title: Prehistoric genomes reveal the genetic foundation and cost of horse domestication.
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.
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Mikkel
authors.identifier: http://orcid.org/0000-0003-2401-9921
authors.initials: M
authors.lastname: Schubert
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Hákon
authors.initials: H
authors.lastname: Jónsson
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
authors.forename: Dan
authors.initials: D
authors.lastname: Chang
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Clio
authors.initials: C
authors.lastname: Der Sarkissian
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Luca
authors.initials: L
authors.lastname: Ermini
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Aurélien
authors.initials: A
authors.lastname: Ginolhac
authors.affiliation: The Bioinformatics Centre, Department of Biology, University of Copenhagen, 2200N Copenhagen, Denmark;
authors.forename: Anders
authors.initials: A
authors.lastname: Albrechtsen
authors.affiliation: Institute of Ecology and Evolution, University of Berne, 3012 Berne, Switzerland; Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;
authors.forename: Isabelle
authors.initials: I
authors.lastname: Dupanloup
authors.affiliation: Institute of Ecology and Evolution, University of Berne, 3012 Berne, Switzerland; Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;
authors.forename: Adrien
authors.initials: A
authors.lastname: Foucal
authors.affiliation: Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Lyngby, Denmark;
authors.forename: Bent
authors.initials: B
authors.lastname: Petersen
authors.affiliation: UCL Genetics Institute, Department of Genetics, Evolution, and Environment, University College London, London WC1E 6BT, United Kingdom;
authors.forename: Matteo
authors.initials: M
authors.lastname: Fumagalli
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Maanasa
authors.initials: M
authors.lastname: Raghavan
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark; National High-Throughput DNA Sequencing Center, University of Copenhagen, 1353K Copenhagen, Denmark;
authors.forename: Andaine
authors.initials: A
authors.lastname: Seguin-Orlando
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Thorfinn S
authors.identifier: http://orcid.org/0000-0001-7576-5380
authors.initials: TS
authors.lastname: Korneliussen
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Amhed M V
authors.initials: AM
authors.lastname: Velazquez
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Jesper
authors.initials: J
authors.lastname: Stenderup
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
authors.forename: Cindi A
authors.initials: CA
authors.lastname: Hoover
authors.affiliation: Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden;
authors.forename: Carl-Johan
authors.initials: CJ
authors.lastname: Rubin
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Ahmed H
authors.initials: AH
authors.lastname: Alfarhan
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Saleh A
authors.initials: SA
authors.lastname: Alquraishi
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Khaled A S
authors.initials: KA
authors.lastname: Al-Rasheid
authors.affiliation: Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland; UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland;
authors.forename: David E
authors.identifier: http://orcid.org/0000-0002-8112-4704
authors.initials: DE
authors.lastname: MacHugh
authors.affiliation: Biochemistry and Molecular Biology, School of Medicine, University of Louisville, Louisville, KY 40292;
authors.forename: Ted
authors.initials: T
authors.lastname: Kalbfleisch
authors.affiliation: Department of Veterinary Science, Gluck Equine Research Center, University of Kentucky, Lexington, KY 40546;
authors.forename: James N
authors.initials: JN
authors.lastname: MacLeod
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
authors.forename: Edward M
authors.initials: EM
authors.lastname: Rubin
authors.affiliation: Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Lyngby, Denmark;
authors.forename: Thomas
authors.identifier: http://orcid.org/0000-0001-6615-1141
authors.initials: T
authors.lastname: Sicheritz-Ponten
authors.affiliation: Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden;
authors.forename: Leif
authors.initials: L
authors.lastname: Andersson
authors.affiliation: Institute for Biochemistry and Biology, Faculty for Mathematics and Natural Sciences, University of Potsdam, 14476 Potsdam, Germany;
authors.forename: Michael
authors.initials: M
authors.lastname: Hofreiter
authors.affiliation: Instituticó Catalana de Recerca i Estudis Avançats, Institut de Biologia Evolutiva (Universitat Pompeu Fabra/Consejo Superior de Investigaciones Cientificas), 08003 Barcelona, Spain; Centro Nacional de Análisis Genómico, 08028 Barcelona, Spain; and.
authors.forename: Tomas
authors.initials: T
authors.lastname: Marques-Bonet
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: M Thomas P
authors.initials: MT
authors.lastname: Gilbert
authors.affiliation: Departments of Integrative Biology and Statistics, University of California, Berkeley, CA 94720.
authors.forename: Rasmus
authors.initials: R
authors.lastname: Nielsen
authors.affiliation: Institute of Ecology and Evolution, University of Berne, 3012 Berne, Switzerland; Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;
authors.forename: Laurent
authors.initials: L
authors.lastname: Excoffier
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Eske
authors.initials: E
authors.lastname: Willerslev
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
authors.forename: Beth
authors.initials: B
authors.lastname: Shapiro
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark; Lorlando@snm.ku.dk.
authors.forename: Ludovic
authors.initials: L
authors.lastname: Orlando
mesh_terms: D000818:Animals; D000829:Animals, Domestic / Q000235:genetics*; D002319:Cardiovascular System / Q000033:anatomy & histology; D004285:Dogs; D019143:Evolution, Molecular; D016678:Genome / Q000502:physiology*; D006614:Hindlimb / Q000033:anatomy & histology / Q000502:physiology; D006736:Horses / Q000033:anatomy & histology / Q000235:genetics*; D006801:Humans; D007178:Inbreeding; D012426:Russia
keywords: Przewalski’s horse; ancient DNA; cost of domestication; horse domestication; positive selection