% of the silver foxes subjected to selection showed sexual activation outside the regular seasonal pattern, and in 1969, after only 7 years of selective breeding, 40% of the selectively bred silver foxes experienced extended breeding periods. Unfortunately, the reorganization towards two annual estrus cycles in the foxes was paralleled with a decreased capacity to reproduce during the regular breeding season. 30% of the foxes failed to produce litters as a result of not mating at all, infertile mating, or having litters that succumbed to inhibited lactation or cannibalism (Belyaev 1979; Belyaev and Trut 1975/2009; Trut et al. 2009). Also, Trut (1999) has reported that no offspring of an extra-seasonal mating has survived to adulthood. While there is potential in the selectively-bred foxes to reproduce more than once a year, there hasn’t been success yet.

Anatomy

In some of the tame foxes, new morphological characteristics appeared that are not found in wild animals, but are commonly seen in domesticated animals, such as various breeds of dogs. Several different aberrations appeared simultaneously, such as a peculiar curled position of the tail over the fox’s back in a semicircular position; brown spots around the ears, neck, and about the shoulder blades; and drooping ears, characteristic of young animals (Abumrad 2009; Belyaev 1979; Faith 2007; Trut 1999; Trut et al. 2009). After 15-20 generations of selective breeding, changes in the parameters of the skeletal system began to arise. Some foxes were born with shortened legs, tails, snouts, teeth, and upper jaws, thinner bones, and widened skulls (Abumrad 2009; Trut 1999; Trut et al. 2009). Some developed underbites or overbites due to the elongation of the lower jaw or shortening of the upper jaw (Trut 1999; Trut et al. 2009). On average, the foxes are longer and larger in body size than their wild counterparts (Trut 1999). Trut (1999) was especially interested in the growth of the skull. In both genders of foxes from the experiment, the cranial height and width tend to be smaller and snouts tend to be shorter and wider than those from the control group of farmed foxes. The cranial morphology of domesticated adult males also became somewhat “feminized” as the skulls of males became more like females and the sexual dimorphism between the two sexes decreased. Analysis of the cranial allometry concluded that the changes in skull proportions resulted from changes in the timing of their growth rates or the first appearance of particular structures (Trut 1999).

Coat color changes; brown mottling, brown spots around the ears, neck, and about the shoulder blades; and white spotting appeared earlier than other changes, premiering in the 8^th generation of foxes without direct selection for appearance or inbreeding in the tame fox population. White spotting in foxes is referred to as whitemarks and one of the most common marks is a white star-shaped spot on the head. In contrast, when an animal experiences large sections of depigmentation on its body, it is referred to as piebald spotting or piebaldism (Abumrad 2009; Belyaev 1979; Belyaev et al. 1981; Kukekova et al. 2008a; Trut 1999; Trut et al. 2009) Belyaev determined that the star-shaped piebald pattern was governed by a gene that he named Star. Foxes homozygous for the Star gene developed piebald spotting, while foxes heterozygous for the gene sported smaller depigmentation. (Trut 1999; Trut et al. 2009). The star-shaped whitemark has since been named Star. Several other distinctive whitemarks have been named in the fox fur trade that closely resemble the names of markings given to other domesticated animals, such as horses and dogs. A fox can sport a single whitemark or more than one whitemark.

Frequencies of Phenotypic Changes in Fox Populations

Note. Adopted from Trut 1999; Trut et al. 2009.

Whitemarks on Red-Colored Red Foxes.

These are the common names given to whitemarks in the fox fur trade.

Standard

Lip

Snip

Stripe

Muzzle

Blaze

Star

Collar

Whitemarks on Silver-Colored Red Foxes.

These are the common names given to whitemarks in the fox fur trade.

Standard

Lip

Snip

Stripe

Muzzle

Blaze

Star

Collar

Conclusions

The color change seen in the foxes seemed to result from shifts in the rates of certain ontogenetic processes, or the timing of an embryo’s development (Trut 1999). Richard Shackelford (1948), the fur animal specialist at the University of Wisconsin in 1953, explained, “Coat color in mammals is generally attributed to melanins, organic compounds containing nitrogen, usually dark in color, and characterized by chemical inactivity” (p. 311). Dr. Lyudmila Trut and Lyudmila Prasolova found that retardation of the development, proliferation, and migration from the neural crest of the embryonic precursors of melanocytes, or primary melanoblasts, is the mechanism underlying depigmentation. Melanoblasts are the embryonic precursors of the pigment cells, melanocysts, which give an animal’s fur its color as they form in the embryonic fox’s neural crest and later move to various parts of the embryo’s epidermis. In foxes that carry even a single copy of the Star gene, melanoblasts pass into the potentially depigmented areas of the epidermis two days later, on average, leading to the death of the tardy melanoblasts and the lack of pigment in the animal’s fur (Trut 1999; Trut et al. 2009). When foxes are selected for tame behavior, they are selected for adrenal glands that have not been fully matured by the migration of neural crests (Abumrad 2009). This retardation leads to the absence of melanocytes from specific areas of the coat and, hence, to its depigmentation (Trut et al. 2009). Because fur color is effected by the migration of neural crests, it is also not fully matured, thus the fur color can look incomplete with patches of missing color or piebald spotting. While this has been discovered, the gene control of the brown mottling seen in some domesticated foxes is still unclear. In dogs, this variation is controlled by one of the mutations at the Agouti locus (Trut et al. 2009).

The results of the Farm-Fox Experiment are impressive. Through methodically applied selective breeding, a unique domesticated fox that looks and behaves similarly to the domesticated dog has been born. As a result of selecting for tame behavior, the foxes from the Institute of Cytology and Genetics are more similar to dogs than wild foxes and show more physical variations like many domesticated breeds. Some foxes have white collars and markings upon their faces like border collies, curly tail carriages like Islandsk Farehounds, floppy ears and widened skills like pugs, long jaws like English bulldogs, and long skulls like Pharaoh hounds (Trut et al. 2009).

Domestication involves changing the behavioral relationship between animals and man and developing mutual trust (Kukekvoa et al. 2011). When subjected to domestication, animals whose evolutionary pathways have not crossed start to evolve in the same direction as they lose the wild, aggressive behavioral response to humans and increase in social tolerance and reduced sensitivity to environmental changes (Price 2002; Trut 1988). Reproductive physiology is changed as sexual maturity is accelerated, fertility is increased, and periods of reproductive seasonality are lost. The activity of the reproductive system becomes relatively uncoupled from the environmental photoperiod, allowing the animal to acquire the ability to breed in any season and sometimes more than once a year (Belyaev 1979; Spady and Ostrander 2007; Trut 1999; Trut et al. 2009). The activity of the hypothalamic-pituitary adrenal axis, the key hormonal regulator of adaptation to stress, becomes weakened. Sexual dimorphism, the sizes of the visceral cranium, and teeth, and thickness of limb bones decrease. Similar morphological changes also appear in domesticated animals such as body size and proportions, coat color, fur length, and hair texture. White spotting, floppy ears, and curly tails have become markers of domestication (Abumrad 2009; Belyaev 1979; Kukekova et al. 2008a; Morey 1994; Trut 2007; Trut et al. 2009) and a piebald-spotted coat is one of the most striking mutations among domestic animals seen frequently in dogs, pigs, horses, cows, guinea pigs, cats, and other domesticated animals (Trut 1999).

Another common factor amongst domesticated animals is the phenomenon of neoteny and pedomorphosis, the retention of juvenile traits by adults (Morey 1994; Price 2002). The retaining of widened skulls, shortened snouts, floppy ears, curly or truncated tails, and the emotional expression of positive responses such as whining, barking, and submissiveness to humans are juvenile traits that certain domesticated individuals retain to adulthood (Morey 1994; Wayne 1986). “When you’re selecting against aggression, what you’re doing is you’re favoring juvenile traits,” explains evolutionary biologist and dog expert Professor Brian Hare from Duke University (Child 2011). “Juveniles and infants show much less aggression than adults and so what the idea is that basically you’ve frozen the development at a much earlier stage, and so you have an animal as an adult that looks and behaves much like a juvenile.”

All of the features commonly observed in domesticated species have been seen in the ICG’s population of domesticated foxes. These animals are capable of developing a trusting relationship with humans, are less sensitive to environmental differences due to hormonal changes, and can reproduce outside of the restrictive breeding season (Belyaev 1979; Oskina 1995; Trut 1999). Some domesticated foxes experience anatomical changes in their teeth, skulls, bones, body sizes and proportions, fur coloration, ears, and tails (Abumrad 2009; Belyaev 1979; Faith 2007; Trut 1999; Trut et al. 2009). The foxes from the Farm-Fox Experiment have also been effected by neotenization and appear and behave more like infants in their mature lives. Floppy ears, for instance, are characteristic of newborn fox pups, but may get carried into adulthood in domestic foxes. Play is another characteristic distinctive to infant foxes, but adult domesticated foxes enjoy the activity (Faith 2007; Kukekova et al. 2008a; Spady and Ostrander 2007; Trut 2001). While selecting for positive responses to humans, the Farm-Fox Experiment essentially bred infant-like foxes that never mature, forever looking and acting like a young fox kit, thus demonstrating that by simply selecting for behavior changes in the animal’s behavior, developmental, physiological, and anatomical changes would follow.

Because of its ground-breaking results, the Farm-Fox Experiment has contributed greatly to the study of animal domestication and genetics. This study has shown that the amenability of silver foxes to domestication is hereditarily determined and the degree to which offspring are domesticated increases with the number of domestic animals in their pedigree (Belyaev and Trut 1975/2009). “The domestic fox is not a domestic dog, but we believe that it has the genetic potential to become more and more doglike,” explains Dr. Trut (1999, p. 169). “We can continue to increase that potential through further breeding, but the foxes will realize it fully only through close contact with human beings.” The Farm-Fox Experiment has also demonstrated that neotenic shifts in developmental rate may arise as a correlated consequence of selection for tameability, or social adaptation to humans (Trut et al. 2009). Tameness, a behavioral trait that includes less fear and aggression toward humans in captivity, is a necessary prerequisite for domestication (Huang et al. 2015). Domestication for behavior is a profound process of selection that involves genetically and environmentally inducing developmental adaptation to man and captivity upon animals, and the ICG has achieved this in the red fox species (Price 1984).

The Farm-Fox Experiment has been highly commended by colleagues for its valued contribution to scientific and genetic research. Brian Hare has declared the Farm-Fox Experiment as “one of the most exciting experiments in biology” (Abumrad 2009). Hare, himself, has worked with the experimental fox populations in order to better understand the evolution and domestication taking place there and to explore new possibilities in dog research. Professor Ray Coppinger from Hampshire College in Massachusetts, another dog researcher interested in how dogs have evolved from wolves, told KPBS San Diego, “I really think that the Belyaev experiment was one of the most significant experiments in evolution that took place in the 20^th century and it effected my life and my thinking in so many ways” (Faith 2007). The ICG’s fox farm experiment has also influenced the study of evolution in humans. “Our present concepts of the human evolution are most greatly influenced by your work on domestication of foxes,” wrote evolutionary anthropologist, R. Wrangham in a letter addressed to Dr. Trut in 2003 (Trut 2007, p. 58). In February 2007, the US Scientist praised the Farm-Fox Experiment:

Since Darwin called attention to the mysteries of correlated alterations in domesticated animals, science had been waiting for explanations. The brilliant experiment of Dmitry Belyaev opened the door for resolving this problem. His work is a breakthrough to a new route important for evolutionary anthropology not only as an amendment to unexplained adaptations, but also because the specific behavioral traits influenced by natural selection are related to the human evolution (Trut 2007, p. 59).

Currently, the Institute of Cytology and Genetics maintains five populations of foxes on their fox farm: the selectively bred tame strain, the selectively bred aggressive strain, an unselectively bred farm-raised strain, an F1 generation developed by crossing tame males to aggressive females, and a backcross population produced by reciprocally breeding F1 foxes back to the tame strain (Kukekova et al. 2008; Statham et al. 2011). By 2009, Trut et al. reported that throughout the entire course of the experiment, 10,500 foxes had been bred and 50,000 offspring had been born and tested for their amenability to domestication. In 2011, the tame fox population at the ICG comprised of 300 breeding animals and the aggressive population of foxes was composed of about 130 breeding individuals (Statham et al. 2011).

Unfortunately, these numbers have dwindled since the past. In 1996, the population of the breeding herd was 700 foxes, but when the experiment was jeopardized by the crisis of the Russian economy, shrinking budgets, and changes in the grant-awarding system in Russia, the ICG had to reduce its population to 100 foxes. Without funds to provide food for the foxes and salaries for the staff, the future of the Farm-Fox Experiment was threatened. Still functioning today, the experiment has been funded through a variety of methods (Trut 1999). “Like many other enterprises in our country, we are becoming more entrepreneurial,” expressed Dr. Trut (1999, p. 169). Most expenses are covered by selling the pelts of the foxes culled from the breeding herd. Some foxes have been sold to Scandinavian fur breeders who have been pressured by animal-rights groups to breed from animals that do not suffer stress in captivity. Still dependent on outside funding, however, the ICG began to search for alternative funding. The domesticated foxes from the Farm-Fox Experiment are now offered as house pets. Trut believes that this commercial venture will lead to interesting, informal experiments, helping the ICG financially and in terms of understanding their creations better (Trut 1999). “If our experiment should continue, and if fox pups could be raised and trained the way dog puppies are now, there is no telling what sort of animal they might one day become,” Trut concludes (Trut 1999, p. 169).

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