title: Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments.
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.
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Pablo
authors.initials: P
authors.lastname: Librado
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Clio
authors.initials: C
authors.lastname: Der Sarkissian
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Luca
authors.initials: L
authors.lastname: Ermini
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Mikkel
authors.identifier: http://orcid.org/0000-0003-2401-9921
authors.initials: M
authors.lastname: Schubert
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Hákon
authors.initials: H
authors.lastname: Jónsson
authors.affiliation: Bioinformatics Centre, Department of Biology, University of Copenhagen, 2200N Copenhagen, Denmark;
authors.forename: Anders
authors.initials: A
authors.lastname: Albrechtsen
authors.affiliation: UCL Genetics Institute, Department of Genetics, Evolution, and Environment, University College London, London WC1E 6BT, United Kingdom;
authors.forename: Matteo
authors.initials: M
authors.lastname: Fumagalli
authors.affiliation: Department of Integrative Biology, University of California, Berkeley, CA 94720-3140;
authors.forename: Melinda A
authors.initials: MA
authors.lastname: Yang
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Cristina
authors.initials: C
authors.lastname: Gamba
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark; National High-Throughput DNA Sequencing Centre, University of Copenhagen, 1353K Copenhagen, Denmark;
authors.forename: Andaine
authors.initials: A
authors.lastname: Seguin-Orlando
authors.affiliation: National High-Throughput DNA Sequencing Centre, University of Copenhagen, 1353K Copenhagen, Denmark;
authors.forename: Cecilie D
authors.initials: CD
authors.lastname: Mortensen
authors.affiliation: Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Lyngby, Denmark;
authors.forename: Bent
authors.initials: B
authors.lastname: Petersen
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
authors.forename: Cindi A
authors.initials: CA
authors.lastname: Hoover
authors.affiliation: Universitat Pompeu Fabra/Consejo Superior de Investigaciones Cientificas, 08003 Barcelona, Spain; Centro Nacional de Análisis Genómico, 08028 Barcelona, Spain;
authors.forename: Belen
authors.initials: B
authors.lastname: Lorente-Galdos
authors.affiliation: National Research Centre Kurchatov Institute, Moscow 123182, Russia;
authors.forename: Artem
authors.initials: A
authors.lastname: Nedoluzhko
authors.affiliation: National Research Centre Kurchatov Institute, Moscow 123182, Russia;
authors.forename: Eugenia
authors.initials: E
authors.lastname: Boulygina
authors.affiliation: National Research Centre Kurchatov Institute, Moscow 123182, Russia;
authors.forename: Svetlana
authors.initials: S
authors.lastname: Tsygankova
authors.affiliation: Agroscope, Swiss National Stud Farm, 1580 Avenches, Switzerland;
authors.forename: Markus
authors.initials: M
authors.lastname: Neuditschko
authors.affiliation: Institute of Genetics, University of Bern, 3001 Bern, Switzerland;
authors.forename: Vidhya
authors.initials: V
authors.lastname: Jagannathan
authors.affiliation: Université de Toulouse, University Paul Sabatier, Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, 31000 Toulouse, France;
authors.forename: Catherine
authors.initials: C
authors.lastname: Thèves
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Ahmed H
authors.initials: AH
authors.lastname: Alfarhan
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Saleh A
authors.initials: SA
authors.lastname: Alquraishi
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Khaled A S
authors.initials: KA
authors.lastname: Al-Rasheid
authors.affiliation: Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Lyngby, Denmark;
authors.forename: Thomas
authors.identifier: http://orcid.org/0000-0001-6615-1141
authors.initials: T
authors.lastname: Sicheritz-Ponten
authors.affiliation: Yakutian Research Institute of Agriculture, 677002 Yakutsk, Sakha, Russia;
authors.forename: Ruslan
authors.initials: R
authors.lastname: Popov
authors.affiliation: North-Eastern Federal University, 677000 Yakutsk, Russia;
authors.forename: Semyon
authors.initials: S
authors.lastname: Grigoriev
authors.affiliation: North-Eastern Federal University, 677000 Yakutsk, Russia;
authors.forename: Anatoly N
authors.initials: AN
authors.lastname: Alekseev
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
authors.forename: Edward M
authors.initials: EM
authors.lastname: Rubin
authors.affiliation: College of Veterinary Medicine, University of Minnesota, St. Paul, MN 55108;
authors.forename: Molly
authors.initials: M
authors.lastname: McCue
authors.affiliation: Agroscope, Swiss National Stud Farm, 1580 Avenches, Switzerland;
authors.forename: Stefan
authors.initials: S
authors.lastname: Rieder
authors.affiliation: Institute of Genetics, University of Bern, 3001 Bern, Switzerland;
authors.forename: Tosso
authors.initials: T
authors.lastname: Leeb
authors.affiliation: Zoological Institute of Russian Academy of Sciences, 199034 Saint-Petersburg, Russia;
authors.forename: Alexei
authors.initials: A
authors.lastname: Tikhonov
authors.affiliation: Université de Toulouse, University Paul Sabatier, Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, 31000 Toulouse, France;
authors.forename: Eric
authors.initials: E
authors.lastname: Crubézy
authors.affiliation: Department of Integrative Biology, University of California, Berkeley, CA 94720-3140;
authors.forename: Montgomery
authors.initials: M
authors.lastname: Slatkin
authors.affiliation: Universitat Pompeu Fabra/Consejo Superior de Investigaciones Cientificas, 08003 Barcelona, Spain; Centro Nacional de Análisis Genómico, 08028 Barcelona, Spain;
authors.forename: Tomas
authors.initials: T
authors.lastname: Marques-Bonet
authors.affiliation: Center for Theoretical Evolutionary Genomics, University of California, Berkeley, CA 94720-3140;
authors.forename: Rasmus
authors.initials: R
authors.lastname: Nielsen
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;
authors.forename: Eske
authors.initials: E
authors.lastname: Willerslev
authors.affiliation: Biotechnology and Food Research, Agrifood Research Finland, 31600 Jokioinen, Finland; Department of Biology, University of Eastern Finland, 70211 Kuopio, Finland.
authors.forename: Juha
authors.initials: J
authors.lastname: Kantanen
authors.affiliation: National Research Centre Kurchatov Institute, Moscow 123182, Russia;
authors.forename: Egor
authors.initials: E
authors.lastname: Prokhortchouk
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark; Université de Toulouse, University Paul Sabatier, Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, 31000 Toulouse, France; lorlando@snm.ku.dk.
authors.forename: Ludovic
authors.initials: L
authors.lastname: Orlando
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D001110:Arctic Regions; D003080:Cold Temperature; D019143:Evolution, Molecular; D016678:Genome; D006736:Horses / Q000235:genetics / Q000502:physiology*; D012800:Siberia
keywords: adaptation; ancient genomics; horse; population discontinuity; regulatory changes