Domesticated silver fox
The domesticated silver fox 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
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.
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." 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."
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."
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. He believed that he could investigate these questions about domestication by attempting to domesticate wild foxes." He decided to study the silver fox and to observe how the fox responds to selective pressures for tame behaviour.
Belyayev chose the silver fox for his experiment, "because it is a social animal and is related to the dog." 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.
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 river otters unaccustomed to people. Few bred successfully in captivity and the attempt was discontinued.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.
Experiment
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.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."
As reported on by Trut, the tests for tameness took the following form, which was still in use as of 2009: "When a cub is one month old, an experimenter offers it food from his hand while trying to stroke and handle the cub. The cubs are tested twice, once in a cage and once while moving freely with other cubs in an enclosure, where they can choose to make contact either with the human experimenter or with another cub. The test is repeated monthly until the cubs are six or seven months old." At the age of seven or eight months, the cubs 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'."
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". The sole criterion for permitting them to breed was their tolerance of human contact.
Results
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. 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. 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. In the tenth generation, floppy ears appeared in a female cub, as well as a piebald coloration on other tame cubs consisting of patches of white and brown on the belly, tail, and paws. A small white star patch appeared on the center of the forehead of one cub also in the tenth generation. 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.
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. 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 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 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 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 cub larger".
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'." 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... . 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."
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." 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. 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."