How to Tame a Fox (and Build a Dog)
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While the genomic analysis progressed, Anna reached out to another specialist, Gordon Lark, a professor of biology at the University of Utah. She thought Lark could help her and Lyudmila follow up on Lyudmila’s earlier work measuring the differences in the anatomy of the tame and control foxes, which had shown that the snouts of the tame adult foxes were shorter and rounder than those of the control foxes, more like those of fox pups, and also of dogs. Anna knew that Lark and his team had measured the length and width of bones in the body and skull of dogs, and she thought he might agree to help them compare the anatomy of dogs with that of the tame foxes.
Lark’s team had discovered that in some dog breeds, animals that had short limbs and short snouts also had wide limbs and wide, rounded snouts—these animals leaned toward a rounded, low to the ground, bulldoggish appearance. Dogs with long graceful limbs and long snouts had relatively narrow snouts, looking more greyhoundish than bull-doggish. Genetic analysis performed by Lark’s team suggested that the relationship between the length and width of their bones was controlled by a small number of genes that affect skeletal growth.6
Anna asked Gordon if he’d be interested in doing a similar study with the silver foxes at the farm. He said he’d love to. But for that, the fox team would need an X-ray device, and Lyudmila didn’t have the funds to buy one. So Lark arranged for a transfer of $25,000 to the Institute of Cytology and Genetics for the purchase. Lyudmila oversaw the project on the Russian end, and she put her colleague and friend, Anastasia Kharlamova, whom Lark likes to call “Lyudmila’s lieutenant,” in charge of everyday operations. Anastasia began taking X-rays of the bodies and skulls of tame, aggressive, and control foxes, and one of Lark’s colleagues set up a website where the X-ray images could be posted, so that the team in Utah could do the analysis of bone width and length, which required their expertise.
This was Lark’s initiation into the intensity and efficiency with which Lyudmila’s team worked. He recalls, “The volume of data that began to pour in was amazing. It was as if the fox team had fifty hours in a day, somehow.” The hard work paid off. Lark’s team determined that the same relationship between bone width and length they had found in dogs—short limbs and short snouts paired with wide limbs and wide, rounded snouts—had developed in the foxes.
Lark and Lyudmila proposed an intriguing idea about why these changes had emerged in the foxes. For foxes in the wild, as pups mature and wean off nursing, the body and face shape change in a manner that provides them with the best chance of survival. When they are pups, their faces are relatively round and their legs are chunky. But, as they mature to adulthood, longer more graceful legs provide more speed for chasing prey and evading predators, and longer, more pointed snouts facilitate probing into the nooks and crannies of thick grasses and undergrowth while foraging for food. In wild foxes, this leads to a change in body shape during development, producing the classic anatomy of adult foxes; but on the farm, the foxes never have to forage, hunt, or evade predators, and selection favors juvenile-like traits, hence the more rounded face and chunky body form continue into adulthood in the tame foxes.7
WHILE LYUDMILA AND LARK WERE WORKING on this study of the anatomy of the tame foxes, Anna, Lyudmila, and their colleagues proceeded with the next stage of the DNA analysis, which was designed to try to link the genomic work on the foxes with their behavior. DNA samples were taken from 685 tame and aggressive foxes and all these animals were videotaped interacting with a researcher at the fox farm. A meticulous, arguably obsessive, analysis of 98 behaviors was conducted, noting characteristics such as “tame sounds,” “aggressive sounds,” “tame ears,” “aggressive pinned-back ears,” “observer can touch fox,” “fox comes to sniff observer’s hand,” “fox rolls onto its side,” and “fox invites observer to touch its belly,” to name just a few. This project, which came to fruition in 2011, was a tremendous undertaking, but fortunately, the results made all of the work worthwhile.
They discovered that the genes associated with many of the changes to the unique behavioral and morphological characteristics of the tame foxes could be mapped onto a specific region of fox chromosome number 12. On this region, the elite and aggressive foxes had different sets of genes, and Lyudmila, Anna, and their team hypothesized that these genes were likely involved with the changes that distinguished the tame foxes from all others.8
Just a year earlier, in 2010, a much heralded paper on dog domestication, published in the prestigious journal Nature, had announced that many of the genetic changes that led to the evolution of dogs from wolves could be traced to genes on just a few chromosomes. Now, Anna and Lyudmila could see whether the genetic changes on fox chromosome 12 that distinguished tame foxes from wild foxes were similar to the genetic changes involved in the domestication of dogs. They hoped that they would find considerable similarity in the two sets of genes, and they did. Many of the genes on chromosome 12 of the foxes that were involved in their domestication were also found on the corresponding dog chromosomes involved in their domestication. It was almost too good to be true.
Fifty-nine years after Dmitri took his long train ride to Estonia to meet with Nina Sorkina at the Kohila fox farm to start breeding the first tamer foxes, and fifty-three years after Lyudmila had joined him in the quest, they knew where at least some of the genes associated with fox domestication were located. Next they would conduct experiments to probe into the specific function of each of the genes and into whether the expression of these genes had been altered to bring about the characteristics of domestication, as Dmitri had suggested from the start, before people even had a lexicon with such terms. By 2011, technology was available to begin doing this.
“Next generation sequencing technology” sped up the rate at which DNA sequences could be read, making it possible for millions, sometimes billions, of small bits of DNA to be read by computer analysis rather than by the human eye. Analyzing the effects of genes and how they are being expressed is still an enormously complex process, because genes generally code for different effects in different cells of the body. Each cell in an animal’s body, except sperm and eggs, has the same set of genes housed in the pairs of its chromosomes. But different genes are turned on or off in skin cells, say, versus blood cells or brain cells, and some genes that are turned on in more than one type of cell code for the production of different proteins in one cell type versus another. Analyzing the full story of the expression of any given gene in one animal versus another therefore involves comparing the amount of different proteins the gene codes for in all the different types of cells in the body. Researchers typically begin by focusing on a particular type of cell in a particular part of the body. So the first question that Anna and Lyudmila had to tackle was what type of cell they would examine. They decided to begin by studying the expression of the set of genes in the foxes’ brain tissue because the brain is the master controller of behavior, and the changes in the foxes had begun with the selection for tameness. The prefrontal cortex had been identified as especially important in controlling behavior, so that is where they drew cells from.9
They were able to identify 13,624 genes, and in a complex analysis of the amount of proteins being produced by those genes in the tame foxes versus the aggressive foxes, they discovered that in 335 of these genes—or about 3%—there were dramatic differences in the protein production levels. For example, the HTR2C gene, which is important in the production of serotonin and dopamine, had higher levels of expression in the tame foxes. What was especially intriguing was that with some of the 335 genes—280 of them—expression was higher in the tame foxes than in the aggressive foxes, while in the rest of them, expression was lower in the tame foxes than in the aggressive foxes. So the change to tamer behavior appeared to involve no simple process. What’s more, there were complex interactions between these genes as well. So complex is the story of the expression of the full set of these genes that it will be the subject of investigation for years to come.
Today, Lyudmila an
d Anna are still engaged in the delicate and time-intensive process of identifying the specific functions of these 335 genes. They have determined that some are involved in hormone production, others in the development of the blood system, susceptibility to disease, fur and skin development, and the production of vitamins and minerals. The effects on hormone production were expected, because they had discovered so many critical hormonal changes in the tame foxes. How the other effects are related to the behavior of the elite foxes remains a mystery. As more pieces of this complex puzzle are put in place, a clearer picture of the destabilization of the silver fox genome will emerge, and with it a much more refined understanding of the process of wolf and fox domestication.10
IN LAUNCHING THE FOX EXPERIMENT Dmitri had theorized that the same fundamental process of selection for tameness was involved in all animal domestications. In the cases of the domestication of the wolf and the fox, he was right that many of the same changes to their genomes and the expression of their genes were likely involved. But how much do these results explain about the process of domestication in other species? Are the same genes and changes in their expression involved?
A recent analysis by Frank Albert and a team of geneticists that included Lyudmila compared the genes involved in the domestication of three species—dogs, pigs, and rabbits—and the expression levels of those genes in the domesticated animals versus the ancestral animals of each—wolves, wild boars, and wild rabbits, respectively. The researchers found little evidence that the exact same set of genes and the same changes in their expression were involved. They did find that two genes associated with brain development might be commonly involved in all three cases of domestication, and further work is underway on that tantalizing finding.11
While for now, the process of the domestication of other species, including that of us humans, remains shrouded in mystery, in principle at least, we should be able to solve the riddle for them all with time. The better the techniques of genetic analysis become and the more that archeology, anthropology, and genetics shed light on the history of the domestication of other species, the more we will understand about how similar the process might have been across species, and whether Dmitri Belyaev was right that selection for tameness and destabilizing selection was behind all cases.
Though the specific genes involved in different species may differ, there are hints that Belyaev was right that the process is similar across species in key ways. Work on domestication genes in many species shows that domestication involves just the sort of complicated set of genetic changes that Belyaev described in his theory of destabilizing selection. For example, work on the domestication of rabbits in Southern France, found that “at least some of the selection occurred on genetic variation that already existed in the population, rather than on new mutations,” just as Dmitri predicted.12 And much of the work being done on domestication shows that, as with the foxes, the expression of genes, not just their presence or absence, is key to domestication.
Also providing some support for Belyaev’s destabilizing selection theory is a promising new theory proposed by Adam Wilkins, Richard Wrangham, and Tecumseh Fitch on why selection for tameness would lead to a cascade of other new traits. They propose that changes to a type of stem cell, called a neural crest cell, may help explain many of the traits that domesticated species share. Very early on in vertebrate embryonic development, these cells move along what is known as the neural crest—a concentration of neurons in the middle of the developing embryo—and migrate to different parts of the body, such as the forebrain, skin, jaws, teeth, larynx, ears, and cartilage. Wilkins and his colleagues hypothesize that selection for tameness may also select for a small reduction in the number of neural crest cells, and that “Most of the modified traits, both morphological and physiological [associated with domestication], can be readily explained as direct consequences of such deficiencies [in neural crest cells], while other traits are explicable as indirect consequences.”13 Exactly how this might occur is unclear, but if correct this might help explain how tameness is linked to the whole suite of traits we see in domesticated species—mottled coloring, floppy ears, shorter snouts, changes in reproduction, a curly tail and so on. It is an intriguing hypothesis and requires further investigation.
EVENTUALLY, THE FOX EXPERIMENT will produce many more exciting discoveries. The experiment has been going on for almost sixty years now, which is eons for a biology experiment. But from an evolutionary perspective, sixty years is only the blink of an eye. What would happen if the experiment ran 100 generations? Or 500 generations? Are there limits to how tame and how symbiotically habituated to life with humans the foxes would become? How much more dog-like in appearance would they get? How smart might they grow to be? Would they develop into staunch guardians, as Pushinka’s bark in the dark to alert and defend Lyudmila might suggest? And perhaps, just perhaps, as Dmitri Belyaev hoped, the work with the foxes will ultimately help to explain how, deep in the chromosomes, a stirring occurred that set the common ancestors of all of the other domesticates on the road to tameness, including the ancestors of humans.
One thing about the domestication of the foxes that has already been definitively determined is that they have become a new line of animal that we humans can take into our lives and love. This, in fact, is Lyudmila’s great hope for her foxes, who have become, in her words, such “dainty, fluffy, charming rogues.”
In 2010, Lyudmila started to seriously explore whether people might want to purchase tame foxes as pets, and a number of foxes have been adopted and are living happily with families in Russia, Western Europe, and North America. The owners write to Lyudmila sometimes to update her about how they and the foxes are doing, which delights her. She likes to pull these letters out on occasion and read them again, smiling about the escapades the owners recount and their affection for the foxes.
One American couple who adopted two foxes, named Yuri and Scarlet, wrote recently that the pair “play well together and are both very social. They both enjoy getting out and seeing everything possible!”14 Another letter arrived recently about a close call experienced by a fox named Arsi: “Arsi . . . had a little accident about a week ago. He stopped eating for a couple of days and threw up a couple of times. I took him in [to the vet] for blood work and an x-ray. [The vet] removed a piece of a rubber toy shaped like a V that came off a ball I had bought him. It’s like looking after a child because they do put everything in their mouths!”
All the letters are special to Lyudmila, but one stands out. “Hi Lyudmila, I am very happy,” the letter begins. The owner adopted a fox named Adis and he reports that “Adis is wonderful . . . when I come home from work Adis wags his tail and likes to kiss me.”15 Kiss me, she thinks every time she reads the letter, how wonderful. How Dmitri would have savored that.
Having celebrated her 83rd birthday in 2016, Lyudmila is still working with the foxes. The wise words uttered by the fox in Saint-Exupéry’s The Little Prince that “you become responsible forever for what you tame,” are Lyudmila’s constant companions. Her dream is to establish a secure and loving future for the foxes. “I hope that it is possible to register them as a new pet species,” Lyudmila says. “One day I will be gone, but I want my foxes to live forever.” She knows that convincing more people to take the foxes into their homes won’t be easy. But easy doesn’t matter to Lyudmila. Easy never has mattered. Possible is what matters.
Fig. 1. A domesticated fox enjoying the summer shade at the fox farm outside of Novosibirsk. Credit: Irena Muchamedshina
Fig. 2. An inquisitive domesticated fox peering out from behind vegetation. Credit: Irena Muchamedshina
Fig. 3. A domesticated fox relaxing. While Siberia is brutally cold during the winter, it gets quite hot during the summer. Credit: Irena Pivovarova
Fig. 4. A domesticated fox pup playing. Credit: Anastasia Kharlamova
Fig. 5. A domesticated fox rests its head on the shoulder of one of the members of the fox team. The bond between tame foxes
and humans emerged early in the fox farm experiment. Credit: Irena Pivovarova
Fig. 6. Left to Right, Lyudmila Trut, Aubrey Manning, Dmitri Belyaev, Galina Kiseleva, all sitting on a bench in front of one of the tame foxes. Years earlier, Lyudmila was seated on this bench when Pushinka barked at an intruder. Credit: Aubrey Manning
Fig. 7. Two domesticated foxes, one with a balloon toy in its mouth. These foxes play with almost any object they can get into their mouths. Credit: Anna Kukekova
Fig. 8. Two domesticated foxes playing in the winter snow. Credit: Aaron Dugatkin
Fig. 9. Two workers carrying domesticated foxes at the fox farm. Winter days at the fox farm can be short and frigid. Credit: Aaron Dugatkin
Fig. 10. Two domesticated fox pups being taken for a walk by Irena Muchamedshina. On occasion, the tame foxes are walked around on a leash and act in an astonishingly dog-like manner. Credit: Anastasia Kharlamova
Fig. 11. A gorgeous domesticated fox. Credit: Institute of Cytology and Genetics