Title

Prehistoric Genomes Reveal the Genetic Foundation and Cost of Horse Domestication

Authors

Mikkel Schubert, University of Copenhagen, Denmark
Hákon Jónsson, University of Copenhagen, Denmark
Dan Chang, University of California - Santa Cruz
Clio Der Sarkissian, University of Copenhagen, Denmark
Luca Ermini, University of Copenhagen, Denmark
Aurélien Ginolhac, University of Copenhagen, Denmark
Anders Albrechtsen, University of Copenhagen, Denmark
Isabelle Dupanloup, University of Berne, Switzerland
Adrien Foucal, University of Berne, Switzerland
Bent Petersen, Technical University of Denmark, Denmark
Matteo Fumagalli, University College London, UK
Maanasa Raghavan, University of Copenhagen, Denmark
Andaine Seguin-Orlando, University of Copenhagen, Denmark
Thorfinn S. Korneliussen, University of Copenhagen, Denmark
Amhed M. V. Velazquez, University of Copenhagen, Denmark
Jesper Stenderup, University of Copenhagen, Denmark
Cindi A. Hoover, Department of Energy Joint Genome Institute
Carl-Johan Rubin, Uppsala University, Sweden
Ahmed H. Alfarhan, King Saud University, Saudi Arabia
Saleh A. Alquraishi, King Saud University, Saudi Arabia
Khaled A. S. Al-Rasheid, King Saud University, Saudi Arabia
David E. MacHugh, University College Dublin, UK
Ted Kalbfleisch, University of Louisville
James N. Macleod, University of KentuckyFollow
Edward M. Rubin, Department of Energy Joint Genome Institute
Thomas Sicheritz-Ponten, Technical University of Denmark, Denmark
Leif Andersson, Uppsala University, Sweden
Michael Hofreiter, University of Potsdam, Germany
Tomas Marques-Bonet, Universitat Pompeu Fabra, Spain
M. Thomas P. Gilbert, University of Copenhagen, Denmark
Rasmus Nielsen, University of California - Berkeley
Laurent Excoffier, University of Berne, Switzerland
Eske Willerslev, University of Copenhagen, Denmark
Beth Shapiro, University of California - Santa Cruz
Ludovic Orlando, University of Copenhagen, Denmark

Abstract

The domestication of the horse ~ 5.5 kya and the emergence of mounted riding, chariotry, and cavalry dramatically transformed human civilization. However, the genetics underlying horse domestication are difficult to reconstruct, given the near extinction of wild horses. We therefore sequenced two ancient horse genomes from Taymyr, Russia (at 7.4- and 24.3-fold coverage), both predating the earliest archeological evidence of domestication. We compared these genomes with genomes of domesticated horses and the wild Przewalski's horse and found genetic structure within Eurasia in the Late Pleistocene, with the ancient population contributing significantly to the genetic variation of domesticated breeds. We furthermore identified a conservative set of 125 potential domestication targets using four complementary scans for genes that have undergone positive selection. One group of genes is involved in muscular and limb development, articular junctions, and the cardiac system, and may represent physiological adaptations to human utilization. A second group consists of genes with cognitive functions, including social behavior, learning capabilities, fear response, and agreeableness, which may have been key for taming horses. We also found that domestication is associated with inbreeding and an excess of deleterious mutations. This genetic load is in line with the "cost of domestication" hypothesis also reported for rice, tomatoes, and dogs, and it is generally attributed to the relaxation of purifying selection resulting from the strong demographic bottlenecks accompanying domestication. Our work demonstrates the power of ancient genomes to reconstruct the complex genetic changes that transformed wild animals into their domesticated forms, and the population context in which this process took place.

Document Type

Article

Publication Date

12-30-2014

Notes/Citation Information

Published in Proceedings of the National Academy of Sciences of the United States of America, v. 111, no. 52, p. E5661-E5669.

Digital Object Identifier (DOI)

http://dx.doi.org/10.1073/pnas.1416991111

Funding Information

This work was supported by the Danish Council for Independent Research, Natural Sciences (FNU); the Danish National Research Foundation (DNFR94); a Marie-Curie Career Integration Grant (FP7 CIG-293845); and the International Research Group Program (IRG14-08), Deanship of Scientific Research (King Saud University, Saudi Arabia). H.J. was supported by a Marie-Curie Initial Training Network Grant (EUROTAST; FP7 ITN-290344); A.G. and L. Ermini were supported by Marie-Curie Intra-European Fellowships (FP7 IEF-299176 and FP7 IEF-302617); M.S. was supported by a Lundbeck Foundation Grant (R52-A5062); I.D., A.F., and L. Excoffier were supported by a Swiss National Science Foundation Grant (31003A-143393); M.H. was supported by a European Research Council (ERC) Consolidator Grant (310763); T.M.-B. was supported by an ERC Starting Grant (260372) and by a Ministerio de Ciencia e Innovación (MICINN) Grant (BFU2011-28549); B.S. was supported by the Packard Foundation; and D.C. was supported by start-up funds to B.S. from the University of California, Santa Cruz.

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