The History of Farm Foxes Undermines the Animal Domestication Syndrome
Authors: Kathryn A. Lord, Greger Larson, Raymond P. Coppinger, Elinor K. Karlsson
Journal: Trends in Ecology & Evolution (2019)

The 'domestication syndrome' has been a central focus of research into the biological processes underlying domestication. The Russian Farm-Fox Experiment was the first to test whether there is a causal relationship between selection for tameness and the domestication syndrome.Historical records and genetic analysis show that the foxes used in the Farm-Fox Experiment originated from fur farms in eastern Canada and that most traits attributed to the behavioral selection for tameness predated the experiment, undermining a central pillar of support for the domestication syndrome.The overall weight of evidence, including data from other species, does not unambiguously support the existence of the domestication syndrome in animals. Competing theories to explain domestication syndrome should be reconsidered after the traits themselves are more clearly connected to the early stages of domestication. The Russian Farm-Fox Experiment is the best known experimental study in animal domestication. By subjecting a population of foxes to selection for tameness alone, Dimitry Belyaev generated foxes that possessed a suite of characteristics that mimicked those found across domesticated species. This 'domestication syndrome' has been a central focus of research into the biological pathways modified during domestication. Here, we chart the origins of Belyaev's foxes in eastern Canada and critically assess the appearance of domestication syndrome traits across animal domesticates. Our results suggest that both the conclusions of the Farm-Fox Experiment and the ubiquity of domestication syndrome have been overstated. To understand the process of domestication requires a more comprehensive approach focused on essential adaptations to human-modified environments. The Russian Farm-Fox Experiment is the best known experimental study in animal domestication. By subjecting a population of foxes to selection for tameness alone, Dimitry Belyaev generated foxes that possessed a suite of characteristics that mimicked those found across domesticated species. This 'domestication syndrome' has been a central focus of research into the biological pathways modified during domestication. Here, we chart the origins of Belyaev's foxes in eastern Canada and critically assess the appearance of domestication syndrome traits across animal domesticates. Our results suggest that both the conclusions of the Farm-Fox Experiment and the ubiquity of domestication syndrome have been overstated. To understand the process of domestication requires a more comprehensive approach focused on essential adaptations to human-modified environments. The domestication syndrome describes a suite of behavioral and morphological characteristics consistently observed in domesticated populations. 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The concept of a domestication syndrome is appealing. The grouping of a collection of traits allows easier identification and facilitates the definition of domesticated taxa. It also inspires a search for causal mechanisms, whether genetic or environmental, responsible for their collective appearance. Characteristics attributed to domestication syndrome vary, but include tamability (see Glossary), loss of reproductive seasonality, and changes in coat color, ear form, tail form, and craniofacial morphology (Figure 1) [1Darwin C. The Variation of Animals and Plants Under Domestication. John Murray, 1868Google Scholar,5Zeuner F.E. A History of Domesticated Animals. Harper & Row, 1963Google Scholar, 6Clutton-Brock J. Domesticated Animals from Early Times. University of Texas Press, 1981Google Scholar, 7Hemmer H. Domestication: The Decline of Environmental Appreciation. Cambridge University Press, 1990Google Scholar, 8Crabtree P.J. 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Insights. 2015; 9: 11-20Crossref PubMed Scopus (39) Google Scholar]. The Russian Farm-Fox Experiment is widely cited as a demonstration that the domestication syndrome exists and that domestication results from selection on tameness, with clear changes in behavior and morphology appearing rapidly. Its founder, Dr Dimitry Belyaev, designed the project to test whether the suite of characteristics that Darwin associated with domestication were linked to selection on tameness [14Belyaev D.K. Destabilizing selection as a factor in domestication.J. Hered. 1979; 70: 301-308Crossref PubMed Scopus (391) Google Scholar,15Trut L. 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.Am. Sci. 1999; 87: 160-169Crossref Scopus (490) Google Scholar]. Starting with 30 male and 100 female silver foxes (Vulpes vulpes) from Soviet fur farms, he selectively bred foxes who responded less fearfully when a hand was inserted into their cage [15Trut L. 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.Am. Sci. 1999; 87: 160-169Crossref Scopus (490) Google Scholar]. The oft-repeated narrative is that with just ten generations of selection on wild foxes, he produced foxes who craved human attention and exhibited a range of unconnected phenotypes including floppy ears, turned-up tails, piebald coats, di-estrous reproductive cycles, and later, shorter and wider faces. Belyaev proposed that selection on behavior altered the regulation of multiple interconnected systems that produced the traits Darwin described [1Darwin C. The Variation of Animals and Plants Under Domestication. John Murray, 1868Google Scholar,14Belyaev D.K. Destabilizing selection as a factor in domestication.J. Hered. 1979; 70: 301-308Crossref PubMed Scopus (391) Google Scholar,15Trut L. 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.Am. Sci. 1999; 87: 160-169Crossref Scopus (490) Google Scholar]. Belyaev's observations, which seemed to prove a causal relationship between selection on tameness and other syndrome traits, led to the acceptance of the domestication syndrome across diverse fields [16Wilkins A.S. Revisiting two hypotheses on the "domestication syndrome" in light of genomic data.Vestn. VOGiS. 2017; 21: 435-442Crossref Scopus (25) Google Scholar, 17Zeder M.A. The domestication of animals.J. Anthropol. 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A Natural History of Domesticated Mammals. Cambridge University Press, 1999Google Scholar]. Scientists investigating the biology of domestication developed hypotheses to explain the suite of traits and many invoked either linkage or pleiotropy. The neural crest hypothesis proposes that domestication is driven by pleiotropic changes to neural crest cells – developmental precursors for nearly all domestication syndrome traits [12Wilkins A.S. et al.The "domestication syndrome" in mammals: a unified explanation based on neural crest cell behavior and genetics.Genetics. 2014; 197: 795-808Crossref PubMed Scopus (313) Google Scholar]. The pedomorphosis hypothesis (sometimes termed neoteny) proposes that domestication alters developmental timing, such that adults retain a suite of juvenile characteristics [23Coppinger R. et al.Degree of behavioral neoteny differentiates canid polymorphs.Ethology. 1987; 75: 89-108Crossref Scopus (59) Google Scholar]. The thyroid rhythm hypothesis proposes that domestication is driven by changes in thyroid hormone release, which alters growth, maturation, and environmental response [24Crockford S.J. Rhythms of Life: Thyroid Hormone & the Origin of Species. Trafford, 2006Google Scholar]. These hypotheses assume that the domestication syndrome exists, but with little supporting data. The defining characteristics vary widely (Figure 1) and have not been observed in most domesticated species [25Sánchez-Villagra M.R. et al.The taming of the neural crest: a developmental perspective on the origins of morphological covariation in domesticated mammals.R. Soc. Open Sci. 2016; 3: 160107Crossref PubMed Scopus (107) Google Scholar]. Many studies fail to distinguish traits that accompanied domestication from those only in modern breeds (Box 1), and some traits are reported anecdotally without any accompanying frequencies or measurements.Box 1Population TypesWe distinguished between three types of populations in evaluating the evidence for domestication syndrome.i.Wild: A wild population is a population that is noncommensal with humans.ii.Domesticated (non-breed): A domesticated population is one that is commensal with humans or otherwise generally reliant on a human-modified environment for survival. A non-breed domesticated population is any population of domesticated individuals that is not part of a breed.iii.Breed: A genetically isolated subpopulation of the domesticated population, usually less than 50–100 generations old, with markedly reduced genetic diversity due to human action. Breeds may be subject to intentional selection for phenotypic extremes. This includes: pedigreed populations selected to a particular standard (e.g., dog breeds); laboratory colonies (e.g., laboratory rats), and populations resulting from human transplantation (e.g., rabbits in Australia). We distinguished between three types of populations in evaluating the evidence for domestication syndrome.i.Wild: A wild population is a population that is noncommensal with humans.ii.Domesticated (non-breed): A domesticated population is one that is commensal with humans or otherwise generally reliant on a human-modified environment for survival. A non-breed domesticated population is any population of domesticated individuals that is not part of a breed.iii.Breed: A genetically isolated subpopulation of the domesticated population, usually less than 50–100 generations old, with markedly reduced genetic diversity due to human action. Breeds may be subject to intentional selection for phenotypic extremes. This includes: pedigreed populations selected to a particular standard (e.g., dog breeds); laboratory colonies (e.g., laboratory rats), and populations resulting from human transplantation (e.g., rabbits in Australia). In the context of this general paucity of empirical data, it is difficult to overstate the importance of the Farm-Fox Experiment for our understanding of animal domestication [16Wilkins A.S. Revisiting two hypotheses on the "domestication syndrome" in light of genomic data.Vestn. VOGiS. 2017; 21: 435-442Crossref Scopus (25) Google Scholar]. It alone claims a causal relationship between selection for tameness and phenotypic changes consistent with the domestication syndrome. Here, we investigate the historical background of the Farm-Fox Experiment and critically evaluate its use as a foundation for the existence of the domestication syndrome. A widespread misconception maintains that the Farm-Fox Experiment started with wild foxes and recapitulated the entire process of domestication [16Wilkins A.S. Revisiting two hypotheses on the "domestication syndrome" in light of genomic data.Vestn. VOGiS. 2017; 21: 435-442Crossref Scopus (25) Google Scholar,20Dobney K. Larson G. Genetics and animal domestication: new windows on an elusive process.J. Zool. 2006; 269: 261-271Google Scholar]. Belyaev himself accurately described the founders as fur-farm foxes, but by referring to the unselected population as 'wild controls', contributed to this misconception [14Belyaev D.K. Destabilizing selection as a factor in domestication.J. Hered. 1979; 70: 301-308Crossref PubMed Scopus (391) Google Scholar]. In reality, the experiment started with a fox population from eastern Canada that had been captive and purpose-bred since the late 1800s, something Belyaev and his colleagues may have been initially unaware of [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar,27Belyaev D.K. Trut L.N. Behavior and reproductive functions of animals. 1. Correlations of behavior type with the time of reproduction and fertility.Byul. Mosk. Obshchestva Ispyt. Prirody Otd. Biol. 1964; 69: 5-19Google Scholar] (Box 2).Box 2The 'Domesticated' Foxes of Prince Edward IslandThe Canadian farm-fox population dates to the mid-19th century, when the fur industry was confronting a supply crisis. Fur traders were anxious to overcome their reliance on wild-caught animals, but repeated attempts to breed foxes in captivity had failed [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar,81Butler L. Distribution and genetics of the color phases of the red fox in Canada.Genetics. 1945; 30: 39-50PubMed Google Scholar]. Wild foxes are generally monogamous, monestrous, seasonal breeders and notorious escape artists [58Asa C.S. Valdespino C. A review of small canid reproduction.in: Sovada M. Carbyn L. The Swift Fox: Ecology and Conservation of Swift Foxes in a Changing World. Canadian Plains Research Center, 2003: 117-123Google Scholar,82Balcom A.B. Fox farming in Prince Edward Island: a chapter in the history of speculation.Q. J. Econ. 1916; 30: 665-681Crossref Scopus (10) Google Scholar]. Whether wild or captive born, most foxes would not breed in captivity, and females often ate their young [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar].The first Canadian fox farm was established in 1887 by Charles Dalton, after he was convinced by Robert Oulton to make the foxes' environment more natural [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. Their farm, in the province of PEI in eastern Canada, had large enclosures furnished with hollow logs as dens. By 1883, they had their first breeding pair, and 4 years later they started the first fox farm with two breeding pairs [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar,82Balcom A.B. Fox farming in Prince Edward Island: a chapter in the history of speculation.Q. J. Econ. 1916; 30: 665-681Crossref Scopus (10) Google Scholar]. They monopolized the market for the next three decades.From the start, the foxes were selected for both appearance and behavior. Dalton bred jet-black foxes, while Oulton favored white barring on guard hairs [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. While we found no reports of intentional selection for affiliative behavior, contemporary experts linked docility to improved fecundity [83Dearborn N. The Domesticated Silver Fox. US Department of Agriculture, 1917Crossref Google Scholar] and the PEI farm foxes were unusually friendly (Figure 3). By 1913, breeding pairs sold for CA$30 000, equivalent to US$500 000 today (https://www.bankofcanada.ca/rates/related/inflation-calculator/) [82Balcom A.B. Fox farming in Prince Edward Island: a chapter in the history of speculation.Q. J. Econ. 1916; 30: 665-681Crossref Scopus (10) Google Scholar].In 1928, Leo Frank, a promoter of the fur industry, supplied 65 fox pairs from Rosebank farm to establish a Russian fur-farm industry (Figure I) [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. Thus, the Russian Farm-Fox Experiment started with foxes descended from a population of unusually friendly Canadian foxes – a phenomenon Belyaev accentuated by preferentially including exceptionally calm foxes [62Dugatkin L.A. Trut L. How to Tame a Fox (and Build a Dog): Visionary Scientists and a Siberian Tale of Jump-Started Evolution. University of Chicago Press, 2017Crossref Google Scholar,84Rayner B.I. Jones J.W. Domestication of the Fox.J. Hered. 1912; 3: 37-45Crossref Scopus (2) Google Scholar,85Statham M.J. et al.On the origin of a domesticated species: identifying the parent population of Russian silver foxes (Vulpes vulpes).Biol. J. Linn. Soc. Lond. 2011; 103: 168-175Crossref PubMed Scopus (54) Google Scholar]. Mitochondrial DNA analyses of 24 Farm-Fox Experiment foxes showed 100% of haplotypes derived from Canadian foxes, predominantly from the east [85Statham M.J. et al.On the origin of a domesticated species: identifying the parent population of Russian silver foxes (Vulpes vulpes).Biol. J. Linn. Soc. Lond. 2011; 103: 168-175Crossref PubMed Scopus (54) Google Scholar].This history reframes the behavioral selection in the Farm-Fox Experiment as selection on standing genetic variation and explains the rapid behavioral change (within ten generations). A study in dogs saw change within just three generations after starting with founders exhibiting the trait of interest (nervousness) [75Murphree O.D. et al.Genetically-determined abnormal behavior in dogs: results of behavioral tests.Cond. Reflex. 1967; 2: 199Google Scholar]. When Belyaev started a rat experiment with commensal rats living close to humans (P. Borodin, personal communication), significant behavioral changes occurred within 13 generations [86Naumenko E.V. et al.Behavior, adrenocortical activity, and brain monoamines in Norway rats selected for reduced aggressiveness towards man.Pharmacol. Biochem. Behav. 1989; 33: 85-91Crossref PubMed Scopus (111) Google Scholar]. When he started with a wild population of river otters (Lutra lutra) unaccustomed to people, few bred successfully in captivity and the experiment was discontinued [87Nicholls H. Taming the beast.New Scientist. 2009; : 40-43Crossref Google Scholar,88Ratliff E. Musi V.J. Taming the Wild. National Geographic, 2011Google Scholar].This history also makes it difficult to validate domestication syndrome. The Farm-Fox Experiment population experienced at least three major founder events at the founding of PEI fox farms, the importation to Russia, and the inclusion in Belyaev's experiment. Like dog breeds, both the selected and unselected fox populations have small effective population sizes, making them susceptible to genetic drift [29Kimura M. Ohta T. The average number of generations until fixation of a mutant gene in a finite population.Genetics. 1969; 61: 763-771Crossref PubMed Google Scholar,89Wright S. Evolution in Mendelian populations.Genetics. 1931; 16: 97-159Crossref PubMed Google Scholar]. Thus, even large allele-frequency differences between the two populations can be explained by chance alone. The Canadian farm-fox population dates to the mid-19th century, when the fur industry was confronting a supply crisis. Fur traders were anxious to overcome their reliance on wild-caught animals, but repeated attempts to breed foxes in captivity had failed [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar,81Butler L. Distribution and genetics of the color phases of the red fox in Canada.Genetics. 1945; 30: 39-50PubMed Google Scholar]. Wild foxes are generally monogamous, monestrous, seasonal breeders and notorious escape artists [58Asa C.S. Valdespino C. A review of small canid reproduction.in: Sovada M. Carbyn L. The Swift Fox: Ecology and Conservation of Swift Foxes in a Changing World. Canadian Plains Research Center, 2003: 117-123Google Scholar,82Balcom A.B. Fox farming in Prince Edward Island: a chapter in the history of speculation.Q. J. Econ. 1916; 30: 665-681Crossref Scopus (10) Google Scholar]. Whether wild or captive born, most foxes would not breed in captivity, and females often ate their young [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. The first Canadian fox farm was established in 1887 by Charles Dalton, after he was convinced by Robert Oulton to make the foxes' environment more natural [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. Their farm, in the province of PEI in eastern Canada, had large enclosures furnished with hollow logs as dens. By 1883, they had their first breeding pair, and 4 years later they started the first fox farm with two breeding pairs [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar,82Balcom A.B. Fox farming in Prince Edward Island: a chapter in the history of speculation.Q. J. Econ. 1916; 30: 665-681Crossref Scopus (10) Google Scholar]. They monopolized the market for the next three decades. From the start, the foxes were selected for both appearance and behavior. Dalton bred jet-black foxes, while Oulton favored white barring on guard hairs [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. While we found no reports of intentional selection for affiliative behavior, contemporary experts linked docility to improved fecundity [83Dearborn N. The Domesticated Silver Fox. US Department of Agriculture, 1917Crossref Google Scholar] and the PEI farm foxes were unusually friendly (Figure 3). By 1913, breeding pairs sold for CA$30 000, equivalent to US$500 000 today (https://www.bankofcanada.ca/rates/related/inflation-calculator/) [82Balcom A.B. Fox farming in Prince Edward Island: a chapter in the history of speculation.Q. J. Econ. 1916; 30: 665-681Crossref Scopus (10) Google Scholar]. In 1928, Leo Frank, a promoter of the fur industry, supplied 65 fox pairs from Rosebank farm to establish a Russian fur-farm industry (Figure I) [26Forester J.E. Forester A.D. Silver Fox Odyssey: History of the Canadian Silver Fox Industry. Canadian Silver Fox Breeders Association, 1973Google Scholar]. Thus, the Russian Farm-Fox Experiment started with foxes descended from a population of unusually friendly Canadian foxes – a phenomenon Belyaev accentuated by preferentially including exceptionally calm foxes [62Dugatkin L.A. Trut L. How to Tame a Fox (and Build a Dog): Visionary Scientists and a Siberian Tale of Jump-Started Evolution. University of Chicago Press, 2017Crossref Google Scholar,84Rayner B.I. Jones J.W. Domestication of the Fox.J. Hered. 1912; 3: 37-45Crossref Scopus (2) Google Scholar,85Statham M.J. et al.On the origin of a domesticated species: identifying the parent population of Russian silver foxes (Vulpes vulpes).Biol. J. Linn. Soc. Lond. 2011; 103: 168-175Crossref PubMed Scopus (54) Google Scholar]. Mitochondrial DNA analyses of 24 Farm-Fox Experiment foxes showed 100% of haplotypes derived from Canadian foxes, predominantly from the east [85Statham M.J. et al.On the origin of a domesticated species: identifying the parent population of Russian silver foxes (Vulpes vulpes).Biol. J. Linn. Soc. Lond. 2011; 103: 168-175Crossref PubMed Scopus (54) Google Scholar]. This history reframes the behavioral selection in the Farm-Fox Experiment as selection on standing genetic variation and explains the rapid behavioral change (within ten generations). A study in dogs saw change within just three generations after starting with founders exhibiting the trait of interest (nervousness) [75Murphree O.D. et al.Genetically-determined abnormal behavior in dogs: results of behavioral tests.Cond. Reflex. 1967; 2: 199Google Scholar]. When Belyaev started a rat experiment with commensal rats living close to humans (P. Borodin, personal communication), significant behavioral changes occurred within 13 generations [86Naumenko E.V. et al.Behavior, adrenocortical activity, and brain monoamines in Norway rats selected for reduced aggressiveness towards man.Pharmacol. Biochem. Behav. 1989; 33: 85-91Crossref PubMed Scopus (111) Google Scholar]. When he started with a wild population of river otters (Lutra lutra) unaccustomed to people, few bred successfully in captivity and the experiment was discontinued [87Nicholls H. Taming the beast.New Scientist. 2009; : 40-43Crossref Google Scholar,88Ratliff E. Musi V.J. Taming the Wild. National Geographic, 2011Google Scholar]. This history also makes it difficult to validate domestication syndrome. The Farm-Fox Experiment population experienced at least three major founder events at the founding of PEI fox farms, the importation to Russia, and the inclusion in Belyaev's experiment. Like dog breeds, both the selected and unselected fox populations have small effective population sizes, making them susceptible to genetic drift [29Kimura M. Ohta T. The average number of generations until fixation of a mutant gene in a finite population.Genetics. 1969; 61: 763-771Crossref PubMed Google Scholar,89Wright S. Evolution in Mendelian populations.Genetics. 1931; 16: 97-159Crossref PubMed Google Scholar]. Thus, even large allele-frequency differences between the two populations can be explained by chance alone. The history of the Farm-Fox population undermines the commonly repeated narrative that a suite of domestication syndrome traits emerged solely as a result of selecting on tameness [15Trut L. 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.Am. Sci. 1999; 87: 160-169Crossref Scopus (490) Google Scholar,28Trut L. et al.Animal evolution during domestication: the domesticated fox as a model.Bioessays. 2009; 31: 349-360Crossref PubMed Scopus (350) Google Scholar]. There is no temporal link between most of the syndrome traits, which first appeared in Prince Edward Island (PEI) fur farms, and the later behavioral selection in Russia. The rate of behavioral change is consistent with selection on standing variation in the population (Box 2). Finally, the small effective population size makes the experimental fox populations highly susceptible to large shifts in allele frequencies due to chance alone [29Kimura M. Ohta T. The average number of generations until fixation of a mutant gene in a finite population.Genetics. 1969; 61: 763-771Crossref PubMed Google Scholar,30Johnson J.L. et al.Genotyping-by-sequencing (GBS) detects genetic structure and confirms behavioral QTL in tame and aggressive foxes (Vulpes vulpes).PLoS One. 2015; 10: e0127013Crossref PubMed Scopus (28) Google Scholar]. Today, the beha