FEATURE ARTICLE
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
Belyaev's Hypothesis
Belyaev began his experiment in 1959, a time when Soviet genetics
was starting to recover from the anti-Darwinian ideology of Trofim
Lysenko. Belyaev's own career had suffered. In 1948 his commitment
to orthodox genetics had cost him his job as head of the Department
of Fur Animal Breeding at the Central Research Laboratory of Fur
Breeding in Moscow. During the 1950s he continued to conduct genetic
research under the guise of studying animal physiology. He moved to
Novosibirsk, where he helped found the Siberian Department of the
Soviet (now Russian) Academy of Sciences and became the director of
the Department's Institute of Cytology and Genetics, a post he held
from 1959 until his death in 1985. Under his leadership the
institute became a center of basic and applied research in both
classical genetics and modern molecular genetics. His own work
included ground-breaking investigations of evolutionary change in
animals under extreme conditions (including domestication) and of
the evolutionary roles of factors such as stress, selection for
behavioral traits and the environmental photoperiod, or duration of
natural daylight. Animal domestication was his lifelong project, and
fur bearers were his favorite subjects.
Early in the process of
domestication, Belyaev noted, most domestic animals had undergone
the same basic morphological and physiological changes. Their bodies
changed in size and proportions, leading to the appearance of dwarf
and giant breeds. The normal pattern of coat color that had evolved
as camouflage in the wild altered as well. Many domesticated animals
are piebald, completely lacking pigmentation in specific body areas.
Hair turned wavy or curly, as it has done in Astrakhan sheep,
poodles, domestic donkeys, horses, pigs, goats and even laboratory
mice and guinea pigs. Some animals' hair also became longer (Angora
type) or shorter (rex type).
Tails changed, too. Many breeds of dogs and pigs carry their tails
curled up in a circle or semicircle. Some dogs, cats and sheep have
short tails resulting from a decrease in the number of tail
vertebrae. Ears became floppy. As Darwin noted in chapter 1 of
On the Origin of Species, "not a single domestic
animal can be named which has not in some country drooping
ears"—a feature not found in any wild animal except the
elephant. Another major evolutionary consequence of domestication is
loss of the seasonal rhythm of reproduction. Most wild animals in
middle latitudes are genetically programmed to mate once a year,
during mating seasons cued by changes in daylight. Domestic animals
at the same latitudes, however, now can mate and bear young more
than once a year and in any season.
Belyaev believed that similarity in the patterns of these traits was
the result of selection for amenability to domestication. Behavioral
responses, he reasoned, are regulated by a fine balance between
neurotransmitters and hormones at the level of the whole organism.
The genes that control that balance occupy a high level in the
hierarchical system of the genome. Even slight alterations in those
regulatory genes can give rise to a wide network of changes in the
developmental processes they govern. Thus, selecting animals for
behavior may lead to other, far-reaching changes in the animals'
development. Because mammals from widely different taxonomic groups
share similar regulatory mechanisms for hormones and neurochemistry,
it is reasonable to believe that selecting them for similar
behavior—tameness—should alter those mechanisms, and the
developmental pathways they govern, in similar ways.
For Belyaev's hypothesis to make evolutionary sense, two more things
must be true. Variations in tamability must be determined at least
partly by an animal's genes, and domestication must place that
animal under strong selective pressure. We have looked into both
questions. In the early 1960s our team studied the patterns and
nature of tamability in populations of farm foxes. We cross-bred
foxes of different behavior, cross-fostered newborns and even
transplanted embryos between donor and host mothers known to react
differently to human beings. Our studies showed that about 35
percent of the variations in the foxes' defense response to the
experimenter are genetically determined. To get some idea of how
powerful the selective pressures on those genes might have been, our
group has domesticated other animals, including river otters
(Lutra lutra) and gray rats (Rattus
norvegicus) caught in the wild. Out of 50 otters caught during
recent years, only eight of them (16 percent) showing weak defensive
behavior made a genetic contribution to the next generation. Among
the gray rats, only 14 percent of the wild-caught yielded offspring
living to adulthood. If our numbers are typical, it is clear that
domestication must place wild animals under extreme stress and
severe selective pressure.