Animal evolution during domestication: the domesticated fox as a model

Trut, Lyudmila; Oskina, Irina; Kharlamova, Anastasiya

doi:10.1002/bies.200800070

Cited by 637Human-Animal Interaction StudiesGenetic and phenotypic traits in livestockAnimal Behavior and Reproduction

Animal evolution during domestication: the domesticated fox as a model

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Trut, Lyudmila, Oskina, Irina, Kharlamova, Anastasiya·2009·BioEssays

DOI 10.1002/bies.200800070PMC PMC2763232

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Abstract

We review the evolution of domestic animals, emphasizing the effect of the earliest steps of domestication on its course. Using the first domesticated species, the dog ( Canis familiaris ), for illustration, we describe the evolutionary peculiarities during the historical domestication, such as the high level and wide range of diversity. We suggest that the process of earliest domestication via unconscious and later conscious selection of human‐defined behavioral traits may accelerate phenotypic variations. The review is based on the results of a long‐term experiment designed to reproduce early mammalian domestication in the silver fox ( Vulpes vulpes ) selected for tameability or amenability to domestication. We describe changes in behavior, morphology and physiology that appeared in the fox during its selection for tameability, which were similar to those observed in the domestic dog. Based on the data of the fox experiment and survey of relevant data, we discuss the developmental, genetic and possible molecular genetic mechanisms underlying these changes. We ascribe the causative role in evolutionary transformation of domestic animals to the selection for behavior and to the neurospecific regulatory genes it affects.

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Belyaev's fox experiment showed that wild foxes selected for tameness started exhibiting traits typical for domesticated dogs, approaching humans eagerly, wagging tails, and playing with experimenters.
“Wild foxes, which are aggressive toward humans, started exhibiting traits typical for domesticated dogs.They approached humans eagerly, wagged their tails and played with the experimenters.37”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [37]
Feminization is associated with reduced reactivity of the hypothalamus-pituitary-adrenal axis, a physiological trait thought to be critical for domestication.
“The process of ‘feminization’ (reduction of androgen levels and rise in estrogen levels [21]) is often associated with reduced reactivity of the hypothalamus-pituitary-adrenal axis [26], a physiological trait thought to be critical for domestication [17, 27].”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [26]
Hypofunction of the HPA axis has been proposed as a key mechanism in the development of tame behaviors in domesticates.
“the hypofunction of which has been proposed as a key mechanism in the development of tame behaviors in domesticates (Trut et al., 2009;Wilkins et al., 2014).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Trut et al., 2009

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The history of farm foxes undermines the animal domestication syndrome
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Structural variants in genes associated with human Williams-Beuren syndrome underlie stereotypical hypersociability in domestic dogs
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The evolution of associative learning: A factor in the Cambrian explosion
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Self-domestication in Homo sapiens: Insights from comparative genomics
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Taming the Past: Ancient DNA and the Study of Animal Domestication
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Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic
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Pet Face: Mechanisms Underlying Human-Animal Relationships
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Evaluating the roles of directed breeding and gene flow in animal domestication
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A comparison of brain gene expression levels in domesticated and wild animals
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A decade of pig genome sequencing: a window on pig domestication and evolution
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Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours
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Self-citation
The genomics of microbial domestication in the fermented food environment
Gibbons, J. G., & Rinker, D. C. (2015) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.07.003 · Cited by 142 · see citing works
Ecological validity of social interaction tests in rats and mice
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Getting Back to Nature: Feralization in Animals and Plants
Gering, E., Incorvaia, D. C., Henriksen, R., Conner, J. K., Getty, T., & Wright, D. (2019) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2019.07.018 · Cited by 127 · see citing works
Does Domestication Cause Changes in Growth Reaction Norms? A Study of Farmed, Wild and Hybrid Atlantic Salmon Families Exposed to Environmental Stress
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Evaluating the self‐domestication hypothesis of human evolution
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How did the domestication of Fertile Crescent grain crops increase their yields?
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Dog Breeds and Their Behavior
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Human Social Evolution: Self-Domestication or Self-Control?
Shilton, D., Breski, M., Dor, D., & Jablonka, E. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.00134 · Cited by 116 · see citing works
The significance and scope of evolutionary developmental biology: a vision for the 21st century
Moczek, A. P., Sears, K. E., Stollewerk, A., Wittkopp, P. J., Diggle, P. K., Dworkin, I. M., Ledón‐Rettig, C. C., Matus, D. Q., Roth, S., Abouheif, E., et al. (2015) · Evolution & Development · doi:10.1111/ede.12125 · Cited by 114 · see citing works
Self domestication and the evolution of language
Thomas, J., & Kirby, S. (2018) · Biology & Philosophy · doi:10.1007/s10539-018-9612-8 · Cited by 108 · see citing works
Demographically-based evaluation of genomic regions under selection in domestic dogs
Freedman, A. H., Schweizer, R. M., Ortega-Del Vecchyo, D., Han, E., Davis, B. W., Gronau, I., Silva, P. M., Galaverni, M., Fan, Z., Marx, P., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005851 · Cited by 104 · see citing works
From the individual to the population – and back again? Emphasising the role of the individual in animal welfare science
Richter, S. H., & Hintze, S. (2018) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2018.12.012 · Cited by 101 · see citing works
Warring brothers: The complex interactions between wolves (Canis lupus) and dogs (Canis familiaris) in a conservation context
Lescureux, N., & Linnell, J. D. C. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.01.032 · Cited by 104 · see citing works
The function and evolution of the Aspergillus genome
Gibbons, J. G., & Rokas, A. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.09.005 · Cited by 103 · see citing works
Genomic responses to selection for tame/aggressive behaviors in the silver fox ( <i>Vulpes vulpes</i> )
Wang, X., Pipes, L., Trut, L. N., Herbeck, Y., Vladimirova, A. V., Gulevich, R. G., Kharlamova, A. V., Johnson, J. L., Acland, G. M., Kukekova, A. V., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800889115 · Cited by 100 · see citing works
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The Domestication Makeup: Evolution, Survival, and Challenges
Ahmad, H. I., Ahmad, M. J., Jabbir, F., Ahmar, S., Ahmad, N., Elokil, A. A., & Chen, J. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2020.00103 · Cited by 98 · see citing works
Behavior Genetics and the Domestication of Animals
Jensen, P. (2014) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-022513-114135 · Cited by 96 · see citing works
Adult Hippocampal Neurogenesis in Natural Populations of MammalsPreprint
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Integrating social ecology in explanations of wolf–dog behavioral differences
Marshall-Pescini, S., Cafazzo, S., Virányi, Z., & Range, F. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.05.002 · Cited by 95 · see citing works
A longitudinal study of phenotypic changes in early domestication of house mice
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Association of HPA axis-related genetic variation with stress reactivity and aggressive behaviour in pigs
Muráni, E., Ponsuksili, S., D’Eath, R. B., Turner, S. P., Kurt, E., Evans, G., Thölking, L., Klont, R. E., Foury, A., Mormède, P., et al. (2010) · BMC Genetics · doi:10.1186/1471-2156-11-74 · Cited by 95 · see citing works
Domestication effects on behavioural and hormonal responses to acute stress in chickens
Ericsson, M., Fallahsharoudi, A., Bergquist, J., Kushnir, M. M., & Jensen, P. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.05.024 · Cited by 93 · see citing works
Comparing wolves and dogs: current status and implications for human ‘self-domestication’
Range, F., & Marshall-Pescini, S. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.01.003 · Cited by 85 · see citing works
“Selection against fear and aggression Belyaev proposed that traits observed in domestic species are the result of selection against fear and aggression, potentially mediated by a dampened reactivity of the hypothalamo–pituitary– adrenal system (HPA axis) manifested in low glucocorticoid levels (Box 2) [6,7].”
Background
Seven considerations about dingoes as biodiversity engineers: the socioecological niches of dogs in Australia
Fleming, P. J. S., Allen, B. L., & Ballard, G. (2012) · Australian Mammalogy · doi:10.1071/am11012 · Cited by 88 · see citing works
Correlated evolution of personality, morphology and performance
Kern, E., Robinson, D., Gass, E., Godwin, J., & Langerhans, R. B. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.04.007 · Cited by 88 · see citing works
Mapping Loci for Fox Domestication: Deconstruction/Reconstruction of a Behavioral Phenotype
Kukekova, A. V., Trut, L. N., Chase, K., Kharlamova, A. V., Johnson, J. L., Temnykh, S. V., Oskina, I. N., Gulevich, R. G., Vladimirova, A. V., Klebanov, S., et al. (2010) · Behavior Genetics · doi:10.1007/s10519-010-9418-1 · Cited by 87 · see citing works
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Epimutations in Developmental Genes Underlie the Onset of Domestication in Farmed European Sea Bass
Anastasiadi, D., & Piferrer, F. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz153 · Cited by 87 · see citing works
A neurochemical hypothesis for the origin of hominids
Raghanti, M. A., Edler, M. K., Stephenson, A. R., Munger, E. L., Jacobs, B., Hof, P. R., Sherwood, C. C., Holloway, R. L., & Lovejoy, C. O. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719666115 · Cited by 84 · see citing works
How domestication alters fish phenotypes
Milla, S., Pasquet, A., Mohajer, L. E., & Fontaine, P. (2020) · Reviews in Aquaculture · doi:10.1111/raq.12480 · Cited by 84 · see citing works
The role of humans in facilitating and sustaining coat colour variation in domestic animals
Linderholm, A. E., & Larson, G. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.03.015 · Cited by 83 · see citing works
Testing the myth: tolerant dogs and aggressive wolves
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Associations between glucocorticoids and sociality across a continuum of vertebrate social behavior
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Artificial Selection on Brain-Expressed Genes during the Domestication of Dog
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Reconsidering the evolution of brain, cognition, and behavior in birds and mammals
Willemet, R. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00396 · Cited by 77 · see citing works
Chicken domestication changes expression of stress-related genes in brain, pituitary and adrenals
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On the origin of a domesticated species: identifying the parent population of Russian silver foxes (Vulpes vulpes): THE ORIGIN OF RUSSIAN SILVER FOXES
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Evolutionary dynamics in the Anthropocene: Life history and intensity of human contact shape antipredator responses
Geffroy, B., Sadoul, B. C., Putman, B. J., Berger‐Tal, O., Garamszegi, L. Z., Møller, A. P., & Blumstein, D. T. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000818 · Cited by 71 · see citing works
The silver fox domestication experiment
Dugatkin, L. A. (2018) · Evolution Education and Outreach · doi:10.1186/s12052-018-0090-x · Cited by 69 · see citing works
Is Behavioral Variation along the Bold-Shy Continuum Associated with Variation in the Stress Axis in Zebrafish?
Oswald, M. E., Drew, R. E., Racine, M., Murdoch, G. K., & Robison, B. D. (2012) · Physiological and Biochemical Zoology · doi:10.1086/668203 · Cited by 69 · see citing works
Neomorphosis and heterochrony of skull shape in dog domestication
Geiger, M., Evin, A., Sánchez-Villagra, M. R., Gascho, D., Mainini, C., & Zollikofer, C. P. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-12582-2 · Cited by 69 · see citing works
Neurobiological underpinnings of dogs’ human-like social competence: How interactions between stress response systems and oxytocin mediate dogs’ social skills
Buttner, A. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.029 · Cited by 67 · see citing works
Embryonic development of goldfish (Carassius auratus): A model for the study of evolutionary change in developmental mechanisms by artificial selection
Tsai, H., Chang, M., Liu, S., Abe, G., & Ota, K. G. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24022 · Cited by 66 · see citing works
Domestication Effects on Stress Induced Steroid Secretion and Adrenal Gene Expression in Chickens
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A domestication related mutation in the thyroid stimulating hormone receptor gene (TSHR) modulates photoperiodic response and reproduction in chickens
Karlsson, A., Fallahshahroudi, A., Johnsen, H., Hagenblad, J., Wright, D., Andersson, L., & Jensen, P. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.02.010 · Cited by 65 · see citing works
Omics Application in Animal Science—A Special Emphasis on Stress Response and Damaging Behaviour in Pigs
Kasper, C., Ribeiro, D. M., de Almeida, A. M., Larzul, C., Liaubet, L., & Muráni, E. (2020) · Genes · doi:10.3390/genes11080920 · Cited by 63 · see citing works
Change in flight initiation distance between urban and rural habitats following a cold winter
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Is domestication driven by reduced fear of humans? Boldness, metabolism and serotonin levels in divergently selected red junglefowl ( Gallus gallus )
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Behavioural correlations of the domestication syndrome are decoupled in modern dog breeds
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The fitness benefit of association with humans: elevated success of birds breeding indoors
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Tail postures and tail motion in pigs: A review
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From Physical Aggression to Verbal Behavior: Language Evolution and Self-Domestication Feedback Loop
Progovac, L., & Benítez‐Burraco, A. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02807 · Cited by 58 · see citing works
The Social Dog
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Volumes of brain structures in captive wild-type and laboratory rats: 7T magnetic resonance in vivo automatic atlas-based study
Welniak–Kaminska, M., Fiedorowicz, M., Orzel, J., Bogorodzki, P., Modlinska, K., Stryjek, R., Chrzanowska, A., Pisula, W., & Grieb, P. (2019) · PLOS ONE · doi:10.1371/journal.pone.0215348 · Cited by 61 · see citing works
Multiple Origins of Agriculture in Eurasia and Africa
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Physiological differences between wild and captive animals: a century-old dilemma.
Turko, A., Firth, B. L., Craig, P. M., Eliason, E., Raby, G., & Borowiec, B. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.246037 · Cited by 53 · see citing works
Maladaptation in feral and domesticated animals
Gering, E., Incorvaia, D. C., Henriksen, R., Wright, D., & Getty, T. (2019) · Evolutionary Applications · doi:10.1111/eva.12784 · Cited by 59 · see citing works
Is evolution of domestication driven by tameness? A selective review with focus on chickens
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Skull morphology diverges between urban and rural populations of red foxes mirroring patterns of domestication and macroevolution
Parsons, K. J., Rigg, A., Conith, A. J., Kitchener, A. C., Harris, S., & Zhu, H. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.0763 · Cited by 62 · see citing works
Applications in the search for genomic selection signatures in fish
LÃ³pez, M. E., Neira, R., & YÃ¡Ã±ez, J. M. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2014.00458 · Cited by 58 · see citing works
Goldfish morphology as a model for evolutionary developmental biology
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Deciphering the Wisent Demographic and Adaptive Histories from Individual Whole-Genome Sequences
Gautier, M., Moazami‐Goudarzi, K., Levéziel, H. H., Parrinello, H., Grohs, C., Rialle, S., Kowalczyk, R., & Flori, L. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw144 · Cited by 59 · see citing works
Sequence comparison of prefrontal cortical brain transcriptome from a tame and an aggressive silver fox (Vulpes vulpes)
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Maladaptation and phenotypic mismatch in hatchery‐reared Atlantic salmon Salmo salar released in the wild
Stringwell, R., Lock, A., Stutchbury, C. J., Baggett, E., Taylor, J. F., Gough, P., & de Leániz, C. G. (2014) · Journal of Fish Biology · doi:10.1111/jfb.12543 · Cited by 57 · see citing works
Relations between temperament and theory of mind development in the United States and China: Biological and behavioral correlates of preschoolers' false-belief understanding.
Lane, J. D., Wellman, H. M., Olson, S. L., Miller, A. L., Wang, L., & Tardif, T. Z. (2012) · Developmental Psychology · doi:10.1037/a0028825 · Cited by 56 · see citing works
Dog Breed Differences in Visual Communication with Humans
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Stress-responsiveness influences baseline glucocorticoid levels: Revisiting the under 3 min sampling rule
Small, T. W., Bebus, S. E., Bridge, E. S., Elderbrock, E. K., Ferguson, S. M., Jones, B. C., & Schoech, S. J. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.01.028 · Cited by 56 · see citing works
Neuroendocrinology of reproduction: Is gonadotropin-releasing hormone (GnRH) dispensable?
Whitlock, K. E., Postlethwait, J. H., & Ewer, J. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.002 · Cited by 56 · see citing works
A striking example of developmental bias in an evolutionary process: The “domestication syndrome”
Wilkins, A. S. (2019) · Evolution & Development · doi:10.1111/ede.12319 · Cited by 55 · see citing works
Domestication leads to increased predation susceptibility
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The neural crest cell hypothesis: no unified explanation for domestication
Johnsson, M., Henriksen, R., & Wright, D. (2021) · Genetics · doi:10.1093/genetics/iyab097 · Cited by 51 · see citing works
Unconscious selection drove seed enlargement in vegetable crops
Kluyver, T. A., Jones, G., Pujol, B., Bennett, C., Mockford, E. J., Charles, M., Rees, M., & Osborne, C. P. (2017) · Evolution Letters · doi:10.1002/evl3.6 · Cited by 54 · see citing works
Human protection drives the emergence of a new coping style in animals
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Selection for tameness, a key behavioral trait of domestication, increases adult hippocampal neurogenesis in foxes
Huang, S., Slomianka, L., Farmer, A. J., Kharlamova, A. V., Gulevich, R. G., Herbeck, Y. E., Trut, L. N., Wolfer, D. P., & Amrein, I. (2015) · Hippocampus · doi:10.1002/hipo.22420 · Cited by 50 · see citing works
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Palaeolithic dogs and Pleistocene wolves revisited: a reply to
Germonpré, M., Sablin, M., Lázničková‐Galetová, M., Després, V. R., Stevens, R. E., Stiller, M., & Hofreiter, M. (2014) · Journal of Archaeological Science · doi:10.1016/j.jas.2014.11.035 · Cited by 52 · see citing works

Fox domestication: Molecular mechanisms involved in selection for behavior
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Genetics of domesticated behavior in dogs and foxes
Kukekova, A. V., Trut, L. N., & Acland, G. M. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85752-9.00007-x
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ДОМЕСТИЦИРУЕМЫЕ ЛИСИЦЫ: МОЛЕКУЛЯРНО-ГЕНЕТИЧЕСКИЕ МЕХАНИЗМЫ, ВОВЛЕКАЕМЫЕ В ОТБОР ПО ПОВЕДЕНИЮ
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A new approach to the study of social behavior and activity in wolf ontogeny
Yachmennikova, A. A., & Poyarkov, A. D. (2011) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2010.09.024
Experimental studies of early canid domestication.
Trut, L. N., Oskina, I. N., & Kharlamova, A. V. (2012) · CABI eBooks · doi:10.1079/9781845939403.0012 · Cited by 7 · see citing works
Self-citation

Authors: Trut, L., Oskina, I., & Kharlamova, A.
Affiliations: Russian Academy of Sciences (RU)
Corresponding author: Trut, Lyudmila
Venue: BioEssays
Publisher: Wiley
Published: 2009-03
Volume: 31
Issue: 3
Pages: 349-360
ISSN: 0265-9247 (ISSN-L)
1521-1878
DOI: 10.1002/bies.200800070
PMC: PMC2763232
OpenAlex: W2119978637
Cited by: 636
References: 80
Citations by year: 2026: 25 · 2025: 36 · 2024: 39 · 2023: 40 · 2022: 51 · 2021: 60 · 2020: 83 · 2019: 55 · 2018: 47 · 2017: 48 · 2016: 38 · 2015: 22 · 2014: 29 · 2013: 19 · 2012: 21
FWCI: 1.38
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 2 d)
Locations: BioEssays (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH077811)
Fogarty International Center (R03TW008098)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: animal domestication, silver fox, dog evolution, behavioral selection, phenotypic variability, molecular genetic mechanisms, long-term selection experiment, dogs
MeSH terms: Animals, Animals, Domestic, Behavior, Animal, Dogs, Biological Evolution, Female, Foxes, Humans, Male, Phenotype, Time Factors, Models, Animal, Neuroendocrine Cells

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Animal evolution during domestication: the domesticated fox as a model

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