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Ancient Horse Samples Offer Hints to Domestication

NEW YORK (GenomeWeb) – An international team has retraced some of the genetic features that seem to characterize domesticated horses with the help of newly generated genome sequences representing ancient, pre-domestication horses from Russia.

As they reported in the early, online edition of the Proceedings of the National Academy of Sciences this week, researchers from Denmark, the US, and elsewhere did genome sequencing on horse remains retrieved from a Siberian permafrost site in the Taymyr peninsula. One of the samples was dated at almost 16,100 years old, while the other appears to be nearly 43,000 years old, marking points in history long before horses were domesticated.

By comparing the genomes to those of half a dozen other horses — five from domestic horse breed's and one wild Przewalski's horse — the team more fully defined relationships between wild and domestic horses, identifying more than 100 genes showing signs of selection that may be related to the domestication process.

"We were thinking, 'Let's compare pre-domesticated horses to modern horses and let's use comparative genomics to tease out what it is [humans have] selected since," senior author Ludovic Orlando, a researcher with the University of Copenhagen's Centre for GeoGenetics, told GenomeWeb.

In a study published last year in Nature, Orlando and colleagues considered sequences from a 700,000-year-old horse fossil from Canada's Yukon Territory, along with sequences from a donkey outgroup and representatives from several horse breeds — an analysis that argued for divergence in the equine lineage that stretches back at least four million years.

Members of the same team decided to use some of the same methods for optimizing ancient DNA in sequencing libraries to look at more recent events in equine evolution, particularly those related to horse domestication, Orlando explained.

Historical evidence puts horse domestication at a point within the past 5,500 or more years, authors of the current study noted. In that time, the animals have helped transform how humans travel, trade products and social practices, and take up arms against one another.

The genetic processes that accompanied the transition from wild to domestic horses remain incompletely defined, they explained, in part because few wild horses have persisted. Those that do — members of the Przewalski's horse breed in Mongolia — are part of a sister lineage to domestic breeds, rather than one that's ancestral to domesticated horses.

"The [Przewalski's horses] were not really good animals to compare domestic horses against because their divergence time was too far off," Orlando said. "So, there's no good, living surrogate for the [ancestral] wild horse, even if there are wild horses around."

Moreover, researchers suspect that genetic diversity in the Przewalski's horse has been winnowed down compared to more ancient wild horses, due to factors such as inbreeding and demographic bottlenecks.

The team attempted to further unravel horse relationships and domestication history using samples from a permafrost site in Siberia where dozens of ancient horse bones were discovered.

Using Illumina sequencing instruments and DNA from two of the samples, the researchers generated sequences that covered the horse reference genome to an average depth of 24.3-fold coverage in the case of the 42,692-year-old sample, and 7.4-fold average coverage for the 16,099-year-old sample.

The samples came from the Late Pleistocene period, Orlando explained, a period in history during which dogs are the only animal that's believed to have been domesticated.

Although the mitochondrial sequences overlapped with the genetic diversity found in present-day horses, the team's phylogenetic look at variants in the protein-coding portions of the genome placed the ancient Russian horses in a group that's genetically distinct of both domestic horses and the Przewalski's horse.

Whereas the domesticated horse lineage appears to have split from the lineage leading to Przewalski's horse roughly 43,000 to 52,000 years ago, the researchers reported, the Russian horses appear to have belonged to a group that diverged from the common ancestor of both of those groups some 127,000 to 159,000 years ago.

"There seems to be three populations of horses," Orlando said. "There are the Przewalski's horse population on one hand and the domestic horses on the other hand. And then there's another one, which is basically the ancient horse population."

Nevertheless, the team saw signs of past mixing between members of the ancient wild lineage represented by the Russian horses and domestic horses. Results from the study suggest that at least 15 percent of domestic horse sequence can be traced back to the wild population, which appears to have admixed with domestic horses after the Przewalski's horse-domestic horse split.

The study's authors suspect this mixing was a consequence of so-called "re-stocking" of domestic horses from wild horse populations, Orlando noted. "Basically, when [humans] started domesticating horses, we re-stocked the domestic gene pool from the wild."

Through a series of subsequent analyses, the team compared features in the wild and domestic horse genomes, searching for sites in the genome that were changed by domestication and could be detected using multiple methods for seeing selection.

That search led to 125 genes in the horse genome that showed potential signs of selection related to domestication. This set included genes believed to be involved in locomotion-related features such as muscle development, bone development, heart formation, and cardiovascular capabilities.

Other genes with potential ties to domestication had proposed roles in the shape of bone in the horse face and head, as well as genes associated with behavioral traits such as cognition, learning, fear, and agreeableness.

Finally, the study's authors also described an apparent jump in deleterious mutations in domesticated horse genomes, which were identified using an indirect approach that picked out sites that are highly conserved in other mammalian sequences but altered in modern horses.

That finding fits with the notion that domestication extracts a toll on the species involved by dialing down the strength of selective processes that normally weed out detrimental variants — a theory proposed in the past based on genetic patterns in other domesticated animals and plants.

Orlando and his team are continuing to apply ancient DNA analysis strategies to test horse samples collected over space and time in the hopes of untangling domestication-related features that may have arisen as horses adapted to handle new jobs humans have given them — from pulling chariots or plows to providing rides for mounted cavalry.

"We have identified a series of archeological 'seams,' as we call them, because we know from the archaeological record and from cultural evidence that things have been changing at those times," Orlando said.

"You can imagine that with chariots, with cavalry, or with something else, we would need to select slightly different things," he said. "So maybe some of those have constituted selective pressures to shape the horse in a given way at a given time."

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