Advertisement

Mammalian Genome

, Volume 23, Issue 1–2, pp 164–177 | Cite as

Genetics of behavior in the silver fox

  • Anna V. Kukekova
  • Svetlana V. Temnykh
  • Jennifer L. Johnson
  • Lyudmila N. Trut
  • Gregory M. AclandEmail author
Article

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.

Keywords

Tame Polymorphism Information Content Aggressive Population Canine Genome Sequence Mammalian Genotyping Service 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

Conflicts of interest

The authors have no conflicts of interest to disclose.

Supplementary material

335_2011_9373_MOESM1_ESM.xls (73 kb)
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 (995 kb)
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)

References

  1. Acland GM, Ostrander EA (2003) The dog that came in from the cold. Heredity 90:201–202PubMedCrossRefGoogle Scholar
  2. 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 182:541–554Google Scholar
  3. Balcom AB (1916) Fox farming in Prince Edwards Island: a chapter in the history of speculation. Q J Econ 30:665–681CrossRefGoogle Scholar
  4. Bardeleben C, Moore RL, Wayne RK (2005) A molecular phylogeny of the Canidae based on six nuclear loci. Mol Phylogenet Evol 37:815–831PubMedCrossRefGoogle Scholar
  5. Baron-Cohen S, Leslie AM, Frith U (1985) Does the autistic child have a ‘theory of mind’? Cognition 21:37–46PubMedCrossRefGoogle Scholar
  6. 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 18:689–696PubMedCrossRefGoogle Scholar
  7. Belyaev DK (1969) Domestication of animals. Science (Russ) 5:47–52Google Scholar
  8. Belyaev DK (1979) Destabilizing selection as a factor in domestication. J Hered 70:301–308PubMedGoogle Scholar
  9. 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 13:359–370CrossRefGoogle Scholar
  10. 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):e1000451PubMedCrossRefGoogle Scholar
  11. 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 11:1784–1795PubMedCrossRefGoogle Scholar
  12. Brüne M (2007) On human self-domestication, psychiatry, and eugenics. Philos Ethics Humanit Med 2:21PubMedCrossRefGoogle Scholar
  13. 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, LondonGoogle Scholar
  14. Clark DL, Boutros NN, Mendez MF (2010) The brain and behavior. An introduction to behavioral neuroanatomy, 3rd edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  15. Clutton-Brock J (1992) The process of domestication. Mammal Rev 22:79–85CrossRefGoogle Scholar
  16. 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, CambridgeGoogle Scholar
  17. Clutton-Brock J (1999) A natural history of domesticated mammals. Cambridge University Press, Cambridge, p 238Google Scholar
  18. 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, 295–312Google Scholar
  19. Darwin C (1868) The variation of animals and plants under domestication. In: Two volumes with illustrations. John Murray, LondonGoogle Scholar
  20. Davis SJ, Valla FR (1978) Evidence for domestication of the dog 12, 000 years ago in the Natufian of Israel. Nature 276(5688):608–610CrossRefGoogle Scholar
  21. Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418:700–707PubMedCrossRefGoogle Scholar
  22. 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:263–273PubMedCrossRefGoogle Scholar
  23. 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):144–153PubMedCrossRefGoogle Scholar
  24. 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):111–122PubMedCrossRefGoogle Scholar
  25. 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):e6584PubMedCrossRefGoogle Scholar
  26. Galibert F, Quignon P, Hitte C, André C (2011) Toward understanding dog evolutionary and domestication history. C R Biol 334:190–196PubMedCrossRefGoogle Scholar
  27. 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 36:473–490CrossRefGoogle Scholar
  28. 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 81:369–375PubMedCrossRefGoogle Scholar
  29. 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 86:216–221PubMedCrossRefGoogle Scholar
  30. 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 16:129–143PubMedCrossRefGoogle Scholar
  31. 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 82:513–518PubMedCrossRefGoogle Scholar
  32. 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 100:5296–5301PubMedCrossRefGoogle Scholar
  33. 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 60–80Google Scholar
  34. 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 DiegoGoogle Scholar
  35. 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 HarborGoogle Scholar
  36. Hare B, Tomasello M (2005b) Human-like social skills in dogs? Trends Cogn Sci 9:439–444PubMedCrossRefGoogle Scholar
  37. Hare B, Tomasello M (2005c) The emotional reactivity hypothesis and cognitive evolution. Trends Cogn Sci 9:464–465CrossRefGoogle Scholar
  38. 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 YorkGoogle Scholar
  39. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298(5598):1634–1636PubMedCrossRefGoogle Scholar
  40. 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 15:226–230PubMedCrossRefGoogle Scholar
  41. Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623PubMedCrossRefGoogle Scholar
  42. 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 20:1–35PubMedCrossRefGoogle Scholar
  43. 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, BerlinGoogle Scholar
  44. 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 399–415Google Scholar
  45. Keeler C, Ridgway S, Lipscomb L, Fromm E (1968) The genetics of adrenal size and tameness in colorphase foxes. J Hered 59:82–84PubMedGoogle Scholar
  46. 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 95:185–194PubMedCrossRefGoogle Scholar
  47. 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, WoodburyGoogle Scholar
  48. 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 17:387–399PubMedCrossRefGoogle Scholar
  49. 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 38:185–194PubMedCrossRefGoogle Scholar
  50. 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–S53PubMedCrossRefGoogle Scholar
  51. 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 41:593–606PubMedCrossRefGoogle Scholar
  52. 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 12:482PubMedCrossRefGoogle Scholar
  53. 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 298:1613–1616PubMedCrossRefGoogle Scholar
  54. 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 1235–1247Google Scholar
  55. 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–R916PubMedCrossRefGoogle Scholar
  56. 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 17:18CrossRefGoogle Scholar
  57. 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 438:803–819Google Scholar
  58. Merla G, Ucla C, Guipponi M, Reymond A (2002) Identification of additional transcripts in the Williams–Beuren syndrome critical region. Hum Genet 110:429–438PubMedCrossRefGoogle Scholar
  59. Miklósi A (2009) Evolutionary approach to communication between humans and dogs. Vet Res Commun 33(Suppl 1):53–59PubMedCrossRefGoogle Scholar
  60. Miklósi A, Topál J (2005) Is there a simple recipe for how to make friends? Trends Cogn Sci 9:463–464PubMedCrossRefGoogle Scholar
  61. Morey DF (2010) Dogs: domestication and the development of a social bond. Cambridge University Press, New YorkGoogle Scholar
  62. Morioka M (2003) Painless civilization: a philosophical critique of desire. Transview Publications, Tokyo. http://www.lifestudies.org/painless01.html. Accessed 28 October 2008
  63. Nes N, Einarsson J, Lohi O, Jarosz S, Scheelje R (1988) Beautiful fur animals and their color genetics. Scientifur, GlostrupGoogle Scholar
  64. Nobis G (1979) Der alteste Haushunde lebte. Umschau 79:610Google Scholar
  65. 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 193–198Google Scholar
  66. Oskina IN, Tinnikov AA (1992) Interaction between cortisol and cortisol-binding protein in silver foxes (Vulpes fulvus). Comp Biochem Physiol Comp Physiol 101:665–668PubMedCrossRefGoogle Scholar
  67. 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:e22821PubMedCrossRefGoogle Scholar
  68. 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 26:2849–2864PubMedCrossRefGoogle Scholar
  69. Pickerel T (2008) The Dog. 5000 years of the dog in art. Merrell Publishers Limited, LondonGoogle Scholar
  70. 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 32:253–268CrossRefGoogle Scholar
  71. 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 33:370–374PubMedGoogle Scholar
  72. Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271CrossRefGoogle Scholar
  73. Price EO, King JA (1968) Domestication and adaptation. In: Hafez ES (ed) Adaptation of domestic animals. Lea and Febiger, Philadelphia, pp 34–45Google Scholar
  74. Robinson GE, Grozinger CM, Whitfield CW (2005) Sociogenomics: social life in molecular terms. Nat Rev Genet 6:257–270PubMedCrossRefGoogle Scholar
  75. Robinson GE, Fernald RD, Clayton DF (2008) Genes and social behavior. Science 322(5903):896–900PubMedCrossRefGoogle Scholar
  76. Rubtsov NB (1998) The fox gene map. ILAR J 39(2/3):182–188PubMedGoogle Scholar
  77. Sablin MV, Khlopachev GA (2002) The earliest ice age dogs: evidence from Eliseevichi I. Curr Anthropol 43:795–799CrossRefGoogle Scholar
  78. Sargan DR, Aguirre-Hernandez J, Galibert F, Ostrander EA (2007) An extended microsatellite set for linkage mapping in the domestic dog. J Hered 98:221–231PubMedCrossRefGoogle Scholar
  79. Savolainen P, Zhang YP, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298:1610–1613PubMedCrossRefGoogle Scholar
  80. 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 103:168–175PubMedCrossRefGoogle Scholar
  81. 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 80:142–155Google Scholar
  82. Switonski M, Szczerbal I, Nowacka-Woszuk J (2009) Comparative genomics of 3 farm canids in relation to the dog. Cytogenet Genome Res 126:86–96PubMedCrossRefGoogle Scholar
  83. Tchernov E, Valla FF (1997) Two new dogs, and other Natufian dogs, from the southern Levant. J Archaeol Sci 24:65–95CrossRefGoogle Scholar
  84. 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 70:1367–1375CrossRefGoogle Scholar
  85. 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 123–137Google Scholar
  86. 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, NovosibirskGoogle Scholar
  87. Trut LN (1999) Early canid domestication: the farm-fox experiment. Am Sci 87:160–169Google Scholar
  88. Trut LN (2001) Experimental studies of early canid domestication. In: Ruvinsky A, Sampson J (eds) The genetics of the dog. CABI, London, pp 15–43CrossRefGoogle Scholar
  89. Trut LN, Plyusnina IZ, Oskina IN (2004a) An experiment on fox domestication and debatable issues of evolution of the dog. Genetika 40:794–807PubMedGoogle Scholar
  90. Trut LN, Plyusnina IZ, Oskina IN (2004b) An experiment on fox domestication and debatable issues of evolution of the dog. Russ J Genet 40:644–655CrossRefGoogle Scholar
  91. Trut L, Oskina I, Kharlamova A (2009) Animal evolution during domestication: the domesticated fox as a model. Bioessays 31(3):349–360PubMedCrossRefGoogle Scholar
  92. Turnbull PF, Reed CA (1974) The fauna from the terminal Pleistocene of Palegawra Cave, a Zarzian occupation site in northeastern Iraq. Fieldiana, Anthropology 63:81–146Google Scholar
  93. 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 15:311–315PubMedCrossRefGoogle Scholar
  94. Vasileva LL, Trut LN (1990) The use of the method of principal components for phenogenetic analysis of the integral domestication trait. Genetika 26:516–524Google Scholar
  95. 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 22:2541–2551PubMedCrossRefGoogle Scholar
  96. 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 276:1687–1689PubMedCrossRefGoogle Scholar
  97. von Eickstedt EF (1934) Rassenkunde und Rassengeschichte der Menschheit [Race theory and racial history of mankind]. F Enke, StuttgartGoogle Scholar
  98. 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):898–902PubMedCrossRefGoogle Scholar
  99. Wayne RK (1993) Molecular evolution of the dog family. Trends Genet 9:218–224PubMedCrossRefGoogle Scholar
  100. Wayne RK, Ostrander EA (1999) Origin, genetic diversity, and genome structure of the domestic dog. Bioessays 21:247–257PubMedCrossRefGoogle Scholar
  101. Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marshall CR (1997) Molecular systematics of the Canidae. Syst Biol 46:622–653PubMedCrossRefGoogle Scholar
  102. 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 184:595–605PubMedCrossRefGoogle Scholar
  103. Wrangham R (2003) The evolution of cooking. In: Brockman J (ed) The new humanists: science at the edge. Sterling Publishing, New York, pp 108–109Google Scholar
  104. 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 62:189–202PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Anna V. Kukekova
    • 1
  • Svetlana V. Temnykh
    • 1
  • Jennifer L. Johnson
    • 1
  • Lyudmila N. Trut
    • 2
  • Gregory M. Acland
    • 1
    Email author
  1. 1.Baker Institute for Animal HealthCornell University College of Veterinary MedicineIthacaUSA
  2. 2.Russian Academy of Sciences, Institute of Cytology and GeneticsNovosibirskRussia

Personalised recommendations