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Genome Sequencing Suggests Yakutian Horses Adapted Rapidly to Subarctic

Yakutian horse

NEW YORK (GenomeWeb) – Yakutian horses appear to have undergone relatively rapid adaptation to their forbidding environment in Siberia's Far East, according to a study published online this week in the Proceedings of the National Academy of Sciences.

An international team led by investigators at the University of Copenhagen did genome sequencing on nine modern-day Yakutian horses, along with two ancient horse samples from the region, one from the early 19th century and another from 5,200 years ago. The genomes were then compared to one another and to existing sequences for dozens of domestic, Przewalski's, and ancient horses.

From these data, the researchers concluded that the present Yakutian horse population is made up of descendants of horses introduced by the Yakut people within the last several centuries, rather than of ancient native horses. Since their arrival, the animals appear to have undergone adaptations — many of them regulatory — to pathways involved in vasoconstriction, hair density, body size, hormones, and metabolism.

"There used to be another population of horses," senior author Ludovic Orlando, a researcher at the University of Copenhagen's Centre for GeoGenetics, told GenomeWeb. "This has become extinct and was totally replaced by horses that came [to the region] 700 years ago."

"That tells you something about how fast adaptation processes can go in mammals," Orlando said.

Although people in Yakutia started farming cattle in around the 19th century, he explained, the Yakutian horses have played a central role in the region's economy for hundreds of years.

In contrast to cattle, which are brought in from the fields during the winter, and free-range reindeer populations managed by the Yakut people, the Yakutian horse represented a domesticated animal that has become intimately adapted to its Siberian Far Eastern environment.

The horses are known for their thick, dense, winter coats and heat maximizing body size — just some of the adaptations that have allowed them to survive outside all year, despite temperatures that dip to around -70C (-94F) in the winter months.

Because the Yakut are traditionally a horse-riding population, Orlando noted, there has been speculation that this group brought horses with them to Siberia when it was displaced from a region around Russia's Lake Baikal by an expanding Mongolian empire in the 13th to 15th century.

Still, there was debate over whether horses found in Yakutia today are descended from animals introduced by the Yakut, from horses present in the region prior to their arrival, or from mixing between domestic and native horses.

To explore horse population history and get a look at genomic adaptations in the Yakutian horses, the researchers used Illumina sequencing to tackle DNA extracted from hair samples for a dozen modern-day Yakutian horses.

They also attempted to sequence DNA from nine ancient horse bone and tooth samples processed with methods tailored to the short pieces of DNA that are typically present in very old samples.

The resequenced genomes reached nine- to almost 22-fold coverage for nine of the modern horses, while two ancient horse samples originating in the Verkhoyansk region — from a 19th century horse and a 5,200 year old "Batagai" horse — yielded high-quality genome and mitochondrial sequences.

"We took two ancient time points in the Yakutian [horse] history," Orlando said, noting that the ancient samples span time points prior to and after the Yakut people's arrival.

After mapping Yakutian horse sequences to a horse reference genome, the researchers compared them to a panel of sequences from modern and ancient horses around the world including 27 animals from domestic breeds as well as three Przewalski's horses.

Their phylogenetic analyses placed the nine modern-day Yakutian horses and the Yakutian horse from the 19th century squarely within the diversity of domesticated horses, falling closest to the Mongolian, Fjord, and Icelandic horses.

On the other hand, a 5,200-year-old horse sample from the same region clustered with a clade of ancient, early-diverged horse lineage that Orlando and his colleagues discovered by sequencing ancient horse samples from Siberia's Taymyr peninsula — work they described in PNAS last year.

"The population from the Taymyr peninsula does not coincide with anything that paleontologists have ever described," Orlando explained, noting that this group is estimated to have diverged from the modern horse lineage around 160,000 years ago. When adjusted for horse generation times, that lineage appears to be about as diverged from modern horses as humans are from Neanderthals, he noted.

The latest findings suggest Taymyr horses may have been both more geographically widespread and long-lived than once suspected, surviving until at least 5,000 years ago.

Prior research suggests modern-day domestic horse breeds have low levels of ancestry from this ancient "Neanderthal horse" as well, providing the opportunity to use the proportion of Taymyr horse sequences as a gauge for more recent admixture between native and domesticated horses in Yakutia.

Rather than finding additional ancestry in the Yakutian horses, though, the team found that both the modern and 19th century genomes had Taymyr horse ancestry levels on par with those described in other domestic horse breeds, arguing against additional mixing in the region.

Instead, the researchers suspect that horses introduced by the Yakut people in roughly the 13th century either displaced or appeared after the extinction of native horses. That, in turn, suggests Yakutian horses have adapted to life in Siberia during a span of just 700 or 800 years, consistent with an apparent founder event in the horse population at around that time.

When the team delved into the genomic nature of these adaptations, it found that many of the genome-wide SNP differences between Yakutian and other modern breeds fell in non-coding, regulatory regions falling within 10,000 bases upstream of transcription start sites.

"This is where [gene] promoters are known to be located," Orlando said, explaining that such changes "are not affecting, directly, the sequence produced by the gene but probably affect expression of the gene itself."

Nevertheless, when protein-coding or candidate copy number changes did appear in the Yakutian horse genomes, they tended to involve genes from the same pathways affected by regulatory changes, particularly those from hair density, body size, hormonal, and metabolic pathways.

Finally, the team saw intriguing changes affecting the horse version of genes implicated in cold adaptations in the woolly mammoth and in human inhabitants of the far north, hinting that such changes represent convergent adaptations.

The researchers are continuing to study the Yakutian horse population and hopes to use gene expression, epigenetic, and metabolomics profiling to further explore the role regulatory regions play in adaptation and to assess the phenotypic effects of these changes.