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Early Canid Domestication: The Farm-Fox Experiment

Foxes bred for tamability in a 40-year experiment exhibit remarkable transformations that suggest an interplay between behavioral genetics and development

Lyudmila Trut

Alternative Explanations

What might have caused these changes in the fox population? Before discussing Belyaev's explanation, we should consider other possibilities. Might rates and patterns of changes observed in foxes be due, for example, to inbreeding? That could be true if enough foxes in Belyaev's founding population carried a recessive mutant gene from the trait along with a dominant normal gene that masked its effects. Such mixed-gene, or heterozygous, foxes would have been hidden carriers, unaffected by the mutation themselves but capable of passing it on to later generations.

As Morey pointed out, inbreeding might well have been rampant during the early steps of dog domestication. But it certainly cannot explain the novel traits we have observed in our foxes, for two reasons. First, we designed the mating system for our experimental fox population to prevent it. Through outbreeding with foxes from commercial fox farms and other standard methods, we have kept the inbreeding coefficients for our fox population between 0.02 and 0.07. That means that whenever a fox pup with a novel trait has been born into the herd, the probability that it acquired the trait through inbreeding (that is, by inheriting both of its mutant genes from the same ancestor) has varied between only 2 and 7 percent. Second, some of the new traits are not recessive: They are controlled by dominant or incompletely dominant genes. Any fox with one of those genes would have shown its effects; there could have been no "hidden carriers" in the original population.

Figure 5. Foxes in Belyaev's experimental groupClick to Enlarge Image Another, subtler possibility is that the novelties in our domesticated population are classic by-products of strong selection for a quantitative trait. In genetics, quantitative traits are characteristics that can vary over a range of possibilities; unlike Gregor Mendel's peas, which were either smooth or wrinkly with no middle ground, quantitative traits such as an animal's size, the amount of milk it produces or its overall friendliness toward human beings can be high, low or anywhere in between. What makes selecting for quantitative traits so perilous is that they (or at least the part of them that is genetic) tend to be controlled not by single genes but by complex systems of genes, known as polygenes. Because polygenes are so intricate, anything that tampers with them runs the risk of upsetting other parts of an organism's genetic machinery. In the case of our foxes, a breeding program that alters a polygene might upset the genetic balance in some animals, causing them to show unusual new traits, most of them harmful to the fox. Note that in this argument, it does not matter whether the trait being selected for is tameness or some other quantitative trait. Any breeding program that affects a polygene might have similar effects.

The problem with that explanation is that it does not explain why we see the particular mutations we do see. If disrupted polygenes are responsible, then the effects of a selection experiment ought to depend strongly on which mutations already existed in the population. If Belyaev had started with 130 foxes from, say, North America, then their descendants today would have ended up with a completely different set of novelties. Domesticating a population of wolves, or pigs, or cattle ought to produce novel traits more different still. Yet as Belyaev pointed out, when we look at the changes in other domesticated animals, the most striking things about them are not how diverse they are, but how similar. Different animals, domesticated by different people at different times in different parts of the world, appear to have passed through the same morphological and physiological evolutionary pathways. How can that be?

Figure 6. Dogs begin forming social bondsClick to Enlarge Image According to Belyaev, the answer is not that domestication selects for a quantitative trait but that it selects for a behavioral one. He considered genetic transformations of behavior to be the key factor entraining other genetic events. Many of the polygenes determining behavior may be regulatory, engaged in stabilizing an organism's early development, or ontogenesis. Ontogenesis is an extremely delicate process. In principle, even slight shifts in the sequence of events could throw it into chaos. Thus the genes that orchestrate those events and keep them on track have a powerful role to play. Which genes are they? Although numerous genes interact to stabilize an organism's development, the lead role belongs to the genes that control the functioning of the neural and endocrine systems. Yet those same genes also govern the systems that control an animal's behavior, including its friendliness or hostility toward human beings. So, in principle, selecting animals for behavioral traits can fundamentally alter the development of an organism.

As our breeding program has progressed, we have indeed observed changes in some of the animals' neurochemical and neurohormonal mechanisms. For example, we have measured a steady drop in the hormone-producing activity of the foxes' adrenal glands. Among several other roles in the body, the adrenal cortex comes into play when an animal has to adapt to stress. It releases hormones such as corticosteroids, which stimulate the body to extract energy from its reserves of fats and proteins.

After 12 generations of selective breeding, the basal levels of corticosteroids in the blood plasma of our domesticated foxes had dropped to slightly more than half the level in a control group. After 28 to 30 generations of selection, the level had halved again. The adrenal cortex in our foxes also responds less sharply when the foxes are subjected to emotional stress. Selection has even affected the neurochemistry of our foxes' brains. Changes have taken place in the serotonin system, thought to be the leading mediator inhibiting animals' aggressive behavior. Compared with a control group, the brains of our domesticated foxes contain higher levels of serotonin; of its major metabolite, 5-oxyindolacetic acid; and of tryptophan hydroxylase, the key enzyme of serotonin synthesis. Serotonin, like other neurotransmitters, is critically involved in shaping an animal's development from its earliest stages.

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