thumb|[[Lyudmila Trut with a domesticated silver fox, 1974]]

The domesticated silver fox (Vulpes vulpes forma amicus) is a form of the silver fox, a melanistic form of the wild red fox, that has been to some extent domesticated under laboratory conditions. 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. The experiment at the Institute of Cytology and Genetics in Novosibirsk, Russia, explored whether selection for behaviour rather than morphology may have been the process that had produced dogs from wolves, by recording the changes in foxes when in each generation only the most 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.

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".

Initial beliefs and research

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."

The available research concluded that domesticated animals differ in several ways from their wild counterparts. Belyayev believed that many domesticated animals had a number of phenotypic traits in common. This hypothesis is called the domestication syndrome; it was challenged in 2019. 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." 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."

Goldman said Belyayev wondered if a breeding program that involved "selecting for tameness and against aggression would result in hormonal and 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."

Belyayev chose the silver fox for his experiment, "because it is a social animal and is related to the dog." 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). 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 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. 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."

Understanding the genetic reasons for wildness compared to tameness may provide more insight into human behaviour and how humans domesticated animals. 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.

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 river otters. Similar research was carried out in Denmark with American minks, producing the domestic mink. 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.

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 penetrant, "but its penetrance is significantly higher in offspring from tame mothers than from aggressive ones". Trut reported that female foxes heterozygous for the gene controlling the star pattern also influenced the number of male cubs, 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 cubs increased over the expected 50% to approximately 54%.

Early in the experiment, Trut and Belyaev started comparing the hormonal responses of the tame and control foxes. 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. In 2007, a system of measuring fox behavior was described that is expected to be useful in QTL mapping to explore the genetic basis of tame and aggressive behavior in foxes.

Breeding for aggression

After initiating his selective breeding program for tameness, Belyayev also began breeding a line of fearful, aggressive foxes.

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. 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".

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, US 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".

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

Its opening was held as part of the Belyaev Conference 2017.

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, US.

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. 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. 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."

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  • Institute of Cytology and Genetics
  • Laboratory of Evolutionary Genetics of Animals
  • Foxes, stress and evolution
  • Fox Domestication: website from Cornell University with detailed information (videos and articles)
  • The Fox Farm Experiment, American Scientist