A Foxy View of Human Beauty: Implications of the Farm Fox Experiment for Understanding the Origins of Structural and Experiential Aspects of Facial Attractiveness

I. E. Elia
The Quarterly Review of Biology
Vol. 88, No. 3 (September 2013), pp. 163-183
DOI: 10.1086/671486
Stable URL: http://www.jstor.org/stable/10.1086/671486
Page Count: 21
  • Download PDF
  • Cite this Item

You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:


Log in to your personal account or through your institution.

A Foxy View of Human Beauty: Implications of the Farm Fox Experiment for Understanding the Origins of Structural and Experiential Aspects of Facial Attractiveness
We're having trouble loading this content. Download PDF instead.


AbstractWithin 20 years, experimental selection of quantified “not too aggressive, not too fearful” behavior to human approach was shown in silver foxes (Vulpes vulpes) to produce a neotenic package of traits in adults: ability to seek, induce, and sustain contact (called friendly or rapport behavior); relatively short limbs and foreshortened skull/face; and light pigmentation areas. Earlier sexual maturation, prolonged receptivity, and larger litters were also noted. The increased estradiol supporting these changes was apparently also responsible for faster skeletal maturation, including earlier fusion of the basicranium causing tooth crowding, but also paedomorphic craniofacial proportions that we find attractive in our own and other species. In this paper, these important findings of the farm fox experiment are juxtaposed with insights from social psychology, physical anthropology, and neuroscience about facial beauty and reaction to it. Since many unrelated species show some or all of the neotenic package or domestication profile when they have achieved rapport past the juvenile stage, craniofacial proportions considered attractive are discussed as genetically and hormonally linked to the evolution of rapport—social contact, trust, and cooperation—whether by natural, intuitive, intentional, or mixed paths of selection.

Notes and References

This item contains 104 references.

  • ['Bakalar N. 2005. Ugly children may get parental short shrift. The New York Times 3 May. http://www.nytimes.com/2005/05/03/health/03ugly.html?_r=0.']
  • ['Barden R. C., Ford M. E., Jensen A. G., Rogers-Salyer M., Salyer K. E. 1989. Effects of craniofacial deformity in infancy and the quality of mother-infant interactions. Child Development 60:819–824.']
  • ['Baumgartner T., Heinrichs M., Vonlanthen A., Fischbacher U., Fehr E. 2008. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58:639–650.']
  • ['Belyaev D. 1979. Destabilizing selection as a factor in domestication. Journal of Heredity 70:301–308.']
  • ['Berry D. S. 2000. Attractiveness, attraction, and sexual selection: evolutionary perspectives on the form and function of physical attractiveness. Advances in Experimental Social Psychology 32:273–342.']
  • ['Berscheid E., Dion K., Walster E., Walster W. G. 1971. Physical attractiveness and dating choice: a test of the matching hypothesis. Journal of Experimental Social Psychology 7:173–189.']
  • ['Brazelton T. B., Nugent J. K. 2011. The Neonatal Behavioral Assessment Scale. Fourth edition. London: Mac Keith Press.']
  • ['Bull R., Rumsey N. 1988. The Social Psychology of Facial Appearance. New York: Springer-Verlag.']
  • ['Buss D. M. 1989. Sex differences in human mate preferences: evolutionary hypotheses tested in 37 cultures. Behavioral and Brain Sciences 12:1–14.']
  • ['Ciochon R. L., Nisbett R. A., Corruccini R. S. 1997. Dietary consistency and craniofacial development related to masticatory function in minipigs. Journal of Craniofacial Genetics and Developmental Biology 17:96–102.']
  • ['Darwin C. 1871. The Descent of Man and Selection in Relation to Sex. London: John Murray.']
  • ['Darwin C. (1871) 2010. The Descent of Man. Abridged, with an introduction by Michael T. Ghiselin. New York: Dover Publications.']
  • ['De Vriendt-Goldman C., Durieux M.-P. 2011. The inter-relationship between examiner, infant and parents in the use of the NBAS. Pages 109–114 in The Neonatal Behavioral Assessment Scale, edited by T. B. Brazelton and J. K. Nugent. London: Mac Keith Press.']
  • ['de Waal F. B. M., Lanting F. 1997. Bonobo: The Forgotten Ape. Berkeley (California): University of California Press.']
  • ['Devor E. J. 1987. Transmission of human craniofacial dimensions. Journal of Craniofacial Genetics and Developmental Biology 7:95–106.']
  • ['Dillon N. 2004. Heterochromatin structure and function. Biology of the Cell 96:631–637.']
  • ['Dion K., Berscheid E., Walster E. 1972. What is beautiful is good. Journal of Personality and Social Psychology 24:285–290.']
  • ['Eagly A. H., Ashmore R. D., Makhijani M. G., Longo L. C. 1991. What is beautiful is good, but … : a meta-analytic review of research on the physical attractiveness stereotype. Psychological Bulletin 110:109–128.']
  • ['Feingold A. 1992. Good-looking people are not what we think. Psychological Bulletin 111:304–341.']
  • ['Ferrari P. F., Visalberghi E., Paukner A., Fogassi L., Ruggiero A., Suomi S. J. 2006. Neonatal imitation in Rhesus macaques. PLoS Biology 4:e302.']
  • ['Field T. M., Vega-Lahr N. 1984. Early interactions between infants with cranio-facial anomalies and their mothers. Infant Behavior and Development 7:527–530.']
  • ['Fisher A. 1987. Africa Adorned. New York: Abrams.']
  • ['Fonagy P., Gergely G., Target M. 2007. The parent-infant dyad and the construction of the subjective self. Journal of Child Psychology and Psychiatry 48:288–328.']
  • ['Foster E. A., Franks D. W., Mazzi S., Darden S. K., Balcomb K. C., Ford J. K. B., Croft D. P. 2012. Adaptive prolonged postreproductive life span in killer whales. Science 337:1313.']
  • ['Gogoleva S. S., Volodin I. A., Volodina E. V., Kharlamova A. V., Trut L. N. 2009. Kind granddaughters of angry grandmothers: the effect of domestication on vocalization in cross-bred silver foxes. Behavioral Processes 81:369–375.']
  • ['Gould S. J. 1979. Mickey Mouse meets Konrad Lorenz. Natural History 88:30–36.']
  • ['Gould S. J. 1982. Change in developmental timing as a mechanism of macroevolution. Pages 333–346 in Evolution and Development: Report of the Dahlem Workshop on Evolution and Development, May 1981, Volume 22, edited by J. T. Bonner. Berlin (Germany): Springer-Verlag.']
  • ['Gross A. E., Crofton C. 1977. What is good is beautiful. Sociometry 40:85–90.']
  • ['Halberstadt J., Rhodes G. 2000. The attractiveness of nonface averages: implications for an evolutionary explanation of the attractiveness of average faces. Psychological Science 11:285–289.']
  • ['Hare B., Tomasello M. 2005. Human-like social skills in dogs? Trends in Cognitive Sciences 9:439–444.']
  • ['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. Current Biology 15:226–230.']
  • ['Harrell A. 2005. Are unattractive kids loved less? Express News University of Alberta 8 April. http://www.archives.expressnews.ualberta.ca/article/2005/04/6524.html.']
  • ['Hershkovitz P. 1977. Living New World Monkeys (Platyrrhini). Chicago (Illinois): University of Chicago Press.']
  • ['Hewlett B. S. 1988. Sexual selection and paternal investment among Aka pygmies. Pages 263–276 in Human Reproductive Behaviour: A Darwinian Perspective, edited by L. Betzig, M. Borgerhoff Mulder, and P. Turke. Cambridge (United Kingdom): Cambridge University Press.']
  • ['Heyning J. E., Dahlheim M. E. 1988. Orcinus orca. Mammalian Species 304:1–9.']
  • ['Holmes S. J., Hatch C. E. 1938. Personal appearance as related to scholastic records and marriage selection in college women. Human Biology 10:65–76.']
  • ["Jacobson M. B. 1981. Effects of victim's and defendant's physical attractiveness on subjects' judgments in a rape case. Sex Roles 7:247–255."]
  • ['Jantz R. L., Jantz L. M. 2012. Cranial Change in America: 1815 to 1980. Presented at 81st Annual Meeting of the American Association of Physical Anthropologists, Portland, Oregon.']
  • ['Jensen P. 2006. Domestication—from behaviour to genes and back again. Applied Animal Behaviour Science 97:3–15.']
  • ['Johnston V. S., Franklin M. 1993. Is beauty in the eye of the beholder? Ethology and Sociobiology 14:183–199.']
  • ['Johnston V. S., Oliver-Rodriguez J. C. 1997. Facial beauty and the late positive component of event-related potentials. Journal of Sex Research 34:188–198.']
  • ['Jokela M. 2009. Physical attractiveness and reproductive success in humans: evidence from the late 20th century United States. Evolution and Human Behavior 30:342–350.']
  • ['Jones D. 1996. Physical Attractiveness and the Theory of Sexual Selection: Results From Five Populations. Ann Arbor (Michigan): Museum of Anthropology, University of Michigan.']
  • ['Jones D., Hill K. 1993. Criteria of facial attractiveness in five populations. Human Nature 4:271–296.']
  • ['Jones D., Brace C. L., Jankowiak W., Laland K. N., Musselman L. E., Langlois J. H., Roggman L. A., Perusse D., Schweder B., Symons D. 1995. Sexual selection, physical attractiveness, and facial neoteny: cross-cultural evidence and implications. Current Anthopology 36:723–748.']
  • ['Kalick S. M., Zebrowitz L. A., Langlois J. H., Johnson R. M. 1998. Does human facial attractiveness honestly advertise health? Longitudinal data on an evolutionary question. Psychological Science 9:8–13.']
  • ['Kirwan J. 1999. Beauty. Manchester (United Kingdom): Manchester University Press.']
  • ['Kukekova A. V., Trut L. N., Chase K., Shepeleva D. V., Vladimirova A. V., Kharlamova A. V., Oskina I. N., Stepika A., Klebanov S., Erb H. N., Acland G. M. 2008. Measurement of segregating behaviors in experimental silver fox pedigrees. Behavior Genetics 38:185–194.']
  • ['Laitman J. T., Heimbuch R. C. 1984. A measure of basicranial flexion in Pan paniscus, the pygmy chimpanzee. Pages 49–63 in The Pygmy Chimpanzee: Evolutionary Biology and Behavior, edited by R. L. Susman. New York: Plenum Press.']
  • ['Laland K. N. 1994. On the evolutionary consequences of sexual imprinting. Evolution 48:477–489.']
  • ['Langlois J. H., Roggman L. A., Casey R. J., Ritter J. M., Rieser-Danner L. A., Jenkins V. Y. 1987. Infant preferences for attractive faces: rudiments of a stereotype? Developmental Psychology 23:363–369.']
  • ["Langlois J. H., Roggman L. A., Rieser-Danner L. A. 1990. Infants' differential social responses to attractive and unattractive faces. Developmental Psychology 26:153–159."]
  • ['Langlois J. H., Ritter J. M., Roggman L. A., Vaughn L. S. 1991. Facial diversity and infant preferences for attractive faces. Developmental Psychology 27:79–84.']
  • ['Langlois J. H., Ritter J. M., Casey R. J., Sawin D. B. 1995. Infant attractiveness predicts maternal behavior and attitudes. Developmental Psychology 31:464–472.']
  • ['Langlois J. H., Kalakanis L., Rubenstein A. J., Larson A., Hallam M., Smoot M. 2000. Maxims or myths of beauty? A meta-analytic and theoretical review. Psychological Bulletin 126:390–423.']
  • ['Lauder J. M. 1988. Neurotransmitters as morphogens. Progress in Brain Research 73:365–387.']
  • ['Leach H. M. 2003. Human domestication reconsidered. Current Anthropology 44:349–368.']
  • ['Leutenegger W. 1980. Monogamy in callitrichids: a consequence of dwarfism? International Journal of Primatology 1:95–98.']
  • ['Lorenz K. 1971. Studies in Animal and Human Behaviour: II. Cambridge (Massachusetts): Harvard University Press.']
  • ['Malatesta C. Z., Culver C., Tesman J. R., Shepard B. 1989. The Development of Emotion Expression During the First Two Years of Life. Chicago (Illinois): University of Chicago Press.']
  • ['Matsuzawa T. 2012. We are 98.77% Chimpanzee. Kyoto University Primate Research Institute. http://www.kyoto-u.ac.jp/en/research/forefront/message/rakuyu11_a.htm.']
  • ['McCabe V. 1984. Abstract perceptual information for age level: a risk factor for maltreatment? Child Development 55:267–276.']
  • ['McCabe V. 1988. Facial proportions, perceived age, and caregiving. Pages 89–95 in Social and Applied Aspects of Perceiving Faces, edited by T. R. Alley. Hillsdale (New Jersey): Lawrence Erlbaum Associates.']
  • ['McCall Smith A. 2003. Morality for Beautiful Girls. London: Abacus.']
  • ['Møller A. P., Thornhill R. 1998. Bilateral symmetry and sexual selection: a meta-analysis. American Naturalist 151:174–192.']
  • ['Montagu A. 1981. Growing Young. New York: McGraw-Hill.']
  • ['Morey D. F. 1992. Size, shape and development in the evolution of the domestic dog. Journal of Archaeological Science 19:181–204.']
  • ['Nelson E. E., Panksepp J. 1998. Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine. Neuroscience and Biobehavioral Reviews 22:437–452.']
  • ['Nida S. A., Williams J. E. 1977. Sex-stereotyped traits, physical attractiveness, and interpersonal attraction. Psychological Reports 41:1311–1322.']
  • ['Okada D., Bingham P. M. 2008. Human uniqueness-self-interest and social cooperation. Journal of Theoretical Biology 253:261–270.']
  • ['Panksepp J., Panksepp J. B. 2000. The seven sins of evolutionary psychology. Evolution and Cognition 6:108–131.']
  • ['Patzer G. L. 1985. The Physical Attractiveness Phenomena. New York: Plenum Press.']
  • ['Penton-Voak I. S., Perrett D. I. 2000. Female preferences for male faces changes cyclically: further evidence. Evolution and Human Behavior 21:39–48.']
  • ['Penton-Voak I. S., Chen J. Y. 2004. High salivary testosterone is linked to masculine male facial appearance in humans. Evolution and Human Behavior 25:229–241.']
  • ['Perrett D. I., May K. A., Yoshikawa S. 1994. Facial shape and judgements of female attractiveness. Nature 368:239–242.']
  • ['Perrett D. I., Lee K. J., Penton-Voak I., Rowland D., Yoshikawa S., Burt D. M., Henzi S. P., Castles D. L., Akamatsu S. 1998. Effects of sexual dimorphism on facial attractiveness. Nature 394:884–887.']
  • ['Pitman R. L., Durban J. W. 2011. Cooperative hunting behavior, prey selectivity and prey handling by pack ice killer whales (Orcinus orca), type B, in Antarctic Peninsular waters. Marine Mammal Science 28:16–36.']
  • ['Quinn P. C., Kelly D. J., Lee K., Pascalis O., Slater A. M. 2008. Preference for attractive faces in human infants extends beyond conspecifics. Developmental Science 11:76–83.']
  • ['Rhodes G., Tremewan T. 1996. Averagness, exaggeration, and facial attractiveness. Psycological Science 7:105–110.']
  • ['Rhodes G., Zebrowitz L. A., Clark A., Kalick S. M., Hightower A., McKay R. 2001. Do facial averageness and symmetry signal health? Evolution and Human Behavior 22:31–46.']
  • ['Ridley M. 1997. The Origins of Virtue: Human Instincts and the Evolution of Cooperation. New York: Viking.']
  • ['Riesenfeld A. 1974. Endocrine and biomechanical control of craniofacial growth: an experimental study. Human Biology 46:531–572.']
  • ['Roberts S. C., Little A. C., Morris Gosling L., Perrett D. I., Carter V., Jones B. C., Penton-Voak I., Petrie M. 2005. MHC-heterozygosity and human facial attractiveness. Evolution and Human Behavior 26:213–226.']
  • ['Ross A. H., Ubelaker D. H., Kimmerle E. H. 2011. Implications of dimorphism, population variation, and secular change in estimating population affinity in the Iberian Peninsula. Forensic Science International 206:214.e1–214.e5.']
  • ['Saetre P., Lindberg J., Leonard J. A., Olsson K., Pettersson U., Ellegren H., Bergström T. F., Vilà C., Jazin E. 2004. From wild wolf to domestic dog: gene expression changes in the brain. Molecular Brain Research 126:198–206.']
  • ['Shackelford T. K., Larsen R. J. 1997. Facial asymmetry as an indicator of psychological, emotional, and physiological distress. Journal of Personality and Social Psychology 72:456–466.']
  • ['Shirley N. R., Jantz R. L. 2011. Spheno-occipital synchondrosis fusion in modern Americans. Journal of Forensic Sciences 56:580–585.']
  • ['Smith M. J., Perrett D. I., Jones B. C., Cornwell R. E., Moore F. R., Feinberg D. R., Boothroyd L. G., Durrani S. J., Stirrat M. R., Whiten S., Pitman R. M., Hiller S. G. 2006. Facial appearance is a cue to oestrogen levels in women. Proceedings of the Royal Society B: Biological Sciences 273:135–140.']
  • ['Soler C., Núñez M., Gutiérrez R., Núñez J., Medina P., Sancho M., Álvarez J., Núñez A. 2003. Facial attractiveness in men provides clues to semen quality. Evolution and Human Behavior 24:199–207.']
  • ['Steiper M. E., Young N. M. 2006. Primate molecular divergence dates. Molecular Phylogenetics 41:384–394.']
  • ["Strand Viđarsdóttir U., O'Higgins P. 2003. Developmental variation in the facial skeleton of anatomically modern Homo sapiens. Pages 114–143 in Patterns of Growth and Development in the Genus Homo, edited by J. L. Thompson, G. E. Krovitz, and A. J. Nelson. Cambridge (United Kingdom): Cambridge University Press."]
  • ['Thornhill R., Gangestad S. W. 1994. Human fluctuating asymmetry and sexual behavior. Psychological Science 5:297–302.']
  • ['Thornhill R., Gangestad S. W., Miller R., Scheyd G., McCullough J. K., Franklin M. 2003. Major histocompatibility genes, symmetry, and body scent attractiveness in men and women. Behavioral Ecology 414:668–678.']
  • ['Trut L. 1999. Early canid domestication: the farm-fox experiment. American Scientist 87:160–169.']
  • ['Trut L. 2001. Experimental studies of early canid domestication. Pages 15–41 in The Genetics of the Dog, edited by A. Ruvinsky and J. Sampson. Wallingford (United Kingdom): CABI Publishing.']
  • ['Trut L., Oskina I., Kharlamova A. 2009. Animal evolution during domestication: the domesticated fox as a model. Bioessays 31:349–360.']
  • ['Tsukiura T., Cabeza R. 2011. Shared brain activity for aesthetic and moral judgments: implications for the beauty-is-good stereotype. Social Cognitive and Affective Neuroscience 6:138–148.']
  • ['Vilà C., Savolainen P., Maldonado J. E., Amorim I. R., Rice J. E., Honeycutt R. L., Crandall K. A., Lundeberg J., Wayne R. K. 1997. Multiple and ancient origins of the domestic dog. Science 276:1687–1689.']
  • ['Visser I. 2011. The Woman Who Swims with Killer Whales. Animal Planet, edited by S. Greenwood. New Zealand: BBC Natural World.']
  • ['Walster E., Aronson V., Abrahams D., Rottman L. 1966. Importance of physical attractiveness in dating behavior. Journal of Personality and Social Psychology 4:508–516.']
  • ["Zakin D. F. 1983. Physical attractiveness, sociability, athletic ability, and children's preference for their peers. Journal of Psychology: Interdisciplinary and Applied 115:117–122."]
  • ['Zebrowitz L. A., Hall J. A., Murphy N. A., Rhodes G. 2002. Looking smart and looking good: facial cues to intelligence and their origins. Personality and Social Psychology Bulletin 28:238–249.']
  • ['Zeder M. A. 2006. Archaeological approaches to documenting animal domestication. Pages 171–180 in Documenting Domestication: New Genetic and Archaeological Paradigms, edited by M. A. Zeder, D. G. Bradley, E. Emshwiller, and B. D. Smith. Berkeley (California): University of California Press.']
  • ['Zeuner F. E. 1963. A History of Domesticated Animals. London: Hutchinson.']