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Genetics of behavior in the silver fox

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Abstract

The silver fox provides a rich resource for investigating the genetics of behavior, with strains developed by intensely selective breeding that display markedly different behavioral phenotypes. Until recently, however, the tools for conducting molecular genetic investigations in this species were very limited. In this review, the history of development of this resource and the tools to exploit it are described. Although the focus is on the genetics of domestication in the silver fox, there is a broader context. In particular, one expectation of the silver fox research is that it will be synergistic with studies in other species, including humans, to yield a more comprehensive understanding of the molecular mechanisms and evolution of a wider range of social cognitive behaviors.

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References

  • Acland GM, Ostrander EA (2003) The dog that came in from the cold. Heredity 90:201–202

    Article  PubMed  CAS  Google Scholar 

  • Albert FW, Carlborg O, Plyusnina I, Besnier F, Hedwig D, Lautenschläger S, Lorenz D, McIntosh J, Neumann C, Richter H, Zeising C, Kozhemyakina R, Shchepina O, Kratzsch J, Trut L, Teupser D, Thiery J, Schöneberg T, Andersson L, Pääbo S (2009) Genetic architecture of tameness in a rat model of animal domestication. Genetics 182:541–554

    Google Scholar 

  • Balcom AB (1916) Fox farming in Prince Edwards Island: a chapter in the history of speculation. Q J Econ 30:665–681

    Article  Google Scholar 

  • Bardeleben C, Moore RL, Wayne RK (2005) A molecular phylogeny of the Canidae based on six nuclear loci. Mol Phylogenet Evol 37:815–831

    Article  PubMed  CAS  Google Scholar 

  • Baron-Cohen S, Leslie AM, Frith U (1985) Does the autistic child have a ‘theory of mind’? Cognition 21:37–46

    Article  PubMed  CAS  Google Scholar 

  • Basheva EA, Torgasheva AA, Sakaeva GR, Bidau C, Borodin PM (2010) A- and B-chromosome pairing and recombination in male meiosis of the silver fox (Vulpes vulpes L., 1758, Carnivora, Canidae). Chromosome Res 18:689–696

    Article  PubMed  CAS  Google Scholar 

  • Belyaev DK (1969) Domestication of animals. Science (Russ) 5:47–52

    Google Scholar 

  • Belyaev DK (1979) Destabilizing selection as a factor in domestication. J Hered 70:301–308

    PubMed  CAS  Google Scholar 

  • Belyaev DK, Plyusnina IZ, Trut LN (1985) Domestication in the silver fox (Vulpes fulvus Desm): changes in physiological boundaries of the sensitive period of primary socialization. Appl Animal Behav Sci 13:359–370

    Article  Google Scholar 

  • Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, Lohmueller KE, Zhao K, Brisbin A, Parker HG, von Holdt BM, Cargill M, Auton A, Reynolds A, Elkahloun AG, Castelhano M, Mosher DS, Sutter NB, Johnson GS, Novembre J, Hubisz MJ, Siepel A, Wayne RK, Bustamante CD, Ostrander EA (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8(8):e1000451

    Article  PubMed  Google Scholar 

  • Breen M, Jouquand S, Renier C, Mellersh CS, Hitte C, Holmes NG, Chéron A, Suter N, Vignaux F, Bristow AE, Priat C, McCann E, André C, Boundy S, Gitsham P, Thomas R, Bridge WL, Spriggs HF, Ryder EJ, Curson A, Sampson J, Ostrander EA, Binns MM, Galibert F (2001) Chromosome-specific single-locus FISH probes allow anchorage of an 1800-marker integrated radiation-hybrid/linkage map of the domestic dog genome to all chromosomes. Genome Res 11:1784–1795

    Article  PubMed  CAS  Google Scholar 

  • Brüne M (2007) On human self-domestication, psychiatry, and eugenics. Philos Ethics Humanit Med 2:21

    Article  PubMed  Google Scholar 

  • Carter H, Blackden MW, Brown P, Buckman P (1900) Beni Hasan part IV, zoological and other details. In: Griffith FL (ed) Archaeological survey of Egypt. Special Publication of the Egypt Exploration Fund, London

    Google Scholar 

  • Clark DL, Boutros NN, Mendez MF (2010) The brain and behavior. An introduction to behavioral neuroanatomy, 3rd edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Clutton-Brock J (1992) The process of domestication. Mammal Rev 22:79–85

    Article  Google Scholar 

  • Clutton-Brock J (1995) Origins of the dog: domestication and early history. In: Serpell J (ed), The domestic dog: its evolution, behavior and interaction with people. Cambridge University Press, Cambridge

  • Clutton-Brock J (1999) A natural history of domesticated mammals. Cambridge University Press, Cambridge, p 238

    Google Scholar 

  • Crockford SJ (2000) Dogs through time: an archaeological perspective. In: Proceedings of the 1st international council for archaeozoology symposium on the history of the domestic dog. British Archaeological Reports. Archaeopress, Oxford, pp 21–28, 295–312

  • Darwin C (1868) The variation of animals and plants under domestication. In: Two volumes with illustrations. John Murray, London

  • Davis SJ, Valla FR (1978) Evidence for domestication of the dog 12, 000 years ago in the Natufian of Israel. Nature 276(5688):608–610

    Article  Google Scholar 

  • Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418:700–707

    Article  PubMed  CAS  Google Scholar 

  • Doyle TF, Bellugi U, Korenberg JR, Graham J (2004) “Everybody in the world is my friend”: hypersociability in young children with Williams syndrome. Am J Med Genet 124A:263–273

    Article  PubMed  Google Scholar 

  • Gacsi M, Miklósi A, Varga O, Topál J, Csányi V (2004) Are readers of our face readers of our minds? Dogs (Canis familiaris) show situation-dependent recognition of human’s attention. Anim Cogn 7(3):144–153

    Article  PubMed  Google Scholar 

  • Gacsi M, Gyori B, Miklósi A, Virányi Z, Kubinyi E, Topal J, Csanyi V (2005) Species-specific differences and similarities in the behavior of hand-raised dog and wolf pups in social situations with humans. Dev Psychobiol 47(2):111–122

    Article  PubMed  Google Scholar 

  • Gacsi M, Györi B, Virányi Z, Kubinyi E, Range F, Belényi B, Miklosi A (2009) Explaining dog–wolf differences in utilizing human pointing gestures: selection for synergistic shifts in the development of some social skills. PLoS One 4(8):e6584

    Article  PubMed  Google Scholar 

  • Galibert F, Quignon P, Hitte C, André C (2011) Toward understanding dog evolutionary and domestication history. C R Biol 334:190–196

    Article  PubMed  Google Scholar 

  • Germonpré M, Sablin M, Stevens R, Hedges R, Hofreiter M, Stiller M, Jaenickedesprese V (2009) Fossil dogs and wolves from palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J Archaeol Sci 36:473–490

    Article  Google Scholar 

  • Gogoleva SS, Volodin IA, Volodina EV, Kharlamova AV, Trut LN (2009) Kind granddaughters of angry grandmothers: the effect of domestication on vocalization in cross-bred silver foxes. Behav Processes 81:369–375

    Article  PubMed  Google Scholar 

  • Gogoleva SS, Volodin IA, Volodina EV, Kharlamova AV, Trut LN (2011) Explosive vocal activity for attracting human attention is related to domestication in silver fox. Behav Processes 86:216–221

    Article  PubMed  Google Scholar 

  • Graphodatsky AS, Perelman PL, Sokolovskaya NV, Beklemisheva VR, Serdukova NA, Dobigny G, O’Brien SJ, Ferguson-Smith MA, Yang F (2008) Phylogenomics of the dog and fox family (Canidae, Carnivora) revealed by chromosome painting. Chromosome Res 16:129–143

    Article  PubMed  CAS  Google Scholar 

  • Gulevich RG, Oskina IN, Shikhevich SG, Fedorova EV, Trut LN (2004) Effect of selection for behavior on pituitary–adrenal axis and proopiomelanocortin gene expression in silver foxes (Vulpes vulpes). Physiol Behav 82:513–518

    Article  PubMed  CAS  Google Scholar 

  • Guyon R, Lorentzen TD, Hitte C, Kim L, Cadieu E, Parker HG, Quignon P, Lowe JK, Renier C, Gelfenbeyn B, Vignaux F, DeFrance HB, Gloux S, Mahairas GG, André C, Galibert F, Ostrander EA (2003) A 1-Mb resolution radiation hybrid map of the canine genome. Proc Natl Acad Sci USA 100:5296–5301

    Article  PubMed  CAS  Google Scholar 

  • Hahn ME (1990) Approaches to the study of genetic influence in developing social behavior. In: Hahn ME, Hewitt JK, Henderson ND, Benno R (eds) Developmental behavior genetics: neural, biometrical and evolutionary approaches. Oxford University Press, New York, pp 60–80

    Google Scholar 

  • Hahn ME, Wright JC (1998) The influence of genes on social behavior of dogs. In: Grandin T (ed) Genetics and the behavior of domestic animals, Chap 10. Academic Press, San Diego

    Google Scholar 

  • Hare B, Tomasello M (2005a) Behavioral genetics of dog cognition. In: Ostrander E et al (eds) The genetics of the dog. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Hare B, Tomasello M (2005b) Human-like social skills in dogs? Trends Cogn Sci 9:439–444

    Article  PubMed  Google Scholar 

  • Hare B, Tomasello M (2005c) The emotional reactivity hypothesis and cognitive evolution. Trends Cogn Sci 9:464–465

    Article  Google Scholar 

  • Hare B, Tomasello M (2006) Behavioral generation of dog cognition: human like social skills in dogs are heritable and desired. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298(5598):1634–1636

    Article  PubMed  CAS  Google Scholar 

  • Hare B, Plyusnina I, Ignacio N, Schepina O, Stepika A, Wrangham R, Trut L (2005) Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol 15:226–230

    Article  PubMed  CAS  Google Scholar 

  • Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623

    Article  PubMed  CAS  Google Scholar 

  • Järvinen-Pasley A, Bellugi U, Reilly J, Mills DL, Galaburda A, Reiss AL, Korenberg JR (2008) Defining the social phenotype in Williams syndrome: a model for linking gene, the brain, and behavior. Dev Psychopathol 20:1–35

    Article  PubMed  Google Scholar 

  • Kaminski J (2009) Dogs (Canis familiaris) are adapted to receive human communication. In: Berthoz A, Christen Y (eds) Neurobiology of “Umwelt”: how living beings perceive the world: research and perspectives in neurosciences. Springer-Verlag, Berlin

    Google Scholar 

  • Keeler C (1974) Behaviour variations associated with colour phase in Red Fox. In: Fox MW (ed) The wild canids: their systematics, behavioral ecology, and evolution. Van Nostrand Reinhold, New York, pp 399–415

    Google Scholar 

  • Keeler C, Ridgway S, Lipscomb L, Fromm E (1968) The genetics of adrenal size and tameness in colorphase foxes. J Hered 59:82–84

    PubMed  CAS  Google Scholar 

  • Kukekova AV, Trut LN, Oskina IN, Kharlamova AV, Shikhevich SG, Kirkness EF, Aguirre GD, Acland GM (2004) A marker set for construction of a genetic map of the silver fox (Vulpes vulpes). J Hered 95:185–194

    Article  PubMed  CAS  Google Scholar 

  • Kukekova AV, Acland GM, Oskina IN, Kharlamova AV, Trut LN, Chase K, Lark KG, Hollis NE, Aguirre GD (2006) The genetics of domesticated behavior in canids: What can dogs and silver foxes tell us about each other? The dog and its genome. Cold Spring Harbor Laboratory Press, Woodbury

    Google Scholar 

  • Kukekova AV, Trut LN, Oskina IN, Johnson JL, Temnykh SV, Kharlamova AV, Shepeleva DV, Gulievich RG, Shikhevich SG, Graphodatsky AS, Aguirre GD, Acland GM (2007) A meiotic linkage map of the silver fox, aligned and compared to the canine genome. Genome Res 17:387–399

    Article  PubMed  CAS  Google Scholar 

  • Kukekova AV, Trut LN, Chase K, Shepeleva DV, Vladimirova AV, Kharlamova AV, Oskina IN, Stepika A, Klebanov S, Erb HN, Acland GM (2008) Measurement of segregating behaviors in experimental silver fox pedigrees. Behav Genet 38:185–194

    Article  PubMed  Google Scholar 

  • Kukekova AV, Vorobieva NV, Beklemisheva VR, Johnson JL, Temnykh SV, Yudkin DV, Trut LN, Andre C, Galibert F, Aguirre GD, Acland GM, Graphodatsky AS (2009) Chromosomal mapping of canine-derived BAC clones to the red fox and American mink genomes. J Hered 100(Suppl 1):S42–S53

    Article  PubMed  CAS  Google Scholar 

  • Kukekova AV, Trut LN, Chase K, Kharlamova AV, Johnson JL, Temnykh SV, Oskina IN, Gulevich RG, Vladimirova AV, Klebanov S, Shepeleva DV, Shikhevich SG, Acland GM, Lark KG (2011a) Mapping loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype. Behav Genet 41:593–606

    Article  PubMed  Google Scholar 

  • Kukekova AV, Johnson JL, Teiling C, Lewyn L, Oskina IN, Kharlamova AV, Gulevich RG, Padtel R, Dubreuil MM, Vladimirova AV, Shepeleva DV, Shikhevich SG, Sun Q, Ponnala L, Temnykh SV, Trut LN, Acland GM (2011b) Sequence comparison of prefrontal cortical brain transcriptome from a tame and an aggressive silver fox (Vulpes vulpes). BMC Genomics 12:482

    Article  PubMed  CAS  Google Scholar 

  • Leonard JA, Wayne RK, Wheeler J, Valadez R, Guillén S, Vilà C (2002) Ancient DNA evidence for old world origin of new world dogs. Science 298:1613–1616

    Article  PubMed  CAS  Google Scholar 

  • Leslie AM (2000) “Theory of mind” as a mechanism of selective attention. In: Gazzaniga MS (ed) Neurosciences, chap 85, 2nd edn. MIT Press, Cambridge, pp 1235–1247

    Google Scholar 

  • Lindberg J, Bjornerfeldt S, Saetre P, Svartberg K, Seehuus B, Bakken M, Vila C, Jazin E (2005) Selection for tameness has changed brain gene expression in silver foxes. Curr Biol 15:R915–R916

    Article  PubMed  CAS  Google Scholar 

  • Lindberg J, Björnerfeldt S, Bakken M, Vilà C, Jazin E, Saetre P (2007) Selection for tameness modulates the expression of heme related genes in silver foxes. Behav Brain Funct 17:18

    Article  Google Scholar 

  • Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, Clamp M, Chang JL, Kulbokas EJ, Zody MC, Mauceli E, Xie X, Breen M, Wayne RK, Ostrander EA, Ponting CP, Galibert F, Smith DR, Dejong PJ, Kirkness E, Alvarez P, Biagi T, Brockman W, Butler J, Chin CW, Cook A, Cuff J, Daly MJ, Decaprio D, Gnerre S, Grabherr M, Kellis M, Kleber M, Bardeleben C, Goodstadt L, Heger A, Hitte C, Kim L, Koepfli KP, Parker HG, Pollinger JP, Searle SM, Sutter NB, Thomas R, Webber C, Baldwin J, Abebe A, Abouelleil A, Aftuck L, Ait-Zahra M, Aldredge T, Allen N, An P, Anderson S, Antoine C, Arachchi H, Aslam A, Ayotte L, Bachantsang P, Barry A, Bayul T, Benamara M, Berlin A, Bessette D, Blitshteyn B, Bloom T, Blye J, Boguslavskiy L, Bonnet C, Boukhgalter B, Brown A, Cahill P, Calixte N, Camarata J, Cheshatsang Y, Chu J, Citroen M, Collymore A, Cooke P, Dawoe T, Daza R, Decktor K, Degray S, Dhargay N, Dooley K, Dooley K, Dorje P, Dorjee K, Dorris L, Duffey N, Dupes A, Egbiremolen O, Elong R, Falk J, Farina A, Faro S, Ferguson D, Ferreira P, Fisher S, Fitzgerald M, Foley K, Foley C, Franke A, Friedrich D, Gage D, Garber M, Gearin G, Giannoukos G, Goode T, Goyette A, Graham J, Grandbois E, Gyaltsen K, Hafez N, Hagopian D, Hagos B, Hall J, Healy C, Hegarty R, Honan T, Horn A, Houde N, Hughes L, Hunnicutt L, Husby M, Jester B, Jones C, Kamat A, Kanga B, Kells C, Khazanovich D, Kieu AC, Kisner P, Kumar M, Lance K, Landers T, Lara M, Lee W, Leger JP, Lennon N, Leuper L, Levine S, Liu J, Liu X, Lokyitsang Y, Lokyitsang T, Lui A, Macdonald J, Major J, Marabella R, Maru K, Matthews C, McDonough S, Mehta T, Meldrim J, Melnikov A, Meneus L, Mihalev A, Mihova T, Miller K, Mittelman R, Mlenga V, Mulrain L, Munson G, Navidi A, Naylor J, Nguyen T, Nguyen N, Nguyen C, Nguyen T, Nicol R, Norbu N, Norbu C, Novod N, Nyima T, Olandt P, O’Neill B, O’Neill K, Osman S, Oyono L, Patti C, Perrin D, Phunkhang P, Pierre F, Priest M, Rachupka A, Raghuraman S, Rameau R, Ray V, Raymond C, Rege F, Rise C, Rogers J, Rogov P, Sahalie J, Settipalli S, Sharpe T, Shea T, Sheehan M, Sherpa N, Shi J, Shih D, Sloan J, Smith C, Sparrow T, Stalker J, Stange-Thomann N, Stavropoulos S, Stone C, Stone S, Sykes S, Tchuinga P, Tenzing P, Tesfaye S, Thoulutsang D, Thoulutsang Y, Topham K, Topping I, Tsamla T, Vassiliev H, Venkataraman V, Vo A, Wangchuk T, Wangdi T, Weiand M, Wilkinson J, Wilson A, Yadav S, Yang S, Yang X, Young G, Yu Q, Zainoun J, Zembek L, Zimmer A, Lander ES (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803–819

    Google Scholar 

  • Merla G, Ucla C, Guipponi M, Reymond A (2002) Identification of additional transcripts in the Williams–Beuren syndrome critical region. Hum Genet 110:429–438

    Article  PubMed  CAS  Google Scholar 

  • Miklósi A (2009) Evolutionary approach to communication between humans and dogs. Vet Res Commun 33(Suppl 1):53–59

    Article  PubMed  Google Scholar 

  • Miklósi A, Topál J (2005) Is there a simple recipe for how to make friends? Trends Cogn Sci 9:463–464

    Article  PubMed  Google Scholar 

  • Morey DF (2010) Dogs: domestication and the development of a social bond. Cambridge University Press, New York

    Google Scholar 

  • Morioka M (2003) Painless civilization: a philosophical critique of desire. Transview Publications, Tokyo. http://www.lifestudies.org/painless01.html. Accessed 28 October 2008

  • Nes N, Einarsson J, Lohi O, Jarosz S, Scheelje R (1988) Beautiful fur animals and their color genetics. Scientifur, Glostrup

    Google Scholar 

  • Nobis G (1979) Der alteste Haushunde lebte. Umschau 79:610

    Google Scholar 

  • Omoto K (2004) Human self-domestication as metaphor revisited. In: Benzing B, Herrmann B (eds) Exploitation and overexploitation in societies past and present. IUAES-Intercongress 2001 Goettingen (Anthropology Series). LIT Verlag, Münster, pp 193–198

    Google Scholar 

  • Oskina IN, Tinnikov AA (1992) Interaction between cortisol and cortisol-binding protein in silver foxes (Vulpes fulvus). Comp Biochem Physiol Comp Physiol 101:665–668

    Article  PubMed  CAS  Google Scholar 

  • Ovodov ND, Crockford SJ, Kuzmin YV, Higham TF, Hodgins GW, van der Plicht J (2011) A 33, 000-year-old incipient dog from the Altai Mountains of Siberia: evidence of the earliest domestication disrupted by the last glacial maximum. PLoS One 6:e22821

    Article  PubMed  CAS  Google Scholar 

  • Pang JF, Kluetsch C, Zou XJ, Zhang AB, Luo LY, Angleby H, Ardalan A, Ekström C, Sköllermo A, Lundeberg J, Matsumura S, Leitner T, Zhang YP, Savolainen P (2009) mtDNA data indicate a single origin for dogs south of Yangtze River, less than 16, 300 years ago, from numerous wolves. Mol Biol Evol 26:2849–2864

    Article  PubMed  CAS  Google Scholar 

  • Pickerel T (2008) The Dog. 5000 years of the dog in art. Merrell Publishers Limited, London

    Google Scholar 

  • Plyusnina IZ, Oskina IN, Trut LN (1991) An analysis of fear and aggression during early development of behavior in silver foxes (Vulpes vulpes). Appl Anim Behav Sci 32:253–268

    Article  Google Scholar 

  • Popova NK, Kulikov AV, Avgustinovich DF, Voitenko NN, Trut LN (1997) Effect of domestication of the silver fox on the main enzymes of serotonin metabolism and serotonin receptors. Genetika 33:370–374

    PubMed  CAS  Google Scholar 

  • Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271

    Article  Google Scholar 

  • Price EO, King JA (1968) Domestication and adaptation. In: Hafez ES (ed) Adaptation of domestic animals. Lea and Febiger, Philadelphia, pp 34–45

    Google Scholar 

  • Robinson GE, Grozinger CM, Whitfield CW (2005) Sociogenomics: social life in molecular terms. Nat Rev Genet 6:257–270

    Article  PubMed  CAS  Google Scholar 

  • Robinson GE, Fernald RD, Clayton DF (2008) Genes and social behavior. Science 322(5903):896–900

    Article  PubMed  CAS  Google Scholar 

  • Rubtsov NB (1998) The fox gene map. ILAR J 39(2/3):182–188

    PubMed  Google Scholar 

  • Sablin MV, Khlopachev GA (2002) The earliest ice age dogs: evidence from Eliseevichi I. Curr Anthropol 43:795–799

    Article  Google Scholar 

  • Sargan DR, Aguirre-Hernandez J, Galibert F, Ostrander EA (2007) An extended microsatellite set for linkage mapping in the domestic dog. J Hered 98:221–231

    Article  PubMed  CAS  Google Scholar 

  • Savolainen P, Zhang YP, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298:1610–1613

    Article  PubMed  CAS  Google Scholar 

  • Statham MJ, Trut LN, Sacks BN, Kharlamova AV, Oskina IN, Gulevich RG, Johnson JL, Temnykh SV, Acland GM, Kukekova AV (2011a) On the origin of a domesticated species: identifying the parent population of Russian silver foxes (Vulpes vulpes). Biol J Linn Soc Lond 103:168–175

    Article  PubMed  Google Scholar 

  • Statham MJ, Sacks BN, Aubry K, Perrine JP, Wisely SM (2011b) The origin of recently established red fox populations in the contiguous United States: translocations or natural range expansions? J Mammal 80:142–155

    Google Scholar 

  • Switonski M, Szczerbal I, Nowacka-Woszuk J (2009) Comparative genomics of 3 farm canids in relation to the dog. Cytogenet Genome Res 126:86–96

    Article  PubMed  CAS  Google Scholar 

  • Tchernov E, Valla FF (1997) Two new dogs, and other Natufian dogs, from the southern Levant. J Archaeol Sci 24:65–95

    Article  Google Scholar 

  • Topal J, Gacsi M, Miklósi A, Viranyi Z, Kubinyi E, Csanyi V (2005) The effect of domestication and socialization on attachment to human: a comparative study on hand-reared wolves and differently socialized dog puppies. Anim Behav 70:1367–1375

    Article  Google Scholar 

  • Trut LN (1980a) The genetics and phenogenetics of domestic behaviour. In: Belyaev DK (ed) Problems in general genetics: proceedings of the xivth international congress of genetics, vol 2. MIR Publications, Moscow, pp 123–137

  • Trut LN (1980b) The role of behavior in domestication-associated changes in animals as revealed with the example of silver fox. Doctoral (Biol.) dissertation. Institute of Cytology and Genetics, Novosibirsk

  • Trut LN (1999) Early canid domestication: the farm-fox experiment. Am Sci 87:160–169

    Google Scholar 

  • Trut LN (2001) Experimental studies of early canid domestication. In: Ruvinsky A, Sampson J (eds) The genetics of the dog. CABI, London, pp 15–43

    Chapter  Google Scholar 

  • Trut LN, Plyusnina IZ, Oskina IN (2004a) An experiment on fox domestication and debatable issues of evolution of the dog. Genetika 40:794–807

    PubMed  CAS  Google Scholar 

  • Trut LN, Plyusnina IZ, Oskina IN (2004b) An experiment on fox domestication and debatable issues of evolution of the dog. Russ J Genet 40:644–655

    Article  CAS  Google Scholar 

  • Trut L, Oskina I, Kharlamova A (2009) Animal evolution during domestication: the domesticated fox as a model. Bioessays 31(3):349–360

    Article  PubMed  Google Scholar 

  • Turnbull PF, Reed CA (1974) The fauna from the terminal Pleistocene of Palegawra Cave, a Zarzian occupation site in northeastern Iraq. Fieldiana, Anthropology 63:81–146

    Google Scholar 

  • Våge DI, Lu D, Klungland H, Lien S, Adalsteinsson S, Cone RD (1997) A non-epistatic interaction of agouti and extension in the fox, Vulpes vulpes. Nat Genet 15:311–315

    Article  PubMed  Google Scholar 

  • Vasileva LL, Trut LN (1990) The use of the method of principal components for phenogenetic analysis of the integral domestication trait. Genetika 26:516–524

    CAS  Google Scholar 

  • Verginelli F, Capelli C, Coia V, Musiani M, Falchetti M, Ottini L, Palmirotta R, Tagliacozzo A, De Grossi Mazzorin I, Mariani-Costantini R (2005) Mitochondrial DNA from prehistoric canids highlights relationships between dogs and South-East European wolves. Mol Biol Evol 22:2541–2551

    Article  PubMed  CAS  Google Scholar 

  • Vilà C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, Honeycutt RL, Crandall KA, Lundeberg J, Wayne RK (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689

    Article  PubMed  Google Scholar 

  • von Eickstedt EF (1934) Rassenkunde und Rassengeschichte der Menschheit [Race theory and racial history of mankind]. F Enke, Stuttgart

    Google Scholar 

  • VonHoldt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P, Degenhardt JD, Boyko AR, Earl DA, Auton A, Reynolds A, Bryc K, Brisbin A, Knowles JC, Mosher DS, Spady TC, Elkahloun A, Geffen E, Pilot M, Jedrzejewski W, Greco C, Randi E, Bannasch D, Wilton A, Shearman J, Musiani M, Cargill M, Jones PG, Qian Z, Huang W, Ding ZL, Zhang YP, Bustamante CD, Ostrander EA, Novembre J, Wayne RK (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464(7290):898–902

    Article  PubMed  CAS  Google Scholar 

  • Wayne RK (1993) Molecular evolution of the dog family. Trends Genet 9:218–224

    Article  PubMed  CAS  Google Scholar 

  • Wayne RK, Ostrander EA (1999) Origin, genetic diversity, and genome structure of the domestic dog. Bioessays 21:247–257

    Article  PubMed  CAS  Google Scholar 

  • Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marshall CR (1997) Molecular systematics of the Canidae. Syst Biol 46:622–653

    Article  PubMed  CAS  Google Scholar 

  • Wong AK, Ruhe AL, Dumont BL, Robertson KR, Guerrero G, Shull SM, Ziegle JS, Millon LV, Broman KW, Payseur BA, Neff MW (2010) A comprehensive linkage map of the dog genome. Genetics 184:595–605

    Article  PubMed  CAS  Google Scholar 

  • Wrangham R (2003) The evolution of cooking. In: Brockman J (ed) The new humanists: science at the edge. Sterling Publishing, New York, pp 108–109

    Google Scholar 

  • Yang F, O’Brien PC, Milne BS, Graphodatsky AS, Solanky N, Trifonov V, Rens W, Sargan D, Ferguson-Smith MA (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62:189–202

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Irina V. Pivovarova, Anastasiya V. Vladimirova, Tatyana I. Semenova, and all the animal keepers at the ICG experimental farm for research assistance. We thank Dr. Aaron Wong and Dr. Mark Neff for providing information on amplification and polymorphism of a large set of newly developed canine SSR markers using a panel of fox DNA samples. We thank Dr. K. Gordon Lark and Kevin Chase, Anastasiya V. Kharlamova, Irina N. Oskina, and Rimma G. Gulevich for insightful discussions. GMA and AVK gratefully acknowledge NEI/NIH grants RO1MH077811, RO1EY006855, and R24GM082910; the support of a Roche Sequencing Grant; a CRIS/USDA Grant; and a CVG Seed Grant Award from the Cornell University Center for Vertebrate Genomics.

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Correspondence to Gregory M. Acland.

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335_2011_9373_MOESM1_ESM.xls

Supplementary Table 1 Ninety-eight binary traits for scoring fox behavior and their contributions to the first two principal components of fox behavior The trait code and a brief description of each trait are listed in columns 2 and 3, respectively. Each trait is a specific behavior that can be reproducibly scored in a binary manner. Columns 4 and 5 (PC1 loading and PC2 loading) list the trait loadings (calculated as trait rotation coefficients using the function prcomp in R) for PC1 and PC2, respectively. For each PC, the 20 discrete behavioral observations (traits) that load most strongly on and thus most strongly determine that PC are indicated in bold. Loadings with opposite signs form opposite extremes of each PC. Comparison of the contributions or loadings for each binary trait for PC1 and PC2 demonstrate the differences between PC1 and PC2. (XLS 73 kb)

335_2011_9373_MOESM2_ESM.pdf

Supplementary Fig. 1 Integrated meiotic linkage map of the silver fox (Vulpes vulpes). The map contains 408 markers. Autosomes were mapped using 916 offspring from 196 families. The X chromosome was mapped with 804 offspring from 147 families. Each linkage group corresponding to a fox chromosome (VVU1–VVU16 and VVUX) is presented on the left side of each panel and aligned with the corresponding segments of the 7.6 × canine genome sequence (CanFam2.0) on the right side of the same panel. Lines connect markers that are both mapped onto the fox meiotic linkage map and identified in the assembly of the canine genome. Markers in bold italic map to unique locations with confidence ≥1000:1 (LOD ≥3.0). Markers in plain format were placed to unique locations with confidence ≥100:1 (LOD ≥2.0). Markers on the far left side of each linkage group have adjacent vertical bars to indicate their most likely position at LOD 2.0. Genetic distances between markers were calculated using the Kosambi mapping function. In general, most dog chromosomes each map to a single fox chromosome. Canine chromosomes that have their homologs divided among more than one fox chromosome are marked by asterisks (*) (see VVU1, 2, 4, 5, and 13). Centromere positions of canine chromosomes are indicated in accordance with the dog genome sequence, assuming that the centromere is located at the beginning of each chromosome. Where different fragments of a single canine chromosome correspond to different fox chromosomal segments, a double slash indicates the break point on the canine chromosome. Positions of markers in the canine sequence are indicated in accordance with the CanFam2.0 assembly, except for markers REN315H04 and AHTH91. In the present study, marker REN315H04 mapped to VVU2 in a region corresponding to CFA2, which is in agreement with the Breen et al. (2001) and Guyon et al. (2003) canine maps and the CanFam1.0 assembly of the canine genome (chr 2: 84,742,789–84,742,951). The CanFam2.0 assembly, however, locates marker REN315H04 on CFA9 (chr 9: 21,100,622–21,100,777). Marker AHTH91 was identified only in the CanFam1.0 assembly (PDF 996 kb)

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Kukekova, A.V., Temnykh, S.V., Johnson, J.L. et al. Genetics of behavior in the silver fox. Mamm Genome 23, 164–177 (2012). https://doi.org/10.1007/s00335-011-9373-z

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