How to Tame a Fox (and Build a Dog)

by Lee Alan Dugatkin

  11. G. Z. Wang et al., “The Genomics of Selection in Dogs and the Parallel Evolution between Dogs and Humans,” Nature Communications 4 (2013), DOI:10.1038/ncomms2814.

  12. Descartes in a letter dated January 29, 1640; see Descartes’s View of the Pineal Gland in “The Stanford Encyclopedia of Philosophy,” http://plato.stanford.edu/entries/pineal-gland/#2.

  13. Larissa Kolesnikova, phone interview with authors.

  14. Larissa Kolesnikova, phone interview with authors.

  15. L. Kolesnikova et al., “Changes in Morphology of Silver Fox Pineal Gland at Domestication,” Zhurnal Obshchei Biologii 49 (1988): 487–492; L. Kolesnikova et al., “Circadian Dynamics of Biochemical Activity in the Epiphysis of Silver-Black Foxes,” Izvestiya Akademii Nauk Seriya Biologicheskaya (May-June 1997): 380–384; L. Kolesnikova, “Characteristics of the Circadian Rhythm of Pineal Gland Biosynthetic Activity in Relatively Wild and Domesticated Silver Foxes,” Genetika 33 (1997): 1144–1148; L. Kolesnikova et al., “The Melatonin Content of the Tissues of Relatively Wild and Domesticated Silver Foxes Vulpes fulvus,” Zhurnal Evoliutsionnoĭ Biokhimii i Fiziologii 29 (1993): 482–496.

  16. John Scandalious, phone interview with authors.

  17. N. Tsitsin, “Presidential Address: The Present State and Prospects of Genetics,” in XIV International Congress of Genetics, ed. D. K. Belyaev, vol. 1 (Moscow: MIR Publishers, 1978), 20.

  18. Penelope Scandalious’s journal, personal communication with authors.

  19. M. King and A. Wilson, “Evolution in Two Levels in Humans and Chimpanzees,” Science 188 (1975): 107–116; when it came to gene expression and mutation, they were referring to changes associated with point mutations.

  20. Aubrey Manning, Skype interview with authors.

  21. Aubrey Manning, Skype interview with authors.

  Chapter 7

  1. L. Mech and L. Boitani, eds., Wolves: Behavior, Ecology, and Conservation (Chicago: University of Chicago Press, 2007).

  2. J. Goodall to W. Schleidt, as cited in “Co-evolution of Humans and Canids,” Evolution and Cognition 9 (2003): 57–72.

  3. L. S. B. Leakey, “A New Fossil from Olduvai,” Nature 184 (1959): 491–494.

  4. A multiregional theory of human evolution that is still championed by some today, with heated debate between them and the dominant “Out of Africa” camp of the research community. The multiregional hypothesis posits that Homo erectus left Africa and colonized the Old World a single time, nearly 2 million years ago, then H. erectus populations diverged from one another, then over the past 2 million years, these loosely associated populations together evolved into modern humans. The out-of-Africa hypothesis posits that hominins experienced two major waves out of Africa, colonizing first as Homo erectus about 2 million years ago, and then as Homo sapiens approximately 100,000 years ago. Modern Homo sapiens emerged in Africa, and in the second wave of colonization, the pre-modern hominins of Europe and Asia, such as Homo erectus and Homo neanderthalensis, were replaced by Homo sapiens. Modified from C. Bergstrom and L. Dugatkin, Evolution (New York: W. W. Norton, 2012).

  5. Later revised to 3.2 million years ago.

  6. D. K. Belyaev, “On Some Factors in the Evolution of Hominids,” Voprosy Filosofii 8 (1981): 69–77; D. K. Belyaev, “Genetics, Society and Personality,” in Genetics: New Frontiers: Proceedings of the XV International Congress of Genetics, ed. V. Chopra (New York: Oxford University Press, 1984), 379–386.

  7. But now is dated between 1.5 and 2 million years ago.

  8. D. K. Belyaev, “On Some Factors in the Evolution of Hominids.”

  9. D. K. Belyaev, “Genetics, Society and Personality.”

  10. The notion of human self-domestication had been mentioned on occasion before Belyaev, but not in a systematic or detailed manner. W. Bagehot, Physics and Politics or Thoughts on the Application of the Principles of “Natural Selection” and “Inheritance” to Political Society (London: Kegan Paul, Trench and Trubner, 1905). In addition, subsequently, self-domestication of humans has been used to describe a process that is quite different from what Belyaev was discussing: P. Wilson, The Domestication of the Human Species (New Haven: Yale University Press, 1991).

  11. B. Hare, V. Wobber, and R. Wrangham, “The Self-Domestication Hypothesis: Evolution of Bonobo Psychology Is Due to Selection against Aggression,” Animal Behaviour 83 (2012): 573–585. Related papers include B. Hare et al., “Tolerance Allows Bonobos to Outperform Chimpanzees on a Cooperative Task,” Current Biology 17 (2007): 619–623; V. Wobber, R. Wrangham, and B. Hare, “Bonobos Exhibit Delayed Development of Social Behavior and Cognition Relative to Chimpanzees,” Current Biology 20 (2010): 226–230; V. Wobber, R. Wrangham, and B. Hare, “Application of the Heterochrony Framework to the Study of Behavior and Cognition,” Communicative and Integrative Biology 3 (2010): 337–339; R. Cieri et al., “Craniofacial Feminization, Social Tolerance, and the Origins of Behavioral Modernity,” Current Anthropology 55 (2014): 419–443.

  12. D. Quammen, “The Left Bank Ape,” National Geographic website, March 2013, http://ngm.nationalgeographic.com/2013/03/125-bonobos/quammen-text.

  13. For a map of what this looks like see: http://mappery.com/map-of/African-Great-Apes-Habitat-Range-Map.

  14. J. Rilling et al., “Differences between Chimpanzees and Bonobos in Neural Systems Supporting Social Cognition,” Social Cognitive and Affective Neuroscience 7 (2012): 369–379.

  15. There is also some evidence that changes associated with self-domestication in bonobos are driven by changes in the expression and timing of regulatory genes associated with the stress hormone system, just as Belyaev thought. The exact role of gene regulation across domesticated species is still unclear: F. Albert et al., “A Comparison of Brain Gene Expression Levels in Domesticated and Wild Animals,” PLOS Genetics 8 (2012); Hare et al., in “The Self-Domestication Hypothesis” note: “An alternative evolutionary scenario to the self-domestication hypothesis is that the observed behavioural differences are due to selection for severe aggression in chimpanzees from a bonobo-like ancestor. Equally, both Pan species could in theory be highly derived from a common ancestor that possessed a mosaic of traits seen in both species. The ontogeny of the bonobo skull argues against these ideas. During growth, chimpanzee skulls follow closely the ontogenetic pattern of their more distant relative, gorillas, Gorilla gorilla . . . , whereas the bonobo cranium remains small and juvenilized compared not only to chimpanzees but also to all other great apes, including australopithecines.”

  16. P. Borodin, “Understanding the Person,” in Dmitry Konstantinovich Belyaev, 2002.

  17. Nikolai Belyaev, Skype interview with authors.

  18. Misha Belyaev, interview with authors.

  19. Misha Belyaev, interview with authors.

  20. Kogan in Dmitry Konstantinovich Belyaev, 2002.

  21. D. Belyaev, “I Believe in the Goodness of Human Nature: Final Interview with the Late D. K. Belyaev,” Voprosy Filosofii 8 (1986): 93–94.

  Chapter 8

  1. A. Miklosi, Dog Behavior, Evolution, and Cognition.

  2. By reducing activity of the adrenal cortex.

  3. I. Plyusnina, I. Oskina, and L. Trut, “An Analysis of Fear and Aggression during Early Development of Behavior in Silver Foxes (Vulpes vulpes),” Applied Animal Behaviour Science 32 (1991): 253–268.

  4. N. Popova, N. Voitenko, and L. Trut, “Change in Serotonin and 5-oxyindoleacetic Acid Content in Brain in Selection of Silver Foxes according to Behavior,” Doklady Akademii Nauk SSSR 223 (1975): 1498–1500; N. Popova et al., “Genetics and Phenogenetics of Hormonal Characteristics in Animals 7. Relationships between Brain Serotonin and Hypothalamo-pituitary-adrenal Axis in Emotional Stress in Domesticated and Non-domesticated Silver Foxes,” Genetika 16 (1980): 1865–1870.

  5. More precisely, they injected foxes with L-tryptophan, a chemical precursor to serotonin.

  6. A. Chiodo and M. Owyang, “A Case Study of a Currency Crisis: The Russian Default of 1998,” Federal Reserve Bank of
St. Louis Review (November/December 2002): 7–18.

  7. L. Trut, “Early Canid Domestication,” 168.

  8. Letter from John McGrew to Lyudmila Trut.

  9. Letter from Charles and Karen Townsend to Lyudmila Trut.

  10. New York Times, February 23, 1997.

  11. A nice timeline of these events can be found at the National Human Genome Research Institute website: http://unlockinglifescode.org/timeline?tid=4.

  Chapter 9

  1. C. Rutz and J. H. St. Clair, “The Evolutionary Origins and Ecological Context of Tool Use in New Caledonian Crows,” Behavioural Process 89 (2013): 153–165.

  2. B. Klump et al., “Context-Dependent ‘Safekeeping’ of Foraging Tools in New Caledonian Crows,” Proceedings of the Royal Society B 282 (2015), DOI:10.1098/rspb.2015.0278.

  3. V. Pravosudovand and T. C. Roth, “Cognitive Ecology of Food Hoarding: The Evolution of Spatial Memory and the Hippocampus,” Annual Review of Ecology, Evolution, and Systematics 44 (2013): 173–193.

  4. J. Dally et al., “Food-Caching Western Scrub-Jays Keep Track of Who Was Watching When,” Science 312 (2006): 1662–1665.

  5. M. Wittlinger et al., “The Ant Odometer: Stepping on Stilts and Stumps,” Science 312 (2006): 1965–1967; M. Wittlinger et al., “The Desert Ant Odometer: A Stride Integrator that Accounts for Stride Length and Walking Speed,” Journal of Experimental Biology 210 (2007): 198–207.

  6. B. Hare et al., “The Domestication of Social Cognition in Dogs,” Science 298 (202):1634–1636. Hare did his dissertation work as a student of Richard Wrangham. His PhD dissertation was entitled “Using Comparative Studies of Primate and Canid Social Cognition to Model Our Miocene Minds” (Harvard University, 2004).

  7. S. Zuckerman, The Social Life of Monkeys and Apes (New York: Harcourt Brace, 1932).

  8. G. Schino, “Grooming and Agonistic Support: A Meta-analysis of Primate Reciprocal Altruism,” Behavioral Ecology 18 (2007): 115–120; E. Stammbach, “Group Responses to Specially Skilled Individuals in a Macaca fascicularis group,” Behaviour 107 (1988): 687–705; F. de Waal, “Food Sharing and Reciprocal Obligations among Chimpanzees,” Human Evolution 18 (1989): 433–459.

  9. A. Harcourt and F. de Waal, eds., Coalitions and Alliances in Humans and Other Animals (Oxford: Oxford University, 1992).

  10. C. Packer, “Reciprocal Altruism in Papio anubis,” Nature 265 (1977): 441–443.

  11. D. Cheney and R. Seyfarth, How Monkeys See the World (Chicago: University of Chicago, 1990).

  12. Hare’s own work on this subject includes Hare et al., “The Domestication of Social Cognition”; M. Tomasello, B. Hare, and T. Fogleman, “The Ontogeny of Gaze Following in Chimpanzees, Pan troglodytes, and Rhesus Macaques, Macaca mulatta,” Animal Behaviour 61 (2001): 335–343; S. Itakura et al., “Chimpanzee Use of Human and Conspecific Social Cues to Locate Hidden Food,” Developmental Science 2 (1999): 448–456; M. Tomasello, B. Hare, and B. Agnetta, “Chimpanzees, Pan troglodytes, Follow Gaze Direction Geometrically,” Animal Behaviour 58 (1999): 769–777; B. Hare and M. Tomasello, “Domestic Dogs (Canis familiaris) Use Human and Conspecific Social Cues to Locate Hidden Food,” Journal of Comparative Psychology 113 (1999): 173–177; M. Tomasello, J. Call, and B. Hare, “Five Primate Species Follow the Visual Gaze of Conspecifics,” Animal Behaviour 55 (1998): 1063–1069.

  13. A. Miklosi et al., “Use of Experimenter-Given Cues in Dogs,” Animal Cognition 1 (1998): 113–121; A. Miklosi et al., “Intentional Behaviour in Dog-Human Communication: An Experimental Analysis of Showing Behaviour in the Dog,” Animal Cognition 3 (2000): 159–166; K. Soproni et al., “Dogs’ (Canis familiaris) Responsiveness to Human Pointing Gestures,” Journal of Comparative Psychology 116 (2002): 27–34.

  14. There is an ongoing debate about wolves’ ability on such tests: A. Miklosi et al., “A Simple Reason for a Big Difference”; A. Miklosi and K. Soproni, “A Comparative Analysis of Animals’ Understanding of the Human Pointing Gesture,” Animal Cognition 9 (2006): 81–93; M. Udell et al., “Wolves Outperform Dogs in Following Human Social Cues,” Animal Behaviour 76 (2008): 1767–1773; C. Wynne, M. Udell, and K. A. Lord, “Ontogeny’s Impacts on Human-Dog Communication,” Animal Behaviour 76 (2008): E1–E4; J. Topal et al., “Differential Sensitivity to Human Communication in Dogs, Wolves, and Human Infants,” Science 325 (2009): 1269–1272; M. Gacsi et al., “Explaining Dog/Wolf Differences in Utilizing Human Pointing Gestures: Selection for Synergistic Shifts in the Development of Some Social Skills,” PLOS ONE 4 (2009), DOI.org/10.1371/journal.pone.0006584; B. Hare et al., “The Domestication Hypothesis for Dogs’ Skills with Human Communication: A Response to Udell et al. (2008) and Wynne et al. (2008),” Animal Behaviour 79 (2010): E1–E6.

  15. B. Hare, “The Domestication of Social Cognition in Dogs.”

  16. Brian Hare, Skype interview with authors.

  17. B. Hare and V. Woods, The Genius of Dogs (New York: Plume, 2013), 78–79.

  18. B. Hare et al., “Social Cognitive Evolution in Captive Foxes Is a Correlated By-product of Experimental Domestication,” Current Biology 15 (2005): 226–230.

  19. Other experiments were done to make sure that the foxes were not picking up olfactory cues from the hidden food.

  20. Brian Hare, Skype interview with authors.

  21. Forty-three tame fox pups and thirty-two control fox pups.

  22. It wasn’t just that control foxes were scared and uncomfortable near humans compared to tame foxes. At Brian’s instruction his assistant Natalie had spent extra time with control foxes before the experiment to see to that and they ran additional experiments to be certain that was not a confounding factor.

  23. Hare and Woods, 87–88.

  24. Irena Muchamedshina, interview with authors.

  25. R. Seyfarth, “Vervet Monkey Alarm Calls: Semantic Communication in a Free-Ranging Primate,” Animal Behaviour 28 (1980): 1070–1094.

  26. Volodin has studied communication in everything from cranes and ground squirrels to dogs and striped possums.

  27. Sveta Gogoleva, email interview with authors.

  28. S. Gogoleva et al., “To Bark or Not to Bark: Vocalizations by Red Foxes Selected for Tameness or Aggressiveness toward Humans,” Bioacoustics 18 (2008): 99–132.

  29. S. Gogoleva et al., “Explosive Vocal Activity for Attracting Human Attention Is Related to Domestication in Silver Fox,” Behavioural Processes 86 (2010): 216–221.

  Chapter 10

  1. They also used microsatellite markers.

  2. A. Kukekova et al., “A Marker Set for Construction of a Genetic Map of the Silver Fox (Vulpes vulpes),” Journal of Heredity 95 (2004): 185–194; A. Graphodatsky et al., “The Proto-oncogene C-KIT Maps to Canid B-Chromosomes,” Chromosome Research 13 (2005): 113–122.

  3. 320 loci. A. Kukekova et al., “A Meiotic Linkage Map of the Silver Fox, Aligned and Compared to the Canine Genome,” Genome Research 17 (2007): 387–399.

  4. They also compared what they had found to the genomic map of the dog. Here, what they learned was that the difference between the 17 chromosomes found in the silver fox, and the 39 typically found in dogs, was the result of various genetic fusion events. Most fox chromosomes were made up of chunks of more than one dog chromosome.

  5. National Institute of Mental Health, Molecular Mechanisms of Social Behavior, MH0077811, 08/01/07–07/31/11; National Institute of Mental Health, Molecular Genetics of Tame Behavior MH069688, 04/01/04–03/31/07.

  6. K. Chase et al., “Genetic Basis for Systems of Skeletal Quantitative Traits: Principal Component Analysis of the Canid Skeleton,” Proceedings of the National Academy of Sciences of the United States of America 99 (2002): 9930–9935; D. Carrier, K. Chase, and K. Lark, “Genetics of Canid Skeletal Variation: Size and Shape of the Pelvis,” Genome Research 15 (2005): 1825–1830.

  7. K. Chase et al., “Genetic Basis for Systems of Skeletal Quantitative Traits”; L. Trut et al., “Morphology and Behavior: Are They Coupled at the Genome Level?” in The Dog and Its Genome, ed. E.
A. Ostrander, U. Giger, and K. Lindblad-Toh (Woodbury, NY: Cold Spring Harbor Laboratory Press, 2005), 81–93.

  8. Using mathematical models developed by geneticists, Anna and Lyudmila constructed a very specific breeding protocol that involved mating tame and aggressive foxes with each other over the course of three generations, so that the molecular genetic analysis would have the maximum power to locate any genes associated with tame behavior; A. Kukekova et al., “Measurement of Segregating Behaviors in Experimental Silver Fox Pedigrees,” Behavior Genetics 38 (2008): 185–194.

  9. A. Kukekova et al., “Sequence Comparison of Prefrontal Cortical Brain Transcriptome from a Tame and an Aggressive Silver Fox (Vulpes vulpes),” BMC Genomics 12 (2011): 482, DOI:10.1186/1471-2164-12-482. Preliminary work done here includes J. Lindberg et al., “Selection for Tameness Modulates the Expression of Heme Related Genes in Silver Foxes,” Behavioral and Brain Functions 3 (2007), DOI:10.1186/1744-9081-3-18; J. Lindberg et al., “Selection for Tameness Has Changed Brain Gene Expression in Silver Foxes,” Current Biology 15 (2005): R915–R916.