Evolutionary genomics and conservation of the endangered Przewalski's horse

Clio Der Sarkissian; Luca Ermini; Mikkel Schubert; Melinda A. Yang; Pablo Librado Sanz; Matteo Fumagalli; Hákon Jónsson; Gila Kahila Bar-Gal; Anders Albrechtsen; Filipe Jorge Garrett Vieira; Bent Petersen; Aurélien Ginolhac; Andaine Seguin-Orlando; Kim Magnussen; Antoine Alphonse Fages; Cristina Gamba; Belen Lorente-Galdos; Sagi Polani; Cynthia Steiner; Markus Neuditschko; Vidhya Jagannathan; Claudia Feh; Charles L. Greenblatt; Arne Ludwig; Natalia I. Abramson; Waltraut Zimmermann; Renate Schafberg; Alexei Tikhonov; Thomas Sicheritz-Ponten; Eske Willerslev; Tomas Marques-Bonet; Oliver A. Ryder; Molly McCue; Stefan Rieder; Tosso Leeb; Montgomery Slatkin; Ludovic Antoine Alexandre Orlando

doi:10.1016/j.cub.2015.08.032

Evolutionary genomics and conservation of the endangered Przewalski's horse

Clio Der Sarkissian, Luca Ermini, Mikkel Schubert, Melinda A. Yang, Pablo Librado Sanz, Matteo Fumagalli, Hákon Jónsson, Gila Kahila Bar-Gal, Anders Albrechtsen, Filipe Jorge Garrett Vieira, Bent Petersen, Aurélien Ginolhac, Andaine Seguin-Orlando, Kim Magnussen, Antoine Alphonse Fages, Cristina Gamba, Belen Lorente-Galdos, Sagi Polani, Cynthia Steiner, Markus NeuditschkoVidhya Jagannathan, Claudia Feh, Charles L. Greenblatt, Arne Ludwig, Natalia I. Abramson, Waltraut Zimmermann, Renate Schafberg, Alexei Tikhonov, Thomas Sicheritz-Ponten, Eske Willerslev, Tomas Marques-Bonet, Oliver A. Ryder, Molly McCue, Stefan Rieder, Tosso Leeb, Montgomery Slatkin, Ludovic Antoine Alexandre Orlando^*

^*Corresponding author for this work

Computational and RNA Biology

94 Citations (Scopus)

Abstract

Przewalski's horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.

Original language	English
Journal	Current Biology
Volume	25
Issue number	19
Pages (from-to)	2577-2583
Number of pages	7
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2015.08.032
Publication status	Published - 2015

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Der Sarkissian, C., Ermini, L., Schubert, M., Yang, M. A., Sanz, P. L., Fumagalli, M., Jónsson, H., Bar-Gal, G. K., Albrechtsen, A., Garrett Vieira, F. J., Petersen, B., Ginolhac, A., Seguin-Orlando, A., Magnussen, K., Fages, A. A., Gamba, C., Lorente-Galdos, B., Polani, S., Steiner, C., ... Orlando, L. A. A. (2015). Evolutionary genomics and conservation of the endangered Przewalski's horse. Current Biology, 25(19), 2577-2583. https://doi.org/10.1016/j.cub.2015.08.032

Der Sarkissian, C, Ermini, L, Schubert, M, Yang, MA, Sanz, PL, Fumagalli, M, Jónsson, H, Bar-Gal, GK, Albrechtsen, A , Garrett Vieira, FJ , Petersen, B, Ginolhac, A, Seguin-Orlando, A, Magnussen, K, Fages, AA, Gamba, C, Lorente-Galdos, B, Polani, S, Steiner, C, Neuditschko, M, Jagannathan, V, Feh, C, Greenblatt, CL, Ludwig, A, Abramson, NI, Zimmermann, W, Schafberg, R, Tikhonov, A, Sicheritz-Ponten, T, Willerslev, E, Marques-Bonet, T, Ryder, OA, McCue, M, Rieder, S, Leeb, T, Slatkin, M & Orlando, LAA 2015, 'Evolutionary genomics and conservation of the endangered Przewalski's horse', Current Biology, vol. 25, no. 19, pp. 2577-2583. https://doi.org/10.1016/j.cub.2015.08.032

@article{ef680b4dc9f94cb0896ddd65dbbe4329,

title = "Evolutionary genomics and conservation of the endangered Przewalski's horse",

abstract = "Przewalski's horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.",

author = "{Der Sarkissian}, Clio and Luca Ermini and Mikkel Schubert and Yang, {Melinda A.} and Sanz, {Pablo Librado} and Matteo Fumagalli and H{\'a}kon J{\'o}nsson and Bar-Gal, {Gila Kahila} and Anders Albrechtsen and {Garrett Vieira}, {Filipe Jorge} and Bent Petersen and Aur{\'e}lien Ginolhac and Andaine Seguin-Orlando and Kim Magnussen and Fages, {Antoine Alphonse} and Cristina Gamba and Belen Lorente-Galdos and Sagi Polani and Cynthia Steiner and Markus Neuditschko and Vidhya Jagannathan and Claudia Feh and Greenblatt, {Charles L.} and Arne Ludwig and Abramson, {Natalia I.} and Waltraut Zimmermann and Renate Schafberg and Alexei Tikhonov and Thomas Sicheritz-Ponten and Eske Willerslev and Tomas Marques-Bonet and Ryder, {Oliver A.} and Molly McCue and Stefan Rieder and Tosso Leeb and Montgomery Slatkin and Orlando, {Ludovic Antoine Alexandre}",

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language = "English",

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T1 - Evolutionary genomics and conservation of the endangered Przewalski's horse

AU - Der Sarkissian, Clio

AU - Ermini, Luca

AU - Schubert, Mikkel

AU - Yang, Melinda A.

AU - Sanz, Pablo Librado

AU - Fumagalli, Matteo

AU - Jónsson, Hákon

AU - Bar-Gal, Gila Kahila

AU - Albrechtsen, Anders

AU - Garrett Vieira, Filipe Jorge

AU - Petersen, Bent

AU - Ginolhac, Aurélien

AU - Seguin-Orlando, Andaine

AU - Magnussen, Kim

AU - Fages, Antoine Alphonse

AU - Gamba, Cristina

AU - Lorente-Galdos, Belen

AU - Polani, Sagi

AU - Steiner, Cynthia

AU - Neuditschko, Markus

AU - Jagannathan, Vidhya

AU - Feh, Claudia

AU - Greenblatt, Charles L.

AU - Ludwig, Arne

AU - Abramson, Natalia I.

AU - Zimmermann, Waltraut

AU - Schafberg, Renate

AU - Tikhonov, Alexei

AU - Sicheritz-Ponten, Thomas

AU - Willerslev, Eske

AU - Marques-Bonet, Tomas

AU - Ryder, Oliver A.

AU - McCue, Molly

AU - Rieder, Stefan

AU - Leeb, Tosso

AU - Slatkin, Montgomery

AU - Orlando, Ludovic Antoine Alexandre

PY - 2015

Y1 - 2015

N2 - Przewalski's horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.

AB - Przewalski's horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.

U2 - 10.1016/j.cub.2015.08.032

DO - 10.1016/j.cub.2015.08.032

M3 - Journal article

C2 - 26412128

AN - SCOPUS:84943405119

SN - 0960-9822

VL - 25

SP - 2577

EP - 2583

JO - Current Biology

JF - Current Biology

IS - 19

ER -

Evolutionary genomics and conservation of the endangered Przewalski's horse

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