Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication

Dogs have an unusual ability for reading human communicative gestures (e.g., pointing) in comparison to either nonhuman primates (including chimpanzees) or wolves [1-8]. Although this unusual communicative ability seems to have evolved during domestication [6, 8], it is unclear whether this evolution occurred as a result of direct selection for this ability, as previously hypothesized [8], or as a correlated by-product of selection against fear and aggression toward humans [9]-as is the case with a number of morphological and physiological changes associated with domestication [11-18]. We show here that fox kits from an experimental population selectively bred over 45 years to approach humans fearlessly and nonaggressively (i.e., experimentally domesticated) are not only as skillful as dog puppies in using human gestures but are also more skilled than fox kits from a second, control population not bred for tame behavior (critically, neither population of foxes was ever bred or tested for their ability to use human gestures) [11, 12]. These results suggest that sociocognitive evolution has occurred in the experimental foxes, and possibly domestic dogs, as a correlated by-product of selection on systems mediating fear and aggression, and it is likely the observed social cognitive evolution did not require direct selection for improved social cognitive ability.