How to Tame a Fox (and Build a Dog)

by Lee Alan Dugatkin

  Fig. 12. Lyudmila Trut with one of her beloved domesticated foxes. Credit: Vasily Kovaly

  Fig. 13. A domesticated fox pup out for a leisurely stroll. Credit: Irena Muchamedshina

  Fig. 14. Tatjana Semenova hugs two domesticated fox pups. Credit: Vladimir Novikov

  Fig. 15. Domesticated fox pups with Irena Muchamedshina. Credit: Irena Muchamedshina

  Fig. 16. Three adorable domesticated fox pups sitting together in the field. Credit: Irena Pivovarova

  Acknowledgments

  First and foremost, we thank Dmitri Belyaev for his brilliant insights, and for launching, more than six decades ago, what was an audacious experiment to domesticate the silver fox. Dmitri has been gone for more than thirty years, yet hardly a day passes when the fox research team in Siberia does not think of this wonderful man and wish he were still there guiding them. He had few regrets when he left, save one; that he had not written his popular book Man Is Making a New Friend, which is truly the heart of the story in this book. One look into the eyes of the tamed foxes, one lick from their loving tongues and wag of their bushy tails, and no one could have any doubt—we humans have indeed made a lovable, and deeply loyal, new friend.

  We hardly know where to begin when it comes to thanking all the people who helped us put this book together. We are deeply indebted to Tamara Kuzhutova, Lyudmila’s dear friend and colleague, who has participated in the fox experiment from its earliest days. We extend sincere thanks to Ekaterina Omelchenko, who, over many years, has mined the experimental data and created an electronic database. We thank Pavel Borodin, Anatoly Ruvinsky, Michael (Misha) Belyaev, Nicholai Belyaev, Svetlana Argutinskaya, and Arkady Markel for all they have done over the years, both as Lyudmila’s collaborators and as her friends. Over the course of this experiment hundreds of researchers have been involved in one way or another, and while we can’t thank them all, we would be remiss not to acknowledge the amazing work of Irena Plysnina, Irena Oskina, Lyudmila Prasolova, Larisa Vasilyeva, Larisa Kolesnikova, Anastasia Kharlamova, Rimma Gulevich, Juriy Gerbek, Lyudmila Kondrina, Klaudia Sidorova, Vasily Evaikin (chief of the fox farm), Ekaterina Budashkinah, Natasha Vasilevskaya, Irena Muchamedshina, Darja Shepeleva, Anastasia Vladimirova, Svetlana Shikhevich, Irena Pivovarova, Tatjana Semenova, and Vera Chaustova (long-term veterinarian on the fox project). We are also deeply indebted to Venya and Galya Esakovi for their love, care, and kindness toward Coco the fox, who lived with them at their home for much of her life.

  While it might seem a tad odd, as coauthors, we would like to thank each other. Lee wishes to thank Lyudmila for her friendship, for allowing him the sheer delight of getting involved in one of the most important science experiments ever undertaken, and for the chance to get to know all the remarkable people involved in this work. Lyudmila wishes to thank Lee for his friendship, for making the journey across time and space to visit her more than once at the fox farm to meet the foxes she cares about so deeply and to talk with the many dear friends and colleagues of Dmitri Belyaev about their memories of him and of all the exciting moments of discovery with the domesticated foxes.

  We are indebted to the following individuals for allowing us to interview them for insight into the people, the wonderful foxes, and the path-breaking science we write of: Anatoly Ruvinksy, Pavel Borodin, Michael (Misha) Belyaev, Nicholai Belyaev, Larisa Vasilyeva, Valery Soyfer, Galina Kiseleva, Vladimir Shumny, Larisa Kolesnikova, Natalie Delaunay, Anna Kukekova, Svetlana Gogoleva, Ilya Ruvinsky, Nicholai Kolchanov, L. V. Znak, Oleg Trapezov, Aubrey Manning, John Scandalious, Brian Hare, Gordon Lark, Francisco Ayala, Bert Hölldobler, Marc Bekoff, and Gordon Burghardt.

  The day-to-day maintenance of hundreds of foxes year after year for close to six decades is an expensive endeavor. Lyudmila is especially grateful to Vladimir Shumny, who served as director of the Institute of Cytology and Genetics from 1985 to 2007, and Nicholai Kolchanov, who serves in that role today, both of whom provided critical financial aid that allowed the fox work to continue through very rough times.

  We thank Susan Rabiner, of the Susan Rabiner Literary Agency, for helping us shape what you have read here. Our editor at the University of Chicago Press, Christie Henry, is as good as they come and has been a delight to work with on this project, and we appreciate the help of Christie’s editorial assistant, Gina Wadas, two anonymous readers of the manuscript, and the Editorial Board at the University of Chicago Press. Comments on various chapters of the book were graciously provided by Pavel Borodin, Carl Bergstrom, Henry Bloom, John Shumate, Aaron Dugatkin, Dana Dugatkin, Michael Sims, and most especially, Emily Loose. Dana Dugatkin transcribed interviews and proofread the manuscript an inordinate number of times; we are indebted to her for all her suggestions. We thank Aaron Dugatkin, who accompanied Lee on the journeys to Akademgorodok in Siberia, transcribed interviews, and enjoyed a daily lunch of shashlik with Lee at Vkusnyy Tsentr. While we were at Akademgorodok, Vladimir Filonenko acted as our intrepid interpreter, and Egor Dyomin shepherded our team from place to place, gliding us gently along the ice-encrusted roads of Novosibirsk. When not in Siberia, we received unparalleled help in translating between Russian and English from Amal El-Sheikh, culture and language consultant at Alverno College. On occasion, Tom Dumstorf at the University of Louisville also provided help with translation.

  Notes

  Chapter 1

  1. Here Belyaev was influenced by the work of one of his intellectual idols, Nikolai Vavilov, in particular Vavilov’s Law of Homologous Series.

  2. In Russian, this sort of settlement is called a Poselok (поселок).

  3. Summarized in his book, N. I. Vavilov, Five Continents (Rome: IPGRI, English translation, 1997).

  4. Vavilov Research Institute: http://vir.nw.ru/history/vavilov.htm#expeditions.

  5 S. C. Harland, “Nicolai Ivanovitch Vavilov, 1885–1942,” Obituary Notices of Fellows of the Royal Society 9 (1954): 259–264.

  6. D. Joravsky, The Lysenko Affair (Cambridge: Harvard University Press, 1979); V. Soyfer, “The Consequences of Political Dictatorship for Russian Science,” Nature Reviews Genetics 2 (2001): 723–729; V. Soyfer, Lysenko and the Tragedy of Soviet Science (New Brunswick: Rutgers University Press, 1994); V. Soyfer, “New Light on the Lysenko Era,” Nature 339 (1989): 415–420.

  7. From the Agricultural Institute of Kiev.

  8. From the Agricultural Institute of Kiev.

  9. Vitaly Fyodorovich.

  10. Soyfer, Lysenko and the Tragedy of Soviet Science.

  11. Soyfer, Lysenko and the Tragedy of Soviet Science, 11; Pravda, October 8, 1929, as cited on in Soyfer, Lysenko and the Tragedy of Soviet Science.

  12. Pravda, February 15, 1935; Izvestia, February 15, 1935. As cited in Joravsky, The Lysenko Affair, 83, and Soyfer, Lysenko and the Tragedy of Soviet Science, 61.

  13. Z. Medvedev, The Rise and Fall of T. D. Lysenko (New York: Columbia University Press, 1969).

  14. Medvedev, The Rise and Fall of T. D. Lysenko.

  15. P. Pringle, The Murder of Nikolai Vavilov (New York: Simon and Schuster, 2008), 5.

  16. Founded in 1916, this institute was funded by a private charity and was part of the People’s Commissariat of Health; S. G. Inge-Vechtomov and N. P. Bochkov, “An Outstanding Geneticist and Cell-Minded Person: On the Centenary of the Birth of Academician B. L. Astaurov,” Herald of the Russian Academy of Sciences 74 (2004): 542–547.

  17. S. Argutinskaya, “Memories,” in Dmitry Konstantinovich Belyaev, ed. V. K. Shumny, P. Borodin, and A. Markel (Novosibirsk: Russian Academy of Sciences, 2002), 5–71.

  18. Argutinskaya, “Memories.” Their son was left to fend for himself, eventually ending up in the care of an aunt.

  19. Joravsky, The Lysenko Affair, 137.

  20. T. Lysenko, “The Situation in the Science of Biology” (address to the All-Union Lenin Academy of Agricultural Sciences, July 31–August 7, 1948). The entire speech, in English, can be found at http://www.marxists.org/reference/archive/lysenko/works/1940s/report.htm.
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  21. From stenographic notes of 1948 meeting, O polozhenii v biologicheskoi nauke. Stenograficheskii otchet sessi VASKhNILa 31 iiula-7 avgusta 1948.

  22. Argutinskaya, “Memories.”

  23. Argutinskaya, “Memories.”

  Chapter 2

  1. K. Roed, O. Flagstad, M. Nieminen, O. Holand, M. Dwyer, N. Rov, and C. Via, “Genetic Analyses Reveal Independent Domestication Origins of Eurasian Reindeer,” Proceedings of the Royal Society of London B 275 (2008): 1849–1855.

  2. Soyfer, Lysenko and the Tragedy of Soviet Science.

  3. As cited in Scientific Siberia (Moscow: Progress, 1970).

  4. The head of the committee was M. A. Olshansky.

  5. Trofimuk’s memoirs of Khrushchev’s visits: http://www-sbras.nsc.ru/HBC/2000/n30-31/f7.html.

  6. Ekaterina Budashkinah, interview with authors, January 2012.

  7. I. Poletaeva and Z. Zorina, “Extrapolation Ability in Animals and Its Possible Links to Exploration, Anxiety, and Novelty Seeking,” in Anticipation: Learning from the Past,” ed. M. Nadin (Berlin: Springer, 2015), 415–430.

  Chapter 3

  1. D. Belyaev to M. Lerner, July 15, 1966. From collection of Lerner letters at the American Philosophical Society.

  2. P. Josephson, New Atlantis Revisited: Akademgorodok, The Siberian City of Science (Princeton: Princeton University Press, 1997).

  3. Josephson, New Atlantis Revisited, 110.

  4. L. Trut, I. Oskina, and A. Kharlamova, “Animal Evolution during Domestication: The Domesticated Fox as a Model,” Bioessays 31 (2009): 349–360.

  5. The term destabilizing selection has other meanings as well within the field of evolutionary biology.

  6. Tamara Kuzhutova, interview with authors, January 2012.

  7. M. Nagasawa et al., “Oxytocin-Gaze Positive Loop and the Coevolution of Human-Dog Bonds,” Science 348 (2015): 333–336; A. Miklosi et al., “A Simple Reason for a Big Difference: Wolves Do Not Look Back at Humans, but Dogs Do,” Current Biology 13 (2003): 763–766.

  8. B. Hare and V. Woods, “We didn’t domesticate dogs, they domesticated us,” 2013, http://news.nationalgeographic.com/news/2013/03/130302-dog-domestic-evolution-science-wolf-wolves-human/.

  9. C. Darwin, The Expression of Emotions in Man and Animals, 2nd ed. (London: J. Murray, 1872).

  10. N. Tinbergen, The Study of Instinct (Oxford: Clarendon Press, 1951); N. Tinbergen, “The Curious Behavior of the Stickleback,” Scientific American 187 (1952): 22–26.

  11. K. Lorenz, “Vergleichende Bewegungsstudien an Anatiden,” Journal fur Ornithologie 89 (1941): 194–293; K. Lorenz, King Solomon’s Ring, trans. Majorie Kerr Wilson (London: Methuen, 1961). Original in German is from 1949.

  Chapter 4

  1. A. Forel, The Social World of the Ants as Compared to Man, vol. 1 (New York: Albert and Charles Boni, 1929), 469.

  2. T. Nishida and W. Wallauer, “Leaf-Pile Pulling: An Unusual Play Pattern in Wild Chimpanzees,” American Journal of Primatology 60 (2003): 167–173.

  3. A. Thornton and K. McAuliffe, “Teaching in Wild Meerkats,” Science 313 (2006): 227–229.

  4. B. Heinrich and T. Bugnyar, “Just How Smart Are Ravens?” Scientific American 296 (2007): 64–71; B. Heinrich and R. Smokler, “Play in Common Ravens (Corvus corax),” in Animal Play: Evolutionary, Comparative and Ecological Perspectives, ed. M. Bekoff and J. Byers (Cambridge: Cambridge University Press, 1998), 27–44; B. Heinrich, “Neophilia and Exploration in Juvenile Common Ravens, Corvus corax,” Animal Behaviour 50 (1995): 695–704.

  5. L. Trut, “A Long Life of Ideas,” in Dmitry Konstantinovich Belyaev, 89–93.

  6. D. Belyaev, A. Ruvinsky, and L. Trut, “Inherited Activation-Inactivation of the Star Gene in Foxes: Its Bearing on the Problem of Domestication,” Journal of Heredity 72 (1981): 267–274.

  7. Thirty-five percent of the variation observed was due to genetic variation: L. Trut and D. Belyaev, “The Role of Behavior in the Regulation of the Reproductive Function in Some Representatives of the Canidae Family,” in Vie Congres International de Reproduction et Insemination Artificielle (Paris: Thibault, 1969), 1677–1680; L. Trut, “Early Canid Domestication: The Farm-Fox Experiment,” American Scientist 87 (1999): 160–169.

  8. F. Albert et al., “Phenotypic Differences in Behavior, Physiology and Neurochemistry between Rats Selected for Tameness and for Defensive Aggression towards Humans,” Hormones and Behavior 53 (2008): 413–421.

  9. Svetlana Gogolova, email interview with authors.

  10. Natasha Vasilevskaya, interview with authors, January 2012.

  11. Aubrey Manning, Skype interview with authors.

  12. Aubrey Manning, Skype interview with authors.

  13. People such as John Fentress, J. P. Scott, Bert Hölldobler, Patrick Bateson, Klaus Immelman, and Robert Hinde.

  14. Bert Hölldobler, Skype interview with authors. Hölldobler attended the 1971 meeting.

  15. D. Belyaev, “Domestication: Plant and Animal,” in Encyclopedia Britannica, vol. 5 (Chicago: Encyclopedia Britannica, 1974): 936–942.

  16. R. Levins, “Genetics and Hunger,” Genetics 78 (1974): 67–76; G. S. Stent, “Dilemma of Science and Morals,” Genetics 78 (1974): 41–51.

  17. Genetics 79 (June 1975 supplement): 5.

  18. S. Argutinskaya, “D. K. Belyaev, 1917–1985, from the First Steps to Founding the Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences of USSR (ICGSBRAS),” Genetika 33 (1997): 1030–1043.

  Chapter 5

  1. P. McConnell, For the Love of a Dog (New York: Ballantine, 2007).

  2. A. Horowitz, “Disambiguating the ‘Guilty Look’: Salient Prompts to a Familiar Dog Behavior,” Behavioural Processes 81 (2009): 447–452; C. Darwin, The Expression of Emotions in Man and Animals (London: J. Murray, 1872); K. Lorenz, Man Meets Dog (Methuen: London, 1954); H. E. Whitely, Understanding and Training Your Dog or Puppy (Santa Fe: Sunstone, 2006); D. Cheney and R. Seyfarth, Baboon Metaphysics: The Evolution of a Social Mind (Chicago: University of Chicago Press, 2007); F. De Waal, Good Natured: The Origins of Right and Wrong in Humans and Other Animals (Cambridge: Harvard University Press, 1997).

  3. A. Horowitz, “Disambiguating the ‘Guilty Look.’”

  4. J. van Lawick-Goodall and H. van Lawick, In the Shadow of Man (New York: Houghton-Mifflin, 1971).

  5. P. Miller, “Crusading for Chimps and Humans,” National Geographic website, December 1995, http://s.ngm.com/1995/12/jane-goodall/goodall-text/1.

  Chapter 6

  1. A. Miklosi, Dog Behaviour, Evolution, and Cognition (Oxford: Oxford University Press, 2014).

  2. M. Zeder, “Domestication and Early Agriculture in the Mediterranean Basin: Origins, Diffusion, and Impact,” Proceedings of the National Academy of Sciences 15 (2008): 11587–11604; “Domestication Timeline,” American Museum of Natural History website, http://www.amnh.org/exhibitions/past-exhibitions/horse/domesticating-horses/domestication-timeline.

  3. M. Deer, “From the Cave to the Kennel,” Wall Street Journal website, October 29, 2011, http://www.wsj.com/articles/SB10001424052970203554104577001843790269560.

  4. M. Germonpre et al., “Fossil Dogs and Wolves from Palaeolithic Sites in Belgium, the Ukraine and Russia: Osteometry, Ancient DNA and Stable Isotopes,” Journal of Archaeological Science 36 (2009): 473–490.

  5. E. Axelsson et al., “The Genomic Signature of Dog Domestication Reveals Adaptation to a Starch-Rich Diet,” Nature 495 (2013): 360–364.

  6. R. Bridges, “Neuroendocrine Regulation of Maternal Behavior,” Frontiers in Neuroendocrinology 36 (2015): 178–196; R. Feldman, “The Adaptive Human Parental Brain: Implications for Children’s Social Development,” Trends in Neurosciences 38 (2015): 387–399; J. Rilling and L. Young, “The Biology of Mammalian Parenting and Its Effect on Offspring Social Development,” Science 345 (2014): 771–776.

  7. S. Kim et al., “Maternal Oxytocin Response Predicts Mother-to-Infant Gaze,” Brain Research 1580 (2014):133–142; S. Dickstein
et al., “Social Referencing and the Security of Attachment,” Infant Behavior & Development 7 (1984): 507–516.

  8. J. Odendaal and R. Meintjes, “Neurophysiological Correlates of Affiliative Behaviour between Humans and Dogs,” Veterinary Journal 165 (2003): 296–301; S. Mitsui et al., “Urinary Oxytocin as a Noninvasive Biomarker of Positive Emotion in Dogs,” Hormones and Behavior 60 (2011): 239–243.

  9. M. Nagasawa et al., “Oxytocin-Gaze Positive Loop and the Coevolution of Human-Dog Bonds”; M. Nagasawa et al., “Dog’s Gaze at Its Owner Increases Owner’s Urinary Oxytocin during Social Interaction,” Hormones and Behavior 55 (2009): 434–441.

  10. The name serotonin was not adopted until later.