Evolutionary biologist and science historian Lee Dugatkin talks about the legendary six-decade Siberian experiment in fox domestication run by Lyudmila Trut, his co-author of a new book and Scientific American article about the research.

Steve Mirsky: Welcome to Scientific American’s Science Talk, posted on April 18, 2017. I’m Steve Mirsky. On this episode -

Lee Dugatkin: At the genetic level, how in the world is it possible that selecting for just behavior, this tame behavior, could lead to all of the other things that they see in these domesticated foxes?

Mirsky: That’s Lee Dugatkin. He’s an evolutionary biologist and science historian at the University of Louisville, and he’s the co-author of a new book titled How to Tame a Fox and Build a Dog. The other author of the book is the extraordinary Lyudmila Trut, professor of evolutionary genetics at the Institute of Cytology and Genetics in Novosibirsk, Siberia, who started running this legendary fox domestication experiment when she was 25 and is still running it at the age of 83. Trut and Dugatkin are also the authors of an article about their research in the May issue of Scientific American called How to Build a Dog.

Trut does not speak much English, so I spoke with Dugatkin by phone. Tell us about this amazing experiment that’s gone on for six decades. What was the impetus for it?

Dugatkin: Dmitry Belyayev, who is the person who got the experiment started initially, was fascinated with the process of domestication. He had worked with domesticated animals in various different places, looking at various different questions early in his career, and he wanted to devise an experiment to test a fairly radical notion that he had about how domestication events begin. So he wanted to do an experiment that he could look at results in real time as it’s happening.

You know, because when we think about domestication, the classic example of dogs from wolves, we’re looking at a process that people still argue, but we’re talking about a process that would take thousands and perhaps 10,000 to 15,000 years to complete, and what Belyayev wanted to do was test his ideas about domestication in real time so that he could watch changes unfold in front of him and his team. So he initiated this silver fox domestication experiment.

Mirsky: How did Lyudmila Trut get involved in this?

Dugatkin: Well so Belyayev came up with this idea initially in the late 1940s, and he ran some very small pilot work on it in the early ‘50s. And what happened was he had an opportunity to really expand and test his ideas in a major way in the late 1950s when he, Belyayev, got a job as a vice director at one of these new very large scale institutes that had been built in Siberia. So Belyayev now had sort of resources and space where he could potentially take this idea he has about how domestication occurred, and we can talk about the details of the hypothesis in a minute, but he now had the resources to test this.

So he’s about to move to Siberia, and he knows that in his new position as vice director at this institute of cytology and genetics out in Novosibirsk, Siberia, that he’s going to have a lot of other things that he has to do in addition to wanting to get the domestication experiment off the ground. And so he’s looking for somebody who can be his main person on this experiment. Someone who could do both the day-to-day work that would be necessary to lead the team that eventually would come about, and somebody he could trust as a person who he thought was both independent and also was a good thinker.

So before he left to take the job in Siberia, he was in Moscow, and he went to Moscow State University, which is one of the finest institutes in the world, and he talked to a colleague of his who was sort of an intellectual descendent of Pavlov, so this was someone who had worked a lot on animal behavior. And he told this fellow Krasinsky that he was interested in finding the right person to lead this new experiment that he wanted to really get off the ground. And Krasinsky spread the word that Belyayev was interested, and one of the people who came to talk to him was Lyudmila Trut. And Lyudmila was at the time just 25 years old. She was just finishing up her degree at Moscow State.

Had done some work on behavior. She was interested in learning more about the experiment, and she met Belyayev. And everything clicked for both of them. Lyudmila was fascinated with Belyayev’s ideas. She also immediately sensed that this was somebody who was not just sort of a visionary scientist, but someone who she could work with that treated her immediately as an equal. He asked her some questions. He told her he wanted to build a dog out of a fox and then laid out the experiment that he had been thinking about for a while.

She was enamored. He liked what she told him about how she might try and do this, and so he offered her the position, and she took her family and hopped on a train and moved from Moscow to Novosibirsk, Siberia, in late 1958, early 1959. And she has been running the experiment every day for the last 58 years.

Mirsky: Unbelievable.

Dugatkin: Yeah, Lyudmila is an incredible person. As I said, she was just 25 when she started it. She had just finished up her undergraduate work, but she was gung ho that this experiment could be path breaking, and she wanted in, and she wanted to be part of this giant new institute that Belyayev was going to be vice director on, and so she took the chance and she went there, and at the start it was very difficult. But after a few years, the experiment sort of – there began to be a team of folks who work with her, and from there, it’s year after year, new discoveries, new ideas about domestication on everything from behavior to morphology to genetics.

Mirsky: So let’s talk about the choice of the fox. Because you’re not going to try to domesticate rattlesnakes. There’s a specific reason why you choose an animal that is already closely related to a domesticated animal.

Dugatkin: That’s right. So people might ask if Belyayev was interested particularly in the domestication of dogs. I mean he was interested in domestication in general, pigs, cows, horses, everything. But in particular, he was fascinated with the domestication of dogs because you know, because of the incredible bond that is developed between humans and dogs. So he wanted to do his experiment in a way to understand that phenomenon in particular.

And one night asked, “Why don’t you just use wolves because that’s what happened over our evolutionary history.” There’s lots of reasons. I mean they’re not easy to work with, and they would be very difficult to do this kind of experiment in. But the major reason Belyayev actually decided to work with foxes was because they were close enough to wolves from an evolutionary perspective right there with canines, but there was sort of a political undercurrent here. There’s a back story about why the foxes were chosen, which is that when the experiment was getting off the ground, in the Soviet Union, it was essentially illegal to do what we might think of as sort of modern western Mendelian genetics.

And what happened was up until the late 1920s or so, the Soviet Union was actually one of the leading places in the world where people were doing cutting edge research in genetics, but a fellow by the name of Trofim Lysenko who was this charlatan pseudo scientist, had managed to wiggle his way up in the kind of scientific hierarchy of the Soviet Union at the time. And he became Stalin’s right hand man for science, and Lysenko argued that what we’d call modern western Mendelian genetics was capitalist bourgeois science that was being done by saboteurs. And he convinced Stalin and many others high up in the ranks of the sort of Soviet science world that this should be illegal essentially.

And eventually what happened is thousands of Soviet geneticists lost their jobs. Hundreds of them were thrown in prison, and a few dozen were actually murdered by Lysenko and his thugs for doing what we’d consider modern genetics. So Lysenko basically argued that this older hypothesis that Lamarck had put out that basically had been disproven by the time Lysenko was rising in power was the correct way to think about genetics, but it was clearly the scientific establishment had already determined long ago that Lamarck’s ideas were wrong.

But Lysenko said they were right, and he convinced people that this is the sort of genetics they should do there. So this is the backdrop. It’s basically illegal to do modern genetics in Russia when Belyayev wants to start this experiment. But of course any experiment in domestication is an experiment in genetics. And so Belyayev has to figure out a way that he can do this experiment and at the same time stay away from Lysenko’s thugs. The beauty of the fox as an experimental subject here is that it’s close enough to wolves that it makes sense to do as an experimental animal.

But in addition, fox fur and mink fur, these were two of the only reliable sources of western income coming into the Soviet Union at that time. Economically they’re in bad straights, and furs, fox furs in particular are a major source of western money coming in, and they need it. So even though what he was going to do was a classic experiment in genetics. By doing it in foxes, he knew that they were less likely to get in trouble with Lysenko’s people because Lysenko’s people knew how much money fox furs were bringing in, and they might sort of turn their head the other way on any experiment that dealt with genetics and foxes because Belyayev basically told him we’re looking at physiology, we’re looking at reproduction, we’re looking at all the things you need to look at to build foxes that have good furs.

Even though really what he was doing was planning out a domestication experiment. He knew if he said that, Lysenko’s people would probably leave them alone, and they were more likely to be left alone also in Siberia than they would have been in Moscow or St. Petersburg. So that’s why they ended up working with foxes. Both because of the biological significance, and also because of the political facts on the ground.

Mirsky: That’s fascinating stuff that, by the way, is not in the article, but is in the book that you and Lyudmila Trut have co-authored called How to Tame a Fox.

Dugatkin: That’s right. So we’ve got a nice section that sort of lays out to the reader all of the Lysenko-related problems that are going on while they’re first beginning the experiment. Those problems, you know, begin to dissipate, and by the late ‘60s, this is no longer an issue. But up through the first decade or so of the experiment, this was a real present danger all the time for them. So they had to be smart about the way they did this.

Mirsky: And just to catch up, Lamarck argued that acquired traits could be inherited, whereas Darwinian theory showed that actually, it was traits that had arisen naturally that were then selected for – and the two outcomes may look the same. But the mechanism was really Darwinian rather than Lamarckian.

Dugatkin: That’s right, so Belyayev was steeped in Darwin’s works. He certainly understood how all that worked, and Lamarck as you described it had posed a counter explanation. Was actually before Darwin’s work that for a while was interesting hypothesis, but this notion that what you – what happens to you during your life from sort of external conditions and behaviors and the way you act can somehow be passed down to your offspring had long even before Belyayev’s experiment been shown to be essentially incorrect.

But Lysenko argued that Lamarck was in fact right on the mark. And part of the reason Lysenko did that, and we get into this a little bit in the book, is that from a political philosophical perspective, Lamarckian change fit better into the Soviet view of the world than classic Darwinian evolution did. So Lysenko tapped into that fact in order to convince people of his pseudo science. He knew people would gravitate towards Lamarckian inheritance because it sort of lined up a little better with Marxism, and so he used that to rise up in the power structure and basically make modern Darwinian Mendelian genetics illegal.

This set the Soviet Union back scientifically for decades. I mean it had major implications in genetics and evolution, obviously, but it also had quite significant implications for the medical research that was going on in the Soviet Union. You can imagine if you’re not going to be allowed to use modern genetics, you’re going to have problems when you study medical issues as well.

Mirsky: Let’s talk about the nuts and bolts of what Trut winds up working on every day for the last 58 years. What do they actually do with these foxes?

Dugatkin: So initially, Belyayev’s hypothesis for how domestication occurred in our evolutionary history went like this. If you look at domesticated species, it turns out that they all share a lot of similarities in terms of the traits they have. So for example, if you think about cows and pigs and dogs and horses and those sorts of things, those animals actually share a lot of traits that sometimes as a cluster recall this domestication syndrome.

So for example, they tend to have floppy ears and curly tails, and they tend to have much more juvenilized facial characteristics. So what Belyayev realized at the start, even back in the late 1940s and early 1950s when he’s just tinkering with these ideas, it is – that’s really sort of incredible that domesticated species would share a lot of these commonalities because we’ve domesticated them for such radically different things. So you know, some of these things we’ve domesticated so we could sit on their back and ride on them like horses.

And other things we’ve domesticated for perhaps protection, and other things we’ve domesticated to produce to give us milk and meat. And yet they all share so many characteristics, and Belyayev hypothesized that the one thing that was true for all domestication events is that the animals had to show sort of pro social behaviors towards humans. They had to be calm and relatively tame. Otherwise, we’d not be able to get anything else that we needed out of them, so we could not domesticate them for transportation or food or defense if we did not have animals that were acting in a fairly calm way with humans.

So Belyayev hypothesized that tameness, that calmness in the animals was the key thing that got all domestication events going. And he further hypothesized that all of these other things we see, the curly tails, the wagging tails, the floppy ears, the juvenile facial characteristics, the fact that domesticated animals tend to have much longer reproductive periods than their wild ancestors. All these things Belyayev hypothesized somehow came along for the ride in the sense that they were somehow genetically linked to tame behavior. He didn’t know how, but that was his hypothesis.

So select for tameness, Belyayev says, and first of all, you’ll get the process of domestication going, and second of all, all these other traits will also begin to appear. So what he and Lyudmila did at the start from Day 1 of the experiment is they devise a very, very simple behavioral set of tests that they’re going to do. Basically Lyudmila is going to approach a fox, note what it does as she approaches. She’s going to note what the fox does when Lyudmila is standing right next to the cage. She’s going to note what the fox does when she opens the door to the cage, and she’s going to note what the fox does when she puts her hand in there or she puts a stick in there or she puts something in there.

And each one of those times, she’s going to note what the animal does, and she’s going to come up with a scale for those that were the calmest towards her and up to the ones that were the most aggressive towards her. And they test hundreds and hundreds and hundreds of these animals every year, and they simply determine the ten percent or so – that number changes slightly over the course of a six-decade experiment. But basically, the top ten percent of the animals in terms of who are the calmest towards humans. Those are the individuals that are going to be the parents for the next generation, and then the next generation, they’re going to do the same thing.

Lyudmila is going to note which of them is the calmest through the standardized approach that they’ve developed. She’s going to test them once when they’re very young, you know, sort of pup stage, and she’s going to test them again when they’re adults, and strictly based on those behavioral tests, she is going to determine who are going to be the parents for the next generation.

And they’ve been doing this every year for 58 years. And what they found even very very early on, was that after just five or six generations for selecting for the calmest animals, they had gone from animals – you know, the first five or six years where they had done this testing, they probably tested a few thousand animals over those first five or six years.

And even the ones initially that had done best on the calmness score, they weren’t particularly tame. They just weren’t as aggressive as everybody else. So when you would look at them today, you wouldn’t think of them as especially calm animals. But compared to what she started with, they were. Yet within five or six generations of this selecting the calmest animals, they had animals that were wagging their tails when Lyudmila would approach them, that were licking her hand when she put them into the cage, and this is strictly as a result of genetic selection.

These animals are not trained to do this. There is no mechanism in the experiment for them to learn anything. They basically – what you’re looking at is the result of genetic selection. All of a sudden within five generations of selection, they have these animals that were extraordinarily docile towards humans. And then slowly but surely, so many of the other traits we see in domesticated animals also began to appear in these tame foxes.

Mirsky: There’s now evidence that this experiment really did in certain ways wind up causing the same genetic changes that the transformation of wolves into dogs experienced.

Dugatkin: Right. So this is still one of the – I would say one of the most active areas of research in the fox domestication experiment these days. So I think there’s a couple things going on here. They’ve been able to identify certain chromosomes in foxes where it looks like most of the genetic change associated with the domestication they’ve been doing for the last 60 years, these areas on one particular fox chromosome seem to be the ones where we see the most genetic change as the result of the domestication experiment. So at one level, they were sort of able to locate the chromosome where most of the genetic change occurred.

The really remarkable thing was that right around the same time that had happened, equivalent work had been done on dog domestication, and because dogs and foxes are evolutionarily close, you can compare the chromosomes in dogs where the evidence for genetic change as a result of domestication, where that occurred compared to where it occurred in the foxes. And when you do that from a genetic perspective, basically you’re looking at what are called homologous chromosomes. Basically, the fox equivalent of the dog chromosomes, or the dog equivalent of the fox chromosomes are compared to one another, and it turns out the same general area where there’s lots of evidence for genetic change associated with the fox domestication is where they found it in the equivalent spots on the dog.

So of course as they were doing this experiment, they had no idea that would be the case, but it’s remarkable that it seems to have – the experiment seems to have produced results that are incredibly parallel at the genetic level to what’s happened with the dog – with dogs. The micro-details, they’re still working out. So there’s one level at which we know what’s going on. The other level is that you’ve got to keep in mind that these domesticated foxes, they look very dog like, but they’re still foxes. And at the genetic level, although we now have evidence of where a lot of the genetic change has occurred during domestication, it’s still just 60 generations. And so genetically, they’re not dramatically different from let’s say a wild fox. Different enough that we’ve got a domesticated species, but not radically different. It looks like a lot of the change that’s occurred has been with respect to not so much the introduction of new genes or the selection of one gene variant versus another as changes in when genes turn on and when they turn off.

So there’s this whole large area of research on gene expression, which is basically asking genes turn on and turn off during different parts of our development, and when that happens dramatically affects what the gene does. And so what Lyudmila and her team have done is work with geneticists from all over the world to look at whether or not they can detect differences in gene expression in these domesticated foxes. And this is very much an ongoing project.

But when they compare the domesticated foxes to normal foxes and other lines of foxes that they’ve been breeding in Siberia, what they find is lots of evidence for changes in gene expression in the tame foxes. So there are a lot of genes that basically over express, which means they produce more of something, and they do it at different times during development in the tame foxes. And there are some genes that under express, meaning the genes don’t produce as much product as they do in a normal fox. Exactly how that translates into what they’re finding with the domesticated foxes remains to be seen.

But the action seems to be both in terms of classic genetic changes, ______ increases or decreases or is replaced by another, but also differences in when the genes turn on and when they turn off. Another related issue is sort of at the genetic level how in the world is it possible that selecting for just behavior, this tame behavior, could lead to all of the other things they see in these domesticated foxes. So we’ve already talked about they have longer reproductive periods, but they also have all these other classic domesticated species traits.

They also are chunkier than a normal fox. When you think of a normal fox, you think of these gracile legs that allow them to run around very quickly. Domesticated foxes are sort of chunkier, lower to the ground than regular foxes. All of these other changes have also occurred in these foxes even though Lyudmila and her team are never choosing the animals based on whether or not they have droopy ears or pup like faces. Only selected on their behavior. So the question is how do all these other things come along. They still don’t know the answer for sure, but there’s an interesting hypothesis that Tecumseh Fitch and Richard Rangum and Brian Hair and others have put out that suggests that it might be that all of these linkages are somehow associated with a set of cells that are really really important early on in development. There are these cells called neural crest cells that are fundamental during very very early development in animals, and it turns out the way these cells move early on in development and the speed at which they move can affect everything from behavior to morphology, including things like curly tails and floppy ears and more pup like faces.

So it might be, and this is still a working hypothesis, it might be that when they’ve been selecting for the tamest animals, one of the effects of that has been to change something about neural crest cell development, either how quickly or how many cells or the way that they’re moving. And that by changing that, because those cells affect all these other traits, you may see changes in those other traits as well. That might be the sort of key to the genetic linkage, although it’s still very much a working hypothesis.

Mirsky: And again, those are neural crest cells?

Dugatkin: That’s right, neural crest cells. There is endless work that’s been done in developmental biology on these cells. These cells develop into all sorts of different cells in animals. Everything from cells associated with morphological and anatomical traits like, you know, body shape and that sort of thing to behavior and the underlying hormones associated with them.

Mirsky: How did you get involved? You have not been doing this research, but you and Lyudmila Trut have a deep friendship now.

Dugatkin: That’s right. So I would say about six or seven years ago, I contacted Lyudmila. We had been in contact before that a little bit, but about six or seven years ago, I had contacted Lyudmila, and I basically said we – there are no books on this experiment, and we need to have a book out there for the general public so they can know the incredible science that’s been going on here for almost six decades. And they also can understand some of the political backdrop we’ve been talking about, and also this – understand this experiment that fundamentally helps us realize why this deep bond between us and our domesticated animals like dogs have occurred. And so I asked her if she’d be interested in working together to write that book.

And Lyudmila said that she would be, and over those last six years, I’ve had the honor and opportunity to visit with Lyudmila and the whole fox research team and the amazing foxes themselves over in Siberia. I’ve been there a couple of times, and through our interactions and through hundreds of hours of interviews with other people who have been involved in the experiment and have now moved all over the globe, we pieced together a way to tell the science, the intrigue, and the love stories all in one relatively concise book.

Mirsky: And of course your own research, which has appeared in Scientific American for a couple decades now, is not completely unrelated to this because you’ve looked at behavior as a function to genes.

Dugatkin: Right, no question about it. My lab has been set up since day one. I look at the evolution of behavior in all sorts of contexts, and that was initially what spurred me to get in touch with Lyudmila because I knew of the fox domestication experiment. Anyone who studies evolution and behavior has heard about it, and I knew little bits and pieces. But until I really worked with Lyudmila, I didn’t realize the depth of what they’ve done.

So the interesting thing about this project compared to others I’ve been involved in is a lot of people know a little bit about it, and the thing is 90 percent plus of it is only published in Russian, and so most people don’t know all the depth that’s involved in this experiment. They’ve done dozens of incredible experiments that have lasted anywhere from a couple years to a couple decades, and of course then all along the way, they’ve been doing the selection for tameness, and there’s this multi-layered set of results that really fundamentally changed not just our view of domestication, but our views on evolution and our views on why it is we have this deep relationship we have with our pets. Lyudmila and her team have reshaped the way we think about this.

And while it’s really a truly collaborative effort – I mean there have been probably hundreds of people over the years that have been involved in this, there’s just no question that Lyudmila is the force behind it. Belyayev was the fellow who came up with the idea and vested her with the power to do this incredible experiment, but Lyudmila is the force that has kept this thing going and continues to keep it going. She’s a remarkable person.

Mirsky: The Scientific American article in the May issue about this work is an original piece, not an excerpt from the book. So you can get a quick overview of the research in the article and then dive in more deeply in their book. That’s it for this episode. Get your science news at our website, www.ScientificAmerican.com. We’re also now bundling our daily 60-second science podcasts into weekly editions posted on YouTube where you can enjoy them by subscribing to the Scientific American channel. And follow us on Twitter where you’ll get a Tweet whenever a new item hits the website. Our Twitter name is @SciAm. For Scientific American science talks, I’m Steve Mirsky. Thanks for clicking on us.

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