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Edited by Andrew G. Clark, Cornell University, Ithaca, NY, and approved October 27, 2015 (received for review July 14, 2015)
Significance
Yakutia is among the coldest regions in the Northern Hemisphere, showing ∼40% of its territory above the Arctic Circle. Native horses are particularly adapted to this environment, with body sizes and thick winter coats minimizing heat loss. We sequenced complete genomes of two ancient and nine present-day Yakutian horses to elucidate their evolutionary origins. We find that the contemporary population descends from domestic livestock, likely brought by early horse-riders who settled in the region a few centuries ago. The metabolic, anatomical, and physiological adaptations of these horses therefore emerged on very short evolutionary time scales. We show the relative importance of regulatory changes in the adaptive process and identify genes independently selected in cold-adapted human populations and woolly mammoths.
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.
Footnotes
↵1P.L. and C.D.S. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: lorlando{at}snm.ku.dk.
Author contributions: L.O. designed research; C.D.S., L.E., S.T., M.N., V.J., R.P., J.K., E.P., and L.O. performed research; A.S.-O., C.D.M., B.P., C.A.H., B.L.-G., A.N., E.B., C.T., A.H.A., S.A.A., K.A.S.A.-R., T.S.-P., R.P., S.G., A.N.A., E.M.R., M.M., S.R., T.L., A.T., E.C., T.M.-B., E.W., J.K., E.P., and L.O. contributed new reagents/analytic tools; P.L., C.D.S., L.E., M. Schubert, H.J., A.A., M.F., M.A.Y., C.G., B.P., M. Slatkin, R.N., and L.O. analyzed data; and L.O. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequencing data reported in this paper have been deposited in the European Nucleotide Archive (accession no. PRJEB10854).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1513696112/-/DCSupplemental.
Freely available online through the PNAS open access option.
Evolutionary genomics of Yakutian horses
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