siberian fox farm experiment

• Open access
• Published: 07 December 2018

The silver fox domestication experiment

• Lee Alan Dugatkin 1  

Evolution: Education and Outreach volume  11 , Article number:  16 ( 2018 ) Cite this article

244k Accesses

19 Citations

418 Altmetric

Metrics details

For the last 59 years a team of Russian geneticists led by Lyudmila Trut have been running one of the most important biology experiments of the 20th, and now 21st, century. The experiment was the brainchild of Trut’s mentor, Dmitri Belyaev, who, in 1959, began an experiment to study the process of domestication in real time. He was especially keen on understanding the domestication of wolves to dogs, but rather than use wolves, he used silver foxes as his subjects. Here, I provide a brief overview of how the silver fox domestication study began and what the results to date have taught us (experiments continue to this day). I then explain just how close this study came to being shut down for political reasons during its very first year.

Introduction, history and findings

Today the domesticated foxes at an experimental farm near the Institute of Cytology and Genetics in Novosibirsk, Siberia are inherently as calm as any lapdog. What’s more, they look eerily dog-like. All of this is the result of what is known as the silver fox, or farm fox, domestication study. It began with a Russian geneticist named Dmitri Belyaev. In the late 1930s Belyaev was a student at the Ivanova Agricultural Academy in Moscow. After he graduated he fought in World War II, and subsequently landed a job at the Institute for Fur Breeding Animals in Moscow.

Both as a result of his reading of Darwin’s The Variation of Animals and Plants Under Domestication (Darwin 1868 ), and his interaction with domesticated animals at the Ivanova Agricultural Academy and at the Institute for Fur Breeding Animals, Belyaev knew that many domesticated species share a suite of characteristics including floppy ears, short, curly tails, juvenilized facial and body features, reduced stress hormone levels, mottled fur, and relatively long reproductive seasons. Today this suite of traits is known as the domestication syndrome. Belyaev found this perplexing. Our ancestors had domesticated species for a plethora of reasons—including transportation (e.g., horses), food (e.g., cattle) and protection (e.g., dogs)—yet regardless of what they were selected for, domesticated species, over time, begin to display traits in the domestication syndrome. Why? Belyaev hypothesized that the one thing our ancestors always needed in a species they were domesticating was an animal that interacted prosocially with humans. We can’t have our domesticates-to-be trying to bite our heads off. And so he hypothesized that the early stages of all animal domestication events involved choosing the calmest, most prosocial-toward-human animals: I will refer to this trait as tameness, though that term is used in many different ways in the literature. Belyaev further hypothesized that all of the traits in the domestication syndrome were somehow or another, though he didn’t know how or why, genetically linked to genes associated with tameness.

Belyaev set out to test these hypotheses using a species he had worked with extensively at the Institute for Fur Breeding: the silver fox, a variant of the red fox ( Vulpes vulpes ). Every generation he and his team would test hundreds of foxes, and the top 10% of the tamest would be selected to parent the next generation. They developed a scale for scoring tameness, and how a fox scored on this scale was the sole criteria for selecting foxes to parent the next generation. Belyaev could then test whether, over generations, foxes were getting tamer and tamer, and whether the traits in the domestication syndrome appeared if they selected strictly based on tameness.

The experiment began in 1959 at the Institute of Cytology and Genetics in Novosibirsk, Siberia, shortly after Belyaev was appointed vice director there. Belyaev immediately recruited 25-year-old Lyudmila Trut to his team (Fig.  1 ). Trut quickly became the lead researcher on the experiment, working with Belyaev on every aspect from the practical to the conceptual. Trut turned 85 years old in November of 2018 and remains the lead investigator on the work to this day (Belyaev died in 1985).

Lyudmila Trut. a 1960 and b 2015

It is not possible here to do justice to all of the results this almost six-decade-long experiment has produced. Here I touch on some of the most salient (see Trut 1999 , Trut et al. 2009 and Dugatkin and Trut 2017 for more). Starting from what amounted to a population of wild foxes, within six generations (6 years in these foxes, as they reproduce annually), selection for tameness, and tameness alone, produced a subset of foxes that licked the hand of experimenters, could be picked up and petted, whined when humans departed, and wagged their tails when humans approached. An astonishingly fast transformation. Early on, the tamest of the foxes made up a small proportion of the foxes in the experiment: today they make up the vast majority.

Belyaev was correct that selection on tameness alone leads to the emergence of traits in the domestication syndrome. In less than a decade, some of the domesticated foxes had floppy ears and curly tails (Fig.  2 ). Their stress hormone levels by generation 15 were about half the stress hormone (glucocorticoid) levels of wild foxes. Over generations, their adrenal gland became smaller and smaller. Serotonin levels also increased, producing “happier” animals. Over the course of the experiment, researchers also found the domesticated foxes displayed mottled “mutt-like” fur patterns, and they had more juvenilized facial features (shorter, rounder, more dog-like snouts) and body shapes (chunkier, rather than gracile limbs) (Fig.  3 ). Domesticated foxes like many domesticated animals, have longer reproductive periods than their wild progenitors. Another change associated with selection for tameness is that the domesticated foxes, unlike wild foxes, are capable of following human gaze as well as dogs do (Hare et al. 2005 ). In a recent paper, a “hotspot” for changes associated with domestication has been located on fox chromosome 15 (Kukekova et al. 2018 ). SorCS , one gene in this hotspot, is linked with synaptic plasticity, which itself is associated with memory and learning, and so together these studies are helping us better understand how the process of domestication has led to important changes in cognitive abilities.

Mechta (Dream), the first of the domesticated foxes to have floppy ears 1969

The domesticated foxes have more juvenilized facial characters, including a shorter, rounder snout, than wild foxes

Right from the start of the experiment, Belyaev hypothesized that the process of domestication was in part the result of changes in gene expression patterns—when genes “turn on” and “turn off” and how much protein product they produce. A recent study examining expression patterns at the genome level, in both domesticated foxes and a second line of foxes that has been under long-term selection for aggressive, rather than tame, behavior, suggests Belyaev was correct (Wang et al. 2018 ). This study identified more than one hundred genes in the prefrontal cortex of the brain that showed different gene expression patterns between domesticated and aggressive foxes. Some of those genes are linked to serotonin receptor pathways that modulate behavioral temperament, including tame and aggressive temperaments.

When Belyaev proposed that the domestication syndrome was linked to tame behavior, he did not have a proposed mechanism, but today we are getting closer to understanding how this works. Very early on in animal development, what are known as neural crest cells migrate from the neural crest to a plethora of locations: glands in the endocrine system, bone, fur, cartilage, the brain and other spots in a developing embryo. The neural crest cell hypothesis for the domestication syndrome proposes that selection for tame behavior results in a reduction of the number of migrating neural crest cells, which subsequently leads to changes in fur coloration, facial structure, the strength of cartilage (floppy ears, curly tails and so on), hormone levels, the length of the reproductive season, and more. This hypothesis may provide the link that Belyaev was missing when he came up with the idea for the experiment (Wilkins et al. 2014 ).

Discussion: a cautionary tale

The silver fox domestication study is often lauded as one of the most important long-term studies ever undertaken in biology. Yet in 1959, the very year it commenced, the work came within a hair’s breath of being shut down by the premier of the Soviet Union. The problem for Belyaev and Trut was that their domestication experiment, like any experiment in domestication, was an experiment in genetics. But work in Mendelian genetics was essentially illegal at the time in the Soviet Union, because of a pseudo-scientific charlatan by the name of Trofim Lysenko (Joravsky 1979 ; Soyfer 1994 ).

In the mid-1920s, the Communist Party leadership, in an attempt to glorify the average citizen, began to promote uneducated men from the proletariat into the scientific community. Lysenko was one of those men. The son of peasant farmers in the Ukraine, Lysenko didn’t learn how to read until he was a teenager, and his education, as it was, amounted to a correspondence degree from gardening school. With no training, he still landed a middle-level job at the Gandzha Plant Breeding Laboratory in Azerbaijan in 1925. Lysenko convinced a Pravda reporter, who was writing a story about the regime’s glorious peasant scientists, that the yield from his pea crop he tended was far above average, and that his technique could save a starving USSR. In the Pravda article the reporter wrote glowingly that “the barefoot professor Lysenko has followers… and the luminaries of agronomy visit… and gratefully shake his hand.” Pure fiction, but the story propelled Lysenko to the national limelight, with Josef Stalin taking pride in what he read.

Over time Lysenko would claim to have done experiments creating grain crops, including wheat and barley, that produced high yields during cold periods of the year, if their seeds had been kept in freezing water for long stretches before planting. What’s more, Lysenko claimed offspring of these plants would also produce higher yields, down through the generations. This method, he said, could quickly double the yield of farmlands in the Soviet Union in just a few years. In truth, Lysenko never undertook any legitimate experiments on increased crop yield. Any “data” he claimed to have produced he simply fabricated.

Soon Stalin was his ally, and Lysenko began a crusade to discredit work in Mendelian genetics because proof of the genetic theory of evolution would likely expose him as a fraud. He denounced geneticists, both overseas and in the Soviet Union, as subversives. His star was rising and at a conference held at the Kremlin in 1935, after Lysenko finished a speech in which he branded Western geneticists as “saboteurs,” Stalin stood up to yell, “Bravo, Comrade Lysenko, bravo.”

Lysenko was placed in charge of all policy regarding the biological sciences in July 1948. The next month, at a meeting of the All-Union Lenin Academy of Agricultural Sciences, he presented a talk that today is regarded as the most disingenuous, dangerous speech in the history of Soviet science. In this speech, “The Situation in the Science of Biology,” Lysenko damned “modern reactionary genetics,” by which he meant Mendelian genetics. At the end of his ranting, the audience cheered wildly. Geneticists present were forced to stand up and refute their scientific knowledge and practices. If they refused, they were thrown out of the Communist Party. In the aftermath of that awful speech thousands of geneticists were fired from their jobs. Dozens, perhaps hundreds, were jailed, and a few were murdered by Lysenko’s henchmen.

Belyaev could not sit by idly. After reading of Lysenko’s speech in the newspaper, he was furious. His wife, Svetlana, remembers it well: “Dmitri was walking toward me with tough sorrowful eyes, restlessly bending and bending the newspaper in his hands.” Another colleague recalls running into him that day and how Belyaev had fumed that Lysenko was “a scientific bandit” (Dugatkin and Trut 2017 ). Ignoring the personal risk, Belyaev began speaking out about the dangers of Lysenkoism to all scientists, whether friend or foe.

The case of Nikolai Vavilov, one of Belyaev’s intellectual idols, illustrates just how dangerous it was to speak out against Lysenko (Medvedev 1969 ; Pringle 2008 ; Soyfer 1994 ). Vavilov studied plant domestication and was also one of the world’s leading botanical explorers, travelling to sixty-four countries collecting seeds. In his lifetime alone, three terrible famines in Russia killed millions of people and Vavilov had dedicated his life to finding ways to propagate crops for his country. His research program centered on finding crop varieties that were less susceptible to disease.

Vavilov’s collecting trips are the stuff of legend. On one of three expeditions, he was arrested at the Iran-Russia border and accused of being a spy, simply because he had a few German botany books with him. On another trip, this one to the border of Afghanistan, he fell as he was stepping between two train cars, and was left dangling by his elbows as the train roared along. On yet a different a trip to Syria he contracted malaria and typhus.

Vavilov collected more live plant specimens than any man or woman in history, and he set up hundreds of field stations for others to continue his work.

Vavilov had actually befriended the young Lysenko in the 1920s, before it became clear that Lysenko was a malevolent charlatan. Over time, Vavilov became suspicious of Lysenko’s results, and in a series of experiments trying to replicate what Lysenko said he had discovered, Vavilov proved to himself, and others that were willing to listen (though not many were), that Lysenko was a fraud. He then became Lysenko’s most fearless opponent. In retaliation, Stalin forbade Vavilov from any more travels abroad and he was denounced in the government newspaper, Pravda . Lysenko warned Vavilov that “when such erroneous data were swept away… those who failed to understand the implications” would also be “swept away.” Vavilov was undeterred, and at a meeting of the All-Union Institute of Plant Breeding declared, “We shall go into the pyre, we shall burn, but we shall not retreat from our convictions.”

In 1940, Vavilov was kidnapped up by four men wearing dark suits and thrown into the KGB’s dreaded Lubyanka Prison in Moscow. Next he was shipped off to an even more remote prison. There, over the course of 3 years, the man who had collected 250,000 domesticated plant samples to solve the puzzle of famine in his homeland was slowly starved to death.

Lysenko’s power had its ebbs and flows. In 1959, as the fox domestication experiment was just beginning, Lysenko was getting frustrated that his hold on Soviet biology was loosening. Something needed to be done. And The Institute of Cytology and Genetics, where the fox domestication experiment had just begun, where Belyaev was vice director, and where they had the audacity to put “Genetics” in the title of the institute, seemed a good place to attack.

The Institute of Cytology and Genetics was part of a new giant scientific city called Akademgorodok. Long before this city was built, Russian writer Maxim Gorky had written of a fictional “town of science… a series of temples in which every scientist is a priest… where scientists every day fearlessly probe deeply into the baffling mysteries surrounding our planet.” Here Gorky envisioned “…foundries and workshops where people forge exact knowledge, facet the entire experience of the world, transforming it into hypotheses, into instruments for the further quest of the truth.” Akademgorodok was what Gorky had in mind. It was home to thousands of scientists housed at the Institute of Cytology and Genetics, the Institute of Mathematics, the Institute of Nuclear Physics, the Institute of Hydrodynamics, and a half dozen other institutes.

In January 1959, a Lysenko-created committee from Moscow was sent to Akademgorodok. This committee had been authorized to determine just what sort of work was being done at the Institute of Cytology and Genetics, and Belyaev, Trut and their colleagues understood the gravity of the situation. “Committee members were, Trut said, “snooping in the laboratories,” and rumors were spreading that the committee was unhappy. When the committee met with Mikhail Lavrentyev, chief of all the institutes at Akademgorodok, they told him that “the direction of the Institute of Cytology and Genetics is methodologically wrong” (Dugatkin and Trut 2017 ). Ominous words from a Lysenkoist group.

Nikita Khrushchev, premier of the USSR, learned of the committee’s report about Akademgorodok. Khrushchev was a supporter of Lysenko, and he decided to see for himself what was happening. In September 1959, while returning from a visit to Mao Tse-Tung in China, he stopped off in Novosibirsk and went to Akademgordok.

The staff of all the science institutes at Akademgorodok gathered for this visit, and Trut remembers that the premier “walked by the assembled staff very fast, not paying any attention to them” as he proceeded to a meeting with administrators. “Khrushchev” Trut recalls was, “very discontented, with the intention to get everyone in trouble because of the geneticists.” What Khrushchev and Akademgorodok administrators said that day was not recorded, but accounts from the time make clear that the premier intended to shut down the Institute of Cytology and Genetics that day, and with it the nascent silver fox domestication experiment.

Fortunately for science, Khrushchev’s daughter, Rada, was with him in Akademgorodok. Rada, a well-respected journalist, had trained as a biologist, and understood very well that Lysenko was a fraud. She somehow managed to convince her father to let the Institute of Cytology and Genetics remain open. In an ironic twist, because Khrushchev felt he had to do something to show his discontent, the day after his visit, he fired the head of the Institute of Cytology and Genetics. Deputy Director Belyaev was now in charge of the institute.

If Rada Khrushchev had not taken a stand for science that day the fox domestication study would likely have ended before it even got off the ground. But, it survived and thrived and continues to shed new light on the process of domestication.

Darwin C. The variation of animals and plants under domestication. London: J. Murray; 1868.

Google Scholar  

Dugatkin LA, Trut LN. How to tame a fox (and build a dog). Chicago: University of Chicago Press; 2017.

Book   Google Scholar  

Hare B, Plyusnina I, Ignacio N, Schepina O, Stepika A, Wrangham R, Trut L. Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol. 2005;15:226–30.

Article   CAS   Google Scholar  

Joravsky D. The Lysenko affair. Cambridge: Harvard University Press; 1979.

Kukekova AV, Johnson JL, Xiang X, Feng S, Liu S, Rando HM, Kharlamova AV, Herbeck Y, Serdyukova NA, Xiong Z, Beklemischeva V, Koepfli K-P, Gulevich RG, Vladimirova AV, Hekman JP, Perelman PL, Graphodatsky AS, Obrien SJ, Wang X, Clark AG, Acland GM, Trut LN, Zhang G. Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours. Nat Ecol Evol. 2018. https://doi.org/10.1038/s41559-018-0611-6 .

Article   PubMed   Google Scholar  

Medvedev Z. The rise and fall of T.D. Lysenko: Columbia University Press; 1969.

Pringle P. The murder of Nikolai Vavilov. New York: Simon and Schuster; 2008.

Soyfer VN. Lysenko and the tragedy of Soviet science. Newark: Rutgers University Press; 1994.

Trut LN. Early canid domestication: the farm-fox experiment. Am Sci. 1999;87:160–9.

Article   Google Scholar  

Trut LN, Oskina I, Kharlamova A. Animal evolution during domestication: the domesticated fox as a model. BioEssays. 2009;31:349–60.

Wang X, Pipes L, Trut LN, Herbeck Y, Vladimirova AV, Gulevich RG, Kharlamova AV, Johnson JL, Acland GM, Kukekova AV, Clark AG. Genomic responses to selection for tame/aggressive behaviors in the silver fox ( Vulpes vulpes ). Proc Natl Acad Sci USA. 2018;115:10398–403.

Wilkins AS, Wrangham R, Fitch TW. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197:795–808.

Download references

Authors’ contributions

The author read and approved the final manuscript.

Acknowledgements

I thank Lyudmila Trut for working with me on our book, How to Tame a Fox and Build a Dog (University of Chicago Press, 2017). Nikolai and Michael Belyaev provided much in the way of assistance, as did Aaron Dugatkin. I thank Dana Dugatkin for proofreading this paper.

Availability of data and materials

No primary data was included in this review.

Competing interests

The author declares no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Author information

Authors and affiliations.

Department of Biology, University of Louisville, Louisville, KY, 40208, USA

Lee Alan Dugatkin

You can also search for this author in PubMed   Google Scholar

Corresponding author

Correspondence to Lee Alan Dugatkin .

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/ ), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and permissions

About this article

Cite this article.

Dugatkin, L.A. The silver fox domestication experiment. Evo Edu Outreach 11 , 16 (2018). https://doi.org/10.1186/s12052-018-0090-x

Download citation

Received : 25 August 2018

Accepted : 26 November 2018

Published : 07 December 2018

DOI : https://doi.org/10.1186/s12052-018-0090-x

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

• Domestication
• Silver foxes

Evolution: Education and Outreach

ISSN: 1936-6434

• Submission enquiries: [email protected]

That Famous Russian Fox Domestication Study May Have Had a Few Crucial Flaws

In 1959, the Soviet zoologist Dmitry Belyaev began selectively breeding silver foxes. Those least afraid of people were chosen to reproduce. His goal was to simulate the process that turned fierce ancient wolves into the dogs now known as our best friends.

The experiment worked, famously well. In 10 generations, Belyaev's lineage of foxes became tame, seeking attention from people and wagging their tails when scientists approached.

But this wasn't the only way the foxes changed. In 1979, Belyaev noted that some of the foxes had begun to look different, developing curly tails, spotting on their coats and floppy, puppy-like ears.

Later, other scientists began noticing some of these same traits in other domesticated species - pigs and goats, birds and fish - which seemed to point to a common genetic path that animals take as they change from wild to tame to domesticated.

This tantalizing notion, now known as domestication syndrome, was first put forward by Charles Darwin, and it has become integral to our understanding of how animal domestication works. But in a new paper, some scientists have challenged its accuracy - and, along the way, common beliefs about what domestication means.

The authors of the paper do not doubt that Belyaev was able to breed tamer foxes. But the Russian experiment fell short of proving the existence of domestication syndrome, they argue, because Belyaev's first foxes were far from wild, and there's no proof certain physical features are common to domesticated species.

"The common story line is that when you select on tameness in an animal species, a whole suite of other traits change in a predictable way," said Elinor Karlsson , a genomic scientist at the University of Massachusetts Medical School and senior author on the study. "And we just couldn't find convincing evidence for that."

A major problem is that Belyaev started with foxes that weren't wild, said Kathryn Lord , an evolutionary biologist at the University of Massachusetts Medical School and lead author of the paper, published Tuesday in the journal Trends in Ecology and Evolution . Genetic testing indicated they originated in eastern Canada, probably at a fur farm on Prince Edward Island, which means the animals were already on the path toward domestication.

There's also evidence that Canadian fur farmers were seeking to produce unusual pelt colors, including with white spotting, which might fetch higher prices. So some of the traits held up by Belyaev as evidence of the domestication syndrome may already have been present in his first batch of foxes.

And those foxes' tendency to produce white spots likely would have become greater when they arrived in Russia, because Belyaev started his experiment with a rather small population of 130 animals, Karlsson said.

"You can get very rapid changes in the frequency or the prevalence of a trait without having done a whole lot of work, just by making the population really, really small," she said.

The other wrinkle is that evidence for the suite of physical traits long said to be shared by dogs, goats, rabbits and other domesticated species is thin, the authors say.

For instance, it's commonly said that domesticated animals have curlier, more upright tails - the difference between a Siberian husky's and a gray wolf's. But Lord and her colleagues found no conclusive evidence that domesticated dogs hold their tails differently from wolves, foxes or other wild canids. They also found little documentation of these traits for other animals.

"I know this is true! It's a thing!" Lord said, acknowledging that even she finds the lack of data frustrating. "But nobody's counted it."

This is important, Karlsson said, because while "tail carriage" is more common in less fearful foxes, it's also seen in some of their wild cousins. That means the adorable, dog-like tails seen in the Russian experiment's foxes may not be linked to genetic changes that enabled their tameness at all. It might just be sheer luck.

"Our main point is not that domestication syndrome doesn't exist, but just that we don't think there is enough evidence to be confident it does exist," said Karlsson in a follow-up email.

None of this matters much to how most of us relate to our dogs and cats (or pigs and goats). But the challenge to common wisdom about how those animals came to be has caused waves in the community of domestication scholars - and gotten a mixed reception.

"The fox experiment is the most celebrated one in studies of domestication, yet details of it have never been fully published or explained, much less critically assessed," said Marcelo Sánchez-Villagra , a paleobiologist at the University of Zurich who has studied domestication syndrome. "This paper to me shows that new, better designed experiments on domestication - of several kinds of animals - are needed to advance the field forward."

Melinda Zeder , senior scientist emeritus at the Smithsonian's National Museum of Natural History, said the Russian farm-fox experiment has "really been oversold," in that many popular portrayals make it out to be grander and more simplified than Belyaev and the scientists who succeeded him meant it to be.

"The caution that they offer here is very useful, to sort of pull back and say this is not the be-all, end-all," Zeder said. But she added that the "case is not as convincing as you would want it to be," in part because, she said, it places too much weight on a lack of studies documenting every domestication syndrome trait in every domesticated animal.

Belyaev was well aware that white spotting was present in his fox population and never claimed it was linked to tameness, said Anna Kukekova , a geneticist at the University of Illinois at Urbana-Champaign who has been studying these foxes for decades. Belyaev detailed this clearly in a paper he published in 1979, she said.

Kukekova said she had other qualms about the new paper, though she agrees that there doesn't seem to be evidence for one easy path to domestication.

"Genes rarely have a single function," she said in an email.

"I would strongly argue [the Russian farm-fox experiment] is still the gold standard," said Lee Dugatkin , a biologist at the University of Louisville and co-author of a book about the Russian experiment, " How to Tame a Fox (and Build a Dog) ."

Dugatkin said he had "major concerns" about the study. He said curly tails didn't show up in the foxes for nine to 10 generations and that the scientists did not select for them once they showed up.

But they grew more common with each tamer generation, he said. The project, which is now run by his co-author, Russian geneticist Lyudmila Trut, has since added two new lineages of foxes, one selected for aggression and another as a control, he said, and they haven't developed curly tails and spotting.

But just because those traits don't show up in other populations "doesn't prove that the traits are directly linked to tameness," said Karlsson, "just that those traits happened to also occur in the population that was selected for tameness. The most likely explanation is that this is due to random chance."

Lord makes no bones about how important Belyaev's work was. "It's an amazing behavioral experiment," she said.

But it could be stronger, Karlsson said.

"That was kind of what inspired us to write the paper," she said. "Because there's nothing more frustrating than when people just assume that something is true that hasn't been proved yet."

2019 © The Washington Post

This article was originally published by The Washington Post .

Every print subscription comes with full digital access

Science News

Fox experiment is replaying domestication in fast-forward.

New book recounts nearly 60-year effort to understand taming process

DOMESTICATION IN ACTION   How to Tame a Fox tells the story of a long-running experiment to domesticate silver foxes (a wild silver fox is shown).

Minette Layne/Flickr ( CC BY-NCE 2.0 )

Share this:

By Tina Hesman Saey

April 29, 2017 at 8:00 am

In 1959, Lyudmila Trut rode trains through Siberia to visit fox farms. She wasn’t looking for furs. She needed a farm to host an audacious experiment dreamed up by geneticist Dmitry Belyaev: to create a domestic animal as docile as a dog from aggressive, wily silver foxes.

Evolutionary biologist Lee Alan Dugatkin helps Trut recount this ongoing attempt to replay domestication in How to Tame a Fox . The mechanics of domestication are still a matter of intense scientific debate. Belyaev’s idea was that ancient humans picked wolves and other animals for docility and that this artificial selection jump-started an evolutionary path toward domestication.

Back in the 1950s, testing the idea was dangerous work, and not just because untamed foxes bite. In 1948, the Soviet Union, under the scientific leadership of Trofim Lysenko, outlawed genetics research. Lysenko had risen to power based on fabricated claims that freezing seeds in water could increase crop yields. “With Stalin as his ally, he launched a crusade to discredit work in genetics, in part, because proof of the genetic theory of evolution would expose him as a fraud,” Dugatkin and Trut write. Geneticists often lost their jobs, were jailed or even killed, as was Belyaev’s own brother. So Belyaev cloaked his domestication experiments in the guise of improving the fur-farming business.

Fox researchers started by testing the temperament of about 100 silver foxes each year. About a dozen of the foxes, slightly calmer than most, were bred annually. Within a few generations, some foxes were a bit more accepting of people than the starting population. That small difference convinced Belyaev of the experiment’s promise, and he recruited Trut to carry out a larger breeding program.

Trut and Dugatkin lovingly recount some of the experiment’s milestones, including the first fox born with a wagging tail and the first one with droopy ears — two hallmarks of domesticated animals. Trut recalls the foxes she’s lived with and, heartbreakingly, the ones she lost, or had to sacrifice to keep the experiment going after the collapse of the Russian economy in 1998 led to funding problems. At every step, the authors skillfully weave the science of domestication into the narrative of foxes becoming ever-more doglike.

Trut has kept Belyaev’s dream alive for nearly 60 years. Now in her 80s, she still runs the experiment and has eagerly collaborated with others to squeeze every drop of knowledge from the project. The work has shown that selecting for tameness alone can also produce a whole suite of other changes (curly tails, droopy ears, spotted coats, juvenile facial features) dubbed the domestication syndrome. With the help of geneticist Anna Kukekova, Trut is searching for the genes involved in this process.

The project now sells some of the foxes as pets to raise money, although one could argue they aren’t fully domesticated. The foxes may wag their tails and flop on their backs to get their bellies rubbed, but Trut says they still don’t follow commands like dogs do. It probably took Stone Age humans hundreds or thousands of years to domesticate wolves. The silver fox experiment has replayed the process in fast-forward. It may speed scientists’ quest to understand the DNA changes that transformed a wolf into a dog.

Buy   How to Tame a Fox (and Build a Dog) from Amazon.com. Sales generated through the links to Amazon.com contribute to Society for Science & the Public’s programs.

More Stories from Science News on Science & Society

Scientists are getting serious about UFOs. Here’s why

‘Then I Am Myself the World’ ponders what it means to be conscious

Twisters asks if you can 'tame' a tornado. We have the answer

The world has water problems. This book has solutions

Does social status shape height?

In ‘Warming Up,’ the sports world’s newest opponent is climate change

‘After 1177 B.C.’ describes how societies fared when the Bronze Age ended

‘Cull of the Wild’ questions sacrificing wildlife in the name of conservation

Subscribers, enter your e-mail address for full access to the Science News archives and digital editions.

Not a subscriber? Become one now .

• The Magazine
• Stay Curious
• The Sciences
• Environment
• Planet Earth

How a Russian Scientist Bred the First Domesticated Foxes

In just five decades, an experiment in Russia has accomplished something that took ancient humans thousands of years.

On a farm in Novosibirsk, Russian geneticist Dmitry K. Belyaev selectively bred hundreds of foxes over multiple generations, eventually creating something never seen before: a domesticated fox. His goal was to recreate the process by which humans gradually turned wild dogs into workers and friends, hopefully learning something about the mechanism of domestication in the process.

Nice Foxes Only

To accomplish his goal, he selected the most docile foxes he could find from fur farms around Russia. He then bred them in successive generations, each time choosing only the tamest individuals. This is similar to the process today by which dog breeders select for desired traits, or how ancient farmers cultivated hardy crops with the highest yields.

Belyaev found that the process worked for fox domestication as well. His experiment started in the late 1950s, and by the early 2000s almost all of the foxes on the farm displayed remarkable changes in behavior,  according to an in-depth report  penned by Lucy Jones of the  BBC .

Foxes are considered notably hard to tame, but Belyaev’s foxes seemed preternaturally easygoing. They looked more like dogs than wild foxes — they would wag their tails and perk up in the presence of humans, and displayed none of the skittishness or aggressiveness usually associated with wild animals. In addition, they enjoyed being petted and would lick their handlers faces — all behaviors that socialized dogs display. And, all of this happened without any training on the part of the researchers. Their only intervention was to selectively breed those foxes that fit in with humans the best.

NPR   spoke to  Ceiridwen Terrill, a professor of Science Writing and Environmental Journalism at Concordia University in Portland, Oregon, who visited the farm and even got to pet the foxes.

“They’re genetically designed to crave human contact,” she says, “so that fox loved having its belly scratched.”

It wasn’t only behavioral changes either. The foxes started to look different over time: their ears got floppier, their legs, tails and snouts got shorter and their skulls got wider. Even their breeding patterns changed, they now mated out of season and had on average one more offspring per litter.

Changes Beyond Behavior

The reasons for this are likely rooted in neurological and endocrinological changes wrought in the foxes through selective breeding, according to  a 2009 paper  by Lyudmila Trut, of the Institute of Cytology and Genetics at the Russian Academy of Sciences, who now oversees the farm.

That paper reviewed the changes caused by domestication and found that, compared to wild foxes, the domesticated animals displayed different levels of certain chemicals in their brains. For example, their adrenal glands are not as active, but they have higher levels of serotonin. Serotonin likely plays a role in mediating aggressive behavior, writes Trut.

The physical alterations in the foxes, similar to the changes that happened in dogs, are likely a byproduct of behavioral selection. The droopiness of their ears may be caused by the slowing of their adrenal glands, says the  BBC , and the others physical disparities could similarly be related to the differences in hormone levels that lead to desirable traits. Dogs likely went through much the same process over the course of hundreds of generations as they gradually adapted to living with us.

Belyaev’s experiment is evidence that our theories of domestication are spot-on; we’ve bent the arc of evolution toward in our favor. Moreover, the process of taming a species affects more than their behavior, domestication alters their looks, and changes the rhythms of their lives.

Swing over to the  BBC   and check out Jones’s entire story , for more details about this decades-long study.

Already a subscriber?

Register or Log In

Keep reading for as low as $1.99!

Sign up for our weekly science updates.

Save up to 40% off the cover price when you subscribe to Discover magazine.

The silver fox domestication experiment

• December 2018
• Evolution: Education and Outreach 11(1)
• This person is not on ResearchGate, or hasn't claimed this research yet.

Abstract and Figures

Discover the world's research

• 25+ million members
• 160+ million publication pages
• 2.3+ billion citations

• Mónica Major González

• GENET SEL EVOL

• REV CHIL HIST NAT

• Brian T. Shea
• Matthew K. Brachmann
• K.J. Parsons

• Nat. Ecol. Evol.

• Richard W. Wrangham
• W. Tecumseh Fitch

• Lenore Pipes
• Andrew G. Clark
• Robert N. Proctor
• Valery N. Soyfer
• Leo Gruliow
• Rebecca Gruliow
• Peter A. Toma
• David Joravsky
• Lee Alan Dugatkin
• Lyudmila Trut
• Charles Robert Darwin
• I.N. Oskina
• Anastasiya V. Kharlamova
• Recruit researchers
• Join for free
• Login Email Tip: Most researchers use their institutional email address as their ResearchGate login Password Forgot password? Keep me logged in Log in or Continue with Google Welcome back! Please log in. Email · Hint Tip: Most researchers use their institutional email address as their ResearchGate login Password Forgot password? Keep me logged in Log in or Continue with Google No account? Sign up

• Bahasa Indonesia
• Slovenščina
• Science & Tech
• Russian Kitchen

How Siberian geneticists domesticated the FOX

Tame foxes are seen here in the enclosure on the experimental farm of the Institute for Cytology and Genetics of the Russian Academy of Sciences Siberian Branch.

Gerda the fox is a favorite among both children and adults in Novosibirsk. She adores playing with tennis balls and having her ears stroked, and loves falling asleep next to her human. “Gerda and I have been together for almost three years now,” says Andrei Kudyakov.

Andrei with Gerda.

“One day, I visited the Institute of Cytology and Genetics farm to look at their foxes out of curiosity. And afterwards, I could not get the idea of having such a lovely creature at home out of my head. A year later, I went back and made my choice in favour of the reddest one.” Gerda lives outside the city, in the countryside, where she has a spacious enclosure outdoors and, when she goes for a walk with Andrei, she wears a harness, attracting the attention of everyone in the neighborhood. By nature she is cheerful, alert, curious and affectionate.

Gerda with her friend.

Gerda is one of the domesticated foxes bred at the Institute of Cytology and Genetics of the Siberian branch of the Russian Academy of Sciences. She is attached to humans at the genetic level and regards them as her friends. This breed of foxes is an inherently unique phenomenon.

The largest evolutionary experiment

The experiment to domesticate foxes was initiated by Academician Dmitry Belyayev in 1959. In the 1970s, he was joined by Lyudmila Trut, then a biology student at MGU (Moscow State University) and now a world-renowned Russian scientist.

Lyudmila Trut and American biologist Lee Alan Dugatkin co-authored a book in 2019 about her work with Belyayev titled How to Tame a Fox (and Build a Dog). According to the book, Belyayev believed that the experiments could also shed light on human evolutionary processes - he proposed that humans were “self-domesticated” apes that had gone through selection for reduced aggression (social tolerance) towards their fellow creatures.

Foxes play at the experimental farm at the Institute of Cytology and Genetics of the Russian Academy of Sciences.

The scientist supposed that the least aggressive individuals were the first to start approaching people, obtaining a selective advantage from their contact with humans in the form of warmth and food, and so, as generation followed generation, they would become domesticated. Wild aurochs became domesticated cows, while ferocious wolves - loyal dogs. It may sound reasonably simple, but in practice, evolutionary processes do not take place so quickly or smoothly. Man can tame many wild animals (bears, cougars, cheetahs - and the people who acquire such pets today frequently become social media stars), but for them to become actual domestic animals - in other words, breed regularly and regard human dwellings as their home - thousands of years of evolution have to go by. However, Soviet scientists needed just 60 years. The idea was to breed animals, by means of selective screening, that from a young age would behave like domestic animals.

“When we set out on the experiment, we sought an animal similar to a dog,” Lyudmila Trut says. “And that was the fox, which at that point had already been bred for dozens of years at Soviet fur farms - in other words, it had already gone through a stage of reproduction under human control and this helped us significantly shorten the timescale of the experiment.”

A tame fox.

The foxes that were mainly bred then were silver foxes imported from Canada in the 1920s. They behaved very aggressively: They would attack humans and viciously bite them, and the fur farms were consequently very surprised at Belyayev’s proposal. “We singled out the foxes that did not manifest a strongly-pronounced ferocity towards humans and were more or less tolerant of humans - and these were isolated cases at our fur farms,” Trut says. Subsequently the chosen foxes were settled at a farm not far from Akademgorodok in Novosibirsk. The first results began to emerge four years later. 

‘It wags its tail like a dog’

The first fox cub that started wagging its tail when a human approached was born in 1963. In subsequent generations, the foxes started licking people’s hands and asking to be stroked or to have their belly rubbed. Then they started accepting eye-to-eye contact, which in nature is regarded as an overt act of aggression. In 1975, the first fox gave birth to a litter while living alongside humans, and then started giving out a cry like a dog’s bark. In the course of domestication, the Belyaev foxes developed markings in the form of ‘stars’, their tail and ears curled and their muzzle began to preserve a juvenile appearance even in adult age. Domestic foxes retain a fairly specific odor from their wild ancestors, but the danger of their biting or behaving aggressively is practically non-existent, scientists believe.

A keeper plays with a tame fox at the farm of the Institute of Cytology and Genetics.

Today, the followers of Dmitry Belyayev are studying the domestication of animals all over the world. Lyudmila Trut continues her research at the Institute of Cytology and Genetics - after all, 60 years is a brief moment in evolutionary terms, and a large number of unanswered questions remain. Can domestic foxes be born if an aggressive fox mates with a tame one? Or why do the Belyayev foxes change appearance in one way and not another?

An employee holds a domesticated fox seen in an enclosure at an experimental farm of the Institute of Cytology and Genetics.

“Our experiment in Novosibirsk has created a completely new fox, one that never existed before. People buy them from us and take them all over the world,” Lyudmila Trut says. She says that no research into the domestication of foxes of this kind has taken place anywhere else in the world - Russian scientists have carried out scientific work on an industrial scale in the world’s largest country. She estimates that over these years they have bred more than 60,000 foxes with a friendly disposition towards humans. “Of course, not all these foxes were kept at the institute. We had outstations, as it were, at fur farms throughout the country, but the domestic fox was developed on our experimental farm at Akademgorodok.”

If using any of Russia Beyond's content, partly or in full, always provide an active hyperlink to the original material.

to our newsletter!

Get the week's best stories straight to your inbox

• What do Kamchatka foxes do when nobody’s watching? (PHOTOS)
• Russian ginger fat cat takes over masterpieces (PHOTOS)
• This Russian sable just kept attracting fans during lockdown (PHOTOS)

This website uses cookies. Click here to find out more.

Cornell Chronicle

• Architecture & Design
• Arts & Humanities
• Business, Economics & Entrepreneurship
• Computing & Information Sciences
• Energy, Environment & Sustainability
• Food & Agriculture
• Global Reach
• Health, Nutrition & Medicine
• Law, Government & Public Policy
• Life Sciences & Veterinary Medicine
• Physical Sciences & Engineering
• Social & Behavioral Sciences
• Coronavirus
• News & Events
• Public Engagement
• New York City
• Photos of the Week
• Big Red Sports
• Freedom of Expression
• Student Life
• University Statements
• Around Cornell
• All Stories
• In the News
• Expert Quotes
• Cornellians

A silver fox bred for tameness at the the Institute for Cytology and Genetics in Novosibirsk, Russia. 

Silver fox study reveals genetic clues to social behavior

By krishna ramanujan.

In 1959, Russian scientists began an experiment to breed a population of silver foxes, selecting and breeding foxes that exhibited friendliness toward people. They wanted to know if they could repeat the adaptations for tameness that must have occurred in domestic dogs. Subsequently they also bred another population of foxes for more aggressive behavior.

After 10 generations, a small fraction of the tame-bred foxes displayed dog-like domesticated behavior when people approached. Over time, an increasing fraction of the foxes showed this friendly behavior.

Now, after more than 50 generations of selective breeding, a new Cornell-led study compares gene expression of tame and aggressive silver foxes in two areas of the brain, shedding light on genes responsible for social behavior.

The study, published online Sept. 18 in the Proceedings of the National Academy of Sciences , identified genes that were altered in tame animals in two areas of the brain involved with learning and memory.

“That such a radical change in temperament could be accomplished so quickly is truly remarkable,” said Andrew Clark, professor in the Department of Molecular Biology and Genetics at Cornell and a senior co-author of the paper.

The research team obtained prefrontal cortex and basal forebrain brain tissue samples of 12 tame and 12 aggressive foxes from the Institute for Cytology and Genetics in Novosibirsk, Russia, where the foxes were bred.

Clark and first author Xu Wang, Ph.D. ’11, a former research associate in Clark’s lab, conducted two types of genetic analysis. In one investigation, they sequenced the RNA produced by all genes, which allowed them to measure how much every gene was turned on. The other test identified different versions of genes, called alleles, and measured how they changed in frequency in the population over generations.

These analyses revealed which brain pathways were altered by breeding tame and aggressive foxes. The prefrontal cortex and basal forebrains are known for handling higher processing of information, including higher-level social interaction. The team was especially interested in neurons classified by the neurotransmitters (brain signaling chemicals) they release: dopamine, serotonin and glutamine.

The pleasure centers in the brain are triggered by dopamine, and Clark said he expected those dopaminergic pathways to be altered in the tame animals.

“Tame animals seem like they are blissed out all the time,” he said. “They’re just so happy and adorable, so I thought certainly the dopaminergic [pathway would be affected]. But there was no signal.”

However, the genes that impact the function of both serotonergic neurons and glutaminergic neurons were clearly affected by selection toward tameness. These neurons are important for learning and memory.

Also, the analyses implicated genes important in the function of the neural crest, a transient group of cells that arises very early in the embryo. These cells migrate to form many types of adult cells, including those that determine skin and hair pigment (melanocytes), peripheral nerves, and the tissues of the face. The signals suggest a link to “domestication syndrome,” a cluster of ancillary traits – white fur spots, shorter nose, curly tail and floppy ears – that pops up in domesticated canines, and in similar forms of other species.

“Darwin, and many others since, observed that when people select for domestication, there is a tendency to see a reversion in these traits to a more juvenile form,” Clark said, adding that more study of the neural crest’s role in domestication syndrome is needed.

The paper was written in tandem with another related study  recently published in Nature Ecology and Evolution (NEE) that includes many of the same co-authors, including Clark, Wang, Lyudmila Trut, co-director at the Institute for Cytology and Genetics, and Anna Kukekova, the NEE paper’s first author and an assistant professor in the Department of Animal Sciences at the University of Illinois. Kukekova has worked with Trut’s lab in Novosibirsk, and is a former research scientist at Cornell’s Baker Institute for Animal Health.

Media Contact

Get Cornell news delivered right to your inbox.

You might also like

Gallery Heading

• Newsletters
• Account Activating this button will toggle the display of additional content Account Sign out

Guarding the Fox House

A famous animal experiment is in peril, after 54 years of work..

Courtesy Ceiridwen Terrill

The battered Volga bounces us along the buckled roads, frozen and thawed over long Siberian winters. With me in the van are geneticist Lyudmila Trut and her assistant Anastāsiya Kharlamova, whom I met earlier that morning at the Institute of Cytology and Genetics in Siberia.  Now in her 70s, Trut, a petite woman in a blue pinstripe jacket and light gray pants, peers through thick glasses, trying to read a scientific paper as we drive. A few minutes later, the driver stops at the dented metal gate to the experimental farm, and Trut leads the way down dilapidated rows of narrow barracks-style sheds, morning glories sprouting from cracks in the paved walkways. The farm houses 3,000 foxes, each open-air wooden shed holding 100 or so animals in adjacent wire cages. The three of us put on white lab coats and prepare to greet the foxes.

When I open the door to one fox’s cage, the only home it will ever know, the little guy doesn’t shrink in fear as a wild creature could be expected to. Instead he lets me scoop him up, then nuzzles my neck and licks my fingers. Kharlamova, a slim young woman with shoulder-length brown hair, explains that the fox is “emotional” because I’m giving him the attention he wants. 

Although domestication of dogs took thousands of years, Russian geneticist Dmitry K. Belyaev tried to reproduce the whole messy process in one human lifetime, eliminating all the dead ends and inefficiencies of chance and human blunder. In 1957, he began a domestication experiment with the farmed fox Vulpes vulpes , a distant cousin of the dog. In March 2011, a National Geographic article described the experiment as if it were finally on the verge of completion. Researchers were scanning the genomes of the “domesticated silver foxes,” it said, in the hopes of finding “key domestication genes.” But there’s a problem with this narrative: Even after 54 years of research, we still don’t know whether the animals have reached the original end point set out by the project’s founder.

Belyaev, who died in 1985 and left Lyudmila Trut in charge of the project, was clear about his goal: The foxes would be considered fully domesticated only when they obeyed human commands as dogs do. That part of the experiment is still unfinished. No evidence exists to tell us whether the foxes can be trained to override their instincts, the way a dog might learn to avoid defecating on the carpet, or to stay at the heel instead of running off to seek the company of other canines. Belyaev would never have called the experiment over until a whole population of foxes had shown that they were biddable, eager to please, and able to pass those qualities to their offspring. Now Trut would like to put those qualities to the test, but her experiment has stalled for lack of money. After 51 generations of foxes, the world’s foremost domestication experiment languishes. If nothing is done to save it, we’ll have missed an opportunity to understand the mechanisms of domestication, of which genetic tameness—friendly behavior that is not learned but inherited—is only one component.

Belyaev began with several hypotheses: People created the dog, and they did it by selecting—first unintentionally and then intentionally—for behavior.  He could replicate and accelerate the dog’s domestication process with the fox, he theorized, by rigorously selecting for tameness, which would eventually allow him to uncover the genetic mechanisms responsible for changing the dog’s wild ancestor into our beloved Fido. From fur farms where foxes had been bred in captivity for more than 50 years, Belyaev chose 130 of the calmest animals, descendants of foxes who’d already passed an unintentional selection test for tameness simply by surviving the original lure, capture, and confinement that literally scares some wild foxes to death. Kits born to Belyaev’s founding population and each succeeding generation of kits were subjected to a standardized tameness test, each animal ranked according to its response to a human experimenter who tried to touch and feed it. Only those foxes that showed tolerance for the nearness of people were selected and bred to produce the next generation, while fearful or aggressive animals were culled. Each generation of foxes grew more approachable, many showing doglike yearning for human contact. The experimental farm presently houses a stable population of genetically tame foxes.

Results of testing by anthropologist Brian Hare and his team at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, have shown that Belyaev’s foxes respond to pointing cues almost as well as dogs, which means they’re attuned to human interaction. But although we have the occasional anecdote of a fox walking on a leash or another sitting for a treat, no systematic socialization and training program has been launched to test the capacity and willingness of the foxes to respond to classic obedience cues— come , sit , down , stay , and settle — defining characteristics of a domestic canine. If fox kits are raised like dog puppies, put to the training test, and pass, then scientists would know that all the genes relevant to domestication are present in their genome. They’d just have to find them.

Unfortunately, the experiment is broke. Grant money is scarce in Russia, where economic crises hit in 1998 and again in 2008. Trut has resorted to selling some of the foxes into the exotic pet trade through SibFox Inc., a private company in Las Vegas. For $6,950, the U.S. distributor promises a tame four-month-old fox “delivered to your door in 90 days.” Since the foxes’ critical window of socialization—the period during which they form primary bonds—closes when the animals are about 60 to 65 days old, it’s no wonder the distributor advises housing the foxes in cages with bottoms or dig guards to prevent escape, because that’s what the foxes try to do. 

But the fact is, people aren’t lining up for pet foxes, and each year Trut and her team must either euthanize or sell several hundred foxes to fur farms because she can barely afford basic upkeep. As of this writing, fewer than five foxes have been sold in the United States as pets, and only a handful live with wealthy Russians. One sent to a home in Moscow went roaming and found himself a wild girlfriend whom he occasionally brought around for dinner. She wouldn’t go near the house, and he stayed only long enough to eat a bit of meat—less a pet than a roommate. Yet Trut soldiers on, trying to preserve the integrity of the genetic line in case funding should materialize for a rigorous socialization and training program. 

For the experiment to continue, fox kits would have to be systematically hand-reared and human-socialized. Then they could be trained and tested for their ability and eagerness to respond to classic obedience commands. If the foxes don’t prove trainable, then perhaps domestication, even when compressed for efficiency, takes longer than one human lifetime and is more complicated than merely selecting for a single behavioral trait. Or perhaps the dog’s ancestor possessed something unique in its genes that gave rise to our closest companion, something that can’t be replicated in the fox just because it’s a social canid. The point is, we won’t know until Belyaev’s experiment is finished. Unless the experiment is helped to reach its conclusion—to understand once and for all whether the foxes have achieved domesticity as Belyaev hoped—more than half a century of intellectual labor and the lives of more than 50,000 foxes will have been wasted.

Trut feels bad about the state of the farm and the plight of hundreds of foxes moaning and chattering for attention from their 3-foot wire cubes. On my last night in Siberia, over a meal of tsar’s hodgepodge—described in the menu as “grilled vegetables with secret sauce and garbage”—a man with his personal fifth of Beluga vodka tells me that getting by in Russia takes a lot of luck. I can’t help thinking those farm foxes need all the luck they can get. They’ve already surprised geneticists by suggesting that selection for a single behavioral trait can trigger “piggy-backing” changes in physiology and appearance, like increased levels of serotonin and piebald coats. There may be more surprises to come, but it will take a major infusion of cash, and a collaboration among scientists, adventurous dog trainers, and Lyudmila Trut to let Belyaev’s experiment—and eventually his foxes—out of the box.

• Advanced search

Advanced Search

Neuromorphological Changes following Selection for Tameness and Aggression in the Russian Farm-Fox experiment

• Find this author on Google Scholar
• Find this author on PubMed
• Search for this author on this site
• ORCID record for Erin E. Hecht
• ORCID record for Todd M. Preuss
• Figures & Data
• Info & Metrics

The Russian farm-fox experiment is an unusually long-running and well-controlled study designed to replicate wolf-to-dog domestication. As such, it offers an unprecedented window onto the neural mechanisms governing the evolution of behavior. Here we report evolved changes to gray matter morphology resulting from selection for tameness versus aggressive responses toward humans in a sample of 30 male fox brains. Contrasting with standing ideas on the effects of domestication on brain size, tame foxes did not show reduced brain volume. Rather, gray matter volume in both the tame and aggressive strains was increased relative to conventional farm foxes bred without deliberate selection on behavior. Furthermore, tame- and aggressive-enlarged regions overlapped substantially, including portions of motor, somatosensory, and prefrontal cortex, amygdala, hippocampus, and cerebellum. We also observed differential morphologic covariation across distributed gray matter networks. In one prefrontal-cerebellum network, this covariation differentiated the three populations along the tame-aggressive behavioral axis. Surprisingly, a prefrontal-hypothalamic network differentiated the tame and aggressive foxes together from the conventional strain. These findings indicate that selection for opposite behaviors can influence brain morphology in a similar way.

SIGNIFICANCE STATEMENT Domestication represents one of the largest and most rapid evolutionary shifts of life on earth. However, its neural correlates are largely unknown. Here we report the neuroanatomical consequences of selective breeding for tameness or aggression in the seminal Russian farm-fox experiment. Compared with a population of conventional farm-bred control foxes, tame foxes show neuroanatomical changes in the PFC and hypothalamus, paralleling wolf-to-dog shifts. Surprisingly, though, aggressive foxes also show similar changes. Moreover, both strains show increased gray matter volume relative to controls. These results indicate that similar brain adaptations can result from selection for opposite behavior, that existing ideas of brain changes in domestication may need revision, and that significant neuroanatomical change can evolve very quickly, within the span of <100 generations.

• domestication
• farm-fox experiment
• neuroimaging
• social behavior
• Introduction

Domestication refers to the process of animal adaptation to the human niche. It represents one of the largest and most rapid evolutionary shifts in life on Earth: the biomass of domesticated animals has increased an estimated 3.5-fold in the last 100 years and now outweighs the biomass of other terrestrial mammals by a factor of ∼25 ( Smil, 2011 ). Correspondingly, the neural changes associated with domestication constitute a major event in the history of brain evolution. Moreover, self-domestication is hypothesized to have played a role in the evolution of our own species ( Brune, 2007 ; Hare, 2017 ; Wrangham, 2018 ). However, surprisingly little is known about the neural correlates of domestication.

Perhaps the most well-known effect of domestication on the brain is a reduction in size ( Kruska, 2005 ). Dogs are the oldest and perhaps the archetypal domesticate, having split from wolves an estimated 10,000-30,000 years ago ( Skoglund et al., 2011 ; MacHugh et al., 2017 ). Past research on the neural correlates of wolf-to-dog domestication has implicated PFC and the limbic system, particularly the hypothalamo-pituitary-adrenal axis. For example, gene expression in the hypothalamus is conserved between wolves and coyotes but diverges significantly in dogs ( Saetre et al., 2004 ). Similarly, genes showing high differentiation between wolves and Chinese native dogs show high expression bias for the brain, particularly those expressed in PFC ( Li et al., 2013 ). In an MRI study of 8 wild carnivore species and 13 domestic dogs, the allometric scaling of corpus callosum size to total brain size was constant across species, except in the rostral component, which interconnects prefrontal cortices ( Spocter et al., 2018 ). Moreover, the enlargement of one component of carnivore PFC, the prorean gyrus, which has extensive connections with other limbic system components ( Cavada and Reinoso-Suárez, 1985 ; Markow-Rajkowska and Kosmal, 1987 ), has been implicated in the emergence of complex social behavior in canid evolution ( Radinsky, 1969 ).

The domestication of wolves into dogs is paralleled by the well-known and long-running Russian fox experiment ( Trut et al., 2009 ). The experiment does not, of course, perfectly recapitulate the “naturally” occurring domestication of any species, and indeed domestication trajectories differ in important ways across species and can involve selection pressures beyond tameness ( Zeder, 2012 ). Nonetheless, the Russian fox experiment offers a singularly well-controlled window on neurobiological shifts associated with tameness ( Zeder, 2012 ). Since 1959, researchers at the Institute of Cytology and Genetics in Novosibirsk have been breeding conventional farm foxes on the basis of their behavioral response to human social contact. The tame strain is selected for high social approach behavior toward humans and produces dog-like behaviors, such as licking and tail wagging. In a parallel experiment, the aggressive strain is selected for the opposite behavior and reacts with defensive aggression when faced with human contact. A third conventional strain is kept on the farm but bred without deliberate selection on behavior ( Statham et al., 2011 ). Behavioral differences between tame and aggressive foxes map to a locus on fox chromosome 12, which is homologous to the locus implicated in wolf-to-dog domestication ( Kukekova et al., 2011a , 2012 ) and the whole-genome sequencing of tame, aggressive, and conventional foxes identifies 103 genomic regions differentiating the three populations including 46 regions, which are syntenic to canine candidate domestication regions ( Kukekova et al., 2018 ). Differential gene expression across strains has been established in PFC, basal forebrain, hypothalamus, and anterior pituitary ( Kukekova et al., 2011b ; Hekman et al., 2018 ; Wang et al., 2018 ; Rosenfeld et al., 2020 ). Additionally, tame foxes show increased adult neurogenesis in the hippocampus in comparison to conventional foxes ( Huang et al., 2015 ). However, the brain-wide neuroanatomical consequences of selection on behavior in the fox model are as yet unknown. In this study, we addressed this question using high-resolution, T2-weighted, whole-brain ex vivo neuroimaging in 10 tame, 10 aggressive, and 10 conventional foxes. These were the same individuals used in previous transcriptomic studies ( Kukekova et al., 2011a , 2012 ), and their behavior was tested and analyzed as previously described ( Kukekova et al., 2008 ). We conducted three types of analyses: a comparison of overall gray matter, white matter, and total brain volumes; a comparison of differences in regional gray matter volumes across strains; and a comparison of strain-wise differences in anatomic covariation across regions, which can identify morphologically coevolving structural networks and link them to individual variation in behavior.

• Materials and Methods

Brain specimens

In the current study, we examined the brains of 10 tame, 10 conventional, and 10 aggressive foxes. All foxes were housed with littermates and mother from birth until weaning at 6 weeks, then housed with littermates for a further 4 weeks, and then singly housed in a shed for young foxes with members of the same strain until ∼7 months of age. After that, all 30 foxes used in this experiment were singly housed in the same shed for adult foxes. At all stages of rearing and maintenance, fox interaction with humans was limited to feeding, veterinary care, and testing behavior in home cages at 5.5-6 months of age. All foxes were male, sexually naive, and ∼1.5 years old at the time of brain extraction in August of 2010. Right hemispheres were preserved for gene expression studies; we report analyses in left hemispheres here. Left hemispheres were formalin-fixed and were maintained in formalin solution until scanning in 2016.

Neuroimaging data acquisition

For imaging, brains were placed in a waterproof plastic container, which was packed with polyethylene beads for stabilization. The container was then pumped full of Fluorinert FC-770 (3M). Fluorinert is a fluorocarbon; it is analogous to a hydrocarbon, but with fluorine taking the place of hydrogen. It thus produces no signal in (typical) MRI, which is tuned to the resonant frequency of hydrogen nuclei. Images were acquired on a 9.4 T/20 cm horizontal bore Bruker magnet, interfaced to an Avance console, with Paravision 5.1 software (Bruker). A 7.2-cm-diameter volume radio frequency coil was used for transmission and reception with a RARE T2 sequence (2 averages, 13 ms TE, 2500 ms TR, rare factor 8). Image resolution was 300 µm 3 with a matrix size of 256 × 100 × 88.

Image analysis

Image preprocessing was accomplished using the FSL software package ( Smith et al., 2004 ; Woolrich et al., 2009 ; Jenkinson et al., 2012 ). Images underwent bias correction and segmentation into white matter and gray matter using FAST ( Zhang et al., 2001 ). In order to provide a common spatial framework for morphometric analysis, an unbiased nonlinear template was built from the 10 conventional foxes' T2-weighted images using the ANTS software package ( Avants et al., 2009 ). This template represents the group average morphology across the conventional fox brain specimens. All subject's T2-weighted images were nonlinearly aligned to this template. We computed the Jacobian determinant image of each deformation field; this represents a spatial map of where and how much each individual subject's scan had to deform to come into alignment with the template. The Jacobian determinant images were then masked with the gray matter segmentation images to produce representations of each subject's gray matter deviation from the template, and were then smoothed with a 0.6 mm (2 voxel) Gaussian kernel. Individual foxes' gray-matter masked, smoothed Jacobian determinant images became the input for each of two independent, complementary statistical morphometric analyses. The average of all foxes' masked Jacobian images is shown in Figure 1 B .

Voxel-based morphometry (VBM) ( Ashburner and Friston, 2000 ) is an inherently hypothesis-based approach that performs GLM at each voxel in the image to determine whether morphology is significantly related to explanatory variables (e.g., group). VBM analysis was accomplished using FSL's randomize tool for voxel-wise Monte Carlo permutation testing of GLMs, which permutes explanatory variables across cases to build up a null distribution, and then tests whether observed associations to explanatory variables significantly differ from this random null distribution ( Winkler et al., 2014 ). On the other hand, source-based morphometry (SBM) ( Xu et al., 2009 ) is a data-driven, model-free approach that identifies patterns of significant morphologic correlation across subjects. In other words, it determines which regions of the brain significantly covary with each other across the entire dataset, while remaining agnostic to putative differences across subjects (e.g., group differences). Post hoc tests can then be used to determine whether these networks show significant associations with variables of interest. This was accomplished using the GIFT SBM toolbox for MATLAB ( Xu et al., 2009 ; http://mialab.mrn.org/software/gift/index.html ; for an in-depth discussion of the method and its applications, see Gupta et al., 2019 ). Multiple linear regression was then used to assess the relationship between factor loadings for covarying gray matter networks and factor loadings for a principal components analysis of fox behavioral traits described below. Past research has used SBM mainly in the context of identifying neuroanatomical differences between patient and control populations (e.g., schizophrenia) ( Xu et al., 2009 ; Turner et al., 2012 ; Rodrigue et al., 2020 ), but several studies have also used SBM in animal studies focused on evolved traits: for example, chimpanzee tool use ( Hopkins et al., 2019 ) and eye gaze ( Hopkins et al., 2020 ); and breed-specialized skills in domestic dogs ( Hecht et al., 2019 ). Covariance in morphology across regions is thought to reflect both shared genetic factors and similar patterns of development and functional specialization; these structurally covarying networks appear to be similar to functionally covarying resting state networks ( Alexander-Bloch et al., 2013 ; Evans, 2013 ; Gupta et al., 2019 ). Although SBM identifies networks of structurally covarying regions, it does not assess white matter connections linking those regions.

Assignment of fox behavioral phenotypes

Fox behavior was tested at 5.5-6 months of age in the standard test described by Kukekova et al. (2008) . Fox behavior during the test was scored from the video records for 98 recordable observations ( Table 1 ). The matrix, including scores for 1003 foxes from Kukekova et al. (2011a) and scores for 30 foxes used in this study, were subjected to principal component analysis (PCA) in R using function: prcomp . The distribution of PC1-PC3 values for 30 foxes whose brains are analyzed are shown in Figure 4 .

• View inline

Trait loadings for PCA of behavior

The T2-weighted conventional fox brain template and labels for some anatomic regions are shown in Figure 1 A . A map of variation in brain anatomy across all strains is shown in Figure 1 B ; a graph of gray matter, white matter, and total brain volumes for each strain are shown in Figure 1 C . One-way ANOVAs revealed a strain-wise difference in total gray matter volume ( F (2,27) = 6.855, p = 0.004). Post hoc Tukey's HSD tests indicated that both tame and aggressive foxes had significantly higher gray matter volume than conventional foxes (tame > conventional: t (18) = 3.370, p = 0.003; aggressive > conventional: t (18) = 3.556, p = 0.002), but did not differ significantly from each other ( t (18) = 0.010, p = 0.992). Strain-wise differences in white matter volume and total brain volume did not reach significance (white matter: F (2,27) = 2.186, p = 0.132; total brain volume: F (2,27) = 1.504, p = 0.240).

• Download figure
• Open in new tab
• Download powerpoint

Brain volume shifts in the Russian farm-fox experiment. A , Group-average template with anatomic labels and approximate cortical functional localizations from the dog ( Evans and de Lahunta, 2013 ). olf, Olfactory; pfc, prefrontal; pmc, premotor; mot, motor; ss, somatosensory; aud, auditory; vis, visual. B , Variation in regional morphology across the dataset. Warmer colors represent more variation. Lateral views of 3D surface renderings and coronal cross-sections are shown. C , Strain-wise differences in gray matter, white matter, and total brain volume. Error bars indicate SEM.

Voxel-based morphometry identified a number of differences between strains ( Fig. 2 ). Carnivore cortical mapping studies have been most extensive in cats and ferrets, but relatively less work has been done in dogs, which are more closely related to foxes. Thus, putative functions of anatomic regions are based on known dog anatomy here but should be considered tentative. Relative to aggressive foxes, tame foxes show expansion in portions of the sylvian gyrus and ectosylvian sulcus (temporal regions that include auditory cortex and other regions, potentially higher-order visual or multisensory cortex; Fig. 2 A ) ( Kosmal, 2000 ). In contrast, compared with tame foxes, aggressive foxes show expansion in portions of the rostral composite gyrus and presylvian sulcus (potentially somatosensory and/or premotor-prefrontal transition cortex) ( Kosmal et al., 1984 ) and in the ectosylvian and sylvian gyri and sylvian sulcus (auditory and association cortex in dogs; Fig. 2 B ) ( Kosmal, 2000 ). Surprisingly, relative to the conventional strain, both tame and aggressive foxes show expansion in similar regions, including portions of the prorean, orbital, frontal, precruciate, and rostral composite gyri (prefrontal, premotor, and motor cortex in dogs) ( Kosmal et al., 1984 ), amygdala, hippocampus, and cerebellum ( Fig. 2 C , D ; overlap shown in Fig. 2 E ). No voxels showed reduced volume in tame or aggressive foxes relative to conventional foxes. Anatomical locations, maximum t statistics, number of voxels, and volume for each cluster are shown in Table 2 .

Clusters resulting from VBM analysis a

Differences in regional gray matter volume between strains. A , Tame > aggressive. B , Aggressive > tame. C , Tame > conventional. D , Aggressive > conventional. E , Tame and aggressive both > conventional. Color code: red represents frontal cortex; green represents amygdala; magenta represents hippocampus; blue and cyan represents cerebellum.

Notably, the hypothalamus was one of the regions with the highest volumetric variation across the entire dataset ( Fig. 1 B ), but direct group-wise comparisons did not identify significant volumetric differences between strains ( Fig. 2 ). Past studies on the farm-fox experiment have implicated the hypothalamo-pituitary-adrenal axis generally (for review, see Trut et al., 2009 ) and gene expression in the hypothalamus specifically ( Rosenfeld et al., 2020 ). Neuroanatomical consequences of rapid selection on behavior can be visible not only in changes to relative volume of brain regions, but also in the degree of morphologic correlation across brain regions, as we recently documented in domestic dog breeds ( Hecht et al., 2019 ). To probe this possibility, we used source-based morphometry, a model-free, ICA-based approach ( Xu et al., 2009 ), to identify structurally covarying multiregion networks across the entire dataset (but white matter connectivity is not assessed with this method). This identified four significantly covarying brain networks ( Fig. 3 ; Table 3 ).

Clusters resulting from SBM analysis

Regionally covarying structural brain networks and relationship to strain membership and individual behavior scores. Red-yellow and blue-green components of each network are anticorrelated; only significant voxels are shown for each network. Bar graphs represent factor loadings for each strain; positive loadings indicate larger volumes in red-yellow regions (represented with red dot), whereas negative loadings indicate larger volumes for blue-green regions (represented with blue dot). Partial regression plots represent significant relationships between factor loadings for Networks 2-4 and behavior measurements PC1-PC3 in each fox. A , Network 1 factor loadings did not differentiate between strains and were not significantly related to behavior scores. B , Network 2 factor loadings differentiated between tame and aggressive strains and were significantly related to PC1 behavior scores. C , Network 3 factor loadings differentiated the tame and aggressive strains from the conventional strain and were significantly related to PC2 behavior scores. D , Network 4 factor loadings did not differentiate between strains and were marginally related to PC3 behavior scores.

We then investigated the extent to which these networks were related to strain membership and to individual behavior scores. Behavior scores were subjected to a PCA analysis, resulting in three components, each of which explains 29.0%, 8.0%, and 6.6% of variance, respectively. We then used multiple linear regression to probe the relationship between factor loadings for these three behavior components ( Table 1 ; Fig. 4 ) and our four morphometry components ( Table 3 ).

Population distributions for the first three PCs (PC1-PC3) of fox behavior. Aggr, “Aggressive” population; Conv, “conventional farm-bred population”; Tame, “tame” population. Black dots represent individual data points. Horizontal bars within each box represent the population median. The whiskers represent the range of data up to 1.5 times the interquartile range.

Network 1 contained clusters in the thalamus, caudate, NAc, cerebellum, and other regions ( Fig. 3 A ). Factor loadings were in opposite directions for the tame and aggressive strains but were centered near zero with wide variance in the conventional strain; however, strain-wise differences did not reach significance ( F (2,27) = 0.475, p = 0.627). Multiple linear regression indicated that factor loadings for Network 1 accounted for 11.6% of the variance in behavior PCA scores, but the overall regression model did not reach significance ( F (3,26) = 1.137, p = 0.352), nor did any of the partial correlations between brain and behavior factor loadings.

Network 2 was mainly comprised of one cluster that covered most of the hypothalamus, plus several other clusters scattered throughout the cerebellum. Factor loadings strongly differentiated the tame and aggressive strains from each other and were centered near zero for the conventional strain. Strain-wise differences were significant ( F (2,27) = 4.495, p = 0.021; Fig. 3 B ). Post hoc tests using Tukey correction for multiple comparisons confirmed that factor loadings significantly differentiated the tame and aggressive strains from each other ( p = 0.016). Loading coefficients for Network 2 accounted for 31.0% of the variance in behavior scores. The overall regression model reached significance ( F (3,26) = 3.908, p = 0.020). In examining partial correlations with individual behavior categories, we applied the Benjamini-Hochberg method for FDR correction. This revealed a significant partial correlation with PC1 behavior scores (β = 0.166, t = 2.964, p =0.006, which exceeded the critical value of 0.017). Generally, behavioral traits with the highest positive loadings for PC1 describe tame behavior and proximity to a human approacher, whereas traits with the most negative loadings describe aggressive behavior and greater distance from a human approacher ( Table 1 ; Fig. 4 ). Examination of the partial correlation scatter plot reveals that tame foxes cluster together with higher scores for both behavior and neuroanatomy, whereas aggressive and conventional foxes cluster together on the lower end of both axes ( Fig. 3 3 ).

Network 3 contained two smaller, discrete clusters in the hypothalamus, plus a large cluster covering much of prefrontal and premotor cortex, including portions of the prorean, orbital, frontal, precruciate, and rostral composite gyri. For this network, factor loadings were similar for the tame and aggressive strains, and both were strongly opposite to the conventional foxes; the strain-wise difference was significant ( F (2,27) = 14.795, p < 0.001; Fig. 3 C ). Post hoc Tukey tests revealed that this network significantly differentiated both the tame strain from the conventional strain ( p = 0.001) and the aggressive strain from the conventional strain ( p = 0.000). Regression analyses revealed that behavior scores accounted for 35.3% of the variance in morphometry loading coefficients. The overall regression model reached significance ( F (3,26) = 4.720, p = 0.009). Examination of partial correlations using Benjamini-Hochberg FDR correction revealed that there was a significant partial correlation with PC2 (β = 0.483, t = 3.251, p = 0.003, which exceeded the critical value of 0.017). For PC2, traits with the highest positive loadings describe active aggressive response and fox position in the front part of the cage, whereas traits with highest negative loadings describe a passive tame response: tolerance of human tactile contact and fox position in the back of the cage ( Table 1 ; Fig. 4 ). Examination of the partial correlation scatter plot reveals that aggressive foxes tended to score high for both the behavior and neuroanatomical measures, whereas conventional foxes tended to score low on both, and tame foxes were tightly clustered in the intermediate range ( Fig. 3 C ).

Network 4 contained a large cluster that spanned regions of the thalamus, most of the hypothalamus, and portions of the NAc/ventral forebrain and caudate ( Fig. 3 D ). There were also several additional clusters located in cortex and cerebellum. Factor loadings were again opposite for the tame and aggressive strains, and centered near zero for the conventional strain; strain-wise differences did not reach significance ( F (2,27) = 1.198, p = 0.312). Loading coefficients for Network 4 accounted for 14.6% of the variance in behavior scores. The overall regression model did not reach significance ( F (3,26) = 1.413, p = 0.242). None of the partial correlations between morphometry and behavior scores reached significance, but there was a marginally positive relationship with PC3 (β = 0.492, t = 1.780, p = 0.087, which did not exceed the critical value of 0.017). In PC3, traits with the highest positive loadings describe neutral exploratory behavior (e.g., “ears are vertical”), whereas traits with the most negative loadings describe prosocial greeting behavior and fox position in the front part of the cage (see Table 1 ). Tame, aggressive, and conventional foxes showed marked overlap in both behavior and neural scores in this analysis ( Fig. 3 D ).

The Russian farm-fox experiment is perhaps the longest-running, best-controlled, and most well-known artificial selection study bearing on the evolution of mammalian behavior. As such, it enables a uniquely powerful window on the neural mechanisms governing behavioral adaptation. This study used high-resolution MRI to examine the brains of these foxes. We found that selection on social behavior has altered the anatomy of distributed gray matter networks, which included, among other regions, PFC, hippocampus, amygdala, caudate, NAc, cerebellum, and hypothalamus. These regions have also been implicated in past studies in these foxes ( Kukekova et al., 2011b ; Huang et al., 2015 ; Hekman et al., 2018 ; Wang et al., 2018 ; Rosenfeld et al., 2020 ) and in past studies on wolf-to-dog domestication ( Nikulina, 1991 ; Saetre et al., 2004 ; Natt et al., 2012 ; Li et al., 2013 ; Ruan and Zhang, 2016 ; Spocter et al., 2018 ; Oshchepkov et al., 2019 ). Interestingly, some of these regions are also affected by domestication in rabbits ( Brusini et al., 2018 ).

Notably, portions of fox PFC appeared in several of our results ( Figs. 2 E , 3 A , 3 C ). How can the functional relevance of this region be interpreted? Although some of these prefrontal results are located on the dorsolateral surface of the brain (i.e., the prorean gyrus), this region is likely not homologous to the granular dorsolateral PFC of humans and macaque monkeys, as that region is thought to be unique to primates ( Preuss, 1995 ; Passingham and Wise, 2012 ). Rather, the connectivity and cytoarchitecture of carnivore PFC ( Narkiewicz and Brutkowski, 1967 ; Kosmal and Dabrowska, 1980 ; Kosmal, 1981a , b ; Stepniewska and Kosmal, 1986 ; Markow-Rajkowska and Kosmal, 1987 ; Rajkowska and Kosmal, 1988 ) are more similar to that of the dysgranular and agranular portions of primate orbitofrontal and ventromedial PFC, regions that function to integrate external multisensory and internal visceromotor information with limbic reward and threat signals to compare the value of potential behavioral choices ( Carmichael and Price, 1996 ; Rudebeck and Murray, 2011 ). Putatively, this circuitry has been altered in tame foxes to bias behavioral decisions toward the reward value of social contact with humans, and in aggressive foxes toward the opposite. This interpretation fits generally with conceptualizations of partially shared circuitry between social approach and social avoidance processing in humans and other species ( Aupperle and Paulus, 2010 ).

However, the current study also produced some findings which were unexpected and suggest revision of existing thinking about domestication. One of these was that total gray matter volume in both the tame strain and the aggressive strain is increased compared with the conventional strain. These findings are in contrast to a number of prior studies which have reported that domestication reduces brain size in diverse species including Atlantic cod ( Mayer et al., 2011 ), guppies ( Burns et al., 2009 ), rainbow trout ( Marchetti and Nevitt, 2003 ), mallard ducks ( Ebinger, 1995 ), rats, mice, gerbils, guinea pigs, rabbits, pigs, sheep, llamas, horses, ferrets, cats, and dogs (for review, see Kruska, 2005 ). Brain size should be interpreted in the context of body size, given that the two covary. While body size measurements were not available for the foxes in our study, Huang et al. (2015) report a 15.9% reduction in body weight in tame compared with conventional foxes, suggesting that, if anything, differences in brain:body size ratios are more pronounced than the brain measurements alone would indicate. What might cause this increase in brain size? One possible explanation might involve neuroplastic changes resulting from differential lifetime experience. The link between naturalistic, enriched environments and larger, more complex brains has been noted for decades ( van Praag et al., 2000 ; Lambert et al., 2019 ). Tame, aggressive, and conventional foxes are all housed in identical conditions and undergo identical treatment with minimally necessary human interaction. Nonetheless, tame foxes, because of their innate predisposition toward prosocial interaction with humans, may effectively experience this environment to be more naturalistic and enriched.

However, this potential interpretation does not explain why the aggressive strain also shows increased gray matter volume relative to controls. Perhaps their constant drive to avoid human contact functions as a sort of enrichment, but we instead favor an alternative explanation. Both the tame and aggressive strains have been subject to intense, sustained selection on behavior, while the conventional strain undergoes no such intentional selection. Thus, it is possible that fast evolution of behavior, at least initially, may generally proceed via increases in gray matter. Several potential mechanisms might underlie this effect. First, because of developmental linkages, selection pressure for increased size in one region may “drag along” enlargement in others to some extent ( Finlay et al., 2001 ), although it seems apparent that the current dataset also reflects at least some degree of modular evolution (i.e., focused selection pressure on specific regions and networks) ( Striedter, 2020 ). Second, selection pressure for expansion of a particular brain region might favor genomic variants leading to changes in expression of genes with potential pleiotropic effects (e.g., transcription factors). Consequently, these gene expression changes could produce expansion not only in that one region but also in others. Normally, trade-offs with metabolic and life history constraints ( Isler and van Schaik, 2009 ) might favor further fine-tuning of the activity of these genes so that the effect occurs more specifically only in the “targeted” brain region, but because captivity reduces the pressure for optimization, this fine-tuning might fail to occur. Third, because of the complex interdependencies between brain systems, adaptive solutions that modify one existing system may stand a high likelihood of producing deleterious effects in others unless additional compensatory adaptations also occur ( De Vries, 2004 ). In the context of extreme selection pressure, these compensatory changes might be more likely to occur via the addition of new neural material rather than via volumetrically net-zero alterations to existing circuits, which putatively would require more fine-tuned genetic changes. In the wild, there would be constant pressure against these “easy, wasteful” solutions, but in the context of the farm-fox experiment, these constraints may have been lessened or removed, as these foxes are not bred for increased meat yields, more rapid maturation, or reduced feeding costs. In general, it is important to note that strong selection for a single dimension of behavior in captivity, as occurred in the farm-fox experiment, is expected to differ in important ways from selection in the wild, which occurs on many behaviors at once. Because of this, experimentally applied selection pressure might be more likely to produce “nonoptimal” brain network changes, in contrast to in the wild, where such shifts might produce detrimental effects on other behaviors, and, importantly, on animal survival. There are multiple potential cellular-level causes for increased gray matter, including increased neuron count, increased neuron size, and/or dendritic changes, such as increased arborization or spine density ( Zatorre et al., 2012 ; Keifer et al., 2015 ). Future research, including single-cell transcriptomics and histologic work, will be required to differentiate among these possibilities.

Notably, a recent skeletal morphology study did not find a significant difference in endocranial volume between tame and conventional foxes ( Kistner et al., 2021 ). The foxes that became the progenitor population for Belyaev's study had existed in a farmed state in Russia for ∼50 years ( Kochergin, 1936 ; Vahrameyev and Belyaev, 1948 ); this original Russian farmed population was itself drawn largely from Eastern Canadian foxes ( Statham et al., 2011 ; Rando et al., 2017 ) bred at fur farms on Prince Edward Island ( Forester and Forester, 1982 ). Kistner et al. (2021) compared endocranial volumes of modern Russian farm-fox skulls to skulls from wild foxes, which had been collected in Canada east of Quebec between 1884 and 1952, with 70% collected between 1894 and 1900. This revealed that endocranial volume in the modern, conventional Russian farm-raised foxes (i.e., those bred without selection on behavior) was significantly reduced compared with the archived Canadian wild skulls. However, no significant difference was observed between modern tame and conventional strains, but notably, like the current study, Kistner et al. (2021) were unable to incorporate body size measurements into their analyses. We also do not know whether the skull morphology of conventional foxes started to show differences at the time when selection of conventional foxes for tameness in Russia began (1959) or whether it became pronounced later when the conventional population was evolving in parallel with the tame population. Together with these findings, the current study hints that the brain volume reduction associated with domestication might occur relatively quickly, before the onset of intentional selection on behavior. Further research is required to establish whether this is true.

A second surprising result from this study was that both tame and aggressive foxes showed enlargement in substantially overlapping gray matter regions, including PFC, amygdala, hippocampus, and cerebellum ( Fig. 2 E ). In addition to these volumetric effects, we also observed strain-wise differences in the degree of morphologic covariation across distributed, multiregion networks. These latter measurements revealed links with individual variation in behavior, including in brain regions that did not show volumetric differences, notably, the hypothalamus. Additionally, Network 3 consisted primarily of the hypothalamus and PFC, two regions strongly implicated in both fox and dog domestication ( Nikulina, 1991 ; Saetre et al., 2004 ; Kukekova et al., 2011b ; Natt et al., 2012 ; Li et al., 2013 ; Ruan and Zhang, 2016 ; Spocter et al., 2018 ; Wang et al., 2018 ; Oshchepkov et al., 2019 ; Rosenfeld et al., 2020 ). In this network, factor loadings did not differentiate the tame from aggressive strains; rather, the selectively bred strains together were differentiated from the conventional strain ( Fig. 3 C ). Together, these results indicate that selection for opposite behavioral responses (docility vs aggression) can produce similar evolved changes in the brain. This has important implications for attempts to evaluate the hypothesis that humans are ourselves self-domesticated ( Sanchez-Villagra and van Schaik, 2019 ), given that similar neuroanatomical patterns of change could now be interpreted to support either selection for increased or decreased aggression in our lineage. Notably, Trut et al. (2017) reported some elements of the “domestication syndrome” in aggressive foxes, including altered timing of annual reproductive activity, facial foreshortening, and facial “star” marking; they thus propose that these traits might result pleiotropically from selection on either tameness or aggression (i.e., as a result of selection on social behavior generally). This calls for additional research on the neural correlates of evolved differences in both docility and aggression at the cellular and genomic levels.

The Russian farm-fox experiment represents a uniquely well-controlled opportunity to study the effects of specific, sustained selection on behavior. Thus, apart from questions of domestication, an additional implication of these results concerns brain evolution on a more general level. We found that intense selection on behavior can produce gross changes in distributed brain morphology extremely rapidly (within the span of well under 100 generations). This suggests that the brains of other animals on this planet, including Homo sapiens , may have undergone similarly precipitous morphologic shifts any time steep selection on behavior was experienced.

a Within each network, the negative components (shown as blue in Fig. 3 ) and positive components (shown as red in Fig. 3 ) are morphologically anticorrelated. Each component contains multiple clusters, indicated by Cluster index. Voxel coordinates are for maximum value in cluster.

E.E.H., T.M.P., D.A.G., and neuroimaging scan costs were supported by National Science Foundation IOS #1457291. A.V.K., sample collection, and behavioral data analysis were supported by National Institutes of Health Grant GM120782. We thank Jaekeun Park and Orion Keifer for assistance with scan acquisition; Olivia Zarella and Jeromy Dooyema for assistance with sample preparation; Yury E. Herbeck and Anastasiya V. Kharlamova for insightful discussions and help in preparation of the experiments at the experimental farm of the Institute of Cytology and Genetics (Novosibirsk, Russia); and Irina V. Pivovarova, Anastasiya V. Vladimirova, Tatyana I. Semenova, Eugene A. Martinov, and all the animal keepers at the Institute of Cytology and Genetics experimental farm for research assistance. L.N.T., the fox colony, sample collection, and behavioral data analysis were supported by the Institute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences grant 0259-2021-0016

The authors declare no competing financial interests.

• Correspondence should be addressed to Erin E. Hecht at erin_hecht{at}fas.harvard.edu

SfN exclusive license .

• Alexander-Bloch A ,
• Ashburner J ,
• Aupperle RL ,
• Tustison N ,
• Brusini I ,
• Carneiro M ,
• Blanco-Aguiar JA ,
• Ferrand N ,
• Villafuerte R ,
• Damberg P ,
• Hallbook F ,
• Fredrikson M ,
• Andersson L
• Saravanan A ,
• Carmichael ST ,
• Reinoso-Suárez F
• De Vries GJ
• de Lahunta A
• Finlay BL ,
• Darlington RB ,
• Forester JE ,
• Forester AD
• Turner JA ,
• Smaers JB ,
• Preuss TM ,
• Hekman JP ,
• Johnson JL ,
• Edwards W ,
• Vladimirova AV ,
• Gulevich RG ,
• Kharlamova AV ,
• Herbeck Y ,
• Acland GM ,
• Raetzman LT ,
• Kukekova AV
• Hopkins WD ,
• Latzman RD ,
• Mareno MC ,
• Schapiro SJ ,
• Gomez-Robles A ,
• Sherwood CC
• Mulholland MM ,
• Reamer LA ,
• Schapiro SJ
• Slomianka L ,
• Farmer AJ ,
• Herbeck YE ,
• Wolfer DP ,
• van Schaik CP
• Jenkinson M ,
• Beckmann CF ,
• Behrens TE ,
• Woolrich MW ,
• Keifer OP Jr . ,
• Gutman DA ,
• Keilholz SD ,
• Gourley SL ,
• Kistner T ,
• Worthington S ,
• Lieberman DE
• Kochergin AF
• Dabrowska J
• Stepniewska I
• Kukekova AV ,
• Shepeleva DV ,
• Oskina IN ,
• Stepika A ,
• Klebanov S ,
• Temnykh SV ,
• Shikhevich SG ,
• Teiling C ,
• Dubreuil MM ,
• Ponnala L ,
• Serdyukova NA ,
• Beklemischeva V ,
• Koepfli KP ,
• Perelman PL ,
• Graphodatsky AS ,
• O'Brien SJ ,
• Clark AG , et al
• Lambert K ,
• Kempermann G ,
• Merzenich M
• Vonholdt BM ,
• Reynolds A ,
• MacHugh DE ,
• Marchetti MP ,
• Markow-Rajkowska G ,
• Skjæraasen JE ,
• Rodewald P ,
• Sverdrup G ,
• Narkiewicz O ,
• Brutkowski S
• Johnsson M ,
• Belteky J ,
• Andersson L ,
• Nikulina EM
• Oshchepkov D ,
• Ponomarenko M ,
• Klimova N ,
• Chadaeva I ,
• Sharypova E ,
• Shikhevich S ,
• Kozhemyakina R
• Passingham RE ,
• Rajkowska G ,
• Stutchman JT ,
• Bastounes ER ,
• Driscoll CA ,
• Rodrigue AL ,
• Alexander-Bloch AF ,
• Knowles EE ,
• Mathias SR ,
• Koenis MM ,
• Perrone-Bizzozero NI ,
• Calhoun VD ,
• Rosenfeld CS ,
• Ortega MT ,
• Behura SK ,
• Rudebeck PH ,
• Lindberg J ,
• Leonard JA ,
• Pettersson U ,
• Ellegren H ,
• Bergstrom TF ,
• Sanchez-Villagra MR ,
• Skoglund P ,
• Gotherstrom A ,
• Jakobsson M
• Johansen-Berg H ,
• Bannister PR ,
• De Luca M ,
• Drobnjak I ,
• Flitney DE ,
• Saunders J ,
• Vickers J ,
• De Stefano N ,
• Matthews PM
• Spocter MA ,
• Wicinski B ,
• Bitterman K ,
• Raghanti MA ,
• Sherwood CC ,
• Jovanovik J ,
• Rusbridge C ,
• Statham MJ ,
• Stepniewska I ,
• Striedter GF
• Kharlamova A
• Michael A ,
• van Erp TG ,
• Ehrlich S ,
• Segall JM ,
• Gollub RL ,
• Csernansky J ,
• Potkin SG ,
• Bustillo J ,
• Vahrameyev KA ,
• van Praag H ,
• Winkler AM ,
• Ridgway GR ,
• Webster MA ,
• Patenaude B ,
• Chappell M ,
• Behrens T ,
• Beckmann C ,
• Wrangham RW
• Pearlson G ,
• Schretlen DJ ,
• Zatorre RJ ,
• Fields RD ,
• Johansen-Berg H

In this issue

• Table of Contents
• Table of Contents (PDF)
• About the Cover
• Index by author
• Ed Board (PDF)

Thank you for sharing this Journal of Neuroscience article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Citation Manager Formats

• EndNote (tagged)
• EndNote 8 (xml)
• RefWorks Tagged
• Ref Manager

• Tweet Widget
• Facebook Like
• Google Plus One

Jump to section

Responses to this article, jump to comment:, related articles, cited by..., more in this toc section, research articles.

• Generalized encoding of the relative subjective value of cognitive effort in dorsal ACC
• Cracking and packing information about the features of expected rewards in the orbitofrontal cortex
• Single-cell Profiling Uncovers Evolutionary Divergence of Hypocretin/Orexin Neuronal Subpopulations

Behavioral/Cognitive

• Striatal serotonin release signals reward value

Is this Siberian fox wild, domesticated or something in between?

• By Ashley Cleek

Irina Mukhamedshina feeds her fox, Viliya. One of the fox’s tricks is to jump on Irina’s shoulder.

Every day at 5 p.m., Irina Mukhamedshina takes her pet fox out for a walk.

They take the elevator down from her sixth floor apartment and walk out into a snowy yard.  The fox, on a leash, runs out and immediately starts tunneling into a pile of snow.

Irina's fox is named Viliya and is both a pet and Irina's dissertation project. Irina is a graduate student at the Institute of Cytology and Genetics  outside of Novosibirsk, the capital of Siberia.

She walks Viliya through apartment blocks and playgrounds. The fox waits patiently to cross the street.

As they walk, groups of women coo at the fox, “what a beauty,” almost like it's a baby. Grown men stop, stare, and snap photos of Viliya.  An elderly woman walking past asks, “Is that a wild animal? Or a domesticated pet?” Irina answers that the fox is somewhere in between.

In fact, Viliya is the result of decades of calculated selection to see if it's possible to repeat the domestication of a wild animal, like a wolf, into a pet, like a dog.

The experiments were begun in Novosibirsk  in the 1950s  by a Russian scientist named Dmitri Belayev. Belayev didn't rely on natural selection. Instead, he selected foxes based on one characteristic: whether or not they would approach humans.

Ludmilla Trut, who was a student of Belayev's and is now the director of the institute, explains that the researchers would go up to cages of foxes at a fur farm, poke a stick into the cage and see how the foxes reacted.

Trut says some foxes would be really aggressive and suddenly attack the stick, while others would run to the corner of the cage and hide. Very few of the foxes would walk toward the stick, smell it, and look directly at the researcher. Trut explains that the researchers took those foxes as the initial population.

After just 10 years, Trut says, the researchers started to see changes. Wild foxes' tails usually stand up straight, but the foxes they selected and bred had tails that were down and even curled. They started wagging their tales. Over generations, the foxes' faces changed from pointed to rounded.

After more than 50 years, scientists are still searching for the genes that make an animal either domestic or wild. Of course, it may take a lot longer.

But another of the original goals was to see if it was possible to train a fox like a dog.  And that's where Irina and Viliya come in.

Back in her apartment, Irina cuts up some cheese and starts issuing commands.

Viliya circles in front of Irina, waiting for a command. Irina tells Viliya to sit. The fox sits. Stand. Viliya stands.

The fox walks backwards on command. Irina makes a circle with her arms and Viliya jumps through it. Irina hides a piece of cheese behind a dresser and commands Viliya to search. Viliya finds it.

So, a tamed fox can be trained. Even so, Irina says Viliya's not fully domesticated. She explains that the foxes have been selected for 50 years for the sole quality of whether or not they were kind to humans.

Irina stresses that even though a fox can obey commands, it doesn't have the concentration of a dog.

The city makes Viliya nervous. The fox can't be left alone in the apartment. She is disobedient and not totally house-trained. Irina plans to breed Viliya and study her offspring. She wants to see how the pups will grow up, especially around dogs and people.

And it's important work because tame foxes are slowly becoming popular pets around the world. Research costs are expensive in Russia and government funding is not always easy to get, so every year, the institute sells a few of the foxes.

On her walks, Irina says people  occasionally  chide her for having a wild animal on a leash. But, she explains to them, Viliya is not a wild animal.

Once, on a walk, Viliya ran off and got lost. But she didn't run to the forest. Viliya went straight to a nearby house. A family let her in and Viliya began playing with their pet dog. They returned the fox to Irina.

As Irina finishes her tea, on the other side of the closed kitchen door, Viliya lies half asleep, waiting for Irina.

One quick look and you would swear she was a dog.

Reporter Ashley Cleek traveled to Russia on a  Social Expertise Exchange fellowship  provided by the Eurasia Foundation.

We’d love to hear your thoughts on The World. Please take our 5-min. survey.

• Yekaterinburg Tourism
• Yekaterinburg Hotels
• Yekaterinburg Bed and Breakfast
• Flights to Yekaterinburg
• Yekaterinburg Restaurants
• Things to Do in Yekaterinburg
• Yekaterinburg Travel Forum
• Yekaterinburg Photos
• Yekaterinburg Map
• All Yekaterinburg Hotels
• Yekaterinburg Hotel Deals

Canadian/American Family Moving to Ek - Yekaterinburg Forum

• Europe    
• Russia    
• Urals District    
• Sverdlovsk Oblast    
• Yekaterinburg    

Canadian/American Family Moving to Ek

• United States Forums
• Europe Forums
• Canada Forums
• Asia Forums
• Central America Forums
• Africa Forums
• Caribbean Forums
• Mexico Forums
• South Pacific Forums
• South America Forums
• Middle East Forums
• Honeymoons and Romance
• Business Travel
• Train Travel
• Traveling With Disabilities
• Tripadvisor Support
• Solo Travel
• Bargain Travel
• Timeshares / Vacation Rentals
• Sverdlovsk Oblast forums
• Yekaterinburg forum

We are a Canadian/American family who will be living in EK part time for the next 2 years !! We have a 4.5 year old and an 11 month old!! I am nervous because it is very hard to find any English friendly information, I've been looking for months trying to prepare as much as possible!!

Looking for any info that would be useful for English speaking family!! I'm in search of internal preschool? and English speaking nanny. I can't find a single one on care.com or any paid site I'm a member of!! Any kid friendly activities, for December are there Christmas festivals? Thank you!!

what's wrong with learning russian? The kid will learn fast and yet speak english at home.

English speaking nanny will be very easy to find, in recent years english courses have been developing a lot in european part of Russia. You'll get english speaking students very easily.

I spend last summer in Yekat, stood there also in spring 2012, and there was a language school for english run by an american. Can't remember the name but should be easy to find. You can ask that kind of people about local possibilities.

There are also a british and an american consulates. These spies should have their own network for english-only services to their families. Maybe first places to ask.

By the way, if you are send there without a clue about russian, it's probably on some expat job and the employer should provide information?

Try expat.ru site.

This is the place of hangouts of expats in Russia.

Just a hint:

It's very unlikely that people in Yekaterinburg will appreciate being called anything like 'Ek' dwellers.

I live in Tyumen, that’s 300 km from Ekaterinburg. Feel free to address if you need any assistance.

I suggest when you arrive go to the Ural State University and put an advert there for an English-speaking nanny. I am sure there will be plenty of students who would like to practice there English with you and get some extra money.

E-burg or Ekat dwellers would be just fine ;-)

We don't celebrate 24/25th of December but we really celebrate the New Year's Eve. And of course, a lot of kid events are organized for this time of the year.

1. For example on the 29th of December they will open an ice town on the main city square "Square of the year 1905". Kids love it there.

http://god2018.su/ledovyj-gorodok-ekaterinburg-2018/#%D0%9E%D1%82%D0%BA%D1%80%D1%8B%D1%82%D0%B8%D0%B5%20%D0%BB%D0%B5%D0%B4%D0%BE%D0%B2%D0%BE%D0%B3%D0%BE%20%D0%B3%D0%BE%D1%80%D0%BE%D0%B4%D0%BA%D0%B0

There will be shows and dances organized. Of course, all of it will be in Russian. I don't know how comfortable you'd feel about it.

The children will love it, you might take a while to adjust.

Hello! Are u still looking for help in Yekaterinburg?

This topic has been closed to new posts due to inactivity.

• Trip to "The Obelisk on the Border Between Europe and Asia" Oct 19, 2023
• Trip to Ganina Yama Sep 06, 2023
• Trip to Yekaterinburg Jul 27, 2023
• Asian grocery store yekaterinburg? Jul 25, 2021
• Taxi or transfer Jan 21, 2020
• Anyone going from US to Yekaterinburg? Nov 02, 2019
• Trans Siberian via Ekaterinsburg Aug 30, 2019
• Halal food and groceries in Yekatrerinburg Aug 02, 2019
• Taxi service from the airport Apr 08, 2019
• Photo of the word Ekaterina or similar Jan 31, 2019
• Can I know the story of this outdoor music score? Jul 28, 2018
• Air conditioning transiberian trains ? Temperature average Jul 11, 2018
• Hiking in Ekaterimburg Jul 09, 2018
• Express Taxi from Arena to Airport on the 21/06/2018 Jun 14, 2018
• Guide in Ekat 2 replies
• Homestay in Ekaterinburg 3 replies
• Yekaterinburg tour wanted - may 2012 2 replies
• Ekaterinburg Can Be Enjoyible? 23 replies
• Yekatrinburg or Nizhny Novgorod? 7 replies
• UralTerra 4 replies
• ekateringburg circus opening times 2 replies

Yekaterinburg Hotels and Places to Stay

• GreenLeaders

• 10 Reasons To Visit Yekaterinburg

10 Reasons to Visit Yekaterinburg

Known as Sverdlovsk during the Soviet era, Yekaterinburg is located at the crossroads of Europe and Asia. Russia’s third city might be a little more subdued than Moscow but is has plenty of culture and urban romanticism to offer. Here are 10 reasons you should buy your ticket to Yekaterinburg right now.

Unique architectural environment, glorious music scene, industrial heritage.

Russia’s best city for business and investment, Yekaterinburg is often referred to as the unofficial capital of the Urals – the region, where Russia’s largest metallurgical enterprises are concentrated. Metal produced by Yekaterinburg plants was used to build some of the world’s most illustrious landmarks: New York’s Statue of Liberty , the Eiffel Tower in Paris and the Houses of Parliament in London. You can learn about the city’s industrial past (and present as well) on one of many city tours and hear about Yekaterinburg’s first metallurgical plant, built in 1704, and see the legendary Uralmash with your own eyes.

Exceptional museums

Memorial, Museum, Theater

Vibrant art scene

Become a Culture Tripper!

Sign up to our newsletter to save up to $1,200 on our unique trips..

See privacy policy .

Dramatic past

Great outdoors, world’s shortest metro.

First opened in 1991, Yekaterinburg Metro was considered the shortest in the world and even got a mention in the Guinness Book of Records . Now it has several stations and the ride from the first to the last will take you only 19 minutes, but be sure to stop and take a closer look at each of them – they are all unique and exceptionally beautiful.

Gemstones and jewellery

Once rich in gemstones and minerals, the Ural Mountains, and Yekaterinburg as the region’s main city, have become a center for jewelry trade, known for brilliant craftsmen, carving masterpieces out of gemstones. You can still hear some beautiful legends, the Mistress of Copper Mountain being the most popular and visit many very real shops, selling locally made jewellery.

https://www.instagram.com/p/41QsojtK7_/?taken-at=504562987

See & Do

Russia's most remote holiday destinations.

The Mystery Behind Russia's Buddhist "Miracle"

The Soviet Union’s Best Heart-Throbs and Pinups

Food & Drink

The best halal restaurants in kazan.

Zhenotdel: The Soviet Union's Feminist Movement

Incredible Photos From the Longest Bike Race in the World

Guides & Tips

A 48 hour guide to astrakhan, russia.

Russian Last Names and Their Meanings

A Soviet Pilot Went Missing in Afghanistan and Was Found 30 Years Later

Unusual Facts About the Soviet Union

A Guide to Cautionary Russian Proverbs and What They Mean

Restaurants

The best halal restaurants in kaliningrad.

Culture Trip Summer Sale

Save up to $1,200 on our unique small-group trips! Limited spots.

• Post ID: 1369984
• Sponsored? No
• View Payload