Monday Pets: The Russian Fox Study

I've decided I want to cover some recent research on social cognition in domesticated dogs. But first, we need some background. So here's a repost from the old blog.

Today I want to tell you about one of my most favorite studies, ever, of animals. Are you ready? It's a FIFTY YEAR LONG longitudinal study of captive silver foxes in Russia. Gather around, pour yourself a cup of your favorite beverage, get comfortable, and enjoy storytime.

In 1948, Soviet scientist Dmitri Belyaev lost his job at the Department of Fur Animal Breeding at the Central Research Laboratory of Fur Breeding in Moscow because of his commitment to classical genetics. At the time, in Soviet Russia, Lysenkoism was all the rage (and by that, I mean, it was state doctrine). Lysenkoism (named for its champion Trofim Lysenko) is akin to Lamarckian inheritance - than acquired characteristics could be passed down to offspring. We now know, of course, that Lamarck was basically wrong and an organism's experiences can not be genetically passed to its offspring (though there may be other mechanisms).

Our hero Belyaev was kicked out of the Fur Breeding Lab in Moscow, but he continued to study genetics under the guise of studying animal physiology throughout the 1950s. Then, in 1959, he became the director of the Institute of Cytology and Genetics of the Russian Academy of Sciences, in Novosibirsk, Russia. He remained director through 1985.

At the time, biologists were puzzled as to how dogs evolved to have different coats than wolves, since they couldn't figure out how the dogs could have inherited those genes from their ancestors. Belyaev saw silver foxes as a perfect opportunity to find out how this happened.

Belyaev believed that the key factor that was selected for was not morphological (physical attributes), but was behavioral. More specifically, he believed that tameness was the critical factor. How amenable was an animal to interacting with humans? This would certainly impact how well an animal would adapt to life with humans.

He hypothesized that selecting for tameness and against aggression would result in hormonal and neurochemical changes, since behavior was ultimately rooted in biology. It could be that the genetic differences that led to the morphological changes that biologists noticed in domesticated dogs (particularly, they noticed differences in fur coloration, and increased skull size relative to body size) were related to the genetic changes that underlied the behavioral temperament that they selected for (tameness and low aggression). He believed that he could investigate some of the questions about domestication by attempting to domesticate wild foxes. Belyaev and his colleagues took wild silver foxes (a variant of the red fox) and bred them, with a strong selection for inherent tameness.

Starting at one month of age, and continuing every month throughout infancy, the foxes were tested for their reactions to an experimenter. Essentially, they were tested for their friendliness. The experimenter would attempt to pet and handle the fox while offering it food. In addition, the experimenters observed whether the foxes preferred to hang out with other foxes, or with humans.

Then, when they reached sexual maturity (7-8 months), they had their final test and assigned an overall tameness score. First, they rated each fox's tendency to approach an experimenter standing at the front of its home pen. They also rated each fox's tendency to bite the experimenters when they tried to touch it. Only those foxes who were least fearful and least aggressive were chosen for breeding. This made for two original groups of foxes: an experimental group, bred for tameness, and a control group. This has been done for over FORTY generations of such foxes. In each successive generation of the experimental group, less than 20% has been allowed to breed each year. (Later, he also bred a line of foxes to be fearful and aggressive, in a similar manner). To ensure that tameness results from genetic selection and not simply from experience with humans, the foxes are not trained and are only allowed short "time dosage" contact with their caretakers and experimenters.

These experimental foxes, which were bred on a single selection criteria, displayed behavioral, physiological, and morphological (i.e. physical) characteristics that were not found in the control foxes, or in some cases, such characteristics were displayed with far higher frequency in the experimental group.

Behavioral changes: The experimental foxes were more eager to hang out with humans, whimpered to attract attention, and sniffed and licked their caretakers. They wagged their tails when they were happy or excited. Does that sound like your pet dog at all? Further, they had reduced fear responses to novel items or situations, and had enhanced exploratory behavior in unfamiliar situations.

Morphological changes: These changes were perhaps the most surprising (and gave the best support to Belyaev's predictions). A much higher proportion of experimental 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."

Physiological changes: The first change detected was in the piuitary-adrenal axis. This system is responsible for the control of adrenaline, among other things. Adrenaline is one hormone that is produced in response to stress, and controls fear-related responses. The experimental foxes had significantly lower adrenaline levels than their control-group cousins. The researchers hypothesized that foxes that are not afraid of humans are going to produce less adrenaline around them. This explains the foxes' tameness, but it doesn't account for their changed fur coloration patterns. The scientists theorized that adrenaline shares a biochemical pathway with melanin, which controls pigment production in fur.

And so it was that selecting for a single behavioral characteristic - tameness (or, put another way, selecting against fear and aggression) - resulted in changes not only in behavior, but also in correlated and unselected physical and physiological changes.

These results have led to speculation that similar models could account for the superior behavioral and cognitive traits (and physical and physiological differences) of domestic dogs over their wolf ancestors.

Belyaev, DK (1969). Domestication of animals. Science, 5 (1), 47-52.

Trut, L. (1999). Early Canid Domestication: The Farm-Fox Experiment American Scientist, 87 (2) DOI: 10.1511/1999.2.160

Trut, L. (2001). Experimental Studies of Early Canid Domestication. In The Genetics of the Dog, A Ruvinsky and J. Sampson, eds.

Want to read more? See the study's main website. Also, see Bora's post on these foxes and developmental timing.