Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse

Ludovic Antoine Alexandre Orlando; Aurélien Ginolhac; Guojie Zhang; Duane Froese; Anders Albrechtsen; Mathias Stiller; Mikkel Schubert; Enrico Cappellini; Bent Petersen; Ida Moltke; Philip L. F. Johnson; Matteo Fumagalli; Julia Thidamarth Vilstrup Mouatt; Maanasa Raghavan; Thorfinn Sand Korneliussen; Anna Sapfo Malaspinas; Josef Vogt; Damian Milosz Szklarczyk; Christian Kelstrup; Jakob Vinther; Andrei Dolocan; Jesper Stenderup; Amhed M. V. Velazquez; James Cahill; Morten Rasmussen; Xiaoli Wang; Jiumeng Min; Grant D. Zazula; Andaine Seguin-Orlando; Cecilie Mortensen; Kim Magnussen; John F. Thompson; Jacobo Weinstock; Kristian Gregersen; Knut H. Røed; Véra Eisenmann; Carl J. Rubin; Donald C. Miller; Douglas F. Antczak; Mads F. Bertelsen; Søren Brunak; Khaled A. S. Al-Rasheid; Oliver Ryder; Leif Andersson; John Mundy; Anders Krogh; Tom Gilbert; Kurt H. Kjær; Thomas Sicheritz-Pontén; Lars Juhl Jensen; Jesper Velgaard Olsen; Michael Hofreiter; Rasmus Nielsen; Beth Shapiro; Jun Wang; Eske Willerslev

doi:10.1038/nature12323

Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse

Ludovic Antoine Alexandre Orlando, Aurélien Ginolhac, Guojie Zhang, Duane Froese, Anders Albrechtsen, Mathias Stiller, Mikkel Schubert, Enrico Cappellini, Bent Petersen, Ida Moltke, Philip L. F. Johnson, Matteo Fumagalli, Julia Thidamarth Vilstrup Mouatt, Maanasa Raghavan, Thorfinn Sand Korneliussen, Anna Sapfo Malaspinas, Josef Vogt, Damian Milosz Szklarczyk, Christian Kelstrup, Jakob VintherAndrei Dolocan, Jesper Stenderup, Amhed M. V. Velazquez, James Cahill, Morten Rasmussen, Xiaoli Wang, Jiumeng Min, Grant D. Zazula, Andaine Seguin-Orlando, Cecilie Mortensen, Kim Magnussen, John F. Thompson, Jacobo Weinstock, Kristian Gregersen, Knut H. Røed, Véra Eisenmann, Carl J. Rubin, Donald C. Miller, Douglas F. Antczak, Mads F. Bertelsen, Søren Brunak, Khaled A. S. Al-Rasheid, Oliver Ryder, Leif Andersson, John Mundy, Anders Krogh, Tom Gilbert, Kurt H. Kjær, Thomas Sicheritz-Pontén, Lars Juhl Jensen, Jesper Velgaard Olsen, Michael Hofreiter, Rasmus Nielsen, Beth Shapiro, Jun Wang, Eske Willerslev

454 Citations (Scopus)

Abstract

The rich fossil record of equids has made them a model for evolutionary processes. Here we present a 1.12-times coverage draft genome from a horse bone recovered from permafrost dated to approximately 560-780 thousand years before present (kyr bp). Our data represent the oldest full genome sequence determined so far by almost an order of magnitude. For comparison, we sequenced the genome of a Late Pleistocene horse (43 kyr bp), and modern genomes of five domestic horse breeds (Equus ferus caballus), a Przewalski's horse (E. f. przewalskii) and a donkey (E. asinus). Our analyses suggest that the Equus lineage giving rise to all contemporary horses, zebras and donkeys originated 4.0-4.5 million years before present (Myr bp), twice the conventionally accepted time to the most recent common ancestor of the genus Equus. We also find that horse population size fluctuated multiple times over the past 2 Myr, particularly during periods of severe climatic changes. We estimate that the Przewalski's and domestic horse populations diverged 38-72 kyr bp, and find no evidence of recent admixture between the domestic horse breeds and the Przewalski's horse investigated. This supports the contention that Przewalski's horses represent the last surviving wild horse population. We find similar levels of genetic variation among Przewalski's and domestic populations, indicating that the former are genetically viable and worthy of conservation efforts. We also find evidence for continuous selection on the immune system and olfaction throughout horse evolution. Finally, we identify 29 genomic regions among horse breeds that deviate from neutrality and show low levels of genetic variation compared to the Przewalski's horse. Such regions could correspond to loci selected early during domestication.

Original language	English
Journal	Nature
Volume	499
Issue number	7456
Pages (from-to)	74-78
Number of pages	5
ISSN	0028-0836
DOIs	https://doi.org/10.1038/nature12323
Publication status	Published - 4 Jul 2013

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Orlando, L. A. A., Ginolhac, A., Zhang, G., Froese, D., Albrechtsen, A., Stiller, M., Schubert, M., Cappellini, E., Petersen, B., Moltke, I., Johnson, P. L. F., Fumagalli, M., Mouatt, J. T. V., Raghavan, M., Korneliussen, T. S., Malaspinas, A. S., Vogt, J., Szklarczyk, D. M., Kelstrup, C., ... Willerslev, E. (2013). Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature, 499(7456), 74-78. https://doi.org/10.1038/nature12323

Orlando, LAA, Ginolhac, A, Zhang, G, Froese, D, Albrechtsen, A, Stiller, M, Schubert, M, Cappellini, E , Petersen, B , Moltke, I, Johnson, PLF, Fumagalli, M, Mouatt, JTV, Raghavan, M, Korneliussen, TS, Malaspinas, AS, Vogt, J, Szklarczyk, DM, Kelstrup, C, Vinther, J, Dolocan, A, Stenderup, J, Velazquez, AMV, Cahill, J, Rasmussen, M, Wang, X, Min, J, Zazula, GD, Seguin-Orlando, A, Mortensen, C, Magnussen, K, Thompson, JF, Weinstock, J, Gregersen, K, Røed, KH, Eisenmann, V, Rubin, CJ, Miller, DC, Antczak, DF, Bertelsen, MF, Brunak, S, Al-Rasheid, KAS, Ryder, O, Andersson, L, Mundy, J, Krogh, A , Gilbert, T , Kjær, KH, Sicheritz-Pontén, T, Jensen, LJ , Olsen, JV, Hofreiter, M, Nielsen, R, Shapiro, B, Wang, J & Willerslev, E 2013, 'Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse', Nature, vol. 499, no. 7456, pp. 74-78. https://doi.org/10.1038/nature12323

@article{7cd6f5a7574141669652c0af11f86aef,

title = "Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse",

abstract = "The rich fossil record of equids has made them a model for evolutionary processes. Here we present a 1.12-times coverage draft genome from a horse bone recovered from permafrost dated to approximately 560-780 thousand years before present (kyr bp). Our data represent the oldest full genome sequence determined so far by almost an order of magnitude. For comparison, we sequenced the genome of a Late Pleistocene horse (43 kyr bp), and modern genomes of five domestic horse breeds (Equus ferus caballus), a Przewalski's horse (E. f. przewalskii) and a donkey (E. asinus). Our analyses suggest that the Equus lineage giving rise to all contemporary horses, zebras and donkeys originated 4.0-4.5 million years before present (Myr bp), twice the conventionally accepted time to the most recent common ancestor of the genus Equus. We also find that horse population size fluctuated multiple times over the past 2 Myr, particularly during periods of severe climatic changes. We estimate that the Przewalski's and domestic horse populations diverged 38-72 kyr bp, and find no evidence of recent admixture between the domestic horse breeds and the Przewalski's horse investigated. This supports the contention that Przewalski's horses represent the last surviving wild horse population. We find similar levels of genetic variation among Przewalski's and domestic populations, indicating that the former are genetically viable and worthy of conservation efforts. We also find evidence for continuous selection on the immune system and olfaction throughout horse evolution. Finally, we identify 29 genomic regions among horse breeds that deviate from neutrality and show low levels of genetic variation compared to the Przewalski's horse. Such regions could correspond to loci selected early during domestication.",

author = "Orlando, {Ludovic Antoine Alexandre} and Aur{\'e}lien Ginolhac and Guojie Zhang and Duane Froese and Anders Albrechtsen and Mathias Stiller and Mikkel Schubert and Enrico Cappellini and Bent Petersen and Ida Moltke and Johnson, {Philip L. F.} and Matteo Fumagalli and Mouatt, {Julia Thidamarth Vilstrup} and Maanasa Raghavan and Korneliussen, {Thorfinn Sand} and Malaspinas, {Anna Sapfo} and Josef Vogt and Szklarczyk, {Damian Milosz} and Christian Kelstrup and Jakob Vinther and Andrei Dolocan and Jesper Stenderup and Velazquez, {Amhed M. V.} and James Cahill and Morten Rasmussen and Xiaoli Wang and Jiumeng Min and Zazula, {Grant D.} and Andaine Seguin-Orlando and Cecilie Mortensen and Kim Magnussen and Thompson, {John F.} and Jacobo Weinstock and Kristian Gregersen and R{\o}ed, {Knut H.} and V{\'e}ra Eisenmann and Rubin, {Carl J.} and Miller, {Donald C.} and Antczak, {Douglas F.} and Bertelsen, {Mads F.} and S{\o}ren Brunak and Al-Rasheid, {Khaled A. S.} and Oliver Ryder and Leif Andersson and John Mundy and Anders Krogh and Tom Gilbert and Kj{\ae}r, {Kurt H.} and Thomas Sicheritz-Pont{\'e}n and Jensen, {Lars Juhl} and Olsen, {Jesper Velgaard} and Michael Hofreiter and Rasmus Nielsen and Beth Shapiro and Jun Wang and Eske Willerslev",

year = "2013",

month = jul,

day = "4",

doi = "10.1038/nature12323",

language = "English",

volume = "499",

pages = "74--78",

journal = "Nature",

issn = "0028-0836",

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TY - JOUR

T1 - Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse

AU - Orlando, Ludovic Antoine Alexandre

AU - Ginolhac, Aurélien

AU - Zhang, Guojie

AU - Froese, Duane

AU - Albrechtsen, Anders

AU - Stiller, Mathias

AU - Schubert, Mikkel

AU - Cappellini, Enrico

AU - Petersen, Bent

AU - Moltke, Ida

AU - Johnson, Philip L. F.

AU - Fumagalli, Matteo

AU - Mouatt, Julia Thidamarth Vilstrup

AU - Raghavan, Maanasa

AU - Korneliussen, Thorfinn Sand

AU - Malaspinas, Anna Sapfo

AU - Vogt, Josef

AU - Szklarczyk, Damian Milosz

AU - Kelstrup, Christian

AU - Vinther, Jakob

AU - Dolocan, Andrei

AU - Stenderup, Jesper

AU - Velazquez, Amhed M. V.

AU - Cahill, James

AU - Rasmussen, Morten

AU - Wang, Xiaoli

AU - Min, Jiumeng

AU - Zazula, Grant D.

AU - Seguin-Orlando, Andaine

AU - Mortensen, Cecilie

AU - Magnussen, Kim

AU - Thompson, John F.

AU - Weinstock, Jacobo

AU - Gregersen, Kristian

AU - Røed, Knut H.

AU - Eisenmann, Véra

AU - Rubin, Carl J.

AU - Miller, Donald C.

AU - Antczak, Douglas F.

AU - Bertelsen, Mads F.

AU - Brunak, Søren

AU - Al-Rasheid, Khaled A. S.

AU - Ryder, Oliver

AU - Andersson, Leif

AU - Mundy, John

AU - Krogh, Anders

AU - Gilbert, Tom

AU - Kjær, Kurt H.

AU - Sicheritz-Pontén, Thomas

AU - Jensen, Lars Juhl

AU - Olsen, Jesper Velgaard

AU - Hofreiter, Michael

AU - Nielsen, Rasmus

AU - Shapiro, Beth

AU - Wang, Jun

AU - Willerslev, Eske

PY - 2013/7/4

Y1 - 2013/7/4

N2 - The rich fossil record of equids has made them a model for evolutionary processes. Here we present a 1.12-times coverage draft genome from a horse bone recovered from permafrost dated to approximately 560-780 thousand years before present (kyr bp). Our data represent the oldest full genome sequence determined so far by almost an order of magnitude. For comparison, we sequenced the genome of a Late Pleistocene horse (43 kyr bp), and modern genomes of five domestic horse breeds (Equus ferus caballus), a Przewalski's horse (E. f. przewalskii) and a donkey (E. asinus). Our analyses suggest that the Equus lineage giving rise to all contemporary horses, zebras and donkeys originated 4.0-4.5 million years before present (Myr bp), twice the conventionally accepted time to the most recent common ancestor of the genus Equus. We also find that horse population size fluctuated multiple times over the past 2 Myr, particularly during periods of severe climatic changes. We estimate that the Przewalski's and domestic horse populations diverged 38-72 kyr bp, and find no evidence of recent admixture between the domestic horse breeds and the Przewalski's horse investigated. This supports the contention that Przewalski's horses represent the last surviving wild horse population. We find similar levels of genetic variation among Przewalski's and domestic populations, indicating that the former are genetically viable and worthy of conservation efforts. We also find evidence for continuous selection on the immune system and olfaction throughout horse evolution. Finally, we identify 29 genomic regions among horse breeds that deviate from neutrality and show low levels of genetic variation compared to the Przewalski's horse. Such regions could correspond to loci selected early during domestication.

AB - The rich fossil record of equids has made them a model for evolutionary processes. Here we present a 1.12-times coverage draft genome from a horse bone recovered from permafrost dated to approximately 560-780 thousand years before present (kyr bp). Our data represent the oldest full genome sequence determined so far by almost an order of magnitude. For comparison, we sequenced the genome of a Late Pleistocene horse (43 kyr bp), and modern genomes of five domestic horse breeds (Equus ferus caballus), a Przewalski's horse (E. f. przewalskii) and a donkey (E. asinus). Our analyses suggest that the Equus lineage giving rise to all contemporary horses, zebras and donkeys originated 4.0-4.5 million years before present (Myr bp), twice the conventionally accepted time to the most recent common ancestor of the genus Equus. We also find that horse population size fluctuated multiple times over the past 2 Myr, particularly during periods of severe climatic changes. We estimate that the Przewalski's and domestic horse populations diverged 38-72 kyr bp, and find no evidence of recent admixture between the domestic horse breeds and the Przewalski's horse investigated. This supports the contention that Przewalski's horses represent the last surviving wild horse population. We find similar levels of genetic variation among Przewalski's and domestic populations, indicating that the former are genetically viable and worthy of conservation efforts. We also find evidence for continuous selection on the immune system and olfaction throughout horse evolution. Finally, we identify 29 genomic regions among horse breeds that deviate from neutrality and show low levels of genetic variation compared to the Przewalski's horse. Such regions could correspond to loci selected early during domestication.

U2 - 10.1038/nature12323

DO - 10.1038/nature12323

M3 - Letter

C2 - 23803765

SN - 0028-0836

VL - 499

SP - 74

EP - 78

JO - Nature

JF - Nature

IS - 7456

ER -

Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse

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