doi: 10.1073/pnas.1513696112. Epub 2015 Nov 23.
Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments
Pablo Librado 1, Clio Der Sarkissian 1, Luca Ermini 1, Mikkel Schubert 1, Hákon Jónsson 1, Anders Albrechtsen 2, Matteo Fumagalli 3, Melinda A Yang 4, Cristina Gamba 1, Andaine Seguin-Orlando 5, Cecilie D Mortensen 6, Bent Petersen 7, Cindi A Hoover 8, Belen Lorente-Galdos 9, Artem Nedoluzhko 10, Eugenia Boulygina 10, Svetlana Tsygankova 10, Markus Neuditschko 11, Vidhya Jagannathan 12, Catherine Thèves 13, Ahmed H Alfarhan 14, Saleh A Alquraishi 14, Khaled A S Al-Rasheid 14, Thomas Sicheritz-Ponten 7, Ruslan Popov 15, Semyon Grigoriev 16, Anatoly N Alekseev 16, Edward M Rubin 8, Molly McCue 17, Stefan Rieder 11, Tosso Leeb 12, Alexei Tikhonov 18, Eric Crubézy 13, Montgomery Slatkin 4, Tomas Marques-Bonet 9, Rasmus Nielsen 19, Eske Willerslev 1, Juha Kantanen 20, Egor Prokhortchouk 10, Ludovic Orlando 21
Affiliations
- PMID:26598656
- PMCID: PMC4687531
- DOI: 10.1073/pnas.1513696112
Item in Clipboard
Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments
Pablo Librado et al. Proc Natl Acad Sci U S A..
Display options
Format
Display options
Format
Abstract
Yakutia, Sakha Republic, in the Siberian Far East, represents one of the coldest places on Earth, with winter record temperatures dropping below -70 °C. Nevertheless, Yakutian horses survive all year round in the open air due to striking phenotypic adaptations, including compact body conformations, extremely hairy winter coats, and acute seasonal differences in metabolic activities. The evolutionary origins of Yakutian horses and the genetic basis of their adaptations remain, however, contentious. Here, we present the complete genomes of nine present-day Yakutian horses and two ancient specimens dating from the early 19th century and ∼5,200 y ago. By comparing these genomes with the genomes of two Late Pleistocene, 27 domesticated, and three wild Przewalski's horses, we find that contemporary Yakutian horses do not descend from the native horses that populated the region until the mid-Holocene, but were most likely introduced following the migration of the Yakut people a few centuries ago. Thus, they represent one of the fastest cases of adaptation to the extreme temperatures of the Arctic. We find cis-regulatory mutations to have contributed more than nonsynonymous changes to their adaptation, likely due to the comparatively limited standing variation within gene bodies at the time the population was founded. Genes involved in hair development, body size, and metabolic and hormone signaling pathways represent an essential part of the Yakutian horse adaptive genetic toolkit. Finally, we find evidence for convergent evolution with native human populations and woolly mammoths, suggesting that only a few evolutionary strategies are compatible with survival in extremely cold environments.
Keywords: adaptation; ancient genomics; horse; population discontinuity; regulatory changes.
Conflict of interest statement
The authors declare no conflict of interest.
Figures
Geographic distribution and population affinities. (A) Geographic location of ancient (blue) and modern (dark red) Yakutian horse samples (SI Appendix, Table S1.1). (B) TreeMix relationships between modern Yakutian horses (brown), ancient horses (blue), Przewalski's horses (green), and our panel of nine domestic breeds (red).
PCA. The analysis was based on genotype likelihoods and 29 genomes representative of present-day Yakutian horses, nine domestic breeds, the Przewalski’s horse population, CGG101397, and extinct horses. The fraction of the total variance explained by each of the three principal components is indicated on the corresponding axes.
Long- and short-termNe changes of the Yakutian horse population. (A) Scaled PSMC profile tracking effective population size changes over the past 2 Mya. (B) Site frequency spectra estimated from the present-day population of Yakutian horses (including CGG101397), expected under the neutral model, and fitted under the best demographic scenario (three-epoch model). (C) Three-epoch demographic model for the Yakutian horse population. This model represents the best fit in ∂a∂i analyses. Kyr, thousand years; LGM, Last Glacial Maximum.
Relative contribution of coding and noncoding regions to adaptation. (A) Red dashed line delimits the neutrality threshold [i.e., the top-0.001%dA quantile of 4d-fold degenerate sites (dA = 0.3448)]. (B) Distribution of the proportion of adaptive mutations across categories, including coding (green, 0d-fold, 2d-fold, and 4d-fold degenerate positions) and noncoding (red, 10 first bins of 1 kb upstream from the TSS) sites. (C)dA pattern at theTGM3 gene (reverse strand). (D)dA pattern at theLECT2 andFBLX21 gene region. chr, chromosome.
Similar articles
- Evolutionary Genomics and Conservation of the Endangered Przewalski's Horse.Der Sarkissian C, Ermini L, Schubert M, Yang MA, Librado P, Fumagalli M, Jónsson H, Bar-Gal GK, Albrechtsen A, Vieira FG, Petersen B, Ginolhac A, Seguin-Orlando A, Magnussen K, Fages A, 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 L.Der Sarkissian C, et al.Curr Biol. 2015 Oct 5;25(19):2577-83. doi: 10.1016/j.cub.2015.08.032. Epub 2015 Sep 24.Curr Biol. 2015.PMID:26412128Free PMC article.
- Prehistoric genomes reveal the genetic foundation and cost of horse domestication.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 AM, Stenderup J, Hoover CA, Rubin CJ, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, MacHugh DE, Kalbfleisch T, MacLeod JN, Rubin EM, Sicheritz-Ponten T, Andersson L, Hofreiter M, Marques-Bonet T, Gilbert MT, Nielsen R, Excoffier L, Willerslev E, Shapiro B, Orlando L.Schubert M, et al.Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):E5661-9. doi: 10.1073/pnas.1416991111. Epub 2014 Dec 15.Proc Natl Acad Sci U S A. 2014.PMID:25512547Free PMC article.
- Horse domestication and conservation genetics of Przewalski's horse inferred from sex chromosomal and autosomal sequences.Lau AN, Peng L, Goto H, Chemnick L, Ryder OA, Makova KD.Lau AN, et al.Mol Biol Evol. 2009 Jan;26(1):199-208. doi: 10.1093/molbev/msn239. Epub 2008 Oct 17.Mol Biol Evol. 2009.PMID:18931383
- Adaptive dimensions of health research among indigenous Siberians.Snodgrass JJ, Sorensen MV, Tarskaia LA, Leonard WR.Snodgrass JJ, et al.Am J Hum Biol. 2007 Mar-Apr;19(2):165-80. doi: 10.1002/ajhb.20624.Am J Hum Biol. 2007.PMID:17286259Review.
- Ancient Genomes Reveal Unexpected Horse Domestication and Management Dynamics.Orlando L.Orlando L.Bioessays. 2020 Jan;42(1):e1900164. doi: 10.1002/bies.201900164. Epub 2019 Dec 6.Bioessays. 2020.PMID:31808562Review.
Cited by
- The Characteristics, Distribution, Function, and Origin of Alternative Lateral Horse Gaits.Vincelette A.Vincelette A.Animals (Basel). 2023 Aug 8;13(16):2557. doi: 10.3390/ani13162557.Animals (Basel). 2023.PMID:37627349Free PMC article.Review.
- Demographic History, Adaptation, and NRAP Convergent Evolution at Amino Acid Residue 100 in the World Northernmost Cattle from Siberia.Buggiotti L, Yurchenko AA, Yudin NS, Vander Jagt CJ, Vorobieva NV, Kusliy MA, Vasiliev SK, Rodionov AN, Boronetskaya OI, Zinovieva NA, Graphodatsky AS, Daetwyler HD, Larkin DM.Buggiotti L, et al.Mol Biol Evol. 2021 Jul 29;38(8):3093-3110. doi: 10.1093/molbev/msab078.Mol Biol Evol. 2021.PMID:33784744Free PMC article.
- Whole-Genome Sequencing of Native Sheep Provides Insights into Rapid Adaptations to Extreme Environments.Yang J, Li WR, Lv FH, He SG, Tian SL, Peng WF, Sun YW, Zhao YX, Tu XL, Zhang M, Xie XL, Wang YT, Li JQ, Liu YG, Shen ZQ, Wang F, Liu GJ, Lu HF, Kantanen J, Han JL, Li MH, Liu MJ.Yang J, et al.Mol Biol Evol. 2016 Oct;33(10):2576-92. doi: 10.1093/molbev/msw129. Epub 2016 Jul 8.Mol Biol Evol. 2016.PMID:27401233Free PMC article.
- Ancient Genomes Reveal the Evolutionary History and Origin of Cashmere-Producing Goats in China.Cai Y, Fu W, Cai D, Heller R, Zheng Z, Wen J, Li H, Wang X, Alshawi A, Sun Z, Zhu S, Wang J, Yang M, Hu S, Li Y, Yang Z, Gong M, Hou Y, Lan T, Wu K, Chen Y, Jiang Y, Wang X.Cai Y, et al.Mol Biol Evol. 2020 Jul 1;37(7):2099-2109. doi: 10.1093/molbev/msaa103.Mol Biol Evol. 2020.PMID:32324877Free PMC article.
- Ten years of the horse reference genome: insights into equine biology, domestication and population dynamics in the post-genome era.Raudsepp T, Finno CJ, Bellone RR, Petersen JL.Raudsepp T, et al.Anim Genet. 2019 Dec;50(6):569-597. doi: 10.1111/age.12857. Epub 2019 Sep 30.Anim Genet. 2019.PMID:31568563Free PMC article.Review.
References
- Stepanova N. On the lowest temperature on Earth. Monthly Weather Review. 1958;86:6–10.
- Pakendorf B, et al. Investigating the effects of prehistoric migrations in Siberia: Genetic variation and the origins of Yakuts. Hum Genet. 2006;120(3):334–353. - PubMed
- Ferret C. Une civilization du cheval. Editions Belin; Paris: 2009.
Publication types
MeSH terms
Related information
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources