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Animal evolution during domestication: the domesticated fox as a model
Open accessAbstract
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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“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]
In the citing paper
“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]
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“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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Citations
Cites
Introduction to Quantitative Genetics.
Edwards, A. W. F., & Falconer, D. S. (1982) · Biometrics · doi:10.2307/2529912 · Cited by 21,447
A User's Guide to Principal Components
Leigh, S. D., & Jackson, J. E. (1993) · Technometrics · doi:10.2307/1269292 · Cited by 3,346
Lin, L., Faraco, J., Li, R., Kadotani, H., Rogers, W., Lin, X., Qiu, X., de Jong, P. J., Nishino, S., & Mignot, E. (1999) · Cell · doi:10.1016/s0092-8674(00)81965-0 · Cited by 2,613
Genome sequence, comparative analysis and haplotype structure of the domestic dog
members, B. S. P., Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S., Karlsson, E. K., Jaffe, D. B., Kamal, M., Clamp, M., Chang, J. L., Kulbokas, E. J., et al. (2005) · Nature · doi:10.1038/nature04338 · Cited by 2,568
A Use's Guide to Principal Components
Jackson, J. E. (1991) · Wiley series in probability and statistics · doi:10.1002/0471725331 · Cited by 2,523
The variation of animals and plants under domestication /
Darwin, C. R. (1905) · J. Murray eBooks · doi:10.5962/bhl.title.84435 · Cited by 1,712
Epigenetic inheritance at the agouti locus in the mouse
Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K., & Whitelaw, E. (1999) · Nature Genetics · doi:10.1038/15490 · Cited by 1,476
Maternal epigenetics and methyl supplements affect agouti gene expression in A vy /a mice
Wolff, G. L., Kodell, R. L., Moore, S. R., & Cooney, C. A. (1998) · The FASEB Journal · doi:10.1096/fasebj.12.11.949 · Cited by 1,057
Rakyan, V. K., Chong, S., Blewitt, M. E., Cuthbert, P. C., Morgan, H. D., Luu, K. V. K., & Whitelaw, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0436776100 · Cited by 642
Early canid domestication: the farm-fox experiment.
Trut, L. (1999) · American Scientist · doi:10.1511/1999.2.160 · Cited by 626
Self-citationMolecular origins of rapid and continuous morphological evolution
Fondon, J. W., & Garner, H. R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408118101 · Cited by 614
Microsatellite instability generates diversity in brain and sociobehavioral traits
Hammock, E. A. D., & Young, L. J. (2005) · Science · doi:10.1126/science.1111427 · Cited by 545
The Domestic Dog: Its Evolution, Behavior and Interactions with People
(2016) · doi:10.1017/9781139161800 · Cited by 530
The Ecology of Reproduction in Wild and Domestic Mammals
Sadleir, R. M. F. S. (1969) · Springer eBooks · doi:10.1007/978-94-011-6527-3 · Cited by 487
Primmer, C. R., Borge, T., Lindell, J., & Sætre, G. (2002) · Molecular Ecology · doi:10.1046/j.0962-1083.2001.01452.x · Cited by 450
The Variation of Animals and Plants under Domestication
Darwin, C. R. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511709517 · Cited by 431
Critical Periods in Behavioral Development
Scott, J. P. (1962) · Science · doi:10.1126/science.138.3544.949 · Cited by 423
Maternal serotonin is crucial for murine embryonic development
Côté, F., Fligny, C., Bayard, E., Launay, J.-M., Gershon, M. D., Mallet, J., & Vodjdani, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606722104 · Cited by 381
Social Cognitive Evolution in Captive Foxes Is a Correlated By-Product of Experimental Domestication
Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., & Trut, L. (2005) · Current Biology · doi:10.1016/j.cub.2005.01.040 · Cited by 347
Self-citationOrigins of the dog: domestication and early history
Clutton–Brock, J. (1995) · Cited by 339
Weaver, I. C. G., Diorio, J. C., Seckl, J. R., Szyf, M., & Meaney, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1321.099 · Cited by 332
Oxidative DNA damage, antioxidants, and cancer
Collins, A. R. (1999) · BioEssays · doi:10.1002/(sici)1521-1878(199903)21:3 · Cited by 316
Michaud, E. J., van Vugt, M. J., Bultman, S. J., Sweet, H. O., Davisson, M. T., & Woychik, R. P. (1994) · Genes & Development · doi:10.1101/gad.8.12.1463 · Cited by 279
CRANIAL MORPHOLOGY OF DOMESTIC AND WILD CANIDS: THE INFLUENCE OF DEVELOPMENT ON MORPHOLOGICAL CHANGE
Wayne, R. K. (1986) · Evolution · doi:10.1111/j.1558-5646.1986.tb00467.x · Cited by 271
McCormick, J. A., Lyons, V., Jacobson, M. D., Noble, J., Diorio, J. C., Nyirenda, M., Weaver, S., Ester, W. A., Yau, J. L. W., Meaney, M. J., et al. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.4.0438 · Cited by 261
From genes to aggressive behavior: the role of serotonergic system
Popova, N. K. (2006) · BioEssays · doi:10.1002/bies.20412 · Cited by 236
The early evolution of the domestic dog
Morey, D. F. (1994) · American Scientist · Cited by 224
Künzl, C., & Sachser, N. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1998.1493 · Cited by 220
The Domestic Dog: its evolution, behavior and interactions with people.
Bradshaw, J. L., & Rooney, N. J. (2016) · Cited by 215
An Experiment on Fox Domestication and Debatable Issues of Evolution of the Dog
Trut, L. N., Plyusnina, I. Z., & Oskina, I. N. (2004) · Russian Journal of Genetics · doi:10.1023/b:ruge.0000033312.92773.c1 · Cited by 197
Self-citationBelyaev, D. K., Plyusnina, I. Z., & Trut, L. N. (1985) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(85)90015-2 · Cited by 170
Self-citationChase, K., Carrier, D. R., Adler, F. R., Jarvik, T., Ostrander, E. A., Lorentzen, T. D., & Lark, K. G. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152333099 · Cited by 168
Weaver, I. C. G., Plante, P. L., Weaver, S., Parent, A., Sharma, S., Diorio, J. C., Chapman, K. E., Seckl, J. R., Szyf, M., & Meaney, M. J. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00635-9 · Cited by 156
From wild wolf to domestic dog: gene expression changes in the brain
Saetre, P., Lindberg, J. H., Leonard, J. A., Olsson, K., Pettersson, U., Ellegren, H., Bergström, T. F., Vilà, C., & JAZIN, E. E. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.05.003 · Cited by 150
Of Minds and Embryos: Left-Right Asymmetry and the Serotonergic Controls of Pre-Neural Morphogenesis
Levin, M. G., Buznikov, G. A., & Lauder, J. M. (2006) · Developmental Neuroscience · doi:10.1159/000091915 · Cited by 137
Canine Behavioral Genetics: Pointing Out the Phenotypes and Herding up the Genes
Spady, T. C., & Ostrander, E. A. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2007.12.001 · Cited by 125
Sundberg, M., Savola, S. P., Hienola, A., Korhonen, L., & Lindholm, D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4906-05.2006 · Cited by 120
Molecular distance and divergence time in carnivores and primates.
Wayne, R. K., Valkenburgh, B. V., & O’Brien, S. J. (1991) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040651 · Cited by 112
Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro
Yu, I. T., Lee, S., Lee, Y.-S., & Son, H. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.03.071 · Cited by 105
Ostrander, E. A., Giger, U., & Lindblad‐Toh, K. (2006) · Medical Entomology and Zoology · Cited by 95
Ostrander, E. A., & Ruvinsky, A. O. (2001) · Cited by 86
Inherited activation-inactivation of the star gene in foxes
Belyaev, D. K., Ruvinsky, A. O., & Trut, L. N. (1981) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a109494 · Cited by 84
Self-citationArgeson, A. C., Nelson, K. K., & Siracusa, L. D. (1996) · Genetics · doi:10.1093/genetics/142.2.557 · Cited by 79
do Val, F. C. (1977) · Evolution · doi:10.1111/j.1558-5646.1977.tb01051.x · Cited by 77
Selection for tameness has changed brain gene expression in silver foxes
Lindberg, J. H., Björnerfeldt, S., Saetre, P., Svartberg, K., Seehuus, B., Bakken, M., Vilà, C., & JAZIN, E. E. (2005) · Current Biology · doi:10.1016/j.cub.2005.11.009 · Cited by 76
Degree of Behavioral Neoteny Differentiates Canid Polymorphs
Coppinger, R., Glendinning, J., Torop, E., Matthay, C., Sutherland, M., & Smith, C. (1987) · Ethology · doi:10.1111/j.1439-0310.1987.tb00645.x · Cited by 75
Measurement of Segregating Behaviors in Experimental Silver Fox Pedigrees
Kukekova, A. V., Trut, L. N., Chase, K., Shepeleva, D. V., Vladimirova, A. V., Kharlamova, A. V., Oskina, I. N., Stepika, A., Klebanov, S., Erb, H. N., et al. (2007) · Behavior Genetics · doi:10.1007/s10519-007-9180-1 · Cited by 72
Self-citationExperimental studies of early canid domestication.
Ln, T. (2001) · CABI Publishing eBooks · doi:10.1079/9780851995205.0015 · Cited by 71
Rg, G., Oskina, I. N., Шихевич, С. Г., Fedorova, E. V., & Ln, T. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.04.062 · Cited by 63
Self-citationA meiotic linkage map of the silver fox, aligned and compared to the canine genomePreprint
Kukekova, A. V., Trut, L. N., Oskina, I. N., Johnson, J. L., Temnykh, S. V., Kharlamova, A. V., Shepeleva, D. V., Gulievich, R. G., Шихевич, С. Г., Graphodatsky, A. S., et al. (2007) · Genome Research · doi:10.1101/gr.5893307 · Cited by 60
Self-citationDestabilizing selection as a factor in domestication
BELYAEV, D. K. (1979) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a109263 · Cited by 57 · cited 2×
“Surveying the observations made during the course of experimental fox domestication, Belyaev found no satisfactory explanation within the traditional genetic framework and came to the idea of destabilizing selection as a factor of domestication.((16)) As destabilizing selection Belyaev designated selection causing des…”
BackgroundRicker, J. P., & Hirsch, J. (1988) · Behavior Genetics · doi:10.1007/bf01067072 · Cited by 55
A Marker Set for Construction of a Genetic Map of the Silver Fox (Vulpes vulpes)
Kukekova, A. V. (2004) · Journal of Heredity · doi:10.1093/jhered/esh033 · Cited by 54
Inheritance of alternative states of the fused gene in mice
Belyaev, D. K., Ruvinsky, A. O., & Borodin, P. M. (1981) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a109436 · Cited by 53
Plyusnina, I. Z., Oskina, I. N., & Trut, L. N. (1991) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(05)80048-6 · Cited by 49
Self-citationWHY 300 SPECIES OF HAWAIIAN DROSOPHILA? THE SEXUAL SELECTION HYPOTHESIS
Ringo, J. M. (1977) · Evolution · doi:10.1111/j.1558-5646.1977.tb01063.x · Cited by 44
Domestication of the Norway rat and its implication for the study of genetics in man.
Richter, C. P. (1952) · PubMed · Cited by 26
Teaching a new dog old tricks: identifying quantitative trait loci using lessons from plants
Chase, K. (1999) · Journal of Heredity · doi:10.1093/jhered/90.1.43 · Cited by 26
Oskina, I. N. (1996) · Cited by 22
Self-citationBreeders, & Balyaev, D. K. (1980) · Mir Publishers eBooks · Cited by 21
Interaction between cortisol and cortisol-binding protein in silver foxes (Vulpes fulvus)
Oskina, I. N., & Tinnikov, A. A. (1992) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(92)90341-m · Cited by 17
Self-citationKharlamova, A. V., Trut, L. N., Carrier, D. R., Chase, K., & Lark, K. G. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm023 · Cited by 16
Self-citationWhy 300 Species of Hawaiian Drosophila? The Sexual Selection Hypothesis
Ringo, J. M. (1977) · Evolution · doi:10.2307/2407536 · Cited by 16
Woods, J. W. (1957) · The Journal of Physiology · doi:10.1113/jphysiol.1957.sp005718 · Cited by 15
Neuroendocrine mechanisms in animal domestication.
Naumenko, E. V., & Belyaev, D. K. (1980) · Cited by 14
Ln, T. (1988) · Journal of Animal Breeding and Genetics · doi:10.1111/j.1439-0388.1988.tb00277.x · Cited by 14
Mating behavior and evolution of the Hawaiian Drosophila
Spieth, H. T. (1987) · Springer eBooks · doi:10.1007/978-94-010-2248-4_7 · Cited by 12
Prasolova, L. A., & Ln, T. (1993) · PubMed · Cited by 11
Change in the pituitary-adrenal function of silver foxes during selection according to behavior.
Ln, T., Naumenko, E. V., & Belyaev, D. K. (1974) · PubMed · Cited by 10
Belyaeva, T. A., Vishnivetsky, P. N., Potapov, V. A., Zhelezova, A. I., & Ромащенко, А. Г. (1992) · Mammalian Genome · doi:10.1007/bf00355724 · Cited by 8
Effects of Maternal Bilateral Adrenalectomy on Fetal Rat Cerebral Cortex
Demır, N., & Demir, R. (2001) · International Journal of Neuroscience · doi:10.3109/00207450108986550 · Cited by 8
Ln, T., Oskina, I. N., Prasolova, L. A., & Pliusnina, I. Z. (1998) · PubMed · Cited by 7
Self-citationInukai, Y., Ikeda, R., & Aiyama, S. (2007) · Cells Tissues Organs · doi:10.1159/000110806 · Cited by 6
[Action of glucocorticoid on bone-forming and bone-resorbing cells].
Hakeda, Y. (2006) · PubMed · Cited by 4
Warf, B. (2010) · Encyclopedia of Geography · doi:10.4135/9781412939591.n300 · Cited by 4
Ontogenesis of endocrine function in silver foxes under domestication
Oskina, I. N. (1995) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(95)92362-w · Cited by 3
Self-citation[Is selection an alternative or complementary to variation].
Ln, T. (1993) · PubMed · Cited by 3
Flagged first, then by citations
3 of the 80 references couldn’t be matched to a known paper.
Research works printed but not linked: 22
- Herre W. K., 1959, Todays status of domestication research, Naturwissenschaftlich Rundsch, 12, 87
- Bogolyubski S. H., 1959, Origin and transformation of domestic animals. Manual for State Universities
- Postel‐Vinay O., 2004, The dog, a biological enigma, La Recherche, 375, 30
- Ayala F. J., 1988, Modern genetics
- Belyaev D. K., 1989, Vavilov's heritage in modern biology, 155
- Belyaev D. K., 1962, On some problems of correlative variability and their significance for the theory of evolution and selection of animals, Proc Siberian Division of SSSR Acad Sci, 10, 111
- Trut L. N., 1980, The role of behavior in domestication‐associated changes in animals as revealed with the example of silver fox. Doctoral (Biol.) Dissertation
- Belyaev D. K., 1983, Reorganization of the seasonal rhythm of reproduction in the silver black foxes during their selection for the capacity to domestication, Zh Obshch Biol, 42, 739
- Oskina I. N., 2000, Pituitary‐adrenal axis and problems of phenotypic diversity under animal domestication, Biodiversity and dynamics of ecosystems in North Eurasia, 1, 82
- Trut L. N., 1972, Change in pituitary‐adrenal function in silver foxes under selection for domestication, Genetika, 5, 35
- Oskina I. N., 2008, Alterations in the hypothalamus‐pituitary‐adrenal and immune systems during selection of animals for tame behavior, VOGiS Herald, 12, 39
- Naumenko E. V., 1980, Problems in general genetics, 12
- Trut L. N., 2000, Phenotypic diversity of domestic animals and temporal developmental parameters, Biodiversity and dynamics of ecosystems in North Eurasia, 1, 119
- 10.1210/me.14.4.506 · DOI
- Oskina I. N. Herbeck Yu. E. Il'ina O. V. andGulevich R. G. 2007.Expression of the glucocorticoid receptor genes in grey rats under selection for behavior. Proceedings of the 20th congress of the pavlov's physiological society. Moscow Russian physician Publishing House. p364(In Russian).
- Buznikov G. A., 1987, Neurotransmitters in ontogenesis
- Kaidanov L. Z., 1989, Animal population genetics, Sov Sci Rev F Physiol Biol, 3, 201
- Spieth H. T., 1974, Genetic mechanisms of speciation in insect, 94
- Schmalhausen I., 1949, The theory of stabilizing selection
- Kirkness E. F., 2006, The dog and its genome, 209
- Romashchenko A. G., 2000, Molecular evolution of Canidae Bsp‐repeats: structure formation and the mechanisms of informational saturation of DNA molecules. In: Shumny VK, Markel AL, eds. Modern concepts of evolutionary genetics. Novosibirsk, ICG SB RAS, 177
- Trut L. N., 2006, The dog and its genome, 81
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Metadata
- 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
- 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
- Locations
- BioEssays (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH077811)
- Fogarty International Center (R03TW008098)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › 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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