In 1959, the Soviet zoologist Dmitry Belyaev began selectively breeding silver foxes. Those least afraid of people were chosen to reproduce. His goal was to simulate the process that turned fierce ancient wolves into the dogs now known as our best friends.
The experiment worked, famously well. In 10 generations, Belyaev’s lineage of foxes became tame, seeking attention from people and wagging their tails when scientists approached.
But this wasn’t the only way the foxes changed. In 1979, Belyaev noted that some of the foxes had begun to look different, developing curly tails, spotting on their coats and floppy, puppy-like ears.
Later, other scientists began noticing some of these same traits in other domesticated species – pigs and goats, birds and fish – which seemed to point to a common genetic path that animals take as they change from wild to tame to domesticated.
This tantalizing notion, now known as domestication syndrome, was first put forward by Charles Darwin, and it has become integral to our understanding of how animal domestication works. But in a new paper, some scientists have challenged its accuracy – and, along the way, common beliefs about what domestication means.
The authors of the paper do not doubt that Belyaev was able to breed tamer foxes. But the Russian experiment fell short of proving the existence of domestication syndrome, they argue, because Belyaev’s first foxes were far from wild, and there’s no proof certain physical features are common to domesticated species.
“The common story line is that when you select on tameness in an animal species, a whole suite of other traits change in a predictable way,” said Elinor Karlsson, a genomic scientist at the University of Massachusetts Medical School and senior author on the study. “And we just couldn’t find convincing evidence for that.”
A major problem is that Belyaev started with foxes that weren’t wild, said Kathryn Lord, an evolutionary biologist at the University of Massachusetts Medical School and lead author of the paper, published Tuesday in the journal Trends in Ecology and Evolution. Genetic testing indicated they originated in eastern Canada, probably at a fur farm on Prince Edward Island, which means the animals were already on the path toward domestication.
There’s also evidence that Canadian fur farmers were seeking to produce unusual pelt colors, including with white spotting, which might fetch higher prices. So some of the traits held up by Belyaev as evidence of the domestication syndrome may already have been present in his first batch of foxes.
And those foxes’ tendency to produce white spots likely would have become greater when they arrived in Russia, because Belyaev started his experiment with a rather small population of 130 animals, Karlsson said.
“You can get very rapid changes in the frequency or the prevalence of a trait without having done a whole lot of work, just by making the population really, really small,” she said.
The other wrinkle is that evidence for the suite of physical traits long said to be shared by dogs, goats, rabbits and other domesticated species is thin, the authors say.
For instance, it’s commonly said that domesticated animals have curlier, more upright tails – the difference between a Siberian husky’s and a gray wolf’s. But Lord and her colleagues found no conclusive evidence that domesticated dogs hold their tails differently from wolves, foxes or other wild canids. They also found little documentation of these traits for other animals.
“I know this is true! It’s a thing!” Lord said, acknowledging that even she finds the lack of data frustrating. “But nobody’s counted it.”
This is important, Karlsson said, because while “tail carriage” is more common in less fearful foxes, it’s also seen in some of their wild cousins. That means the adorable, dog-like tails seen in the Russian experiment’s foxes may not be linked to genetic changes that enabled their tameness at all. It might just be sheer luck.
“Our main point is not that domestication syndrome doesn’t exist, but just that we don’t think there is enough evidence to be confident it does exist,” said Karlsson in a follow-up email.
None of this matters much to how most of us relate to our dogs and cats (or pigs and goats). But the challenge to common wisdom about how those animals came to be has caused waves in the community of domestication scholars – and gotten a mixed reception.
“The fox experiment is the most celebrated one in studies of domestication, yet details of it have never been fully published or explained, much less critically assessed,” said Marcelo Sánchez-Villagra, a paleobiologist at the University of Zurich who has studied domestication syndrome. “This paper to me shows that new, better designed experiments on domestication – of several kinds of animals – are needed to advance the field forward.”
Melinda Zeder, senior scientist emeritus at the Smithsonian’s National Museum of Natural History, said the Russian farm-fox experiment has “really been oversold,” in that many popular portrayals make it out to be grander and more simplified than Belyaev and the scientists who succeeded him meant it to be.
“The caution that they offer here is very useful, to sort of pull back and say this is not the be-all, end-all,” Zeder said. But she added that the “case is not as convincing as you would want it to be,” in part because, she said, it places too much weight on a lack of studies documenting every domestication syndrome trait in every domesticated animal.
Belyaev was well aware that white spotting was present in his fox population and never claimed it was linked to tameness, said Anna Kukekova, a geneticist at the University of Illinois at Urbana-Champaign who has been studying these foxes for decades. Belyaev detailed this clearly in a paper he published in 1979, she said.
Kukekova said she had other qualms about the new paper, though she agrees that there doesn’t seem to be evidence for one easy path to domestication.
“Genes rarely have a single function,” she said in an email.
“I would strongly argue [the Russian farm-fox experiment] is still the gold standard,” said Lee Dugatkin, a biologist at the University of Louisville and co-author of a book about the Russian experiment, “How to Tame a Fox (and Build a Dog).”
Dugatkin said he had “major concerns” about the study. He said curly tails didn’t show up in the foxes for nine to 10 generations and that the scientists did not select for them once they showed up.
But they grew more common with each tamer generation, he said. The project, which is now run by his co-author, Russian geneticist Lyudmila Trut, has since added two new lineages of foxes, one selected for aggression and another as a control, he said, and they haven’t developed curly tails and spotting.
But just because those traits don’t show up in other populations “doesn’t prove that the traits are directly linked to tameness,” said Karlsson, “just that those traits happened to also occur in the population that was selected for tameness. The most likely explanation is that this is due to random chance.”
Lord makes no bones about how important Belyaev’s work was. “It’s an amazing behavioral experiment,” she said.
But it could be stronger, Karlsson said.
“That was kind of what inspired us to write the paper,” she said. “Because there’s nothing more frustrating than when people just assume that something is true that hasn’t been proved yet.”
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