Dugatkin Evo Edu Outreach (2018) 11:16

https://doi.org/10.1186/s12052-018-0090-x Evolution: Education and Outreach

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The silver fox domestication experiment

Lee Alan Dugatkin*

Abstract 
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.
Keywords:  Domestication, Evolution, Silver foxes

Introduction, history and findings domesticated species, over time, begin to display traits
Today the domesticated foxes at an experimental farm in the domestication syndrome. Why? Belyaev hypoth-
near the Institute of Cytology and Genetics in Novosi- esized that the one thing our ancestors always needed
birsk, Siberia are inherently as calm as any lapdog. What’s in a species they were domesticating was an animal that
more, they look eerily dog-like. All of this is the result interacted prosocially with humans. We can’t have our
of what is known as the silver fox, or farm fox, domes- domesticates-to-be trying to bite our heads off. And so he
tication study. It began with a Russian geneticist named hypothesized that the early stages of all animal domes-
Dmitri Belyaev. In the late 1930s Belyaev was a student at tication events involved choosing the calmest, most
the Ivanova Agricultural Academy in Moscow. After he prosocial-toward-human animals: I will refer to this trait
graduated he fought in World War II, and subsequently as tameness, though that term is used in many differ-
landed a job at the Institute for Fur Breeding Animals in ent ways in the literature. Belyaev further hypothesized
Moscow. that all of the traits in the domestication syndrome were
Both as a result of his reading of Darwin’s The Varia- somehow or another, though he didn’t know how or why,
tion of Animals and Plants Under Domestication (Darwin genetically linked to genes associated with tameness.
1868), and his interaction with domesticated animals at Belyaev set out to test these hypotheses using a species
the Ivanova Agricultural Academy and at the Institute for he had worked with extensively at the Institute for Fur
Fur Breeding Animals, Belyaev knew that many domes- Breeding: the silver fox, a variant of the red fox (Vulpes
ticated species share a suite of characteristics including vulpes). Every generation he and his team would test
floppy ears, short, curly tails, juvenilized facial and body hundreds of foxes, and the top 10% of the tamest would
features, reduced stress hormone levels, mottled fur, and be selected to parent the next generation. They developed
relatively long reproductive seasons. Today this suite of a scale for scoring tameness, and how a fox scored on
traits is known as the domestication syndrome. Belyaev this scale was the sole criteria for selecting foxes to par-
found this perplexing. Our ancestors had domesticated ent the next generation. Belyaev could then test whether,
species for a plethora of reasons—including transporta- over generations, foxes were getting tamer and tamer,
tion (e.g., horses), food (e.g., cattle) and protection (e.g., and whether the traits in the domestication syndrome
dogs)—yet regardless of what they were selected for, appeared if they selected strictly based on tameness.
The experiment began in 1959 at the Institute of
Cytology and Genetics in Novosibirsk, Siberia, shortly
*Correspondence: [email protected] after Belyaev was appointed vice director there. Belyaev
Department of Biology, University of Louisville, Louisville, KY 40208, USA

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Dugatkin E vo Edu Outreach (2018) 11:16 Page 2 of 5

immediately recruited 25-year-old Lyudmila Trut to his a small proportion of the foxes in the experiment: today
team (Fig. 1). Trut quickly became the lead researcher on they make up the vast majority.
the experiment, working with Belyaev on every aspect Belyaev was correct that selection on tameness alone
from the practical to the conceptual. Trut turned 85 years leads to the emergence of traits in the domestication
old in November of 2018 and remains the lead investiga- syndrome. In less than a decade, some of the domesti-
tor on the work to this day (Belyaev died in 1985). cated foxes had floppy ears and curly tails (Fig. 2). Their
It is not possible here to do justice to all of the results stress hormone levels by generation 15 were about half
this almost six-decade-long experiment has produced. the stress hormone (glucocorticoid) levels of wild foxes.
Here I touch on some of the most salient (see Trut 1999, Over generations, their adrenal gland became smaller
Trut et  al. 2009 and Dugatkin and Trut 2017 for more). and smaller. Serotonin levels also increased, producing
Starting from what amounted to a population of wild “happier” animals. Over the course of the experiment,
foxes, within six generations (6  years in these foxes, as researchers also found the domesticated foxes displayed
they reproduce annually), selection for tameness, and mottled “mutt-like” fur patterns, and they had more juve-
tameness alone, produced a subset of foxes that licked nilized facial features (shorter, rounder, more dog-like
the hand of experimenters, could be picked up and pet- snouts) and body shapes (chunkier, rather than gracile
ted, whined when humans departed, and wagged their limbs) (Fig.  3). Domesticated foxes like many domesti-
tails when humans approached. An astonishingly fast cated animals, have longer reproductive periods than
transformation. Early on, the tamest of the foxes made up 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 syn-
aptic 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.
Right from the start of the experiment, Belyaev hypoth-
esized 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 expres-
sion patterns at the genome level, in both domesticated
foxes and a second line of foxes that has been under

Fig. 2  Mechta (Dream), the first of the domesticated foxes to have

Fig. 1  Lyudmila Trut. a 1960 and b 2015 floppy ears 1969
Dugatkin Evo Edu Outreach (2018) 11:16 Page 3 of 5

like any experiment in domestication, was an experiment

in genetics. But work in Mendelian genetics was essen-
tially 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 pro-
mote uneducated men from the proletariat into the sci-
entific 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 edu-
cation, 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 Labora-
tory in Azerbaijan in 1925. Lysenko convinced a Pravda
reporter, who was writing a story about the regime’s glo-
Fig. 3  The domesticated foxes have more juvenilized facial
characters, including a shorter, rounder snout, than wild foxes rious 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
long-term selection for aggressive, rather than tame, Lysenko has followers… and the luminaries of agronomy
behavior, suggests Belyaev was correct (Wang et al. 2018). visit… and gratefully shake his hand.” Pure fiction, but the
This study identified more than one hundred genes in the story propelled Lysenko to the national limelight, with
prefrontal cortex of the brain that showed different gene Josef Stalin taking pride in what he read.
expression patterns between domesticated and aggres- Over time Lysenko would claim to have done experi-
sive foxes. Some of those genes are linked to serotonin ments creating grain crops, including wheat and barley,
receptor pathways that modulate behavioral tempera- that produced high yields during cold periods of the year,
ment, including tame and aggressive temperaments. if their seeds had been kept in freezing water for long
When Belyaev proposed that the domestication syn- stretches before planting. What’s more, Lysenko claimed
drome was linked to tame behavior, he did not have a offspring of these plants would also produce higher
proposed mechanism, but today we are getting closer yields, down through the generations. This method, he
to understanding how this works. Very early on in ani- said, could quickly double the yield of farmlands in the
mal development, what are known as neural crest cells Soviet Union in just a few years. In truth, Lysenko never
migrate from the neural crest to a plethora of locations: undertook any legitimate experiments on increased crop
glands in the endocrine system, bone, fur, cartilage, the yield. Any “data” he claimed to have produced he simply
brain and other spots in a developing embryo. The neu- fabricated.
ral crest cell hypothesis for the domestication syndrome Soon Stalin was his ally, and Lysenko began a crusade
proposes that selection for tame behavior results in a to discredit work in Mendelian genetics because proof
reduction of the number of migrating neural crest cells, of the genetic theory of evolution would likely expose
which subsequently leads to changes in fur coloration, him as a fraud. He denounced geneticists, both overseas
facial structure, the strength of cartilage (floppy ears, and in the Soviet Union, as subversives. His star was ris-
curly tails and so on), hormone levels, the length of the ing and at a conference held at the Kremlin in 1935, after
reproductive season, and more. This hypothesis may pro- Lysenko finished a speech in which he branded Western
vide the link that Belyaev was missing when he came up geneticists as “saboteurs,” Stalin stood up to yell, “Bravo,
with the idea for the experiment (Wilkins et al. 2014). Comrade Lysenko, bravo.”
Lysenko was placed in charge of all policy regarding
Discussion: a cautionary tale the biological sciences in July 1948. The next month, at a
The silver fox domestication study is often lauded as one meeting of the All-Union Lenin Academy of Agricultural
of the most important long-term studies ever undertaken Sciences, he presented a talk that today is regarded as the
in biology. Yet in 1959, the very year it commenced, the most disingenuous, dangerous speech in the history of
work came within a hair’s breath of being shut down by Soviet science. In this speech, “The Situation in the Sci-
the premier of the Soviet Union. The problem for Bely- ence of Biology,” Lysenko damned “modern reactionary
aev and Trut was that their domestication experiment, genetics,” by which he meant Mendelian genetics. At the
Dugatkin E vo Edu Outreach (2018) 11:16 Page 4 of 5

end of his ranting, the audience cheered wildly. Geneti- All-Union Institute of Plant Breeding declared, “We shall
cists present were forced to stand up and refute their go into the pyre, we shall burn, but we shall not retreat
scientific knowledge and practices. If they refused, they from our convictions.”
were thrown out of the Communist Party. In the after- In 1940, Vavilov was kidnapped up by four men wear-
math of that awful speech thousands of geneticists were ing dark suits and thrown into the KGB’s dreaded Lub-
fired from their jobs. Dozens, perhaps hundreds, were yanka Prison in Moscow. Next he was shipped off to
jailed, and a few were murdered by Lysenko’s henchmen. an even more remote prison. There, over the course of
Belyaev could not sit by idly. After reading of Lysenko’s 3 years, the man who had collected 250,000 domesticated
speech in the newspaper, he was furious. His wife, Svet- plant samples to solve the puzzle of famine in his home-
lana, remembers it well: “Dmitri was walking toward land was slowly starved to death.
me with tough sorrowful eyes, restlessly bending and Lysenko’s power had its ebbs and flows. In 1959, as
bending the newspaper in his hands.” Another colleague the fox domestication experiment was just beginning,
recalls running into him that day and how Belyaev had Lysenko was getting frustrated that his hold on Soviet
fumed that Lysenko was “a scientific bandit” (Dugatkin biology was loosening. Something needed to be done.
and Trut 2017). Ignoring the personal risk, Belyaev began And The Institute of Cytology and Genetics, where the
speaking out about the dangers of Lysenkoism to all sci- fox domestication experiment had just begun, where
entists, whether friend or foe. Belyaev was vice director, and where they had the audac-
The case of Nikolai Vavilov, one of Belyaev’s intellectual ity to put “Genetics” in the title of the institute, seemed a
idols, illustrates just how dangerous it was to speak out good place to attack.
against Lysenko (Medvedev 1969; Pringle 2008; Soyfer The Institute of Cytology and Genetics was part of a
1994). Vavilov studied plant domestication and was also new giant scientific city called Akademgorodok. Long
one of the world’s leading botanical explorers, travelling before this city was built, Russian writer Maxim Gorky
to sixty-four countries collecting seeds. In his lifetime had written of a fictional “town of science… a series of
alone, three terrible famines in Russia killed millions of temples in which every scientist is a priest… where sci-
people and Vavilov had dedicated his life to finding ways entists every day fearlessly probe deeply into the baf-
to propagate crops for his country. His research program fling mysteries surrounding our planet.” Here Gorky
centered on finding crop varieties that were less suscepti- envisioned “…foundries and workshops where people
ble to disease. forge exact knowledge, facet the entire experience of the
Vavilov’s collecting trips are the stuff of legend. On one world, transforming it into hypotheses, into instruments
of three expeditions, he was arrested at the Iran-Russia for the further quest of the truth.” Akademgorodok was
border and accused of being a spy, simply because he had what Gorky had in mind. It was home to thousands of
a few German botany books with him. On another trip, scientists housed at the Institute of Cytology and Genet-
this one to the border of Afghanistan, he fell as he was ics, the Institute of Mathematics, the Institute of Nuclear
stepping between two train cars, and was left dangling by Physics, the Institute of Hydrodynamics, and a half dozen
his elbows as the train roared along. On yet a different a other institutes.
trip to Syria he contracted malaria and typhus. In January 1959, a Lysenko-created committee from
Vavilov collected more live plant specimens than any Moscow was sent to Akademgorodok. This committee
man or woman in history, and he set up hundreds of field had been authorized to determine just what sort of work
stations for others to continue his work. was being done at the Institute of Cytology and Genet-
Vavilov had actually befriended the young Lysenko ics, and Belyaev, Trut and their colleagues understood
in the 1920s, before it became clear that Lysenko was a the gravity of the situation. “Committee members were,
malevolent  charlatan. Over time, Vavilov became suspi- Trut said, “snooping in the laboratories,” and rumors
cious of Lysenko’s results, and in a series of experiments were spreading that the committee was unhappy. When
trying to replicate what Lysenko said he had discovered, the committee met with Mikhail Lavrentyev, chief of
Vavilov proved to himself, and others that were will- all the institutes at Akademgorodok, they told him that
ing to listen (though not many were), that Lysenko was “the direction of the Institute of Cytology and Genetics
a fraud. He then became Lysenko’s most fearless oppo- is methodologically wrong” (Dugatkin and Trut 2017).
nent. In retaliation, Stalin forbade Vavilov from any more Ominous words from a Lysenkoist group.
travels abroad and he was denounced in the government Nikita Khrushchev, premier of the USSR, learned of the
newspaper, Pravda. Lysenko warned Vavilov that “when committee’s report about Akademgorodok. Khrushchev
such erroneous data were swept away… those who failed was a supporter of Lysenko, and he decided to see for
to understand the implications” would also be “swept himself what was happening. In September 1959, while
away.” Vavilov was undeterred, and at a meeting of the
Dugatkin Evo Edu Outreach (2018) 11:16 Page 5 of 5

returning from a visit to Mao Tse-Tung in China, he Competing interests

The author declares no competing interests.
stopped off in Novosibirsk and went to Akademgordok.
The staff of all the science institutes at Akademgoro- Funding
dok gathered for this visit, and Trut remembers that the None.
premier “walked by the assembled staff very fast, not pay-
ing any attention to them” as he proceeded to a meet- Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
ing with administrators. “Khrushchev” Trut recalls was, lished maps and institutional affiliations.
“very discontented, with the intention to get everyone in
trouble because of the geneticists.” What Khrushchev and Received: 25 August 2018 Accepted: 26 November 2018
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 References
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was with him in Akademgorodok. Rada, a well-respected of Chicago Press; 2017.
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aged to convince her father to let the Institute of Cytol- Joravsky D. The Lysenko affair. Cambridge: Harvard University Press; 1979.
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Acknowledgements Wilkins AS, Wrangham R, Fitch TW. The “domestication syndrome” in mammals:
I thank Lyudmila Trut for working with me on our book, How to Tame a Fox and a unified explanation based on neural crest cell behavior and genetics.
Build a Dog (University of Chicago Press, 2017). Nikolai and Michael Belyaev Genetics. 2014;197:795–808.
provided much in the way of assistance, as did Aaron Dugatkin. I thank Dana
Dugatkin for proofreading this paper.

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