Prehistoric genomes reveal the genetic foundation and cost of horse domestication

Mikkel Schubert; Hákon Jónsson; Dan Chang; Clio Der Sarkissian; Luca Ermini; Aurélien Ginolhac; Anders Albrechtsen; Isabelle Dupanloup; Adrien Foucal; Bent Petersen; Matteo Fumagalli; Maanasa Raghavan; Andaine Seguin-Orlando; Thorfinn Sand Korneliussen; Amhed M.V. Velazquez; Jesper Stenderup; Cindi A Hoover; Carl-Johan Rubin; Ahmed H Alfarhan; Saleh A Alquraishi; Khaled A S Al-Rasheid; David E MacHugh; Ted Kalbfleisch; James N MacLeod; Edward M Rubin; Thomas Sicheritz-Ponten; Leif Andersson; Michael Hofreiter; Tomas Marques-Bonet; M. Thomas P. Gilbert; Rasmus Nielsen; Laurent Excoffier; Eske Willerslev; Beth Shapiro; Ludovic Antoine Alexandre Orlando

doi:10.1073/pnas.1416991111

Prehistoric genomes reveal the genetic foundation and cost of horse domestication

Mikkel Schubert, Hákon Jónsson, Dan Chang, Clio Der Sarkissian, Luca Ermini, Aurélien Ginolhac, Anders Albrechtsen, Isabelle Dupanloup, Adrien Foucal, Bent Petersen, Matteo Fumagalli, Maanasa Raghavan, Andaine Seguin-Orlando, Thorfinn Sand Korneliussen, Amhed M.V. Velazquez, Jesper Stenderup, Cindi A Hoover, Carl-Johan Rubin, Ahmed H Alfarhan, Saleh A AlquraishiKhaled A S Al-Rasheid, David E MacHugh, Ted Kalbfleisch, James N MacLeod, Edward M Rubin, Thomas Sicheritz-Ponten, Leif Andersson, Michael Hofreiter, Tomas Marques-Bonet, M. Thomas P. Gilbert, Rasmus Nielsen, Laurent Excoffier, Eske Willerslev, Beth Shapiro, Ludovic Antoine Alexandre Orlando

Computational and RNA Biology

162 Citations (Scopus)

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.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	111
Issue number	52
Pages (from-to)	E5661–E5669
Number of pages	9
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1416991111
Publication status	Published - 30 Dec 2014

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Schubert, M., Jónsson, H., Chang, D., Der Sarkissian, C., Ermini, L., Ginolhac, A., Albrechtsen, A., Dupanloup, I., Foucal, A., Petersen, B., Fumagalli, M., Raghavan, M., Seguin-Orlando, A., Korneliussen, T. S., Velazquez, A. M. V., Stenderup, J., Hoover, C. A., Rubin, C-J., Alfarhan, A. H., ... Orlando, L. A. A. (2014). Prehistoric genomes reveal the genetic foundation and cost of horse domestication. Proceedings of the National Academy of Sciences of the United States of America, 111(52), E5661–E5669. https://doi.org/10.1073/pnas.1416991111

Schubert, M, Jónsson, H, Chang, D, Der Sarkissian, C, Ermini, L, Ginolhac, A, Albrechtsen, A, Dupanloup, I, Foucal, A, Petersen, B, Fumagalli, M, Raghavan, M, Seguin-Orlando, A, Korneliussen, TS, Velazquez, AMV, Stenderup, J, Hoover, CA, Rubin, C-J, Alfarhan, AH, Alquraishi, SA, Al-Rasheid, KAS, MacHugh, DE, Kalbfleisch, T, MacLeod, JN, Rubin, EM, Sicheritz-Ponten, T, Andersson, L, Hofreiter, M, Marques-Bonet, T, Gilbert, MTP, Nielsen, R, Excoffier, L, Willerslev, E, Shapiro, B & Orlando, LAA 2014, 'Prehistoric genomes reveal the genetic foundation and cost of horse domestication', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 52, pp. E5661–E5669. https://doi.org/10.1073/pnas.1416991111

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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.",

author = "Mikkel Schubert and H{\'a}kon J{\'o}nsson and Dan Chang and {Der Sarkissian}, Clio and Luca Ermini and Aur{\'e}lien Ginolhac and Anders Albrechtsen and Isabelle Dupanloup and Adrien Foucal and Bent Petersen and Matteo Fumagalli and Maanasa Raghavan and Andaine Seguin-Orlando and Korneliussen, {Thorfinn Sand} and Velazquez, {Amhed M.V.} and Jesper Stenderup and Hoover, {Cindi A} and Carl-Johan Rubin and Alfarhan, {Ahmed H} and Alquraishi, {Saleh A} and Al-Rasheid, {Khaled A S} and MacHugh, {David E} and Ted Kalbfleisch and MacLeod, {James N} and Rubin, {Edward M} and Thomas Sicheritz-Ponten and Leif Andersson and Michael Hofreiter and Tomas Marques-Bonet and Gilbert, {M. Thomas P.} and Rasmus Nielsen and Laurent Excoffier and Eske Willerslev and Beth Shapiro and Orlando, {Ludovic Antoine Alexandre}",

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T1 - Prehistoric genomes reveal the genetic foundation and cost of horse domestication

AU - Schubert, Mikkel

AU - Jónsson, Hákon

AU - Chang, Dan

AU - Der Sarkissian, Clio

AU - Ermini, Luca

AU - Ginolhac, Aurélien

AU - Albrechtsen, Anders

AU - Dupanloup, Isabelle

AU - Foucal, Adrien

AU - Petersen, Bent

AU - Fumagalli, Matteo

AU - Raghavan, Maanasa

AU - Seguin-Orlando, Andaine

AU - Korneliussen, Thorfinn Sand

AU - Velazquez, Amhed M.V.

AU - Stenderup, Jesper

AU - Hoover, Cindi A

AU - Rubin, Carl-Johan

AU - Alfarhan, Ahmed H

AU - Alquraishi, Saleh A

AU - Al-Rasheid, Khaled A S

AU - MacHugh, David E

AU - Kalbfleisch, Ted

AU - MacLeod, James N

AU - Rubin, Edward M

AU - Sicheritz-Ponten, Thomas

AU - Andersson, Leif

AU - Hofreiter, Michael

AU - Marques-Bonet, Tomas

AU - Gilbert, M. Thomas P.

AU - Nielsen, Rasmus

AU - Excoffier, Laurent

AU - Willerslev, Eske

AU - Shapiro, Beth

AU - Orlando, Ludovic Antoine Alexandre

PY - 2014/12/30

Y1 - 2014/12/30

N2 - 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.

AB - 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.

U2 - 10.1073/pnas.1416991111

DO - 10.1073/pnas.1416991111

M3 - Journal article

C2 - 25512547

SN - 0027-8424

VL - 111

SP - E5661–E5669

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 52

ER -

Prehistoric genomes reveal the genetic foundation and cost of horse domestication

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