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 cisregulatory 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. The Yakutian horse is the most northerly distributed horse on the planet and certainly the most resistant to cold. In contrast to SignificanceYakutia 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.

Fast, Accurate and Automatic Ancient Nucleosome and Methylation Maps with epiPALEOMIX

“…We also included five nonhuman organisms, including four ancient equine specimens (∼0.1–42 kya; Schubert et al 2014; Der Sarkissian et al 2015; Librado et al 2015) and a single aurochs (∼6.7 kyr old) (Park et al 2015). …”

“…Minimum DNA concentration requirements, thus, apply before consistent measures of cytosine methylation can be recovered with this technology (Smith et al 2015). Other direct approaches, such as enrichment procedures based on methylated binding domains (MBD), have been used (Seguin-Orlando, Gamba, et al 2015) but their performance is generally limited given the extensive fragmentation of aDNA templates. In contrast, indirect approaches exploiting the chemical degradation reactions affecting DNA post-mortem are particularly suited to the chemical nature of aDNA.…”

The Evolutionary Origin and Genetic Makeup of Domestic Horses

“…The horse itself currently holds the world record for the oldest genome ever sequenced, which was characterized from bone material preserved in the Yukon permafrost and dated to 560-780 KYA . More recent horse genomes have been now sequenced, including two radiocarbon dated to 43 and 16 KYA and spanning the Upper Paleolithic , one 5,200 years old from the Holocene , and a handful that lived within the last couple of centuries (Der Sarkissian et al 2015;Librado et al 2015). Many more are underway with the aim to reconstruct the history of genetic changes that have accompanied the emergence of the modern horse.…”

“…Presentday mitochondrial haplogroups are almost evenly distributed worldwide and coalesce 93-160 KYA (Lippold et al 2011a;Achilli et al 2012;Schubert et al 2014;Der Sarkissian et al 2015;Librado et al 2015), a time that not only predates the earliest archaeological evidence of domestication, but also the expansion of anatomically modern humans out of Africa. These studies estimated that a minimum of 17 (Achilli et al 2012) and 46 (Lippold et al 2011a) maternal lines successfully passed and survived into the domestic gene pool, with the latter estimate representing 73% of the mtDNA haplotypes that were already segregating prior to domestication (Lippold et al 2011a).…”

“…In addition to Przewalski's and domestic horses, complete genome sequencing of ancient horses recently revealed the existence of a third divergent lineage corresponding to a wild population that inhabited the Holarctic region Librado et al 2015) This population is currently known from the genomes of only three fossil specimens but survived at least until 5.2 KYA, a period contemporary with the early stages of the domestication process. Schubert et al (2014) found that this population significantly contributed to the genetic makeup of domestic horses, with at least 12.9% of modern domestic genomes showing ancestry to this nowextinct lineage (Figure 2).…”