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Darwin, Meet Friendly Mr. Fox

By Katherine Xue, Contributing Writer

The mid-20th century Soviet Union was not a friendly place for biologists. Stalin’s regime had outlawed all research in genetics—declaring the science and its founder Gregor Mendel antithetical to Marxist teachings—and waged a vicious campaign to execute or imprison the field’s adherents.

After losing his job at Moscow’s Central Research Laboratory of Fur Breeding, geneticist Dmitry Belyaev resolved to continue his forbidden work at a research institute in Siberia, designing a covert genetic experiment on the silver fox Vulpes vulpes, a color variant of the familiar red fox.

Belyaev and his students began their study by carefully observing 130 silver foxes for their interactions with humans. Only the tamest—the foxes that remained still when approached and didn’t attack their human handlers—were allowed to breed. Belyaev’s hypothesis: by selectively breeding for tameness, he could produce heritable changes in behavior to recapitulate the domestication of wild canines.

Fifty years later, the silver foxes at the Siberian Institute of Cytology and Genetics are as tame as dogs. They wag their tails and whine when humans approach; they jump into researchers’ arms and try to lick their faces. These behaviors are hard-wired: tame foxes have tame offspring, and when aggressive foxes raise the offspring of tame foxes, the pups stay tame.

But “friendliness” wasn’t the only change. Though Belyaev’s foxes were selected for tameness, other changes soon followed: piebald coats, floppy ears, curly tails. Subtler changes, too—shorter snouts and smaller skulls, a longer developmental window for social bonding—physical effects with surprising relations to behavior, all compressed into about 40 vulpine generations.

We typically think of evolution working with sandpaper or a fine-tooth comb—incremental changes, accumulating slowly over millenia. What’s astonishing about Belyaev’s silver foxes is how everything happened at once, and fast, both behavioral changes and seemingly unrelated ones. It’s possible that these alterations came about through a huge number of genetic mutations, each affecting different traits. But it seems more likely, given the rapidity of change, that a small number of genetic changes had major physiological effects.

There are other examples of wide-acting genes like those that tamed the silver fox. Major changes in the course of the domestication of maize from teosinte, its wild ancestor, were driven by mutations in a single gene that inverted the structure of the corn kernel’s casing to expose its fleshy interior. Centuries after Darwin collected his famous Galapagos finches, researchers have found a protein whose timing and levels of expression alter beak size. Increasingly, our picture of nature suggests that natural selection acts on living things in unexpected ways, with a change in a single gene sometimes driving large-scale alterations, and other times fine-tuning what’s already there.

The organization of our genes might explain how large physiological changes arise. The complexity of living things may seem to suggest that they are brittle and precarious, like a game of Jenga where the smallest mutation can bring the tower toppling down. From this perspective, major evolutionary changes would seem to require painstakingly precise, minute alterations.

But instead, it seems that living things are organized to tolerate and even promote change. Biological processes are often modularized, and through many levels of hierarchical regulation, small refinements in key genes—like changes in the location and timing of expression—can make large-scale rearrangements while preserving core functions.

In animals, for instance, a group of genes called the “Hox cluster” determines where body parts form. By simply changing where these genes are expressed, scientists have engineered mutant fruit flies with fully formed legs in place of their antennae. It seems like living things have evolved to become evolvable, their very organization suited to change and adaptability.

As for the friendly foxes, recent studies have begun to associate tameness with a particular segment of the fox genome, a region also linked to domestication in dogs. Research suggests that the changes in Belyaev’s foxes may stem from hormones that control both stress and the timing of development, explaining the retention of juvenile traits like floppy ears. But we’re far from unraveling exactly what these hormones do, let alone their far-reaching effects. For now, the story of the tame silver foxes is still evolving.

This article has been revised to reflect the following correction:

CORRECTION: Nov. 2

An earlier version of this article incorrectly stated that geneticist Dmitry Belyaev conducted research on silver foxes in the mid-19th century. In fact, he worked in the mid-20th century.

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