Tuesday, October 20

Russian foxes bred for tameness may not be the domestication story we thought

For
the last 60 years, scientists in Siberia have bred silver foxes to be
increasingly tame, with the goal of revealing the evolutionary and genetic
underpinnings of domestication. This research also famously showed a link
between tameness and such physical changes as curled tails and spotted coats, known
as “domestication syndrome.”

But
that story is flawed, some researchers now claim. The foxes weren’t totally
wild to begin with, and some of the traits attributed to domestication existed
long before the experiment began, Elinor Karlsson, a biologist at the
University of Massachusetts Medical School in Worcester, and her colleagues
argue. What’s more, the researchers cast doubt on whether domestication
syndrome even exists,
in a paper published online December 3 in Trends in Ecology and Evolution.

The
impressively long silver fox experiment, ongoing at the Russian Academy of
Sciences’ Institute of Cytology and Genetics in Novosibirsk since 1960, didn’t seek to
breed foxes that looked so different from their wild counterparts. But several
generations after geneticist Dmitry Belyaev took 130 silver foxes (Vulpes vulpes) from Soviet fur farms and
began selecting for friendliness toward humans, the physical changes emerged. Floppy
ears, piebald coats and other traits were known in other domesticated mammals,
so the changes have since been thought of as a syndrome of traits inherently
linked to the process of domestication of wild animals.

It’s
no secret that the foxes weren’t truly “wild,” Karlsson says. The Soviet foxes
originally came from fur farms on Prince Edward Island in Canada, with
selective breeding dating back to at least the 1880s. One of Karlsson’s
colleagues, on vacation on the island, stumbled across fur farm photographs
from the 1920s during a visit to a local museum. Those foxes appeared tame with
spotted coats — one of the same domestication traits claimed as a by-product of
the Russian experiment that supposedly took generations to emerge.  

“These
photos dated from decades before the project had even started,” Karlsson says.
The images “seemed to raise a lot of questions about exactly what had happened
during the course of that project in terms of genetic changes in that
population.”

Leo Frank holding a fox
In this image, fur farmer Leo Frank holds an apparently tame silver fox in his arms on Prince Edward Island in Canada in 1922.Keystone-Mast Collection/California Museum of Photography/University of California, Riverside

This
timeline undermines the narrative that the domestication syndrome traits sprang
entirely out of Belyaev’s selection for tameness, Karlsson and her colleagues
say.

“It
changes the clock on [the changes],” Karlsson says. “These traits didn’t get
created within 10 generations. They were actually preexisting in the
population.”

Lyudmila Trut, who has been involved in the silver fox experiment from the start and now runs it, disputes Karlsson’s argument. Trut admits that a small percentage of the fur farm foxes (less than 10 percent) were not very fearful or aggressive towards humans. But “we repeatedly visited those large fur farms,” and none of the other traits associated with domestication syndrome were present, she claims. Karlsson’s allegation that tameness and white spotting were imported into the experiment along with the Canadian foxes is “a misguided contention, to say the least,” Trut says. In particular, spots “arose only under selection for tameness.”

Karlsson says the timeline revelation prompted by the photos not only raised questions about the experiment but also led her and her colleagues to reconsider a bigger question: What’s the evidence supporting domestication syndrome? They soon found that not only was domestication syndrome loosely defined, so was domestication itself. “Everybody kind of comes up with a different constellation of traits,” she says.

So
the team developed its own criteria for the syndrome. For instance, the traits
should appear shortly after the onset of breeding for tameness, and grow in
frequency and degree with increasing tameness. She and her team then applied
these criteria to “domestication syndrome” traits reported in the foxes and
other domesticated animals, including pigs, goats and mice. No single species met
all criteria, undermining the validity of a shared syndrome between
domesticated mammals, the team claims. 

Christina Hansen Wheat, a behavioral ecologist at Stockholm University, agrees that the theory of domestication syndrome isn’t well-supported by evidence. “I find it problematic that we continue to conduct research on domestication based on too broad and unclear definitions and untested hypotheses,” she says. “We need to reevaluate our expectations of the consequences of domestication.”

But
other researchers are casting their own doubts on the scientists’ takedown.

Adam
Wilkins, an evolutionary biologist at Humboldt University of Berlin, says Karlsson’s
study misrepresents domestication syndrome. It treats the syndrome as a
specific and constant set of characteristics across domesticated mammals. But domestication
syndrome has been envisioned as differing from species to species, he says. For
instance, it may result in floppy ears in domesticated rabbits, pigs and sheep,
but in smaller but similarly shaped ears in cats, ferrets, and camels.

In the Russia experiment, the physical traits didn’t crop up until six to 10 generations in, says Lee Alan Dugatkin, a behavioral ecologist at the University of Louisville in Kentucky who wrote a book on the Russian foxes with Trut (SN: 4/29/17). “It’s not as if those things were there when they got the foxes,” he says. “It’s extraordinarily unlikely that there was kind of hidden genetic variation for these traits.”

The fur farm images from the 1920s “could easily have [shown] animals that had been trained or learned how to be friendly with the person in the picture,” Dugatkin says. “That’s very different than suggesting that the animals [on Prince Edward Island] are inherently friendly.”

silver fox in Madison, Wisconsin
A silver fox from a fur farm in Madison, Wisc., shows white spots similar to those that emerged among foxes bred for tameness in Siberia (image taken ca.1932).L.J. Cole and R.M. Shackelford/The American Naturalist 1943

Dispute
aside, Karlsson says she still views the fox experiment as tremendously
important. Belyaev and his colleagues “were remarkably successful in selecting
on behavioral traits and showing that they can create populations that have
very different behaviors,” she says, noting that this has spurred ongoing research
into the genetic and neurological elements to these behavioral changes (SN: 8/6/18). Such
research may also unlock secrets about humans, particularly with regards to
mental illnesses, Karlsson says.

Going
forward, Karlsson thinks that research on domestication would be well-served by
stepping away from domestication syndrome and thinking more about how these
animals may be self-domesticating, driving their own modifications by adapting
to people. As human influence grows in wild spaces, many species are likely
changing in response to us, she says.

“Rather
than worrying about our assumptions for what domestication is, looking at how
species are changing to adapt to our presence would be — in some ways — a more
intriguing way to think about the problem,” Karlsson says.