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
Selection and Development
Evidently, then, selecting foxes for domestication may have
triggered profound changes in the mechanisms that regulate their
development. In particular, most of the novel traits and other
changes in the foxes seem to result from shifts in the rates of
certain ontogenetic processes—in other words, from changes in
timing. This fact is clear enough for some of the novelties
mentioned above, such as the earlier eye opening and response to
noises and the delayed onset of the fear response to unknown
stimuli. But it also can explain some of the less obvious ones.
Floppy ears, for example, are characteristic of newborn fox pups but
may get carried over to adulthood.
Even novel coat colors may be attributable to changes in the timing
of embryonic development. One of the earliest novel traits we
observed in our domesticated foxes was a loss of pigment in parts of
the head and body. Belyaev determined that this piebald pattern is
governed by a gene that he named Star. Later my colleague
Lyudmila Prasolova and I discovered that the Star gene
affects the migration rate of melanoblasts, the embryonic
precursors of the pigment cells (melanocytes) that give
color to an animal's fur. Melanocytes form in the embryonic fox's
neural crest and later move to various parts of the embryo's
epidermis. Normally this migration starts around days 28 to 31 of
the embryo's development. In foxes that carry even a single copy of
the Star gene, however, melanoblasts pass into the
potentially depigmented areas of the epidermis two days later, on
average. That delay may lead to the death of the tardy melanoblasts,
thus altering the pigmentation in ways that give rise to the
distinctive Star pattern.
One developmental trend to which we have devoted particular
attention has to do with the growth of the skull. In 1990 and 1991,
after noticing abnormal developments in the skulls and jaws of some
of our foxes, we decided to study variations in the animals' cranial
traits. Of course, changes in the shape of the skull are among the
most obvious ways in which dogs differ from wolves. As I mentioned
earlier, Morey believes that they are a result of selection (either
natural or artificial) for reproductive timing and smaller body size.
In our breeding experiment, we
have selected foxes only for behavior, not size; if anything, our
foxes may be slightly longer, on average, than the ones Belyaev
started with 40 years ago. Nevertheless, we found that their skulls
have been changing. In our domesticated foxes of both sexes, cranial
height and width tended to be smaller, and snouts tended to be
shorter and wider, than those of a control group of farmed foxes.
Another interesting change is that the cranial morphology of
domesticated adult males became somewhat "feminized." In
farmed foxes, the crania of males tended to be larger in volume than
those of females, and various other proportions differed sharply
between the sexes. In the domesticated foxes the sexual dimorphism
decreased. The differences in volume remained, but in other respects
the skulls of males became more like those of females. Analysis of
cranial allometry showed that the changes in skull proportions
result either from changes in the timing of the first appearance of
particular structures or from changes in their growth rates. Because
we studied the skulls only of adult foxes, however, we cannot judge
whether any of these changes are pedomorphic, as Morey believes they
are in dogs.
The most significant changes in developmental timing in our foxes
may be the smallest ones: those that have to do with reproduction.
In the wild, foxes reach sexual maturity when they are about 8
months old. They are strict seasonal breeders, mating once a year in
response to changes in the length of the day (in Siberia the mating
season runs from late January to late March) and giving birth to
litters ranging from one to thirteen pups, with an average of four
or five. Natural selection has hard-wired these traits into foxes
with little or no genetic variation. Fur farmers have tried for
decades to breed foxes that would reproduce more often than
annually, but all their attempts have failed.
In our experimental fox population, however, some reproductive
traits have changed in a correlated manner. The domesticated foxes
reach sexual maturity about a month earlier than nondomesticated
foxes do, and they give birth to litters that are, on average, one
pup larger. The mating season has lengthened. Some females breed out
of season, in November–December or April–May, and a few
of them have mated twice a year. Only a very small number of our
vixens have shown such unusual behavior, and in 40 years, no
offspring of an extraseasonal mating has survived to adulthood.
Nevertheless, the striking fact is that, to our knowledge,
out-of-season mating has never been previously observed in foxes
experiencing a natural photoperiod.