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Since How to Tame a Fox (and Build a Dog) was published in 2017, molecular genetics research connected to the silver fox domestication experiment has appeared in Nature and Proceedings of the National Academy of Sciences. Lee Alan Dugatkin writes about his connection to the project, the role of neural crest cells in domesticating foxes, and how dogs, bonobos, and humans ﬁt into the picture.
Not long after arriving in Novosibirsk, Siberia, in January 2012, my 17-year-old son Aaron and I could barely see. We had come in the middle of winter, prepared for the -35-degree temperatures with ski masks, but our glasses iced up every time we stepped outside. Through the snow, ice, and wind, we soon learned the trick: pull down on the mask around the mouth to avoid the condensation that otherwise builds up there.
Each morning we’d meet our driver and begin the 45-minute drive to the Institute of Cytology and Genetics. This trip, the first of two that I would make to the institute, was focused on research for a book that I was co-authoring on the Russian silver fox domestication experiment, which had been going on since 1959.
The experiment first came to my attention in graduate school, where I studied evolutionary biology and behavior. When I became a professor of biology at the University of Louisville, my fascination with it continued, and I developed an email relationship with Lyudmila Trut, the Russian geneticist who had been leading the experiment since 1959. After the exchange of countless emails over two years, we had decided to collaborate on a book; now we would be meeting face-to-face for the first time.
At the institute and at the farm where the foxes lived, we interviewed everyone and anyone associated with the experiment, poking and probing, not just for information about the study, but what it was like to be part of the daily routine. Aaron, who had learned a little Cyrillic to help us navigate the streets of Novosibirsk (and Moscow before that), transcribed the interviews on his laptop, which were being translated into English in real time by our interpreter, Vladimir.
The people we talked to—ranging in age from their 20s to their 90s who had been devoted to the experiment—were gracious and thrilled that an American scientist thought enough of their work to not just collaborate, but to also spend time in Siberia in the dead of winter. After these interviews and my many days with the 78-year-old Trut, I came to see her as one of the most remarkable people I have ever had the pleasure of knowing.
History of the Experiment
Even before receiving her Ph.D. in 1966, Trut was already in charge of the day-to-day operations under her mentor, Dmitri Belyaev, the originator of the silver fox project. From Belyaev‘s reading of Charles Darwin’s book, The Variation of Animals and Plants Under Domestication, and his own work at the Institute for Fur Breeding Animals in Moscow in the 1940s and early 1950s, Belyaev knew that many domesticated mammals share similar traits: floppy ears, curly tails, reduced stress hormone levels, variation in fur/skin coloration, reduced skull size, juvenilized facial and body features, reduced sexual dimorphism in facial and body features via feminization (domesticated males are more similar to females than were their wild ancestors), and relatively long reproductive periods. While there is some debate as to just how common such characteristics are across species, today this suite of traits is known as the domestication syndrome.
Belyaev was fascinated with these shared characteristics. He hypothesized that the early stages of animal domestication involved choosing the friendliest, most docile animals, because the one thing our ancestors always needed in a species they were domesticating—be it for food, transportation, protection, or companionship—was an animal that interacted relatively prosocially toward them. Belyaev also hypothesized that somehow, and he did not know how, many of the traits domesticated species share were linked to genes associated with tameness.
Working with a colleague who was in charge of a small population of foxes being bred for shiny (salable) furs near Tallinn, Estonia, in 1952, Belyaev initiated a pilot experiment testing these ideas in silver foxes (Vulpes vulpes). Each year, they selected a few of the friendliest foxes and preferentially bred those individuals. Within three breeding seasons, they were seeing promising results: the foxes were a little calmer than their parents, grandparents, and great-grandparents.
In 1959, Belyaev expanded this work into a large-scale study when he moved to the newly established Institute of Cytology and Genetics, located outside of Novosibirsk, the third largest city in Russia. He quickly recruited the 25-year-old Trut to work with him on this experiment. (Belyaev died in 1985.)
Within six generations (six years), intense selection for friendliness—by breeding the tamest ten percent of males and females—produced some foxes that licked the hands of experimenters, wagged their tails when humans approached, and whined when humans departed. These animals were never taught or trained; their prosociality toward humans was solely the result of genetic selection.
During the early years of the experiment, about two percent of the population showed such prosocial behaviors. Today, more than 75 percent of the experimental population displays these traits. What’s more, as Belyaev predicted, with selection for friendliness, a suite of other characteristics emerged in the experimental fox population.
In less than ten generations, some of the animals had floppy ears and curly tails. Within 15 generations, baseline corticosteroid levels (a measure of stress) were about half those of typical foxes. Over the course of the experiment, Belyaev, Trut, and their team also found that the domesticated foxes exhibited significant variation in fur patterns and extended reproductive periods. They also displayed rounder and shorter, more juvenilized, dog-like snouts and shorter, thicker limbs.
The silver fox experiment has shed new light on the evolution of social cognition in nonhuman animals (similar characteristics to those of human persons). Work in this area began in 2002, when Brian Hare, at the time a Ph.D. student at Harvard University, began looking at the ability of nonhumans to follow human gaze and gestures. Prior work had shown that when researchers placed two opaque containers on a table and put food under one, chimpanzees did not use human gaze or gestures to determine where the food was, but Hare and his colleagues found that dogs easily solved the same sort of task using human gaze and gestures.
Why were dogs so good at this test of social cognition? Hare first examined whether it was because dogs spend their whole lives with humans, and so might learn how to do this. He tested dog pups of different ages, as well as dogs that had lots of interactions with humans and those that had few interactions, and in almost all cases, the dogs solved the task, suggesting it wasn’t experience with humans per se that made dogs good at this. Hare next considered the possibility that all canid species were adept at this, regardless of experience with humans. When he tested both wolves and dogs, dogs (again) solved the problem, but wolves did not. Being a canid per se was not the answer.
Hare next began to think that perhaps dogs were so good at this social cognition task because during the process of domestication, dogs that were astute at picking up on social cues emitted by humans were rewarded for doing so (likely with food and shelter). In a paper in Science, he and his colleagues hypothesized “that individual dogs that were able to use social cues more flexibly than could their last common wolf ancestor … were at a selective advantage.”
Hare’s Ph.D. advisor, Richard Wrangham, suggested an alternative hypothesis. Perhaps the ability to follow human gaze and gestures was a byproduct of domestication: that is, during the process of domestication, instead of our ancestors having preferentially bred dogs that have this ability, selection had been for friendliness toward humans, and that the reason dogs follow gaze and touch today is because this ability is genetically correlated with friendliness. Selection for friendliness and following gaze and touch come along for the ride. Together, Hare and Wrangham constructed a way to experimentally distinguish between these hypotheses using the silver foxes of the Novosibirsk project—the only domesticates where we know exactly what the selection pressures are and have been; Trut and her team select which individuals breed, based on friendliness and only friendliness, not on social cognition skills.
Hare knew that in addition to the domesticated foxes, the experiment has a control line of foxes that are selected randomly with respect to their friendliness to humans. If Hare’s hypothesis was correct, foxes in both the domesticated and control lines would fare poorly on the social cognition test, but if Wrangham was correct—that is, if social cognition was a byproduct of domestication—then the domesticated foxes would show social cognition skills on a par with dogs, but the control foxes would not.
Hare traveled to Novosibirsk and, working with Trut and others, tested these alternative hypotheses. They ran a series of experiments that involved gazing and then touching one of two objects placed in front of the foxes. Domesticated fox pups were significantly more likely than pups from the control group to follow human gazing at and touching cues. In a separate experiment, they found that domesticated pups were not only better than control pups, but just as good as dog pups, on this social cognition task. Together, these findings suggest that social cognition in domesticated species is indeed a byproduct of selection for friendliness, rather than direct selection for the ability to follow gaze or gestures.
Molecular Genetic and Neural Crest Cells
Much of the recent work on the domesticated foxes has probed deep into their genome for clues about the process of domestication. In a 2018 paper published in Nature: Ecology and Evolution, Anna Kukekova, Trut, and their colleagues uncovered a cluster of genes associated with domestication on fox chromosome 15. SorCS, one of the genes associated with memory and learning functions, forms a bridge between molecular genetic work and the social cognition studies discussed earlier.
Right from the start of the silver fox study, Belyaev had hypothesized that some of the changes that occur during domestication were a consequence of changes in gene expression patterns: when genes “turn on” and “turn off,” and how much protein they produce. In a 2018 paper in Proceedings of the National Academy of Sciences, Kukekova, Trut, and Andrew Clark’s team at Cornell University followed up on earlier work on gene expression in domesticated foxes by comparing patterns in the domesticated animals versus another line of foxes from the Novosibirsk experiment that for the last 40-plus years have been selected for aggressive, rather than friendly, behavior toward humans. They found 146 genes in the prefrontal cortex and 33 genes in the basal forebrain that showed different patterns in domesticated and aggressive foxes, including genes associated with serotonin receptor pathways that modulate friendly and aggressive temperament.
Molecular genetic work on the silver foxes is also helping explain the domestication syndrome. Kukekova and her colleagues’ Proceedings of the National Academy of Sciences paper describes changes in the frequency of alleles linked to neural crest cells. Adam Wilkins and his colleagues have hypothesized that changes in the behavior of such neural crest cells may be critical for many of the phenomena that characterize the domestication syndrome.
The argument goes like this: much work shows that very early in mammalian embryonic development, neural crest cells migrate to the brain, face, jaws, ears, tail, skin, and many other parts of the body. Wilkins and colleagues hypothesize that when our ancestors selected for calm, friendly behavior early in the process of domestication, they indirectly selected for a reduction in the number of migrating neural crest cells, and that, as a result, “most of the modified traits, both morphological and physiological [associated with the domestication syndrome], can be readily explained as direct consequences of such deficiencies [in neural crest cells]…”. For example, a decrease in neural crest cells that develop into cartilage might explain floppy ears and curly tails, both of which are in part due to reduced amounts of cartilage.
Self-Domestication in Bonobos and Humans
Around 1980, findings from the fox domestication experiment led Belyaev to propose an audacious idea about human evolution. In a keynote speech he gave in 1984 at the XV International Genetics Congress, he proposed that we are the product of a process of self-domestication. “The social environment created by man himself has become, for him, quite a new ecological milieu,” Belyaev told his audience.
This led to new natural selection pressures, and Belyaev came to think that “under these conditions, selection required from individuals some new properties: obedience to the requirements and traditions of the society, i.e., self-control in social behavior.” In particular, humans who were better able to cope with stress, to stay calm rather than strike out in aggression, had a selective advantage. “One can hardly doubt,” Belyaev noted in his speech, “that the word and its meaning has become for man an incomparably stronger stressful factor than a club blow for a Neanderthal man.” This in turn favored our ancestors selecting calmer, “tamer” mates and groupmates, setting the process of self-domestication in motion.
Before delving a bit deeper into the possibility of human self-domestication, let’s examine some evidence that self-domestication has occurred in another primate, the bonobo (Pan paniscus), a sister species to the chimpanzee, and its closest evolutionary relative.
Bonobos live in matriarchal societies, where females form alliances and voluntarily share food, even with strangers. Bonobos play often and sexual behavior is used as a greeting, a form of play, and a means of resolving conflicts. Chimp society, in contrast, is patriarchal. Males are dominant to females and fight with one another to rise up in the hierarchy. They sometimes form alliances, but unlike female coalitions in bonobos, chimp alliances sometimes raid and viciously attack individuals in other groups.
Contemporary populations of bonobos, but not chimpanzees, show behavioral, morphological, and endocrinological profiles that are strikingly similar to those seen in other domesticated species, including the domesticated foxes. Bonobos are far more cooperative and altruistic than chimpanzees. They have more juvenilized skeletal features and lower stress hormone levels. They display more variation in color (e.g., white color tufts and pink lips), and have smaller skulls (but have more gray matter in their brains devoted to areas linked with empathy). All of which is to say: bonobos act and look domesticated.
But if humans didn’t domesticate bonobos—and we didn’t—who (or what) did? Hare, Wrangham, and Victoria Wobber, who had just completed her Ph.D. with Wrangham at Harvard, suggested in a paper in 2012 that bonobos domesticated themselves. Here’s how: chimpanzees and bonobos began to diverge from a common ancestor approximately 2 million years ago, at about the time the Congo River was forming in Africa. By chance, the formation of the Congo River split the population of the common ancestor of bonobos and chimpanzees into two groups, with the lineage that led to bonobos living in a small area to the south of the Congo River, and the chimpanzee lineage living north of the river, in a much larger area stretching across west and central Africa.
With this division, the bonobo lineage happened to find itself in an area with higher-quality foods than the chimpanzee lineage, and because there were no gorillas to the south of the Congo River, as there were to the north, the bonobo lineage had less competition for food with other large primates. Intense competition with gorillas would likely have favored more aggressive individuals in the chimpanzee lineage, while reduced competition and more reliable sources of food may have provided proto-bonobos with more time for play and cooperation.
Hare (who is now an associate professor in evolutionary anthropology at the Center for Cognitive Neuroscience at Duke University and founder of the Duke Canine Cognition Center) and his colleagues hypothesize that bonobos who played and cooperated with one another to obtain food, shelter, and sexual partners fared better than aggressive intolerant types. At this stage of bonobo evolutionary history, the argument goes, females may have selected the least aggressive, most friendly males as mates, self-domesticating themselves in a process similar to that outlined by Belyaev for humans. This preference may have been specific to the early stages of bonobo self-domestication; indeed, recent work in modern female bonobos has found that they are no more likely than chimpanzees to choose the calmest, friendliest males as mates.
Circling back to our own species, comparisons between humans and domesticated animals, as well as between humans and other primates, suggest that we display the morphological, endocrinological, and behavioral signs of a self-domesticated species. Anatomical studies have found that modern humans show feminization of facial features compared to ancestral Homo species (as well as other closely-related species), and a recent molecular genetic study of neural crest cells (published in Science) suggests a possible mechanism for such changes.
Compared with other primate species, modern humans also have a prolonged juvenile stage, wherein young are reliant for long periods on their parents, and we generally display relatively juvenilized traits for longer periods of time. Hormone profiles, especially those associated with androgens, suggest reduced aggressive tendencies in modern humans, and behavioral comparisons of aggression between humans and other closely-related species find that we in fact display much less aggressive behavior, particularly reactive aggressive behavior (more on that below). In addition, broad-scale genomic comparisons suggest natural selection has operated on Homo sapiens in a manner similar to the “selective sweeps” (in which many traits increase in frequency simultaneously) that we see in domesticated species like dogs, cats, horses, and cattle.
The fullest treatment to date of human self-domestication can be found in Richard Wrangham’s 2019 book, The Goodness Paradox: The Strange Relationship Between Virtue and Violence in Human Evolution. In his book, Wrangham turns to the silver fox domestication experiment as a base from which to explore all discussions of domestication; indeed, he refers to the process of human self-domestication, as a case of what he calls “Belyaev’s Law.”
Wrangham hypothesizes that the process of human self-domestication began about 300,000 years ago. But how and why? The answer, he suggests, centers on an evolutionary shift from reliance on reactive aggression toward reliance on proactive aggression. Wrangham defines reactive aggression as “a response to a threat or frustrating event … that it is always associated with anger, as well as with a sudden increase in sympathetic activation, a failure of cortical regulation, and an easy switching among targets.”
In contrast, proactive aggression involves “a purposeful planned attack with an external or internal reward as a goal. It is characterized by attention to a consistent target, and often by a lack of emotional arousal.” When our ancestors began to rely more on proactive aggression, Wrangham proposes, we began to domesticate ourselves, as we moved away from a more typical primate social system, where a few strong, hyper-aggressive, reactive individuals dominated and secured most of the mating within a group.
Language, Wrangham proposes, facilitated proactive aggression, leading to a social system where proactive individuals could plan and work together to threaten, and if need be, punish hyper-aggressive, reactive individuals, dramatically reducing the total amount of aggression in early human societies. Once a shift toward proactive aggression—and self-domestication—was under way, other traits in the domestication syndrome began to appear, perhaps because the evolution from reactive to proactive aggression caused a reduction in the number of neural crest cells migrating during early stages of development. Tests of the human self-domestication hypothesis are in their early stages and it will be fascinating to see how this idea fares with time.
As they have from the initiation of the experiment, the now 86-year-old Trut and her colleagues in Novosibirsk continue to test hundreds of foxes each year, preferentially breeding the friendliest individuals. While much of the work today centers on molecular genetics, changes in behavior, morphology, neurobiology, and endocrinology continue to be recorded. 2020 marks the start of the seventh decade of this experiment, making it one of the longest, continually running, controlled experiments ever undertaken. That said, 60 years is but the blink of an eye in terms of evolutionary time. Who knows what new discoveries might emerge if this experiment continues for 100 years, or 200? Time will tell.
Financial Disclosure: The author has no conflicts of interest to report.
This article first appeared in the Spring 2020 issue of our Cerebrum magazine. Click the cover for the full e-magazine.