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China-led Study Unearths Sequences Under Selection in Tibetan Boar, Domestic Pigs

NEW YORK (GenomeWeb News) – A study appearing online yesterday in Nature Genetics highlights the genomic changes, adaptation, and selective sweeps that have shaped wild boar and pig populations in Asia and beyond.

An international team led by investigators in China began by sequencing the genome of a Tibetan wild boar, before doing low-coverage resequencing on dozens more wild boars and pigs. Comparisons of the sequences and variants therein offered a peek at existing genetic diversity and relationships between pig populations, along with past events in pig evolution and domestication.

In particular, the researchers picked up on apparent sites of artificial selection in the genomes of domestic pigs in China and genes involved in a range of domestic pig traits. They also narrowed in on genomic regions and candidate genes suspected of contributing to adaptations found in wild boars from the Tibet plateau.

"Comparing the genome of the Tibetan wild boar with those of neighboring Chinese domestic pigs … showed the impact of thousand[s] of years of artificial selection and different signatures of selection in wild boar and domestic pig," the study's co-senior authors Ruiqiang Li, with Peking University and the Novogene Bioinformatics Institute, and Sichuan Agricultural University's Xuewei Li, and their colleagues wrote.

"We also report genetic adaptations in Tibetan wild boar that are associated with high altitudes and characterize the genetic basis of increased salivation in domestic pig," they added.

Although the Tibetan wild boar has been subject to natural sources of selection related to its origins on the high-altitude Tibetan plateau, the researchers noted, the animals have only recently been exposed to the sorts of human-imposed selection sources that have acted on domestic pig genomes.

"The sequence of Tibetan wild boar, a representative of Asian wild boar, and comparative analyses with the domestic Duroc pig genome can potentially shed light on pig genomic diversity and the genetic components that are shaped by high-altitude adaptation in Tibetan wild boar and by artificial selection in domestic pigs," they wrote.

The researchers used a combination of whole-genome shotgun sequencing and Illumina short read sequencing to tackle the genome of a female Tibetan wild boar, generating sequences that cover the animal's genome at a depth of around 131-fold.

After piecing wild boar sequences together into a 2.43 billion base genome assembly, the team annotated the new genome and compared it to that of the domestic Duroc pig, sequenced by members of the Swine Genome Sequencing consortium last year.

Analysis of the Tibetan wild boar sequence led to 21,806 predicted protein-coding genes, including 10,190 of the same genes described in the Duroc pig and in humans and another 3,074 genes that appear to be specific to the Tibetan wild boar lineage.

Since the split between lineages leading to the Tibetan wild boar and the Duroc pig — estimated at some 6.9 million years ago in the current study — the wild boar appears to have acquired genes contributing to DNA replication, blood circulation, and immune-related processes, the researchers reported.

Expansions to gene families seem to have been less common in the Tibetan wild boar lineage than in the lineage leading to Duroc pigs, they added, though the wild boar genome contains a wealth of ferritin-coding genes suspected of helping the animals deal with the low oxygen levels found at high elevations.

A search for sequences under selection in the genomes of the wild and domestic representatives provided additional clues about genes that have helped Tibetan wild boars flourish at high altitude, the group found, including genes involved in hypoxia, reproduction, and ultraviolet light response.

On the other hand, the domestic Duroc pig genome houses a more pronounced set of genes participating in the interferon-induced immunity and genes contributing to olfaction, the study authors found. In those animals, sequences under positive selection tended to fall in and around genes participating in energy metabolism, muscle growth, and the like.

To get a closer look at population and evolutionary patterns in pigs and boars, the investigators went on to do low-coverage genome re-sequencing on another 30 Tibetan wild boars from half a dozen locations, 15 domestic pigs from China, and three Chinese wild boars.

Together with sequences from pigs assessed for prior studies, the resequenced genomes made it possible to pick up on variants that informed the team's population and selection studies of the pigs and boars.

For example, researchers found that boars and pigs from Europe clustered separately from those in Asia. They also saw genetic differences between Tibetan wild boars and Chinese boars and pigs and between domestic pigs in southwest and southeast China.

Based on patterns at nearly 9.5 million SNPs in the expanded sequence set, the team began teasing apart the selection effects of artificial breeding and domestication in pigs from natural selection on the Tibetan wild boars — an analysis that pointed to more widespread effects for selective processes introduced by humans during pig domestication.

Indeed, study authors noted, the findings support the notion that "artificial selection is more powerful than natural selection in shaping the genome, resulting in rapid changes in phenotypic and/or behavioral traits in domestic pigs."

Along with similar olfaction- and muscle-related adaptations to those detected in the Duroc pig genome, for example, the population data pinpointed sequences that seem to boost saliva production by domestic pigs, they reported, perhaps bolstering the release of pheromones or other chemical signals carried in domestic swine spit.

"In addition to enhancing mate recognition, increased saliva secretion and a possibly associated increase in amylase [enzyme] may also help domestic pig maximize its digestive efficiencies when supplied with starch-rich concentrates," the researchers noted, "or may serve as an indicator of hunger in order to take in more food."

Last month, members of another international team published a study in Genome Biology that used genome sequences from five pig species and one African common warthog, an outgroup animal from another species, to explore pig speciation in island regions of Southeast Asia.