Illuminating the Genetic Foundation and Cost of Horse Domestication with Ancient DNA

In contrast with many other domesticated animals, no suitable outgroup exists for examining the genetic basis of the 5.5k year history of horse domestication; the only wild relatives of the domestic horse, the Przewalski's horses, nearly went extinct, and a large portion of their genetic variation was lost. The other members of the genus Equus, on the other hand, split from horses ca. 4-4.5M years ago. We therefore sequenced DNA from two ancient horses excavated in Taymyr, Russia, both of which predated the earliest archeological evidence of horse domestication. By contrasting these to 5 domestic breeds and a Przewalski’s horse, we discovered evidence of genetic structure within Eurasia in the late Pleistocene, and found that the ancient population to which these individuals belonged contributed significantly to the genetic variation of domesticated horses, but not to the Przewalski’s horses. We found that horse domestication was associated with increased levels of inbreeding and an accumulation of deleterious mutations. This is similar to what has been observed for dogs, rice, and tomatoes, which has been termed the ‘cost of domestication’, and is attributed to a relaxation of purifying selection. Using four different computational methods, we furthermore detected evidence for positive selection in a set of 125 genes, including genes involved in a suite of behavioral, neurological and physical characteristics. Our results demonstrates the power of ancient DNA to reveal the complex genetic changes underlying the process of domestication, and offers a model for unraveling the recent history of modern animals, domestic or wild.