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 (1, 5) , Cecilie E. Mortensen (5) , Bent Petersen (6) , Cindi A. Hoover (7) , Belen Lorente-Galdos (8, 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. Alquraishin (14) , Khaled A. S. Al-Rasheidn (14) , Thomas Sicheritz-Ponten (6) , Ruslan Popov (15) , Semyon Grigoriev (16) , Anatoly N Alekseev (16) , Edward M. Rubin (7) , Molly Mccue (17) , Stefan Rieder (11) , Tosso Leeb (12) , Alexei Tikhonov (18) , Eric Crubézy (13) , Montgomery Slatkin (4) , Tomas Marques-Bonet (8, 9) , Rasmus Nielsen (19) , Eske Willerslev (1) , Juha Kantanen (20, 21) , Egor Prokhortchouk (10) , Ludovic Orlando (1, 13)

1 Section for GeoGenetics
2 Bioinformatics Centre
3 UCL-GEE - Dept of Genetics, Evolution and Environment [London]
4 Department of Integrative Biology
5 National High-Throughput DNA Sequencing Centre
6 Center for Biological Sequence Analysis, Department of Systems Biology
7 DOE - Department of Energy / Joint Genome Institute
8 UPF - Universitat Pompeu Fabra [Barcelona]
9 Centro Nacional de Análisis Genómico
10 National Research Centre Kurchatov Institute
11 Agroscope, Swiss National Stud Farm
12 Institute of Genetics
13 AMIS - Anthropologie Moléculaire et Imagerie de Synthèse
14 KSU - King Saud University [Riyadh]
15 Yakutian Research Institute of Agriculture
16 North-Eastern Federal University
17 College of Veterinary Medicine
18 Zoological Institute of Russian Academy of Sciences
19 CTEG - Center for Theoretical Evolutionary Genomics [Berkeley]
20 Agrifood Research Finland
21 University of Eastern Finland

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. ancient genomics | adaptation | population discontinuity | regulatory changes | horse

Mots clés: ancient genomics; adaptation; population discontinuity; regulatory changes; horse

Domaines: Anthropologie biologique

Pablo Librado, Clio Der Sarkissian, Luca Ermini, Mikkel Schubert, Hákon Jónsson, et al.. Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments. Proceedings of the National Academy of Sciences of the United States of America, 2015, ⟨10.1073/pnas.1513696112⟩. ⟨hal-01256914⟩