What Makes a Fox Tame?

Dr. Trut with a Tame Fox

Thanks to my friend Nora, another dog lover, for recommending the 2017 book:  How to Tame a Fox (And Build a Dog) by Lee Alan Dugatkin and Lyudmila Trut.  The book chronicles an extended experiment done in Siberia started in the 1950s by two amazing geneticists, Dmitri Belyaev and Lyudmila Trut. They risked their careers and lives during a time of Soviet animosity toward geneticists, using foxes to probe basic questions about how animals become domesticated. I was fascinated by their work and wanted to check out what has happened since publication of the book.

Creating Tame Foxes

Dmitri noticed that domesticated animals shared certain, mostly juvenile, features not common in adult wild animals:  floppy ears, curly tails, more rounded facial features, and coat colors with patches, blazes and spots.  No wonder I call my dogs babies.  But not all animals can be domesticated.  Although the zebra can sometimes be bred to a horse, showing a close genetic link, European colonists in Africa were never able to domesticate the zebra, which, unlike horses, were resistant to diseases transmitted by the tsetse fly. 

Dmitri Belyaev with domesticated foxes in March 1984. Photo Credit: Sputnik, via Alamy

The Soviet Union was breeding foxes in farms for the lucrative fur market.  Red foxes had already been bred into a more prized silver coat color by Canadians and the Soviets developed their own colonies from these animals.  They were kept single-housed in cages and were particularly aggressive.  The caretakers needed to wear thick gloves, even while providing food, as the foxes snarled and snapped.  A miserable life for the animals and not very nice for the caretakers either.

The experiment was simple.  Look for the least aggressive foxes during this normal handling, breed them together and then keep breeding the animals that were calmest around humans.  Like with zebras, the experiment could fail, but they had hope because domesticated dogs and wolves both originated from a common ancestor.  There was a chance it would work and it could be justified with the Soviet authorities economically to allow the project to proceed. 

Within 3 generations they began to see significantly calmer behavior around humans, and within 4 generations they had a lone pup, Ember, who wagged his tail for them.  It took several litters for this behavior to show up in Ember’s pups, leading to a line of foxes with tail wagging propensities.  By the 5th generation, they were finding pups who wanted to nuzzle up to the humans and would lay on their backs for a tummy rub.  In each generation, larger percentages of the pups would display these behaviors, and by generation 8, some of their tails began to curl.  Their natural puppy playfulness lasted longer than the normal foxes and some even began to maintain non-aggressive eye contact with their caretakers.  In the 10th generation, Mechta became the first fox to keep floppy ears into adulthood.  These more juvenile physical features, in different combinations in different individuals, were showing up based on selection only for behavior.  Vocalizations similar to human laughter also began to appear and the foxes were able to respond to human training and hand signals like dogs.  Amazing!

Fox bred for dog-like behavior towards humans.

Photo Credit: Jennifer Johnson, Darya Shepeleva, and Anna Kukekova

What Caused the Apparent Domestication?

The scientists wanted to understand how these changes were happening and compared the tame colony of foxes with another group purposely selected for aggressive behavior toward humans.  It was hard to find caretakers willing to care for this aggressive group, but they have been invaluable for comparison.  These carefully bred colonies of foxes were almost lost in the break-up of the Soviet Union and subsequent changes, but support from the world wide scientific and humanitarian community helped save the foxes.  It’s unclear if these Russian foxes can be adopted into the US, but it looks like there have been importation issues and scams. Beware that they are still much wilder than a domesticated dog and can be quite a handful to care for…. super high energy, dig a lot and have a propensity to mark with very strong smelling urine.

There is scientific controversy over whether this population of foxes was really a good example of domestication because tame foxes also appear to have existed in the original Canadian colony of silver foxes, but in my mind that does not diminish the value of having those two distinct populations of foxes for comparison.  They behave consistently on opposite ends of the spectrum of behavior toward humans. 

Lyudmila and her colleagues had to make good guesses about what might be different between the tame and aggressive foxes and then measure those things one at a time.  That was the state of science at the time and later studies verified those results.  There was not too much surprise that the levels of stress hormones were higher in the aggressive than the tame foxes.  It was also consistent to find higher levels of the neurotransmitters serotonin and dopamine in regions of the tame fox brains as they are often called “happy” and “feel good” neurotransmitters.  Higher levels of glutamate, the primary excitatory neurotransmitter in the brain, and molecules involved in its signaling were observed in the aggressive lines.  Fetal development and even hippocampal regenerative capacity (associated with a more supple memory forming apparatus), were found to have been altered in the tame animals.  These may explain how some of the physical and behavioral traits were linked.

It’s Complicated

More recently, scientists prefer to compare differences between populations at the genetic and transcript levels without making guesses.  This unbiased approach allows us to learn about changes we may not anticipate, and there are always surprises in such studies.  What does that all mean?  Well genes are encoded in our DNA blueprint and are the same all over the body for an individual.  Transcripts, or the messenger RNA transcribed from the genes, are the subset of genes actually used in each tissue and so vary with each tissue of the body.  It allows each cell type and tissue to have a different structure and function in the body, otherwise we would just be one big blob. Scientists can compare either the entire genome or the transcriptome to look for differences.

With these methods, 70 genes and 159 splice variants were different between the tame and aggressive lines over three brain regions.   Look at the heat map below of the transcriptome from the hypothalamus of a dozen each tame vs. aggressive foxes shown vertically.  Horizontally, the amount of expression for one gene is shown as an intensity between very low (bright red), medium (black) and very high (bright green). I think they’re pretty and hold a lot of information if you unfocus your eyes a bit and look at the overall color schemes on each side of the square.

Computer algorithms search the voluminous data for patterns while comparing each mRNA transcript between the two groups.  Overall you can see some transcripts are higher (green) or lower (red) in expression depending on whether the animal was tame or aggressive, but it isn’t consistent with every individual in the group.  Looks complicated, yes, and that’s my point.  Lots of things are happening- some changes may be causing many other changes in a cascade and there is not just one magic switch for it all.  Within those changes, patterns in different pathways were evaluated and found in the systems related to development, differentiation, and, surprisingly, immunity. 

There is much work to be done and new publications continue to pour out from analyzing these animals and what may have led them to be able to be sociable with people.  Although tame foxes are not the same as dogs and there are bound to be some differences, this is a fascinating set of experiments, now going on for over 60 years, due to the bravery and diligence of a few brave scientists in Siberia.

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