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How to Tame a Fox (and Build a Dog):



Visionary scientists and a Siberian tale of jump-started evolution



Lee Alan Dugatkin and Lyudmila Trut



New Scientist



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Certain characteristics appear with tameness: floppy ears, forehead markings and curly tails

NEARLY 60 years ago, Russian scientist Dmitri Belyaev began a remarkable experiment that still runs to this day. His aim was to selectively breed wild silver foxes to see if it was possible to bring about a similar transformation to the one that turned wolves into dogs. How To Tame A Fox, co-authored by US biologist Lee Dugatkin and by Belyaev's longterm collaborator, Lyudmila Trut, is a charming account of this study, which has intrigued behavioural geneticists and evolutionary biologists for decades.

Begun in secret at the tail end of Trofim Lysenko's devastating rule over Soviet genetics, Belyaev's study was expected to take a long time to produce significant results, if it ever did. Although foxes had been bred in captivity for their fur since the end of the 19th century, they remained as bitey and cross as they had been all those decades earlier.

Under Belyaevs leadership, Trut and her co-workers used standardised tests to identify the least aggressive animals, and then mated them together. Within three years, the foxes began to accept humans and breed slightly earlier in the year. After four years, one cub, Ember, wagged his tail when Trut approached the cage. After eight generations, curly tails appeared. A few years later, some foxes began to breed more than once a year.

These findings were significant. In On the Origin of Species, Charles Darwin wrote that in virtually every domesticated mammal species, certain characteristics often appeared alongside tameness: floppy ears, star-shaped forehead markings, multiple breeding periods and reduced, often curly tails. (Camels are an obvious exception, but they are so bad-tempered that they are arguably not tame at all.)

Belyaev became convinced that this revealed something about the genes involved in domestication. He put forward the rather vague notion that domestication involves a period of destabilising selection, affecting the hormonal control of development. Dugatkin and Trut recast this idea in terms of gene regulation, but it isn't clear what extra insight into domestication this gives.

When Belyaev began the study, DNAs role as the hereditary material in animals was only suspected. Now, whole genomes can be compared and scientists can study where and when genes are expressed. As well as a story of scientific determination, How to Tame a Fox is therefore also a striking description of how much science has progressed.

Yet while the social context is informative and Truts memories are often heart-warming, I wanted more science. There are repeated references to how cute, loyal, irresistible and rambunctious the tame foxes are, but not one set of data showing the speed with which selection had an effect.

Only five pages are given over to summarising the molecular genetic data from the past decade or so, to no very great conclusion. The group has recently identified 335 genes that show differences in their activity in tame and control foxes, some of which affect hormone levels. But theres little evidence that these same genes were involved in wolf domestication.

For the moment, the persistent reappearance of the same suite of characteristics in various domesticated species remains a mystery. The most likely explanation, as Belyaev suggested, is that they are all focused on prolonging infancy, leading to changes in hormones and behaviour. Strikingly, these changes arent seen in the line of aggressive foxes that Belyaev astutely set up in parallel to the domestication study. Those foxes are simply very, very cross.

After about 20 generations, the tamed foxes became truly like dogs: loyal and unbearably cute. It is now possible to adopt a tame fox - the substantial fee goes towards supporting the research project. After reading How to Tame a Fox I am very tempted, but my cats would object.

(LRB)

THERE'S A SCENE in Antoine de Saint-Exupery's The Little Prince where the alien prince, fallen to Earth, comes across a fox. 'Come and play with me,' he proposes to the fox, who replies, 'I can't play with you. I'm not tamed.'The prince, who's never heard the word 'tamed' before, asks what it means. 'It's something that's too often neglected,' the fox tells him. 'It means, 'to create ties.' If you tame me, we'll need each other. You'll be the only boy in the world for me. I'll be the only fox in the world for you. If you tame me, it will be as if the sun came to shine on my life. I shall know the sound of a step that will be different from all the others.'

In 1952, nine years after Saint-Exupery's book was published, the Russian geneticist Dmitri Belyaev set out, like the Little Prince, to tame a fox - or rather, foxes. His goal was to better understand how domesticated dogs evolved from the wolf, and he proposed to do this by domesticating the silver fox, the wolf's genetic cousin. By mimicking the wolf's transformation with a close relative, Belyaev thought, we could better understand one of the great mysteries of prehistory: the dog's route to domestication.

We know more about this process now than we did when Belyaev embarked on his research project decades ago. To his scientific peers, Belyaev's belief that he could replicate 10,000 years of evolution and breeding in a few decades with a species that had never been domesticated before seemed entirely fanciful. But he turned out to be right: within a few years of starting his experiment, the foxes were already showing signs of domestication; within decades, they were on their way to becoming their own species. How to Tame a Fox (And Build a Dog) traces the history of Belyaev's experiment against the background of first the Soviet Union and then post-Cold War Russia. It's co-authored by the geneticist Lyudmila Trut, who joined Belyaev's team early on and has been the lead researcher of the fox domestication project since 1959, and the evolutionary biologist Lee Alan Dugatkin.

Domesticated animals exist in a peculiar gray area between the world of humanity and the rest of nature. From the Book of Genesis to the modern environmental movement, we tend to understand nature as something that we stand apart from and exert power over, whether to dominate or to protect. But cats, dogs, horses, and other domesticated creatures exist in a liminal space between these two worlds. As W. G. Sebald says of the dog, 'His left (domesticated) eye is attentively fixed on us; the right (wild) one has a little less light, strikes us as averted and alien.'

Domestication is not simply the engineering of a change in animal behavior; it is a matter, as Dugatkin and Trut write in their opening pages, of 'constructing a brand new biological creature.' Dogs, after all, are a separate species from wolves, and housecats are so different from their feline cousins that it's not entirely clear from which species they were domesticated (though most biologists agree that it was probably the Middle Eastern wildcat). Domestication is not just a question of selectively breeding some traits at the expense of others; it's about fundamentally changing the animal.

Across species, domesticated animals seem to share a number of traits that differentiate them from their wild counterparts. Most have shorter faces and curly and floppy tails, traits associated with delayed physiological development and remaining in a stage of perpetual adolescence; biologists refer to this as neoteny. Domestic animals also tend to develop different coloration patterns, and unlike their wild cousins, who mate only once a year, they're fertile year round. Other traits are significant but harder to measure: a dog may not have the same apparent aptitude for solving puzzles as a wolf, but will display more social intelligence in its ability to manipulate human emotions.

The riddle of domestication has always been how to unravel this ball of traits, and learn how they came to be associated with one another. Were early domestic animals selected for their usefulness to humans (cats for pest control, dogs for security and hunting), and then socialized from there? Were their neotenic traits necessary for their domestication, as animals that remained juveniles were perhaps easier to train? Was the wolf's nature as a pack animal, and responsiveness to socialization and group identity, crucial to its taming? And what of the superficial aesthetic differences - do they have any bearing on domestication? 'Farmers raising cows, after all, had nothing to gain from their cows having black-and-white spotted hides,' Dugatkin and Trut note. 'Why would pig farmers have cared whether their pigs had curly tails?'

Belyaev's hypothesis was that the single most important defining trait was comfort around human beings. Zebra and deer, for example, share many traits in common with horses but have long resisted any attempts at domestication. Zebra, under constant threat from predators, have developed a fierce defensiveness, whereas deer remain skittish and are universally nervous around humans. What separates both of these animals from their close genetic cousin the horse is the latter's tolerance of humans. Early attempts to domesticate horses, DNA evidence suggests, were based on selecting for agreeableness and manipulating the horse's innate fear response.

Among the numerous traits that identify domestic animals, then, Belyaev used as his sole criterion tolerance for human beings. Foxes tend to be either aggressive or skittish around humans; Belyaev and his team focused on those that seemed least defensive. These were bred together, and successive generations were likewise measured for their tolerance for humans, with the researchers hoping that eventually this quality could be bred in offspring.

Within three breeding seasons, the researchers were seeing results: 'Some of the pups of the foxes they'd selected were a little calmer than their parents, grandparents, and great-grandparents,' Trut and Dugatkin write. 'They would still sneer and react aggressively sometimes when their keepers approached them, but at other times they seemed almost indifferent.' Even more surprising, though, was how quickly these behavioral changes were accompanied by other differences. In a matter of years, hormones associated with stress decreased, while levels of serotonin (which decreases anxiety and elevates one's mood) increased. The foxes went from being merely indifferent around the researchers to actively soliciting their affection. Eventually, their tails would even wag at the sight of humans - something no other animal besides a dog has been known to do.

Selecting for tameness also led to a series of physical changes: Belyaev's foxes had bushier tails, shorter faces, lighter fur. Which is to say: Traits that were not in any way selected for nonetheless began to assert themselves. At one point, the foxes began making a sound that at first confounded Trut and her team, until she realized that they appeared to be mimicking human laughter. As they ultimately concluded, the tame foxes were making this noise 'in order to attract human attention and prolong interaction with people.' They were displaying the same kind of social intelligence that dogs do when they perform tricks for their masters.

The fox experiment bore out Belyaev's initial hypothesis about tolerance for humans as the key to domestication. These results suggest that many of the various other traits associated with domestication are in fact already latent in animals' genetic codes; it's just that, in the wild, these traits are 'inactive,' rarely expressing themselves. Selective breeding can allow them to come to the fore relatively quickly. 'Shake up the fox genome by placing foxes in a new world where calm behavior toward humans is the ultimate currency,' Dugatkin and Trut conclude, 'and you'll get lots of other changes - mottled fur, curly, wagging tails, and better social cognition as well.'

ยค The story of Belyaev and Trut's decades-long experiment is fascinating, though in How to Tame a Fox's telling some important details get left out. In crafting a heartwarming story of how easy it was to create docile, loving pets, Dugatkin and Trut don't dwell on the fact that they were also trying to create exceptionally aggressive foxes to further test the hypothesis. Nor were they just breeding foxes: other species, including rats and beavers, were also bred for both aggressiveness and tameness. According to one anecdotal report of the project that isn't mentioned in the book, Soviet officials had planned to use the most aggressive beavers as a line of defense against a possible US invasion. One wonders what other strange tidbits might have come to light had the authors not chosen to selectively shape their narrative. As a result, the book itself feels much like its subjects: bred for tameness.

It might have been better had How to Tame a Fox not been co-written by one of the principal researchers, so as to introduce a modicum of objectivity and critical distance into the writing. At times the book reads like a third-person memoir: 'Pushinka [one of the foxes] lay by Lyudmila's feet while she worked at her desk, and she loved for Lyudmila to play with her and take her for walks around the area. A favorite game was when Lyudmila would hide a treat in her pocket and Pushinka would try to snatch it out.' Such passages are often lovely and do help to convey the remarkable level of domestication the foxes had achieved in such a small span of years (and only the coldest hearted won't melt at the photos of the foxes themselves). But in a book that largely skimps on the scientific and philosophical implications of its narrative, they can feel a bit too sentimental. It is also odd to read passages that describe Trut as 'a woman of great warmth and an unassuming demeanor,' whose 'formidable energy and determination made her a force to be reckoned with' when she is also listed as a co-author of the book.

One thing How to Tame a Fox does reveal is the precariousness inherent in government-funded research, with lessons that go far beyond Soviet Russia. In the early '50s, when Belyaev began his project, the entire field of genetics was under assault in the USSR. A well-placed friend of Stalin, Trofim Lysenko, had promised that he could increase crop yields by freezing seeds before planting. Lysenko's claim was not only false, it ran counter to the prevailing understanding of crop genetics. Since Lysenko knew geneticists could unmask him as a fraud, he began a campaign to discredit the entire discipline, labeling them as 'saboteurs.' Thus, when Belyaev first described his research program to Trut, he told her it could not appear to have anything to do with genetics; instead, it had to be described as an inquiry into 'fox physiology.'

After Stalin's death, Lysenko's stranglehold on the discipline loosened, and geneticists could once again work without fear of reprisal. But with the fall of the Soviet Union and the economic crash of the 1990s, research budgets were slashed, and the project nearly ended for lack of funds. Trut took to begging passersby for food to feed her starving animals; eventually she was forced to sell some of the domestic foxes for pets, and some in the control groups for fur. Only an internationally published paper on her results saved the project, triggering a fundraising campaign that kept the animals alive.

Belyaev died in 1986, but he had hoped to one day write a book himself, which he planned to call Man Is Making a New Friend. How to Tame a Fox (and Build a Dog) is not far off from what Belyaev envisioned: written for a general audience, it chronicles the story of a scientific gambit that was more successful that even its creators had dreamed. It's an inspiring reminder of how much we still don't know about the world, and how much can be learned by taking bold chances. It's also a cautionary tale about the risks of state-funded science that has nearly as much relevance to Trump's United States, where federal research budgets are in danger of being slashed right and left, as it does to Stalin's Russia.

But Belyaev's experiment didn't just produce new knowledge; it also created a new species of animal, one that's become entirely dependent on humans, and it's worth asking what the ethical and philosophical consequences of this might be. Some scientists believe that wolves actively participated in their own domestication; thousands of years ago, certain wolves may have made the calculation that, by sucking up to humans, they could live an easier life. These wolves gave up autonomy and freedom in exchange for food, shelter, and protection. The gamble ultimately paid off: there are now only about three hundred thousand wolves in the wild, and over half a billion dogs.

But a dog's life is not an easy one, especially without a human being to care for it. Many contemporary breeds lack the skills to fend for themselves, having depended on their masters for generations. Perhaps in the future wild foxes will go extinct, and the only foxes that remain will be the domesticated ones, the ones that have endeared themselves to humans to such a degree that even in times of strife and scarcity we will look out for them. But the precarious state of Belyaev's project may well signal another outcome, one in which these foxes, who've thrown their all in with their human protectors, may find a darker fate awaiting them. If the money to keep the program going dries up, and there's no market for them as pets, what then? In The Little Prince, Saint-Exupery's protagonist does indeed tame his new friend, but before he does the fox offers this warning: 'People have forgotten this truth. But you mustn't forget it. You become responsible for what you've tamed.'












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