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When scientists ponder how animals cameto be domesticated, they almost in-

evitably wind up thinking about dogs. The dogwas p robably the first domestic animal, and it isthe one in w hich domestication has p rogressedthe furthest—far enough to turn Canis lupus into

Canis familiaris. Evolutionary theorists have longspeculated about exactly how dogs’ associationwith human beings may have been linked totheir divergence from their wild wolf forebears,a topic that anthropologist Darcy Morey has dis-cussed in some detail in the pages of this maga-zine (July–August 1994).

As Morey pointed out, debates about theorigins of animal domestication tend to focuson “the issue of intentionality”—the extent to

which domestication was the result of deliber-ate hu man choice. Was dom estication actually“self-domestication,” the colonization of newecological niches by animals such as wolves?

Or did it result from intentional decisions byhuman beings? How you answer those ques-tions will determine how you understand themorphological and physiological changes thatdomestication has brought about—whether asthe results of the pressure of natural selectionin a new n iche, or as deliberately cultivated ad -vantageous traits.

In many w ays, though, the question of inten-tionality is beside the point. Domestication wasnot a single event but rather a long, complexprocess. Natural selection and artificial selectionmay both have operated at different times or

even at the same time. For example, even if pre-

historic people deliberately set out to domesti-cate wolves, natural selection would still havebeen at work. The selective regime may havechanged d rastically when w olves started livingwith people, but selective pressure continuedregardless of anything Homo sapiens chose to do.

Another problem with the debate over in-tentionality is that it can overshadow other im-portant questions. For example, in becomingdomesticated, animals have und ergone a hostof changes in morph ology, physiology and be-havior. What do those changes have in com-

mon? Do they stem from a single cause, and if

so, what is it? In the case of the dog, Moreyidentifies one comm on factor as pedomorphosis,the retention of juvenile traits by adu lts. Thosetraits include both morphological ones, suchas skulls that are unusually broad for their

length, and behavioral ones, such as whining,barking and submissiveness—all characteris-tics that wolves outgrow bu t that d ogs do not.Morey considers pedom orphosis in dogs a by-product of natural selection for earlier sexualmaturity and smaller body size, features that,according to evolutionary theory, ought to in-crease the fitness of animals engaged in colo-nizing a new ecological niche.

The common patterns are not confined to asingle species. In a wide range of mammals—herbivores and predators, large and small—

domestication seems to have brought with itstrikingly similar changes in appearance and be-

havior: changes in size, changes in coat color,even changes in the animals’ reproductive cy-cles. Our research group at the Institute of Cy-tology and Genetics in N ovosibirsk, Siberia, hasspent decades investigating such patterns andother questions of the early evolution of domes-tic animals. Our work grew out of the interestsand ideas of the late director of our institu te, thegeneticist Dmitry K. Belyaev.

Like Morey, Belyaev believed that the pat-terns of changes observed in domesticated an i-mals resulted from genetic changes that oc-curred in the course of selection. Belyaev,however, believed that the key factor selected

for was not size or reproduction, but behavior—specifically am enability to dom estication, ortamability. More than any other quality, Belyaevbelieved, tamability must have determined howwell an animal would adapt to life among hu-man beings. Because behavior is rooted in biol-ogy, selecting for tameness and against aggres-sion means selecting for physiological changesin the systems that govern the body’s hormonesand neurochemicals. Those changes, in turn,could have had far-reaching effects on the de-velopment of the animals themselves, effects

160 American Scientist, Volume 87

© Sigma Xi, The Scientific Research Society.

Reproduction w ith p ermission only. Contact perm [email protected]

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 N. Trut

Lyudmila N. Trut is head of

the research group at the

Institut e of Cytology and

Genetics of the Siberian

Department of the Russian

Academy of Sciences, in

N ovosibirsk. She received her

doctoral degree in 1980. Her

current research interests are

the patterns of evolutionary

transformations at the early

steps of animal domestication.

Her research group is develop-

ing the problem of domestica-

tion as an evolutionary event

with the use of experimental

models, including the silver

fox, the American m ink, the

river otter and the wild gray

rat. Address: Institute of

Cytology and Genetics of the

Russian Academy of Sciences,

630090 Novosibirsk 90,

Russia. Internet:

[email protected].



that might well explain why different animalswould respond in similar ways w hen subjectedto the same kinds of selective pressures.

To test his hypothesis, Belyaev decided toturn back the clock to the point at which ani-mals received the first challenge of domestica-

tion. By replaying the process, he would be ableto see how changes in behavior, physiology and

morphology first came about. Of course, repro-ducing the ways and means of those ancienttransformations, even in the roughest outlines,would be a formidable task. To keep th ings asclear and simple as possible, Belyaev designed aselective-breeding program to reproduce a sin-gle major factor, strong selection pressure fortamability. He chose as his experimental modela species taxonomically close to the dog butnever before domesticated: Vulpes vulpes, the sil-ver fox. Belyaev’s fox-breeding experiment oc-cupied the last 26 years of his life. Today, 14

years after his death, it is still in progress.Through genetic selection alone, our researchgroup has created a population of tame foxesfundam entally different in temperament and be-havior from their wild forebears. In the processwe h ave observed some striking changes inphysiology, morphology and behavior, which

mirror the changes known in other domestic an-

imals and bear out man y of Belyaev’s ideas.

Belyaev’s Hypothesis

Belyaev began his experiment in 1959, a timewhen Soviet genetics was starting to recoverfrom the anti-Darwinian ideology of TrofimLysenko. Belyaev’s own career had suffered. In1948 his comm itment to orthod ox genetics hadcost him his job as head of the Department of Fur Animal Breeding at the Central ResearchLaboratory of Fur Breeding in Moscow. Duringthe 1950s he continued to conduct genetic re-

1999 March–April 161


Reproduction w ith p ermission only. Contact [email protected]

Figure 1. In the late 1950s, the Russ ian geneticist Dmi try K. Belyaev began a decades-long effort to breed a population of tame foxes. Belyaev,

then director of the Institute of Cytology and Genetics of the U.S.S.R. (now Russian) Academy of Sciences in Novosibirsk, Siberia, hoped to

show that physical and morphological changes in domestic animals such as dogs could have resulted from selection for a single behavioral

trait, friendliness toward people. Fourteen years after his death, the experiment continues, and the results appear to support Belyaev’s

hypothes is. (All photographs courtesy o f the author.)



search under the guise of studying animalphysiology. He moved to Novosibirsk, wherehe helped found the Siberian Department of

the Soviet (now Russian) Academy of Sciencesand became the director of the Department’sInstitute of Cytology and Genetics, a post heheld from 1959 until his death in 1985. Underhis leadership the institute became a center of basic and ap plied research in both classical ge-netics and modern molecular genetics. Hisown work included ground-breaking investi-gations of evolutionary change in animals un-der extreme conditions (including domestica-

tion) and of the evolutionary roles of factorssuch as stress, selection for behavioral traitsand the environmental photoperiod, or dura-tion of natural d aylight. Animal domestication

was his lifelong project, and fur bearers werehis favorite subjects.

Early in the process of domestication,Belyaev noted, most domestic animals had un-dergone the same basic morphological andphysiological changes. Their bodies changed insize and proportions, leading to the app earanceof dwarf and giant breeds. The normal patternof coat color that had evolved as camouflage inthe wild altered as well. Many domesticatedanimals are piebald, completely lacking pig-mentation in specific body areas. Hair turnedwavy or curly, as it has done in Astrakhan

sheep, poodles, domestic donkeys, horses, pigs,

goats and even laboratory mice and guineapigs. Some animals’ hair also became longer(Angora type) or shor ter (rex type).

Tails changed, too. Many breeds of dogs andpigs carry their tails curled up in a circle orsemicircle. Some dogs, cats and sheep haveshort tails resulting from a decrease in the nu m-ber of tail vertebrae. Ears became floppy. AsDarwin noted in chapter 1 of On the Origin of

Species, “not a single domestic animal can benamed which has not in some country d roopingears”—a feature not found in any wild animal

except the elephant. Another m ajor evolution-ary consequence of domestication is loss of theseasonal rhythm of reproduction. Most wild an-

imals in middle latitudes are genetically pro-grammed to mate once a year, during matingseasons cued by changes in daylight. Domesticanimals at the same latitudes, however, now canmate and bear young more than once a yearand in any season.

Belyaev believed that similarity in the pat-terns of these traits was the result of selection foramenability to dom estication. Behavioral re-sponses, he reasoned, are regulated by a finebalance between neurotransmitters and hor-mones at the level of the whole organism. The

genes that control that balance occupy a highlevel in the hierarchical system of the genome.

Even slight alterations in those regulatory genescan give rise to a wide network of changes inthe developm ental processes they govern. Thus,selecting animals for behavior may lead to oth-er, far-reaching changes in the animals’ devel-opment. Because m ammals from widely differ-ent taxonomic groups share similar regulatorymechanisms for hormones an d neurochemistry,it is reasonable to believe that selecting them forsimilar behavior—tameness—should alter thosemechanisms, and the developmental pathwaysthey govern, in similar ways.

For Belyaev’s hypothesis to make evolution-ary sense, two more things must be true. Varia-

tions in tamability must be determined at leastpartly by an animal’s genes, and domesticationmust place that animal under strong selectivepressure. We have looked into both questions.In the early 1960s our team studied the patternsand nature of tamability in populations of farmfoxes. We cross-bred foxes of different behavior,cross-fostered newborns and even transplantedembryos between donor and host mothersknown to react differently to hum an beings. Ourstudies showed that about 35 percent of the vari-ations in the foxes’ defense response to the ex-




wavy or curly hair

rolled tails

shortened tails, fewer vertebrae

floppy ears

changes in reproductive cycle

piebald coat color

appearance of dwarf and giant varieties

sheep, poodles, donkeys, horses, pigsgoats, mice, guinea pigs

dogs, pigs

dogs, cats, sheep

dogs, cats, pigs, horses, sheep, goats, cattle

all except sheep

all

all

Figure 2. Early in the process of domestication, Darwin noted long ago, animals often undergo similar mor-

phological and physiological changes. Because behavior is rooted in biology, Belyaev believed that selection

for behavior implied selection for physiological characteristics that would have broader effects on the ani-

mals’ development. These effects might explain patterns in the responses of various animals to domestication.



perimenter are genetically determined. To getsome idea of how powerful the selective pres-sures on those genes might have been, ourgroup has domesticated other animals, includ-ing river otters (Lutra lutra) and gray rats (Rattus

norvegicus) caught in the wild. Out of 50 otterscaught during recent years, only eight of them(16 percent) showing weak defensive behaviormade a genetic contribution to the next genera-

tion. Among the gray rats, only 14 percent of thewild-caught yielded offspring living to adult-hood. If our numbers are typical, it is clear thatdomestication must place wild animals underextreme stress and severe selective pressure.

The Experiment

In setting up our breeding experiment, Belyaev

bypassed that initial trauma. He began with 30male foxes and 100 vixens, most of them from acommercial fur farm in Estonia. The foundingfoxes were already tamer than their wild rela-tives. Foxes had been farmed since the beginningof this century, so the earliest steps of domestica-

tion—capture, caging and isolation from otherwild foxes—had already left their marks on ourfoxes’ genes and behavior.

From the outset, Belyaev selected foxes fortameness and tameness alone, a criterion wehave scrupu lously followed . Selection is strict;in recent years, typically not more than 4 or 5percent of male offspring and about 20 percentof female offspring h ave been allowed tobreed. To ensure that their tameness resultsfrom genetic selection, we d o not tra in the fox-

es. Most of them spend their lives in cages andare allowed only brief “time dosed” contactswith hu man beings. Pups are caged with their

mothers until they are 11 ⁄ 2 to 2 months old.Then they are caged with their litter mates butwithout their mothers. At three months, eachpu p is moved to its own cage.

To evaluate the foxes for tameness, we givethem a series of tests. When a p up is one monthold, an experimenter offers it food from hishand while trying to stroke and handle the pup .The pups are tested twice, once in a cage andonce while moving freely with other pu ps in anenclosure, where they can choose to make con-tact either with the hum an experimenter or with

another pu p. The test is repeated month ly untilthe pu ps are six or seven months old.

At seven or eight months, when the foxesreach sexual maturity, they are scored for tame-ness and assigned to one of three classes. Theleast domesticated foxes, those that flee from ex-perimenters or bite when stroked or handled,are assigned to Class III. (Even Class III foxesare tamer than the calmest farm-bred foxes.Among other things, they allow themselves tobe han d fed.) Foxes in Class II let themselves bepetted and handled but show no emotionallyfriendly response to experimenters. Foxes inClass I are friendly toward experimenters, wag-

ging their tails and w hining. In the sixth gener-ation bred for tameness we had to add an evenhigher-scoring category. Members of Class IE,the “domesticated elite,” are eager to establishhum an contact, whimp ering to attract attentionand sniffing and licking experimenters likedogs. They start displaying this kind of behav-ior before they are one month old. By the tenth

generation, 18 percent of fox pup s were elite; by

the 20th, the figure had reached 35 percent. To-day elite foxes make up 70 to 80 percent of ourexperimentally selected popu lation.

Now, 40 years and 45,000 foxes after Belyaevbegan, our experiment has achieved an arrayof concrete results. The most obviou s of them isa unique population of 100 foxes (at latestcount), each of them the p rodu ct of between 30and 35 generations of selection. They are un-usual animals, docile, eager to please and un-mistakably domesticated. When tested ingroups in an enclosure, pup s compete for atten-




Figure 3. Piebald coat color is one of the most s triking

mutations among domestic animals. The pattern is

seen frequently in dogs (border collie, top right), pigs,

horses and cows. Belyaev’s hypothesis predicted that

a similar mutation he called Star, seen occasionally in

farmed foxes, would occur with increasing frequency

in f oxes sel ected for tamability. The ph otograph

above shows a fox in the selected population w ith the

Star mutation.



tion, snarling fiercely at one another as theyseek the favor of their hum an han dler. Over theyears several of our domesticated foxes haveescaped from the fur farm for days. All of themeventually returned . Probably they would h avebeen unable to survive in the wild.

Physical Changes

Physically, the foxes differ markedly from theirwild relatives. Some of the d ifferences have ob-

vious links to the changes in their social be-havior. In dogs, for example, it is well knownthat the first weeks of life are crucial for form-ing primary social bonds w ith hum an beings.

The “wind ow” of bonding opens when a p up -py becomes able to sense and explore its sur-roundings, and it closes when the pup startsto fear unknown stimuli. According to ourstudies, nondomesticated fox pups start re-sponding to auditory stimuli on day 16 afterbirth, and their eyes are completely open byday 18 or 19. On average, our domesticated foxpups respond to sounds two days earlier andopen their eyes a day earlier than th eir nondo-mesticated cousins. Nond omesticated foxesfirst show the fear respon se at 6 weeks of age;domesticated ones show it after 9 weeks or

even later. (Dogs show it at 8 to 12 weeks, de-

pend ing on the breed .) As a result, domesticat-ed pups have more time to become incorpo-rated into a hu man social environment.

Moreover, we have found that the delayeddevelopment of the fear response is linked tochanges in p lasma levels of corticosteroids, hor-mones concerned with an animal’s adaptationto stress. In foxes, the level of corticosteroids ris-es sharply between the ages of 2 to 4 monthsand reach adult levels by the age of 8 months.One of our studies found that the more ad-vanced an animal’s selection for domesticated

behavior was, the later it showed the fear re-sponse and the later came the surge in its plas-ma corticosteroids. Thus, selection for d omesti-cation gives rises to changes in the timing of thepostnatal d evelopment of certain p hysiologicaland hormonal mechanisms underlying the for-mation of social behavior.

Other physical changes mirror those in dogsand other domesticated animals. In our foxes,novel traits began to appear in the eighth totenth selected generations. The first ones we not-

ed w ere changes in the foxes’ coat color, chiefly aloss of pigment in certain areas of the body, lead-ing in some cases to a star-shaped p attern on the

face similar to that seen in some breeds of dog.Next came traits such as floppy ears and rolledtails similar to those in some breeds of dog. After15 to 20 generations we noted the appearance of foxes with shorter tails and legs and with un-derbites or overbites. The novel traits are stillfairly rare. Most of them show up in no morethan a few animals per 100 to a few per 10,000.Some have been seen in commercial popula-tions, though at levels at least a magnitude low-er than we recorded in our domesticated foxes.

Alternative Explanations

What might have caused these changes in the

fox population? Before discussing Belyaev’sexplanation, we should consider other possi-bilities. Might rates and patterns of changes ob-served in foxes be due, for example, to in-breeding? That could be true if enough foxes inBelyaev’s found ing popu lation carried a reces-sive mutant gene from the trait along with adominant normal gene that masked its effects.Such m ixed-gene, or heterozygous, foxes wouldhave been hidden carriers, unaffected by themutation themselves but capable of passing iton to later generations.




Figure 4. In typical silver foxes, such as those in the founding population of Belyaev’s breeding experiment, ears are erect, the tail is low

slung and the fur is sil ver-black, save for the tip of the tail. (All drawings of fo xes were made from the author’s photographs.)



As Morey pointed out, inbreeding mightwell have been ram pant d uring the early steps

of dog domestication. But it certainly cannotexplain the novel traits we have observed inour foxes, for tw o reasons. First, we designedthe mating system for our experimental foxpopulation to prevent it. Through outbreedingwith foxes from comm ercial fox farms and oth-er standard methods, we have kept the in-breeding coefficients for our fox population be-tween 0.02 and 0.07. That means that whenevera fox pup with a n ovel trait has been born into

the herd, the probability that it acquired thetrait through inbreeding (that is, by inheritingboth of its mutant genes from the same ances-tor) has varied between only 2 and 7 percent.

Second, some of the new traits are not reces-sive: They are controlled by dominant or in-completely dominant genes. Any fox with oneof those genes would have shown its effects;there could h ave been no “hidd en carriers” inthe original popu lation.

Another, subtler possibility is that the novel-ties in our domesticated population are classicby-products of strong selection for a quantita-tive trait. In genetics, quantitative traits arecharacteristics that can vary over a range of possibilities; unlike Gregor Mendel’s peas,which were either smooth or wrinkly with n o

midd le ground, quan titative traits such as an

animal’s size, the amount of milk it producesor its overall friendliness toward human be-ings can be high, low or anyw here in between.What m akes selecting for quan titative traits soperilous is that they (or at least the part of themthat is genetic) tend to be controlled n ot by sin-gle genes but by complex systems of genes,known as polygenes. Because polygenes are sointricate, anything that tamp ers with themruns th e risk of upsetting other p arts of an or-ganism’s genetic machinery. In the case of ourfoxes, a breeding program that alters a poly-

gene might upset the genetic balance in someanimals, causing them to show unusual newtraits, most of them harmful to the fox. Note

that in this argument, i t does not matter

whether the trait being selected for is tamenessor some other quantitative trait. Any breedingprogram that affects a polygene might havesimilar effects.

The problem with that explanation is that itdoes not explain why we see the particularmutations we do see. If disrupted polygenesare responsible, then the effects of a selectionexperiment ought to depend strongly onwhich mu tations already existed in the pop u-lation. If Belyaev had started with 130 foxesfrom, say, North America, then their descen-




Figure 5. Foxes in Belyaev’s experimental group were selected to breed depending

on how they reacted to their human keepers. Vicious foxes (top left) were excluded

from the experimental population. Foxes showing slight fear and no viciousness

toward humans were used in cross-breeding for the next generation (top right).

Their offspring (photograph, bott om) were calm and show ed no negative emotional

responses to people.



dants today would have ended u p with a com-pletely different set of novelties. Domesticat-ing a population of wolves, or pigs, or cattleought to produce novel traits more differentstill. Yet as Belyaev p ointed out, w hen we look at the changes in other domesticated animals,

the most striking things about them are nothow diverse they are, but how similar. Differ-ent animals, domesticated by different peopleat different times in different parts of theworld, appear to have passed through thesame morphological and physiological evolu-tionary pathways. How can that be?

According to Belyaev, the answer is not thatdomestication selects for a quantitative trait butthat it selects for a behavioral one. He considered

genetic transformations of behavior to be the keyfactor entraining other genetic events. Many of the polygenes determining behavior may be reg-ulatory, engaged in stabilizing an organ ism’s ear-

ly development, or ontogenesis. Ontogenesis is anextremely delicate process. In principle, evenslight shifts in the sequence of events could throwit into chaos. Thus the genes that orchestrate thoseevents and keep them on track have a powerfulrole to play. Which genes are they? Although nu-merous genes interact to stabilize an organism’sdevelopment, the lead role belongs to the genesthat control the functioning of the neural and en-docrine systems. Yet those same genes also gov-ern the systems that control an animal’s behavior,includ ing its friendliness or hostility toward hu-man beings. So, in principle, selecting animals for

behavioral traits can fundamentally alter the d e-

velopment of an organism.As our breeding program has progressed, we

have indeed observed changes in some of the an-imals’ neurochemical and neurohormonal mech-anisms. For example, we have measured a steadydrop in the hormone-producing activity of thefoxes’ adrenal glands. Among several other rolesin the body, the adrenal cortex comes into playwhen an an imal has to adap t to stress. It releaseshormones such as corticosteroids, which stimu-late 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 plasmaof our domesticated foxes had dropp ed to slight-ly more than half the level in a control group. Af-ter 28 to 30 generations of selection, the level hadhalved again. The adrenal cortex in our foxes also

responds less sharply when the foxes are subject-ed to emotional stress. Selection has even affectedthe neurochemistry of our foxes’ brains. Changeshave taken place in the serotonin system, thoughtto be the leading mediator inhibiting animals’ ag-gressive behavior. Compared with a controlgroup, the brains of our domesticated foxes con-tain h igher levels of serotonin; of its majormetabolite, 5-oxyindolacetic acid; and of trypto-phan hydroxylase, the key enzyme of serotoninsynthesis. Serotonin, like other neurotransmitters,is critically involved in shaping an animal’s de-

velopment from its earliest stages.

Selection and DevelopmentEvidently, then, selecting foxes for domestica-tion may have triggered p rofound changes inthe mechanisms that regulate their develop-ment. In particular, most of the novel traits andother changes in the foxes seem to result fromshifts in the rates of certain ontogeneticprocesses—in other words, from changes intiming. This fact is clear enough for some of the novelties mentioned above, such as the ear-lier eye opening and response to noises andthe delayed onset of the fear response to un-know n stimu li. But it also can explain some of the less obvious ones. Floppy ears, for exam-

ple, are characteristic of newborn fox pu ps bu tmay get carried over to ad ulthood.

Even novel coat colors may be attributable tochanges in the timing of embryonic develop-ment. One of the earliest novel traits we ob-served in our domesticated foxes was a loss of pigment in parts of the head and body. Belyaevdetermined that this piebald pattern is governedby a gene that he named Star . Later my col-league Lyud mila Prasolova and I discoveredthat the Star gene affects the migration rate of melanoblasts, the embryonic precursors of the pig-




Figure 6. Dogs begin forming social bonds with human beings as soon as they can see and hear; they stop

bonding once they start showing fear of the unknown. In foxes bred for tamability, the window of bonding

opens earlier and closes l ater than it does in ordinary farmed foxes.

response to sound fear of unknown eyes fully open window of socialization

4 6 8 10 1215 16 17 18 1911 12 13 14

days weeks

farmed foxes

domesticated foxes

dogs



ment cells (melanocytes) that give color to an ani-mal’s fur. Melanocytes form in the embryonicfox’s neural crest and later move to various partsof the embryo’s epidermis. Normally this migra-tion starts around days 28 to 31 of the embryo’sdevelopment. In foxes that carry even a singlecopy of the Star gene, however, melanoblasts passinto the potentially depigmented areas of the epi-dermis two days later, on average. That delay

may lead to the death of the tardy melanoblasts,thus altering the pigmentation in ways that giverise to the distinctive Star pattern.

One developmental trend to which we havedevoted p articular attention has to do with thegrowth of the skull. In 1990 and 1991, afternoticing abnormal developments in the skullsand jaws of some of our foxes, we decided to

stud y variations in the an imals’ cranial traits. Of course, changes in the shape of the skull areamong the most obvious ways in which dogsdiffer from wolves. As I mentioned earlier,Morey believes that they are a result of selec-tion (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, ourfoxes may be slightly longer, on average, than theones Belyaev started with 40 years ago. Never-theless, we found that their sku lls have beenchanging. In our domesticated foxes of both sex-es, cranial height and width tended to be smaller,and snouts tended to be shorter and wider, thanthose of a control group of farmed foxes.

Another interesting change is that the cra-

nial morphology of domesticated ad ult m alesbecame somewhat “feminized.” In farmed fox-es, the crania of males tended to be larger in

volume than those of females, and various oth-er proportions differed sharply between thesexes. In the d omesticated foxes the sexual di-morphism decreased. The differences in vol-um e remained, but in other respects the skullsof males became more like those of females.Analysis of cranial allometry showed that thechanges in skull proportions result either fromchanges in the timing of the first app earance of particular structures or from changes in theirgrowth rates. Because we studied the skullsonly of adu lt foxes, however, we cannot judgewhether any of these changes are pedomor-ph ic, as Morey believes they are in d ogs.

The most significant changes in developmen-tal timing in our foxes may be the smallest ones:those that have to d o with reproduction. In thewild, foxes reach sexual maturity when they areabout 8 months old. They are strict seasonalbreeders, mating once a year in response tochanges in the length of the day (in Siberia themating season runs from late January to lateMarch) and giving birth to litters ranging fromone to thirteen pup s, with an average of four orfive. Natural selection has hard-wired thesetraits into foxes with little or no genetic varia-

tion. Fur farmers have tried for decades to breedfoxes that would reproduce more often than an-

nually, but all their attempts have failed.In our experimental fox population, howev-

er, some reprod uctive traits have changed in acorrelated manner. The domesticated foxesreach sexual maturity about a month earlierthan n ondomesticated foxes do, and they givebirth to litters that are, on average, one puplarger. The mating season has lengthened.Some females breed out of season, in Novem-ber–December or April–May, and a few of them have mated twice a year. Only a verysmall number of our vixens have shown such




Figure 7. Changes in the foxes’ coat color were the

first novel traits noted, appearing in the eighth to

tenth selected generations. The expression of the

traits varied, following classical rules of genetics. In

a fox homozygous for the Star gene, large areas of

depigmentation similar to those in some dog breeds

are seen (top). In addition some foxes displayed the

brown mottling seen in some dogs, w hich appeared

as a semirecessive trait.



unusua l behavior, and in 40 years, no offspringof an extraseasonal mating has survived toadulthood. Nevertheless, the striking fact is

that, to our knowledge, out-of-season matinghas never been previously observed in foxes

experiencing a natu ral photoperiod.

Lessons Learned

Forty years into our unique lifelong experiment ,we believe that Dmitry Belyaev would bepleased with its progress. By intense selectivebreeding, we have compressed into a fewdecades an ancient process that originally un-folded over thousands of years. Before our eyes,“the Beast” has turned into “Beauty,” as the ag-gressive behavior of our herd’s wild progeni-tors entirely disappeared. We have watched

new morp hological traits emerge, a process pre-viously known only from archaeological evi-dence. Now we know that these changes can

burst into a p opulation early in dom estication,triggered by the stresses of captivity, and that

many of them result from changes in the timingof developmental processes. In some cases thechanges in timing, such as earlier sexual matu-rity or retarded growth of somatic characters,resemble pedom orphosis.

Some long-standing p uzz les remain. We be-lieved at the start that foxes could be made toreproduce twice a year and all year round , likedogs. We would like to understand why thishas turned out not to be quite so. We are alsocurious about how the vocal repertoire of foxeschanges under domestication. Some of the calls




12,400depigmentation (Star )

domesticatedpopulation

nondomesticatedpopulation

animals per 100,000 with trait

brown mottling

gray hairs

floppy ears

short tail

tail rolled in circle

710

450 86

500 100

230 170

140 2

9,400 830

(percent)

increase infrequency

+1,646

+423

+400

+35

+6,900

+1,033

characteristic

Figure 8. Foxes in the domesticated population show an unusually high incidence of certain other changes,

including (clockwise from top left) floppy ears, shortened legs and tails, tails curled upward like dogs’, and

underbites and overbites. The rates of some common aberrations are compared in the table. In addition to the

Star depigmentation pattern, the increased incidence of dog like tail characteristics w as most marked.



of our adult foxes resemble those of dogs and ,like those of dogs, app ear to be holdovers frompup pyhood, but only further stud y will revealthe details.

The biggest unanswered question is just howmuch further our selective-breeding experimentcan go. The domestic fox is not a d omestic dog,but w e believe that it has the genetic potential tobecome more and more d oglike. We can contin-

ue to increase that potential through furtherbreeding, but the foxes will realize it fully onlythrough close contact with human beings. Overthe years, other investigators and I have raisedseveral fox pups in domestic conditions, eitherin the laboratory or at home as pets. They haveshown themselves to be good-tempered crea-tures, as devoted as dogs but as independ ent as

cats, capable of forming deep-rooted pair bondswith hu man beings—mutu al bonds, as those of us who work with them know. If our experi-ment should continue, and if fox pups could beraised and trained the way dog puppies arenow, there is no telling wh at sort of animal they

might one d ay become.Whether that will happen remains to be seen.

For the first time in 40 years, the future of ourdomestication experiment is in doubt, jeopar-dized by the continuing crisis of the Russianeconomy. In 1996 the population of our breed-ing herd stood at 700. Last year, with no fundsto feed the foxes or to pay the salaries of ourstaff, we had to cut the number to 100. Earlierwe w ere able to cover most of our expenses byselling the pelts of the foxes culled from the

breeding herd. Now that source of revenue hasall but dried u p, leaving us increasingly depen-dent on outside funding at a time when shrink-

ing budgets and changes in the grant-award ingsystem in Russia are making long-term experi-ments such as ours harder and harder to sus-tain. Like many other enterpr ises in our country,we are becoming more entrepreneurial. Recent-ly we have sold some of our foxes to Scandina-vian fur breeders, who have been pressured byanimal-rights groups to develop animals thatdo n ot suffer stress in captivity. We also plan tomarket pups as house pets, a commercial ven-ture that should lead to some interesting, if in-formal, experiments in its own right. Many av-enues of both applied and basic research remainfor us to pursue, provided we save our unique

fox population.

Acknowledgments

This article is dedicated to the memory of Dmitry K.

Belyaev. The research was supported by grants

RBD000 and RBD300 from the International Sci-

entific Funds, grants 93-04-06936 and 96-04-49972

from the Russian Fund of Fundamental Research,

and grant 1757 of the Russian University Fund.

The author expresses her gratitude to Anna Fadeeva

for translation of the manuscript from Russian into

English. She is also grateful to Irina Plysnina for

help during preparation of the manuscript and to

Yekaterina Omelchenko for technical assistance.

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Figure 9. Forty years into the experiment, between 70 and 80 percent of the foxes

bred for tameness are members of the human-friendly “domesticated elite.” When

raised as pets, they are devoted, affectionate and capable of forming strong social

bonds with people (here, with technical assistant Marina Nurgalieva). The foxes

seek out human contact and lick experimenters’ hands and faces. The friendly

behavior is evident before the fox pups are a month old.

Links to Internet

resources for further

exploration of “Early

Canid Domestication:

The Farm-Fox

Experiment” are avail-

able on the American

Scientist Web site:

http:/ / www.amsci.org/

amsci/ articles/

articles99/ trut.html

trut-fox-study

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