Dmitry Konstantinovich Belyaev
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Dmitri Konstantinovich Belyaev (Russian: Дмитрий Константинович Беляев, 17 July 1917 – 14 November 1985) was a Russian geneticist who served as director of the Institute of Cytology and Genetics (IC&G) of the Soviet Academy of Sciences from 1959 to 1985. His decades-long effort to breed domesticated foxes has been described by the New York Times as “arguably the most extraordinary breeding experiment ever conducted.” A 2010 article in Scientific American stated that Belyaev “may be the man most responsible for our understanding of the process by which wolves were domesticated into our canine companions.”
Beginning in the 1950s, in order to uncover the genetic basis of the distinctive behavioral and physiological attributes of domesticated animals, Belyaev and his team spent decades breeding the wild silver fox (Vulpes vulpes) and selecting for reproduction only those individuals in each generation that showed the least fear of humans. After several generations of controlled breeding, a majority of the silver foxes no longer showed any fear of humans and often wagged their tails and licked their human caretakers to show affection. They also began to display spotted coats, floppy ears, curled tails, as well as other physical attributes often found in domesticated animals, thus confirming Belyaev’s hypothesis that both the behavioral and physical traits of domesticated animals could be traced to “a collection of genes that conferred a propensity to tameness—a genotype that the foxes perhaps shared with any species that could be domesticated.”
Belyaev, who especially during the early years of his experiment was risking his life by defying the anti-Darwinian, anti-Mendelian Soviet scientific establishment, has been recognized in recent years by major scientific journals as a pioneering figure in modern genetics.
Early life and education
Belyaev was born on July 17, 1917, in Protasovo, a town in the Russian province of Kostroma. He was his family’s fourth and youngest son. His father, Konstantin Pavlovich, was a priest. His brother Nikolai, who was 18 years his senior, was a prominent geneticist who worked with Sergei Sergeievich Tchetverikov (1880-1959), a pioneer of population genetics.
“It was his brother's influence that caused him to have this special interest in genetics,” Belyaev’s protégé, Lyudmilla Trut, later said. Both Belyaev brothers were Darwinists and believers in Mendelian genetics. At the time Belyaev came of age, however, life was dangerous in the Soviet Union for genetics with such views, because the Stalinist regime supported the scientific theories of agronomist Trofim Lysenko and outlawed research inspired by the rival views of Gregor Mendel. As Trut recalled, “genetics was considered fake science.” Indeed, under the rule of Stalin, leading geneticists who believed in Darwinian evolution and Mendelian genetics were considered enemies of the state. Several of them were sent to prison, and at least one, Nikolai Ivanovich Vavilov, was sentenced to death. Nikolai Konstantinovich Belyaev was arrested in August 1937, and was executed without a trial on November 10 of that year.
The next year, Dmitri Konstantinovich Belyaev graduated from the Ivanovo Agricultural Institute and began working in the Department of Fur Animal Breeding at the Central Research Laboratory in Moscow, which was affiliated with the Ministry of Foreign Trade. In 1941, he was conscripted into the military, and was wounded and received several military decorations. He then resumed work at the laboratory.
Despite the persecution of adherents of Darwinism and Mendelian genetics, Belyaev wrote a dissertation on “The variation and inheritance of silver-colored fur in silver-black foxes” and continued to hold fast to his belief in evolution and Mendelian genetics. Still, to be safe, he disguised his genetics research as studies in animal physiology. Nonetheless, his known interest in genetics led in 1948 to his dismissal from his position as head of the Department of Fur Animal Breeding.
After the death of Stalin in 1953, the Soviet persecution of geneticists began to ease. From 1958 to the end of his life, Belyaev worked for the Siberian Division of the USSR Academy of Sciences, which he helped found. In 1963, he became Director of the Institute of Cytology and Genetics (IC&G) in Novosibirsk, and held that position until his death. Under his leadership, according to one source, “the institute became a center of basic and applied research in both classical genetics and modern molecular genetics.”
Belyaev’s fox experiment
In Siberia, Belyaev “was able to study genetics in relative freedom,” according to the New York Times. One subject that fascinated him was the question of how such a remarkable 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 genetics of domestication had also been of great interest to Darwin. It was recognized that domesticated animals differ in several ways from their wild counterparts, but it was not known what principle of selection had guided the Neolithic farmers who had first domesticated these species thousands of years ago. Belyaev’s hypothesis was that “all domesticated species had been selected for a single criterion: tameness.”
Belyaev 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.” In other words, “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.” In more scientific terms, Belyaev’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.”
In the words of a 2010 article in Scientific American, Belyaev 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.”
Belyaev chose the silver fox, Vulpus vulpus, a variant of the red 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. Belyaev 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 Belyaev’s life.
In 1958, then, Belyaev asked his assistant Lyudmila Trut, who was then a graduate student, to visit various Soviet fur farms and to “select the calmest foxes she could find, to serve as the base population for Belyaev's experiment” at the then-new IC&G. They “began with 30 male foxes and 100 vixens, most of them from a commercial fur farm in Estonia.” From the beginning, Belyaev 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.
As a 2011 article in National Geographic put it, Belyaev’s goal was “to unlock domestication's molecular mysteries.” Darwin had shown that domesticated animals “tend to be smaller, with floppier ears and curlier tails than their untamed progenitors,” attributes that “tend to make animals appear appealingly juvenile to humans.” Also, they often have spotted coats, “while their wild ancestors' coats are solid.” These and other traits “exist in varying degrees across a remarkably wide range of species, from dogs, pigs, and cows to some nonmammalians like chickens, and even a few fish.” Belyaev proposed that as animals grew tamer through selective breeding, such traits might begin to appear. Animal-behavior expert Tecumseh Fitch has stated that the experiment’s “audacity” is “difficult to overestimate,” given that the “selection process on dogs, horses, cattle or other species had occurred, mostly unconsciously, over thousands of years…the idea that Belyaev’s experiment might succeed in a human lifetime must have seemed bold indeed.”
Breeding and testing
The experiment began in 1959, at a time “when Soviet genetics was starting to recover from the anti-Darwinian ideology of Trofim Lysenko.” Still, in order to avoid interference by the authorities, Belyaev continued to frame his research “only in terms of physiology, leaving out any mention of genes.” Trut later recalled “that when Soviet leader Nikita Khrushchev arrived to inspect the institute, he was overheard to say, ‘What, are those geneticists still around? Were they not destroyed?’” But Belyaev enjoyed the protection of his boss’s “careful politics” and was also helped by “favorable articles on genetics written by Khrushchev's journalist daughter.”
Belyaev set down strict guidelines for the breeding program. “Starting at one month of age, and continuing every month throughout infancy,” according to Scientific American, “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 hang out 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.” By way of ensuring that the pups’ tameness was a result of genetic selection and not of interactions with human beings, the foxes were not subjected to any kind of training and were only permitted brief periods of contact with people.
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 human 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, Belyaev 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.”
Once the foxes in each generation had been classified in this manner, only the least fearful and least aggressive foxes were selected for breeding. “In each successive generation, less than 20 percent of individuals were allowed to breed,” and the sole criterion for permitting them to breed was “their tolerance of human contact.”
Within a very short time, Belyaev’s experiment began to show results. “By 1964 the fourth generation was already beginning to live up to the researchers' hopes,” reported National Geographic. “Trut can still remember the moment when she first saw a fox wag its tail at her approach. Before long, the most tame among them were so doglike that they would leap into researchers' arms and lick their faces. At times the extent of the animals' tameness surprised even the researchers. Once, in the 1970s, a worker took one of the foxes home temporarily as a pet. When Trut visited him, she found the owner taking his fox for walks, unleashed, ‘just like a dog. I said “Don't do that, we'll lose it, and it belongs to the institute!”’ she recalls. ‘He said “just wait,” then he whistled and said, “Coca!” It came right back.’” By the time the selectively bred foxes had reached their tenth generation, 18 percent of the fox puppies were in the elite category; by the 20th generation, that figure had climbed to 35 percent. As of 2009, elite foxes made up 70 to 80 percent of the population.
The changes manifested by the tame foxes over the generations, moreover, were not only behavioral but also physiological, just as Belyaev had expected. The first physiological change detected in the tame foxes was a lower adrenaline level. Belyaev 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. As they became tamer, more and more of the foxes began showing “signs of the domestication phenotype”; Trut later recalled that in the early 1980s “we observed a kind of explosion-like change of the external appearance.” After eight to ten generations, the tame foxes began to develop particolored 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 pup larger.”
After over 40 generations of breeding, in short, Belyaev 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 Belyaev’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 herself 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 Belyaev’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.”
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.” Ray Coppinger, a dog biologist at Hampshire College in Massachusetts, noted that at one time “Soviet science was in a desperate state and Belyaev’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 author of the National Geographic article about the experiments, however, noted 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.” In 2010-12, 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 US border and shipped to the Austin Zoo and Animal Sanctuary.” In 2011, two Americans set up a website through which Americans could order foxes from the lab, but as of April 2014 the site no longer existed.
After initiating his selective breeding program for tameness, Belyaev also began breeding a line of fearful, aggressive foxes. In addition, he started domesticating other animals. He and his team started working with rats in 1972, and later with mink, 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. After Belyaev’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 60 or so generations,” reported the Times. When geneticist Svante Pääbo was in Novosibirsk in 2003, he visited the institute, and “was stunned” by the two groups off rats. “After just 30 years of selection,” Pääbo said, “the IC&G researchers had fashioned two populations that could hardly be more different.”
Significance of experiment
Belyaev’s experimental animals have been said to “form an unparalleled resource for studying the process and genetics of “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.” 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.” In a 2005 paper for Current Biology, 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 Belyaev and his team “didn't select for a smarter fox but for a nice fox,” Hare said, “they ended up getting a smart fox.” Belyaev’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.”
National Geographic has made much the same point, suggesting that the genetic explanation for the difference between wildness and tameness “has implications for understanding not just how we domesticated animals, but how we tamed the wild in ourselves as well.” The magazine’s writer asked: “Out of 148 large mammal species on Earth, why have no more than 15 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?”
The Brazilian scientist Claudio J. Bidau has suggested that Darwin, who was intrigued and puzzled by “the striking similarities developed by widely different domesticated animals and plants,” would have “truly appreciated” Belyaev’s experiment.
After Belyaev's Death
Belyaev 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. 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 “Belyaev 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.”
After the Soviet Union’s collapse, government funding for scientific projects became more difficult to come by, and “the researchers could do little more than keep the fox population alive.” Trut struggled to keep the project funded. When Anna Kukekova, a Russian-born postdoctoral student in molecular genetics at Cornell, read about the project's financial difficulties, she secured funding from the National Institutes of Health (NIH) and joined in Trut's effort to complete Belyaev’s work, making it a joint Russian-American initiative. The New York Times reported in 2006 on Frank Albert, a graduate student at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, who at the time was helping to continue Belyaev’s work by studying the genetic roots of the differences between the tame and hyperaggressive rats. In 2009, Albert and several colleagues published a paper in Genetics about the results of their cross-breeding of tame and hyperaggressive rats, a stock of which they had established in Leipzig. 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.”
“Understanding what has changed in these animals is going to be incredibly informative,” Elaine Ostrander of the National Human Genome Research Institute at the NIH told National Geographic in 2011. “Everyone is waiting with great excitement for what they come out with.”
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Belyaev, D. K. & L.N. Trut (1964). Behaviour and reproductive function of animals. II. Correlated changes under breeding for tameness. Bulletin of the Moscow Society of Naturalists Biological Series (in Russian) 69(5): 5-14.
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