Looking at a small dog like a Chihuahua or a Pomeranian, it can be hard to imagine that such a creature is in any way related to a wolf. Yet every modern dog breed, no matter how big, small, or cute, can trace its genetic lineage directly back to a population of wild wolves living on the steppes of Siberia some 27,000 years ago. Over the intervening millennia, these proto-dogs evolved into hundreds of different breeds bearing distinctive traits such as friendliness towards humans, floppy ears, curly tails, rounded skulls, and spotted coats – traits also present in other domesticated animals like pigs and cows and which geneticists have collectively termed domestication syndrome. But while this origin story has long been suspected, the exact details of the domestication process have baffled biologists for over a century. Then, in 1952, a groundbreaking experiment in fox breeding by a maverick Soviet scientist began to shed some light on how wolves went from wild predators to man’s best friend.

In his epoch-making 1859 work On the Origin of Species, Charles Darwin used the selective breeding of domesticated animals like pigeons to explain natural evolution in the wild. In so doing, Darwin suggested that the selective breeding of certain animals, including dogs, could have taken place unconsciously, with the breeder being unaware that the process was even taking place. But what specific traits did Ice Age humans unconsciously select for which lead to wolves evolving into dogs? A number of theories have emerged over the years. The pedomorphosis hypothesis posits that humans adopted and raised wolf puppies with cuter, more child-like features such as round heads, short snouts, large eyes, and floppy ears, and that these traits were unconsciously selected for and passed down through the generations. In contrast, the neural crest hypothesis suggests that the change in skull shape came about as a result of increased interaction between wolves and humans, which lead to a less hostile and demanding living environment for the wolves and thus a gradual decrease in required brain size. Yet another hypothesis holds that the physical traits characteristic to dogs are genetically linked to metabolic changes which emerged as wolves began scavenging garbage from human campsites and had to adapt to a diet richer in starches. Finally, the behavioural hypothesis posits that wolves who were less frightened and aggressive around humans were more successful, and that these more agreeable behavioural traits were genetically linked to – and evolved alongside with – physical traits like floppy ears and curly tails. It was this latter hypothesis which Dmitry Belyayev set out to test in the early 1950s.

Belyayev was born on July 17, 1917 in the town of Protasovo, and graduated from the Ivanovo Agricultural Institute in 1940. After a brief stint at the Central Research Laboratory’s Department of Fur Animal Breeding in Moscow, in 1941 Belyayev was drafted into the Red Army and served as an infantryman until the end of the Second World War, returning to the institute in 1946. In 1952, while working at the Institute of Cytology and Genetics in Novosibirsk, Siberia, Belyayev and graduate student Lyudmila Trut set up an experimental farm for breeding silver foxes in order to investigate the process of canine domestication.

Belyayev’s choice of foxes as research subjects was deliberate and strategic: not only are foxes social creatures like wolves, but they have been hunted and bred in Russia for their pelts for centuries, allowing Belyayev to disguise his experiments as an economic venture. This was vital to longevity of his work, for under the regime of Josef Stalin it was illegal in the Soviet Union to practice genetics. In the 1930s, an intense rivalry developed between two of the USSR’s leading agronomists, Nikolai Vavilov and Trofim Lysenko. While Vavilov upheld the widely-accepted principles of Mendelian genetics, Lysenko championed an alternate philosophy known as vernalization, which he claimed could increase the yield of Soviet crops manyfold. But vernalization was simply a rehashing of the long-discredited pre-Darwinian theory of Lamarckism, which held that attributes acquired by an organism during its lifetime could be passed on to its offspring. For example, according to this theory a bodybuilder’s children would inherit their large muscles. While Lysenko’s ideas were pseudoscientific nonsense, they won the support of Soviet Politburo, who saw vernalization as being more in line with Communist ideology than Mendelian genetics, which they associated with Social Darwinism and Capitalism. As a result, Lysenko rose rapidly through the ranks of the Soviet government and in 1941 denounced Vavilov as a traitor. Vavilov was duly arrested and imprisoned, dying of starvation in prison in 1943. Meanwhile, Lysenko’s ideas were implemented across the Soviet Union, leading to widespread crop failure and famines that killed millions of Soviet citizens. After the war, the eugenics policies of the Nazis cast further suspicion on Mendelian genetics, and in 1948 it was officially declared pseudoscience. Hundreds of geneticists were fired from their jobs, with many being arrested, imprisoned, or even executed without trial – including Dmitri Belyayev’s own brother. Belyayev himself managed to escape the purge, but it would not be until 1959 under the administration of Premier Nikita Khrushchev that the ban on genetics research would finally be lifted. Meanwhile, Belyalev and Trut carried on discreetly with their fox experiments.

Belyayev believed that the evolution of dogs was driven by a single characteristic: tameness. According to this theory, wolves who behaved less aggressively around humans were evolutionarily selected for, with all the physical traits characteristic to dogs developing as a mere side effect of this single selection pressure. In order to test this hypothesis, Belyayev and Trut acquired 30 male foxes and 100 vixens from Russian commercial fur farms and selected only the tamest and friendliest kits for breeding. As Trut later explained, tameness was determined according to a strict procedure:

“When a pup is one month old, an experimenter offers it food from his hand while trying to stroke and handle the pup. The pups are tested twice, once in a cage and once while moving freely with other pups in an enclosure, where they can choose to make contact either with the human experimenter or with another pup. The test is repeated monthly until the pups are six or seven months old.”

Each kit was classified according to one of three categories. Class III were the wildest foxes, who behaved aggressively towards humans, Class II were foxes who allowed humans to pet and handle them but did not actively seek out human contact, while Class I were the friendliest foxes. Eventually, Belyayev and Trut added a fourth category, IE or “domesticated elite,” for foxes who actively sought out human contact and sniffed, licked, and played with the experimenters just like dogs. In order to ensure that the foxes’ tameness was solely the result of genetics and not prolonged contact with humans, experimenters were allowed only a minimal amount of interaction with the animals.

The results were dramatic. By the tenth generation, 18% of the foxes were classified as IE or “elite”; by the 20th generation this figure had risen to almost 35%. At the same time, the foxes underwent pronounced physical and physiological changes, becoming more and more doglike with each generation:

“[The foxes] displayed behavioural, physiological, and anatomical characteristics that were not found in the wild population, or were found in wild foxes but with much lower frequency….Many of the domesticated foxes had floppy ears, short or curly tails, extended reproductive seasons, changes in fur coloration, and changes in the shape of their skulls, jaws, and teeth. They also lost their ‘musky fox smell.’

By the 20th generation, certain foxes even began developing shorter tails and legs, pronounced overbites and underbites, and piebald coats, while by the 30th generation nearly 80% were classified as “elite”

In 1978 Belyayev presented his initial findings at the 14th International Congress of Genetics in Moscow. In his lecture, Belyayev hypothesized that a reduction in aggression corresponded to changes in an animal’s endocrine system, such as decreased production of adrenaline and other stress hormones. The genes controlling these processes were in turn located on the same chromosomes as those controlling various physical traits like skull shape and fur colouration, meaning that as the former changed, the others followed. This process went against accepted theories of dog domestication as it did not necessarily require direct intervention by humans. Wolves who were less afraid and acted less aggressively towards humans were less likely to be killed and more likely to gain access to leftover food, meaning that – at least initially – dogs could have effectively domesticated themselves. But having only bred 20 generations of foxes over 26 years, Belyayev admitted that the experiment was not yet complete and that there was still much work to be done.

But Belyayev would not live to see the conclusion of his experiments, dying of cancer in 1985. In his absence Lyudmila Trut took over the project and ran it for another 40 years, breeding some 45,000 foxes over 35 generations. The collapse of the Soviet Union in 1991 caused government funds to dry up, nearly spelling the end of the project, but after a 1999 article in Scientific American brought Trut’s research to the world’s attention, Anna Kukenova, a postdoctoral student in molecular genetics at Cornell University, managed to secure funding from the National Institutes of Health to keep the project going. In 2010, the lab attempted to raise funds by selling some of its domesticated foxes as pets at $6000 apiece. However, few animals were ordered, and those that were ended up being confiscated at the US border and sent to animal sanctuaries. In the end the scheme lasted barely two years, with all sales ending in 2012. And perhaps this is for the best, for according to Amy Bassett, founder of the Canid Conservation Center – the current home of Belyayev’s foxes – even domesticated foxes make terrible pets:

“You can easily train and manage behavioural problems in dogs, but there are a lot of behaviours in foxes, regardless of if they’re Russian or U.S., that you will never be able to manage. You can be sitting there drinking your cup of coffee and turning your head for a second, and then taking a swig and realizing, ‘Yeah, Boris [the fox] came up here and peed in my coffee cup.’”

Nonetheless, the nearly seven-decades-long Fox Farm Experiment has become one of the most famous and widely-cited studies in the field of evolutionary biology, providing compelling evidence for the behavioural theory of canine evolution.

…or has it? Despite the seemingly conclusive nature of Belyayev and Trut’s results, recently-uncovered evidence has cast serious doubt on the validity of their experiments.

In 2015, canine researcher Raymond Coppinger visited the Summerside International Fox Museum and Hall of Fame in Prince Edward Island, Canada. What he found there stunned him. Prince Edward Island had been a global centre of fox pelt production since 1887, when Charles Dalton and Robert Oulton established Canada’s first commercial fox farm. Foxes are notoriously difficult to breed in captivity, being monogamous and reluctant to mate in cages, but by making the animals’ enclosures larger and more natural Dalton and Oulton managed to crack the secret of fox breeding and quickly came to dominate the market, their pelts selling for nearly $1400 apiece by 1910. While touring the Summerside Museum, Coppinger stumbled across photos of commercially-bred foxes from the 1920s and 1930s which exhibited many of the traits Belyayev had reported in his own foxes, including floppy ears, curly tails, piebald coats, and friendliness around humans. This indicated that the process of domestication had started long before the Russian experiments. Then, while combing through old sales records, Coppinger landed on another bombshell: the original 65 breeding pairs which founded the Russian fox fur industry had been purchased from Prince Edward Island in the 1920s. And it was from their descendants that Belyayev acquired the initial batch of animals for his famous experiments.

According to Coppinger, these revelations throw the validity of Belyayev’s theories – and the entire concept of domestication syndrome – into serious doubt. Not only was the process of selecting for the friendliest foxes well underway before Belyayev started his experiments, but the double events of foxes being imported into Russia and being selected by Belyayev likely further contaminated his results via a phenomenon known as the founder effect. The founder effect occurs when a small segment of a population is transplanted to a new location and allowed to breed. Traits which are rare in the original population – such as reduced aggression – may by random chance be proportionally overrepresented in the smaller sub-population, and will thus become increasingly common as that population breeds and grows. This is, for example, why certain genetic diseases are more prevalent in isolated religious groups like the Amish or Ashkenazi Jews who only marry within their communities: breeding within a limited gene pool can cause certain harmful genes which are normally rare in the larger population to accumulate within the group. In the case of foxes, the already high incidence of dog-like traits caused by selective breeding was amplified by the transplantation of a small population to Russia, and further still by Belyayev selecting only the tamest foxes from their descendants for his experiments. Further experiments using DNA analysis support this hypothesis, indicating that the significance of the Fox Farm Experiment was overstated and that the dog-like traits Belyayev observed were largely brought about not by selective breeding for tameness but rather by a simple genetic accident. According to Elinor Karlsson, a colleague of Coppinger’s:

“Not only did the Prince Edward Island story really bring into question exactly what had happened in terms of the Russian project, but once you took foxes out of the picture there really wasn’t a whole lot of evidence for domestication syndrome anywhere else either…P.E.I. farmers were actually kind of doing already the experiment that Belyaev thought he was starting in Russia – breeding for the friendliest foxes. It kind of disrupts that basic idea that we selected on the behaviour and we got changes in the way (foxes) looked, because (P.E.I. farmers) were actually doing both at the same time.
So where does this leave us regarding the evolution of dogs?

While the specifics of Belyayev’s theories may be in question, according to scientists like Dr. Brian Hare of Duke University’s Canine Cognition Centre, the overall theory that dogs essentially domesticated themselves – at least initially – still holds up – especially against older theories of humans adopting wolf pups and raising them to be hunting companions. This is because Ice Age humans were already efficient hunters and intolerant of competing predators, and by 43,000 years ago had essentially wiped out all the other carnivorous megafauna in Europe, including sabre-toothed cats and hyenas. Indeed, throughout history humans have exterminated wolves wherever they went; the last wolf in England was killed in the 16th Century on the orders of King Henry VII, while by 1930 there was not a single wolf left in the contiguous 48 states of America. Thus, according to Dr. Hare, only the friendliest wolves – and those who learned to read human expressions and gestures – would have been tolerated enough to scavenge garbage from human campsites. Only once these traits had already been established would humans have started to adopt these porto-dogs and use them as hunting assistants or – in dire circumstances – as walking reservoirs of emergency meat.

Yet despite these advances, no-one has yet come up with a definitive theory of dog domestication, and research carries on worldwide.

If you liked this article, you might also enjoy our new popular podcast, The BrainFood Show (iTunes, Spotify, Google Play Music, Feed), as well as:

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Bonus Fact

While it is commonly known that a female fox is called a vixen, what about male foxes? While the most common answer is simply “a fox”, in fox breeding the most commonly-used term is “reynard,” and indeed in French “renard” without the Y is the basic term for a fox. But strangely, it wasn’t always this way. Until around 900 years ago the French word for fox was goupil, from the Latin vulpecula, which also gave us the scientific name for foxes, Vulpes vulpes, and the adjective vulpine, meaning “foxlike.” However, in the 12th Century folk tales starring a trickster character named Reynard the Fox became extremely popular – so popular, in fact, that “reynard” soon replaced “goupil” as the French word for fox, and this has remained in the language ever since. This would be equivalent to us referring to mice as “mickeys,” all while having no idea they were called something else prior to the introduction of the Walt Disney character.