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{{Short description|Type of fox}}
[[File:L. Trut and domestic Fox-1974.jpg|thumb|[[Lyudmila Trut]] with a domesticated silver fox, 1974]]
The '''domesticated silver fox''' (''Vulpes vulpes'' [[Form (zoology)|forma]] ''amicus'') is a form of the [[Silver fox (animal)|silver fox]] that has been to some extent [[Domestication|domesticated]] under laboratory conditions. The silver fox is a [[Melanism|melanistic]] form of the wild [[red fox]]. Domesticated silver foxes are the result of an experiment designed to demonstrate the power of [[selective breeding]] to transform species, as described by [[Charles Darwin]] in ''[[On the Origin of Species]]''.{{r|Darwin (1859)}} The experiment at the [[Institute of Cytology and Genetics]] in [[Novosibirsk]], [[Russia]], explored whether selection for behaviour rather than [[Morphology (biology)|morphology]] may have been the process that had produced [[dog]]s from [[Wolf|wolves]], by recording the changes in foxes when in each generation only the most [[Taming|tame]] foxes were allowed to breed. Many of the descendant foxes became both tamer and more dog-like in morphology, including displaying mottled- or spotted-coloured fur.{{r|Trut (1999)}}{{r|Trut (2017)}}

In 2019, an international research team questioned the conclusion that this experiment had provided strong support for the validity of [[domestication syndrome]]. They did conclude that it remains "a resource for investigation of the genomics and biology of behavior".<ref>{{Cite web|title=Famous Fox Domestication Experiment Challenged|url=https://www.the-scientist.com/news-opinion/famous-fox-domestication-experiment-challenged-66817|access-date=6 January 2021|website=The Scientist Magazine®|language=en}}</ref><ref name="lord">{{cite journal|last1=Lord|first1=Kathryn A.|last2=Larson|first2=Greger|last3=Coppinger|first3=Raymond P.|last4=Karlsson|first4=Elinor K.|year=2020|title=The History of Farm Foxes Undermines the Animal Domestication Syndrome|journal=Trends in Ecology & Evolution|volume=35|issue=2|pages=125–136|doi=10.1016/j.tree.2019.10.011|pmid=31810775|doi-access=free|bibcode=2020TEcoE..35..125L |url=https://repository.escholarship.umassmed.edu/bitstream/20.500.14038/25872/2/PIIS0169534719303027.pdf}}</ref>

==Initial beliefs and research==
[[Dmitry Belyayev (zoologist)|Dmitry Belyayev]] questioned how the diversity of canine breeds had arisen from the domestic dog's lupine ancestors. Like other scientists, he "could not figure out what mechanism could account for the differences in anatomy, physiology, and behavior" that were obvious in dogs, but he was confident that the answer lay "in the principles of [[Mendelian inheritance]]."<ref name=bestfriend>{{cite web|last=Goldman|first=Jason|title=Man's new best friend? A forgotten Russian experiment in fox domestication|url=http://blogs.scientificamerican.com/guest-blog/2010/09/06/mans-new-best-friend-a-forgotten-russian-experiment-in-fox-domestication/|publisher=Scientific American|access-date=23 May 2014|date=6 September 2010}}</ref> The genetics of domestication had also been of great interest to Darwin.

The available research concluded that domesticated animals differ in several ways from their wild counterparts. Belyayev believed that many [[Domestication of animals|domesticated animals]] had a number of [[Phenotype|phenotypic]] traits in common. This hypothesis is called the [[domestication syndrome]]; it was challenged in 2019.<ref name="lord"/>

Scientists did not know what principle of selection had guided the Neolithic farmers who had first domesticated these species thousands of years ago. Belyayev's hypothesis was that "all domesticated species had been selected for a single criterion: tameness."<ref>{{Cite news|url=https://www.livescience.com/38241-how-wolf-turned-to-dog.html|title=Darwin's Dark Knight: Scientist Risked Execution for Fox Study (Op-Ed)|work=Live Science|access-date=2 October 2017}}</ref> Belyayev further theorized that this attribute "had dragged along with it most of the other features that distinguish domestic animals from their wild forebears, like droopy ears, patches of white in the fur and changes in skull shape."<ref name=rats>{{cite web|last=Wade|first=Nicholas|title=Nice Rats, Nasty Rats: Maybe It's All in the Genes|url=https://www.nytimes.com/2006/07/25/health/25rats.html?ei=5090&en=ee8f5fbaf0576814&ex=1311480000&partner=rssuserland&emc=rss&pagewanted=all|work=The New York Times|access-date=23 May 2014|date=25 July 2006}}</ref> Jason Goldman of ''[[Scientific American]]'' said, "Belyaev hypothesized that the anatomical and physiological changes seen in domesticated animals could have been the result of selection on the basis of behavioral traits. More specifically, he believed that tameness was the critical factor."<ref name=bestfriend />

Academic Claudio J. Bidau wrote that Belyayev's suspicion was "that domestication was ruled by a process of 'destabilizing selection' affecting mechanisms of ontogenetic neuroendocrine control, either directly or indirectly in response to the appearance of a factor of stress", and that "the key factor of domestication producing striking similar results in many species is selection for tameness."<ref name=domesticate>{{cite journal |last1=Bidau |first1=Claudio J. |title=Domestication through the Centuries: Darwin's Ideas and Dmitry Belyaev's Long-Term Experiment in Silver Foxes |journal=Gayana (Concepción) |date=2009 |volume=73 |pages=55–72 |doi=10.4067/S0717-65382009000300006 |doi-access=free }}</ref>

Goldman said Belyayev wondered if a breeding program that involved "selecting for tameness and against aggression would result in [[Hormones|hormonal]] and [[Neurochemicals|neurochemical]] changes, since behavior ultimately emerged from biology. Those hormonal and chemical changes could then be implicated in anatomy and physiology. It could be that the anatomical differences in domesticated dogs were related to the genetic changes underlying the behavioral temperament for which they selected (tameness and low aggression). He believed that he could investigate these questions about domestication by attempting to domesticate wild foxes."<ref name=bestfriend /> He decided to study the silver fox and to observe how the fox responds to selective pressures for tame behaviour.<ref name="Trut">{{cite journal | last1 = Trut | first1 = Lyudmila N. | year = 1999 | title = Early Canid Domestication: The Farm-Fox Experiment | journal = American Scientist | volume = 87 | issue = 2| pages = 160–169 | doi = 10.1511/1999.2.160 | bibcode = 1999AmSci..87.....T }}</ref>

Belyayev chose the silver fox for his experiment, "because it is a social animal and is related to the dog."<ref name=rats /> The silver fox had, however, never before been domesticated. Belyayev designed a selective-breeding program for the foxes that was intended to reproduce a single major factor, namely "a strong selection pressure for tamability". This breeding experiment would be the focus of the last 26 years of Belyayev's life.{{r|Trut (1999)}}

==Domestication==
The fox species had been hard to domesticate. It would not breed in cages. Belyayev himself failed to establish a captive breeding population of [[Lutra lutra|river otter]]s unaccustomed to people. Few bred successfully in captivity and the attempt was discontinued.<ref name="lord"/>

Belyayev did not initiate the domestication process of the [[Arctic fox]], but rather began the scientifically rigorous documentation of the existing process, which had then been ongoing for 66 years. The domestication was well documented, satisfying Belyayev's desire to understand the domestication process from its inception with a given species.<ref name="lord"/>

==Experiment==
[[File:Lyudmila Trut with domesticated fox.jpg|thumb|[[Lyudmila Trut]] with a domesticated silver fox]]
[[Lyudmila Trut]] was a graduate who was chosen as manager of the program. In 1952, she began to collect the tamest foxes from fur farms. They "began with 30 male foxes and 100 vixens, most of them from a commercial fur farm in Estonia." From the beginning, Belyayev chose foxes solely for tameness, allowing only a tiny percentage of male offspring, and a slightly larger percentage of females, to breed. The foxes were not trained, in order to ensure that their tameness was a result of genetic selection and not of environmental influences. For the same reason, they spent most of their lives in cages and were permitted only brief encounters with human beings.{{r|Trut (1999)}}

Belyayev set down strict guidelines for the breeding program. Goldman said, "Starting at one month of age, and continuing every month throughout infancy, the foxes were tested for their reactions to an experimenter. The experimenter would attempt to pet and handle the fox while offering it food. In addition, the experimenters noted whether the foxes preferred to spend time with other foxes, or with humans." After the fox had reached sexual maturity at an age of seven to eight months, "they had their final test and assigned an overall tameness score." Among the factors that went into this score were the tendency "to approach an experimenter standing at the front of its home pen" and "to bite the experimenters when they tried to touch it."<ref name=bestfriend /> 

As reported on by Trut, the tests for tameness took the following form, which was still in use as of 2009: "When a pup is one month old, an experimenter offers it food from his hand while trying to stroke and handle the pup. The pups are tested twice, once in a cage and once while moving freely with other pups in an enclosure, where they can choose to make contact either with the human experimenter or with another pup. The test is repeated monthly until the pups are six or seven months old." At the age of seven or eight months, the pups are given a tameness score and placed in one of three groups. The least domesticated are in Class III; those that allow humans to pet and handle them, but that do not respond to contact with friendliness, are in Class II; the ones that are friendly with humans are in Class I. After only six generations, Belyayev and his team had to add a higher category, Class IE, the "domesticated elite", which "are eager to establish human contact, whimpering to attract attention and sniffing and licking experimenters like dogs. They start displaying this kind of behavior before they are one month old. By the 20th generation 35% were 'elite', and by the 30th generation 70% to 80% of the selected generation was 'elite.'"{{r|Trut (1999)}}

Once the foxes in each generation had been classified according to the latest research, only the least fearful and least aggressive foxes were selected for breeding. Goldman said, "In each successive generation, less than 20 percent of individuals were allowed to breed".<ref name=bestfriend /> The sole criterion for permitting them to breed was their tolerance of human contact.<ref name=rats />

==Results==
[[File:Adisey fox.JPG|thumb|Domesticated male fox in a Russian household]]
In 1978, Belyayev reported at an Invitational Lecture at the 14th International Congress of Genetics in Moscow the types of changes that were observed by Belyayev and Trut in the tame-selected foxes.<ref name="talk">{{cite journal|last1=Belyaev|first1=D.K.|title=Destabilizing selection as a factor in domestication|journal=The Journal of Heredity|date=1978|volume=70|issue=5|pages=301–308|doi=10.1093/oxfordjournals.jhered.a109263|pmid=528781}}</ref> As early as the second generation, counting from 1959, the "tameness" score of the selected population continued to increase every generation. "Tail wagging" was observed in one male fox by the fourth generation (1963).<ref name="book">{{cite book|last1=Dugatkin|first1=L.A.|last2=Trut|first2=L.N.|title=How to Tame a Fox (and Build a Dog): Visionary Scientists and a Siberian Tale of Jump-Started Evolution|date=2017|publisher=University of Chicago Press|location=Chicago|pages=240}}</ref> As early as 1962 changes in the animals' reproductive behavior started taking place. They found that some of the "tame" foxes were showing signs of [[Estrous cycle|"proestrus"]], as early as October–November, as opposed to the normal time of January–March.

By 1972, some of the females were coming into estrus in the October–November period. The males, by contrast, were not ready for mating. By 1976, the tamest females mated as early as 20 December; some of the females gave birth and then mated again in March–April.<ref name="talk"/> In the 10th generation (1969), "floppy ears" appeared in a female pup, as well as a piebald coloration on other tame pups consisting of patches of white and brown on the belly, tail, and paws. A small white "star patch" appeared in the middle of forehead of one pup also in the 10th generation.<ref name="book"/> Other correlated changes in the domesticated foxes reported by Belyaev included a shortened tail, a shortening and widening of the skull, and the tail rolled over the back.<ref name="talk"/>

The changes manifested by the tame foxes over the generations, moreover, were not only behavioral but also physiological, just as Belyayev had expected. The first physiological change detected in the tame foxes was a lower adrenaline level. Belyayev and his team "theorized that adrenaline might share a biochemical pathway with melanin, which controls pigment production in fur", a hypothesis that has since been confirmed by research.<ref name=bestfriend /> After eight to ten generations, the tame foxes began to develop multi-colored coats, a trait found more in domesticated animals than in wild ones; this was followed by the development of "floppy ears and rolled tails similar to those in some breeds of dog". After 15 to 20&nbsp;generations, a very small percentage of the tame foxes developed shorter tails and legs and underbites or overbites. The experimenters also discovered that the domesticated foxes show a "fear response" several weeks later than their wild counterparts, and that this delay is "linked to changes in plasma levels of corticosteroids, hormones concerned with an animal's adaptation to stress". After 12&nbsp;generations of selective breeding, the corticosteroid level in the tame foxes' plasma was "slightly more than half the level in a control group". After 28 to 30&nbsp;generations, "the level had halved again." At the same time, the tame foxes' brains contained higher levels of [[serotonin]]. Moreover, tame male foxes' skulls gradually became narrower, more like those of females, and litters became "on average, one pup larger".{{r|Trut (1999)}}

After over 40 generations of breeding, in short, Belyayev produced "a group of friendly, domesticated foxes who 'displayed behavioral, physiological, and anatomical characteristics that were not found in the wild population, or were found in wild foxes but with much lower frequency….Many of the domesticated foxes had floppy ears, short or curly tails, extended reproductive seasons, changes in fur coloration, and changes in the shape of their skulls, jaws, and teeth. They also lost their 'musky fox smell'."<ref name=bestfriend /> It was Belyayev's view that these new attributes, which were extremely similar to the attributes of other domesticated animals, "was the result of selection for amenability to domestication." His reasoning was that behavior is "regulated by a fine balance between neurotransmitters and hormones at the level of the whole organism ...&nbsp;. Because mammals from widely different taxonomic groups share similar regulatory mechanisms for hormones and neurochemistry, it is reasonable to believe that selecting them for similar behavior – tameness – should alter those mechanisms, and the developmental pathways they govern, in similar ways."{{r|Trut (1999)}}

Trut wrote in 1999 "that after 40 years of the experiment, and the breeding of 45,000 foxes, a group of animals had emerged that were as tame and as eager to please as a dog." Fitch described the tame foxes as "incredibly endearing". ''The New York Times'' wrote that they
: "were clean and quiet and made excellent house pets, though — being highly active — they preferred a house with a yard to an apartment. They did not like leashes, though they tolerated them."<ref name=rats/>
Ceiridwen Terrill of Concordia University, who described Belyayev's fox farm in 2012 as looking like a set of "dilapidated army barracks", with "rows and rows of sheds that house about a hundred foxes each", said that the foxes were so tame that when she reached into a cage to show one of them some affection, it plainly "loved having its belly scratched". Some of the foxes had even been trained to fetch and sit.<ref name=newbest>{{cite web |title=Domesticated Foxes: Man's New Best Friend? |url=https://www.npr.org/2012/03/18/148758624/domesticated-foxes-mans-new-best-friend |publisher=[[National Public Radio]] |access-date=16 June 2014 |date=18 March 2012}}</ref> So it was, in the words of ''[[Scientific American]]'', that
:"selecting for a single behavioral characteristic — allowing only the tamest, least fearful individuals to breed — resulted in changes not only in behavior, but also in anatomical and physiological changes that were not directly manipulated."<ref name=bestfriend/>

==Significance==
Belyayev's experimental animals and their descendants have been said to "form an unparalleled resource for studying the process and genetics of domestication".<ref name=rats/> [[Brian Hare]], a biological anthropologist, wanted to study "the unusual ability of dogs to understand human gestures". Hare
: "wanted to know if dogs' powerful rapport with humans was a quality that the original domesticators of the dog had selected for, or whether it had just come along with the tameness, as implied by Belyaev's hypothesis".<ref name=rats/> 
He discovered
: "that the fox kits from Belyaev's domesticated stock did just as well as puppies in picking up cues from people about hidden food, even though they had almost no previous experience with humans."<ref name=rats/>

Hare suggested that selection for tameness
: "may have been sufficient to produce the unusual ability of dogs to use human communicative gestures"
and that the inability of wild wolves to pick up human cues is caused by their fear of humans. While Belyayev and his team "didn't select for a smarter fox but for a nice fox",
Hare said, "they ended up getting a smart fox."

Belyayev's research, Hare further argues, has implications for the origins of human social behavior:
:"Are we domesticated in the sense of dogs? No. But I am comfortable saying that the first thing that has to happen to get a human from an apelike ancestor is a substantial increase in tolerance toward one another. There had to be a change in our social system."<ref name=natgeo>{{cite magazine |last=Ratliff |first=Evan |title=Taming the Wild |url=https://www.nationalgeographic.com/magazine/article/animal-domestication |archive-url=https://web.archive.org/web/20210410224715/https://www.nationalgeographic.com/magazine/article/animal-domestication |url-status=dead |archive-date=April 10, 2021 |magazine=National Geographic |access-date= 19 April 2021 |date=March 2011}}</ref>

Understanding the genetic reasons for wildness compared to tameness may provide more insight into human behaviour and how humans domesticated animals.<ref name=natgeo/> ''[[National Geographic]]'''s Evan Ratliff asked:
:"Out of 148&nbsp;large mammal species on Earth, why have no more than 15&nbsp;ever been domesticated? Why have we been able to tame and breed horses for thousands of years, but never their close relative the zebra, despite numerous attempts?"<ref name=natgeo/>

==After Belyayev's death==
Belyayev died of cancer in 1985. After his death, his experiment was continued by Trut, who brought international attention to it with a 1999 article in ''American Scientist''.<ref name=newsci /> By that year, after 40 years and 45,000 foxes, the experimenters had a population of 100 foxes, the product of 30 to 35 generations of selection. Trut expressed the belief in that year that "Belyayev would be pleased" with the posthumous results of his experiment, which has "compressed into a few decades an ancient process that originally unfolded over thousands of years", causing "the aggressive behavior of our herd's wild progenitors" to "entirely disappear". The experimenters, she wrote, "have watched new morphological traits emerge, a process previously known only from archaeological evidence." Trut suggested that the most important remaining question is "just how much further our selective-breeding experiment can go".{{r|Trut (1999)}}

The collapse of the Soviet Union resulted in declining funds towards scientific research, complicating Belyayev's and Trut's research continuation. They had difficulties even keeping the foxes alive. Belyayev died in 1985 before he could salvage the institute, so Trut fought to maintain the fox research. The experiment was under the supervision of Lyudmila Trut, till her death on 9th October 2024.<ref>{{Cite web |last=Mooallem |first=Jon |title=Lyudmila Trut, Who Bred Wild Foxes Into Docile Pets, Dies at 90 |url=https://www.wsj.com/arts-culture/books/lyudmila-trut-wild-foxes-dies-age-90-f4ac3ace |access-date=2025-03-02 |website=WSJ |language=en-US}}</ref><ref>{{Cite web|url=http://www.bionet.nsc.ru/en/science/applied-research/domestication-of-foxes-and-problems-of-modern-animal-breeding.html|title=Domestication of foxes and problems of modern animal breeding|website=www.bionet.nsc.ru|access-date=5 July 2016}}</ref><ref>{{cite web|url=https://www.pbs.org/newshour/science/domesticated-foxes-genetically-fascinating-terrible-pets|title=Why domesticated foxes are genetically fascinating (and terrible pets)|work=pbs.org|date=31 March 2017}}</ref>{{r|Trut (2017)}} When Anna Kukekova, a Russian-born postdoctoral researcher in molecular genetics at [[Cornell University]], read about the project's financial difficulties, she secured funding from the [[National Institutes of Health]] and joined in Trut's effort to complete Belyayev's work, making it a joint Russian-American initiative.<ref name=natgeo /><ref>{{cite journal|last1=Hare|first1=Brian|title=Social Cognitive Evolution in Captive Foxes Is a Correlated By-Product of Experimental Domestication|journal=Current Biology|volume=15|issue=3|pages=226–230|pmid=15694305|display-authors=etal|year=2005|doi=10.1016/j.cub.2005.01.040|s2cid=1592440|doi-access=free|bibcode=2005CBio...15..226H }}</ref>{{r|Ratliff (2011)}}


==Further research==
The results from the experiments led the scientists at the institute to research domestication of other animals, such as rats in 1972, [[mink]], and [[European otter|river otter]]s.{{r|Ratliff (2011)}} Similar research was carried out in Denmark with [[American mink]]s, producing the [[domestic mink]].{{r|Price (2008)}} The project also bred the least-tameable foxes to study social behavior in canids. These foxes avoided human contact, as do their wild behavioral phenotypes.{{r|Trut (2017)}}{{r|Trut (2012)}}

Detailed genetic and physiological studies on the foxes have been done by Trut and colleagues. For example, the "star-shaped" pattern was found to be controlled by one dominant gene that was incompletely [[Penetrance|penetrant]], "but its penetrance is significantly higher in offspring from tame mothers than from aggressive ones..."<ref>{{cite journal|last1=Belyaev|first1=D. K.|last2=Ruvinsky|first2=A. O.|last3=Trut|first3=L. N.|title=Inherited activation-inactivation of the star gene in foxes: Its bearing on the problem of domestication|journal=The Journal of Heredity|date=1981|volume=72|issue=4|pages=264–274|doi=10.1093/oxfordjournals.jhered.a109494|pmid=7288139|doi-access=}}</ref> Trut reported that female foxes heterozygous for the gene controlling the star pattern also influenced the number of male pups, increasing the number of males over the expected 50%. As the fox experiment has progressed over time, it was found that in general the number of male pups increased over the expected 50% to approximately 54%.<ref>{{cite journal|last1=Trut|first1=L. N.|title=Sex ratio in silver foxes: effects of domestication and the star gene|journal=Theoretical and Applied Genetics|date=1996|volume=92|issue=1|pages=109–115|doi=10.1007/s001220050100|pmid=24166124}}</ref>

Early in the experiment, Trut and Belyaev started comparing the hormonal responses of the tame and control foxes.<ref name="talk"/><ref name="Trut (2012)"/> They showed that selection for tame behavior caused the levels of [[Corticosteroid|11-oxycorticosteroids]] in the blood to be reduced; selection had also caused the morphology of adrenal glands to change. Levels of the sex hormones [[estradiol]] and [[progesterone]] differed. Belyaev stated: "Perhaps the most important observation emerging from this series of experiments is the fact that tame females exhibit statistically significant changes in certain neurochemical characteristics in such regions of the brain as the hypothalamus, midbrain, and hippocampus. The level of [[serotonin]] and its metabolite 5-hydroxyindoleacetic acid turned out to be higher in tame than in unselected females. This fact fits the type of behavior, since serotonin is known to inhibit some kinds of aggression. Serotonin plays a role in the central regulation of the [[Hypothalamic–pituitary–adrenal axis|hypothalmic-hypophyseal-adrenal]]-sexual system. Thus, selection for tame behavior is associated with changes in both the central and peripheral mechanisms of the neuro-endocrine control of [[ontogeny]]."<ref name="talk"/>

Trut and her colleagues have applied modern molecular techniques to the fox populations with the aim of not only identifying which genes are involved in domestication, but also in determining how changes in the fox genome compare to those of the domesticated dog.<ref name="map">{{cite journal|last1=Kukekova|first1=A.V.|last2=Trut|first2=L.N.|last3=Oskina|first3=I.N.|last4=Kharlamova|first4=A.V.|last5=Shikhevich|first5=S.G.|last6=Kirkness|first6=E.F.|last7=Aguirre|first7=G.D.|last8=Acland|first8=G.M.|title=A marker set for construction of a genetic map of the silver fox (''Vulpes vulpes'')|journal=Journal of Heredity|date=2004|volume=95|issue=3|pages=185–194|doi=10.1093/jhered/esh033|pmid=15220384|doi-access=free}}</ref><ref name="map2">{{cite journal|last1=Kukekova|first1=A.V.|last2=Trtu|first2=L.N.|last3=Oskina|first3=I.N.|last4=Johnson|first4=J.L.|last5=Temnykh|first5=S.V.|last6=Kharlamova|first6=A.V.|last7=Shepeleva|first7=D.V.|last8=Gulievich|first8=R.G.|last9=Shikhevich|first9=S.G.|last10=Graphodatsky|first10=A.S.|last11=Aquirre|first11=G.D.|last12=Acland|first12=G.M.|title=A meiotic linkage map of the silver fox, aligned and compared to the canine genome|journal=Genome Research|date=2007|volume=17|issue=3|pages=387–399|doi=10.1101/gr.5893307|pmid=17284676|pmc=1800930|doi-access=free}}</ref><ref>{{cite journal|last1=Kukekova|first1=A.V.|last2=Trut|first2=L.N.|last3=Chase|first3=K.|last4=Shepeleva|first4=D.V.|last5=Vladimirova|first5=A.V.|last6=Kharlamova|first6=A.V.|last7=Oskina|first7=I.N.|last8=Stepika|first8=A.|last9=Klebanov|first9=S.|last10=Erb|first10=H.N.|last11=Acland|first11=G.M.|title=Measurement of segregating behaviors in experimental silver fox pedigrees|journal=Behavior Genetics|date=2008|volume=38|issue=2|pages=185–194|doi=10.1007/s10519-007-9180-1|pmc=2374754|pmid=18030612}}</ref><ref name="loci">{{cite journal|last1=Kukekova|first1=A.V.|last2=Trut|first2=L.N.|last3=Chase|first3=K.|last4=Kharlamova|first4=A.V.|last5=Johnson|first5=J.L.|last6=Temnykh|first6=S.V.|last7=Oskina|first7=I.N.|last8=Gulevich|first8=R.G.|last9=Vladimirova|first9=A.V.|last10=Klebanov|first10=S.|last11=Shepeleva|first11=D.V.|last12=Shikhevich|first12=S.G.|last13=Acland|first13=G.M.|last14=Lark|first14=K.G.|title=Mapping loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype|journal=Behavior Genetics|date=2011|volume=41|issue=4|pages=593–606|doi=10.1007/s10519-010-9418-1|pmc=3076541|pmid=21153916}}</ref> 400 canine microsatellites that are evenly distributed across the canine genome were analyzed in the fox genome. Based on amounts of homozygosity in both tame and aggressive foxes, it was found that there was no evidence of inbreeding between the two groups of foxes. In order to help understand the neurobiology of behavior, fox and dog orthologs of [[serotonin]] receptor genes were cloned.<ref name="map"/> Using 320 microsatellites Trut and co-workers showed that all 16 fox [[autosomes]] and one X chromosome were covered, and that there was a high conservation of marker order between homologous regions of foxes and dogs, even though the fox genome has 16 pairs of [[Centromere|metacentric]] [[autosomes]] and the dog has 37 pairs of [[Centromere|acrocentric]] [[autosomes]].<ref name="map2"/> Additional studies by these workers has shown that "tameness" and "aggressiveness" is associated with at least two loci.<ref name="loci"/>

In 2005, [[DNA microarrays]] were utilized to find the differences in genetic expression between domesticated, non-domesticated (farm-raised), and wild foxes. It was found that there was a difference of 40 gene expressions between the domesticated and non-domesticated foxes. Although there was a difference in the genes of the three groups, the experimenters did not look into the behavioural and functional consequences of these differences.<ref>{{cite journal | last1 = Lindberg | first1 = Julia | last2 = Björnerfeldt | first2 = Susanne | last3 = Saetre | first3 = Peter | last4 = Svartberg | first4 = Kenth | last5 = Seehuus | first5 = Birgitte | last6 = Bakken | first6 = Morten | last7 = Vilà | first7 = Carles | last8 = Jazin | first8 = Elena | year = 2005 | title = Selection for tameness has changed brain gene expression in silver foxes | journal = Current Biology | volume = 15 | issue = 22| pages = R915–6 | doi = 10.1016/j.cub.2005.11.009 | pmid = 16303546 | s2cid = 15140061 | doi-access = free | bibcode = 2005CBio...15.R915L }}</ref> In 2007, a system of measuring fox behavior was described that is expected to be useful in [[Quantitative trait locus|QTL mapping]] to explore the genetic basis of tame and aggressive behavior in foxes.{{r|Kukekova (2007)}}

===Breeding for aggression===
After initiating his selective breeding program for tameness, Belyayev also began breeding a line of fearful, aggressive foxes.<ref name=bestfriend/> In addition, he started domesticating other animals. He and his team started working with rats in 1972, and later with minks and, briefly, with river otters, although this last experiment was abandoned because the species "proved difficult to breed". The experiments with rats and minks, however, proved successful, with the subjects becoming tame alongside the foxes.<ref name=natgeo/> After Belyayev's death, his rat experiment was carried on by Irina Plyusnina. "Siberian gray rats caught in the wild, bred separately for tameness and for ferocity", reported ''[[The New York Times]]'', "have developed ... entirely different behaviors in only&nbsp;60 or so generations".<ref name=rats/> When geneticist [[Svante Pääbo]] was in Novosibirsk in 2003, he visited the institute, and "was stunned" by the two groups of rats. "After just 30&nbsp;years of selection", Pääbo said, "the IC&G researchers had fashioned two populations that could hardly be more different."<ref name=newsci>
{{cite magazine
 |last=Nicholls |first=Henry
 |date=5 October 2009
|title=My little zebra: The secrets of domestication
 |magazine=[[New Scientist]]
 |url=https://www.newscientist.com/article/mg20427281.500-my-little-zebra-the-secrets-of-domestication.html
 |access-date=16 June 2014
}}
</ref>

In 2006, Frank Albert, a graduate student at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, was helping to continue Belyayev's work by studying the genetic roots of the differences between the tame and hyper-aggressive rats.<ref name=rats/> In 2009, Albert and several colleagues published a paper in ''[[Genetics (journal)|Genetics]]''<ref name=Albert-Carlborg-etal-2009/> about the results of their cross-breeding of tame and hyper-aggressive rats, a stock of which they had established in Leipzig.<ref name=Albert-Carlborg-etal-2009>
{{cite journal
 |author1=Albert, F.W.   |author2=Carlborg, Ö.
 |author3=Plyusnina, I.  |author4=Besnier, F.
 |author5=Hedwig, D.     |author6=Lautenschläger, S.
 |author7=Lorenz, D.     |author8=McIntosh, J.
 |author9=Neumann, C.    |author10=Richter, H.
 |author11=Zeising, C.   |author12=Kozhemyakina, R.
 |author13=Shchepina, O. |author14=Kratzsch, J.
 |author15=Trut, L.      |author16=Teupser, D.
 |author17=Thiery, J.    |author18=Schöneberg, T.
 |author19=Andersson, L. |author20=Pääbo, S. 
 |display-authors=6
 |year=2009
 |title=Genetic architecture of tameness in a rat model of animal domestication
 |journal=Genetics
 |volume=182  |issue=2  |pages=541–554
 |pmc=2691762  |doi=10.1534/genetics.109.102186
 |pmid=19363126
 |url=http://www.zora.uzh.ch/100828/1/541.full.pdf
}}
</ref> In 2011, it was reported that Albert's team had "found several key regions of the genome that have a strong effect on tameness" and that they suspected the involvement of "at least half a dozen genes". The next step was "to locate individual genes that influence tameness and aggression".<ref name=newsci/>

[[Elaine Ostrander]] of the [[National Human Genome Research Institute]] at the [[National Institutes of Health]] told ''[[National Geographic]]'' in 2011, "Understanding what has changed in these animals is going to be incredibly informative. Everyone is waiting with great excitement for what they come out with."<ref name=natgeo/>

==Status==
In 2014, officials stated that the number of foxes was never reduced and is still stable at about 2,000&nbsp;foxes.{{r|End}} {{as of|2016|August}}, there are 270&nbsp;tame vixens and 70&nbsp;tame dogs on the farm.<ref>{{cite news |url=http://www.bbc.com/earth/story/20160912-a-soviet-scientist-created-the-only-tame-foxes-in-the-world |title=A Soviet scientist created the only tame foxes in the world |website=BBC Earth |date=13 September 2016}}</ref>{{r|Trut (2017)}}

The suggestion has been made "that the foxes be made available as pets, partly to ensure their survival should the Novosibirsk colony be wiped out by disease". [[Raymond Coppinger]], a dog biologist at Hampshire College in Massachusetts, noted that at one time "Soviet science was in a desperate state and Belyayev's foxes were endangered", but his own efforts "to obtain some of the foxes to help preserve them" had been unsuccessful, with the animals apparently having "left Russia only once, for Finland, in a colony that no longer survives".<ref name=rats/> The author of the ''[[National Geographic]]'' article about the experiments, however, said that his translator, Luda Mekertycheva, had adopted two foxes from Novosibirsk and that they had proven to be wonderful companions who "jump on my back when I kneel to give them food, sit when I pet them, and take vitamins from my hand".<ref name=natgeo/>

Between 2010 and 2012, a firm called "SibFox" was advertising foxes from the Novosibirsk lab for about $6,000 apiece, although, according to ''[[Popular Science]]'', "it's not clear that anyone ever actually received one of these foxes." Reportedly, "two foxes that actually shipped to the States ended up confiscated at the U.S. border and shipped to the Austin Zoo and Animal Sanctuary."<ref name=petfox>{{cite magazine |last=Nosowitz |first=Dan |title=Can I have a pet fox? |url=http://www.popsci.com/science/article/2012-10/fyi-domesticated-foxes?nopaging=1 |magazine=[[Popular Science]] |access-date=16 June 2014|date=23 June 2013}}</ref><ref name=sibfox>{{cite web |title=Sibfox FAQ |url=http://sibfox.com/faq/# |access-date=16 June 2014 |url-status=dead |archive-url=https://web.archive.org/web/20120220115333/http://sibfox.com/faq/ |archive-date=20 February 2012 }}</ref>

The sculpture "Dmitriy Belyaev and Domesticated Fox" was built near Institute of Cytology and Genetics (Novosibirsk) in the honor of the 100th anniversary of the birth of Dmitry Konstantinovich Belyaev. The tamed fox gives the scientist a paw and wags its tail. Konstantin Zinich, sculptor (Krasnoyarsk):

{{quote|The philosophy of touching a fox and a man is rapprochement, kindness, there is no aggression from the fox – it was wild, and he made it genetically domesticated.<ref>{{cite web |url=http://www.bionet.nsc.ru/index/press-czentr/pressa-o-nas/2017/08/09/v-novosibirske-otkryili-pamyatnik-uchenomu-s-dobroj-lisoj/ |title=В Новосибирске открыли памятник ученому с доброй лисой &#124; ИЦиГ |publisher=www.bionet.nsc.ru}}</ref>}}

Its opening was held as part of the ''Belyaev Conference 2017''.<ref>{{cite web |title=Belyaev Conference 2017 |language=en |publisher=conf.bionet.nsc.ru |url=http://conf.bionet.nsc.ru/belyaev100/en/ |access-date=17 June 2021 |url-status=live|archive-url=https://web.archive.org/web/20170228100947/http://conf.bionet.nsc.ru:80/belyaev100/en/ |archive-date=28 February 2017 }}</ref><ref>{{cite journal |first1=Yuriy L. |last1=Orlov |first2=Ancha V. |last2=Baranova |first3=Yuriy E. |last3=Herbeck |date=28 December 2017 |title=Evolutionary Biology at Belyaev Conference – 2017 |journal=BMC Evolutionary Biology |volume=17 |issue=2 |pages=260 |doi=10.1186/s12862-017-1102-0 |pmid=29297302 |pmc=5751664 |doi-access=free |bibcode=2017BMCEE..17S.260O }}</ref>

As of 2023, 12 sterilized foxes have been exported from the Institute of Cytology and Genetics to the Judith A. Bassett Canid Education and Conservation Center in Santa Ysabel, California.<ref>{{cite web |last1=Trabulsi |first1=Maya |title=Outfoxing the wild: How Russian domesticated foxes could save lives |url=https://www.kpbs.org/news/local/2023/04/28/russian-domesticated-foxes-trained-nosework-save-lives-santa-ysabel |website=KPBS Public Media |access-date=12 October 2023 |ref=kpbs |language=en |date=28 April 2023}}</ref>

==Criticisms==
Elinor Karlsson, a biologist at the [[University of Massachusetts Medical School]], and colleagues published a paper on December 3, 2019, in ''Trends in Ecology and Evolution'' arguing domestication syndrome may not actually exist, that the foxes were not totally wild to begin with, and that some of the traits attributed to domestication existed long before the experiment began.<ref name=":0">{{cite web |first1=Jake |last1=Buehler |url=https://www.sciencenews.org/article/russian-foxes-tameness-domestication | title=Foxes bred for tameness may not be the domestication story we thought | date=31 December 2019 |website=Science News }}</ref><ref>{{cite journal | url=https://ora.ox.ac.uk/objects/uuid:78fcafc9-55d3-4675-ac3e-d9f08c33e33a/files/m1eb6249648b367354e0db3da43763a49 | doi=10.1016/j.tree.2019.10.011 | title=The History of Farm Foxes Undermines the Animal Domestication Syndrome | date=2020 | last1=Lord | first1=Kathryn A. | last2=Larson | first2=Greger | last3=Coppinger | first3=Raymond P. | last4=Karlsson | first4=Elinor K. | journal=Trends in Ecology & Evolution | volume=35 | issue=2 | pages=125–136 | pmid=31810775 | bibcode=2020TEcoE..35..125L | doi-access=free }}</ref> Karlsson does not question the value of the experiment, instead calling for a focus on other issues and downplaying or rejecting the "domestication syndrome" hypothesis. Conversely, Adam Wilkins of Humboldt University of Berlin, challenges Karlsson's criticisms, analyzing how subtle developmental causes can produce an array of diverse and non-uniform "domestication syndrome" effects in different species.<ref>{{Cite journal |last=Wilkins |first=Adam S. |date=1 July 2014 |title=The "Domestication Syndrome" in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics |journal=Genetics |volume=197 |issue=3 |pages=795–808 |doi=10.1534/genetics.114.165423 |pmid=25024034 |pmc=4096361 }}</ref> Lee Alan Dugatkin further notes that the evidence that the foxes were already part-domesticated is slim and equivocal, and that the foxes did in fact gain new traits only after the experiment began: “It’s extraordinarily unlikely that there was kind of hidden genetic variation for these traits.”<ref name=":0" />

==See also==
* [[de novo domestication|''De novo'' domestication]]
* [[Experimental evolution]]
* [[Fuegian dog]], an extinct domesticated South American fox
* [[Genomics of domestication]]
* [[Neoteny]]
* [[List of domesticated animals]]

==References==
{{reflist|25em|refs=
<ref name="Darwin (1859)">
{{cite book
 |last=Darwin  |first=Charles
 |title=On the Origin of Species
 |quote=by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life
 |orig-year=1859 |year=1963
 |publisher=Heritage Press
 |location=Norwalk, CT
 |edition=reprint
 |at=Chapter&nbsp;1
}}
</ref>
<ref name="Trut (2017)">
{{cite book 
 |last1=Trut     |first1=Lyudmila
 |last2=Dugatkin |first2=Lee Alan
 |date=23 March 2017
|title=How to Tame a Fox (and Build a Dog): Visionary scientists and a Siberian tale of jump-started evolution
 |publisher=University of Chicago Press
 |location=Chicago, IL
 |isbn=978-0226444185
 |edition=1st
}}
</ref>
<ref name="End">
{{cite web
 |title=Конец Эксперимента. Ученые Уничтожают Ручных Лисиц и Норок
 |language=ru
 |trans-title=The end of an experiment: Scientists kill domesticated foxes and minks
 |url=http://smartnews.ru/regions/novosibirsk/9289.html#item-160304
 |website=Smartnews.ru
}}
</ref>
<ref name="Kukekova (2007)">
{{cite journal
 |last1=Kukekova |first1=A.V.      |last2=Trut       |first2=L.N.
 |last3=Chase    |first3=K.        |last4=Shepeleva  |first4=D.V.
 |last5=Vladimirova |first5=A.V.   |last6=Kharlamova |first6=A.V.
 |last7=Oskina   |first7=I.N.      |last8=Stepika    |first8=A.
 |last9=Klebanov |first9=S.        |last10=Erb       |first10=H.N.
 |last11=Acland  |first11=G.M.
 |display-authors=6
 |year=2007
 |title=Measurement of segregating behaviors in experimental silver fox pedigrees
 |journal=Behavior Genetics
 |volume=38  |issue=2  |pages=185–94
 |pmid=18030612 |pmc=2374754 |doi=10.1007/s10519-007-9180-1
}}
</ref>

<ref name="Price (2008)">
{{cite book
 |last=Price |first=Edward
 |year=2008
 |title=Principles and Applications of Domestic Animal Behavior
 |page=229
 |publisher=Cambridge University Press
 |access-date=7 January 2016
|url=https://books.google.com/books?id=Ww07sIWTYAAC&pg=PA229
 |isbn=9781780640556
}}
</ref>
<ref name="Ratliff (2011)">
{{cite magazine
 |last=Ratliff |first=Evan
 |date=March 2011
 |title=Animal domestication: Taming the wild
 |magazine=[[National Geographic]]
 |page=2
 |url=http://ngm.nationalgeographic.com/2011/03/taming-wild-animals/ratliff-text/2
 |url-status=dead
 |archive-url=https://web.archive.org/web/20151122033644/http://ngm.nationalgeographic.com/2011/03/taming-wild-animals/ratliff-text/2
 |archive-date=22 November 2015
}}
</ref>
<ref name="Trut (1999)">
{{cite journal
 |last1=Trut |first1=Lyudmila
 |title=Early canid domestication: The farm-fox experiment
 |year=1999
 |journal=[[American Scientist]]
 |volume=87  |issue=2  |page=160
 |doi=10.1511/1999.2.160 |jstor=27857815
 |bibcode=1999AmSci..87.....T
}}
</ref>
<ref name="Trut (2012)">
{{cite book
 |last1=Trut |first1=Lyudmila N.
 |last2=Oskina |first2=Irina N.
 |last3=Kharlamova |first3=Anastasiya V.
 |date=2012
 |article=Experimental studies of early canid domestication
 |editor-last1=Ostrander |editor-first1=Elaine A.
 |editor-last2=Ruvinsky |editor-first2=Anatoly
 |title=Genetics of the Dog
 |edition=2nd  |pages=12–37
 |publisher=CAB International
 |isbn=9781845939410
 |url=https://books.google.com/books?id=R-C3D2QBGsgC&pg=PA12
 |access-date=12 January 2016
}}
</ref>

}} <!-- end of "refs=" -->

==External links==
* [http://www.bionet.nsc.ru/en Institute of Cytology and Genetics]
* [http://www.bionet.nsc.ru/booklet/Engl/EnglLabaratories/LabEvolutionaryGeneticsAnimalsEngl.html Laboratory of Evolutionary Genetics of Animals]
* [http://en.metkere.com/2014/07/foxes.html Foxes, stress and evolution]
* [http://cbsu.tc.cornell.edu/ccgr/behaviour/Index.htm Fox Domestication]: website from Cornell University with detailed information (videos and articles)
* [https://web.archive.org/web/20100215131052/http://www.hum.utah.edu/~bbenham/2510%20Spring%2009/Behavior%20Genetics/Farm-Fox%20Experiment.pdf The Fox Farm Experiment], ''American Scientist''

{{Animal domestication}}
{{Domestic dog}}

[[Category:Foxes]]
[[Category:Selection]]
[[Category:Animal breeding]]
[[Category:Domesticated foxes]]
[[Category:Mammals as pets|Silver fox]]
[[Category:Animals in captivity|Silver fox]]
[[Category:Research in the Soviet Union]]
[[Category:Animal breeds originating in the Soviet Union]]
[[Category:Domestication of particular species]]
[[Category:Dog breeds originating in the Soviet Union]]