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Population history and genomic signatures for high-altitude adaptation in Tibetan pigs.

Ai H, Yang B, Li J, Xie X, Chen H, Ren J - BMC Genomics (2014)

Bottom Line: Several geographically isolated pig populations are distributed throughout the Plateau.Tibetan pig populations have experienced substantial genetic differentiation.Different Tibetan pig populations appear to have both distinct and convergent adaptive loci for the harsh environment of the Plateau.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory for Animal Biotechnology of Jiangxi Province and the Ministry of Agriculture of China, Jiangxi Agricultural University, Nanchang 330045, P, R China. renjunjxau@hotmail.com.

ABSTRACT

Background: The Tibetan pig is one of domestic animals indigenous to the Qinghai-Tibet Plateau. Several geographically isolated pig populations are distributed throughout the Plateau. It remained an open question if these populations have experienced different demographic histories and have evolved independent adaptive loci for the harsh environment of the Plateau. To address these questions, we herein investigated ~ 40,000 genetic variants across the pig genome in a broad panel of 678 individuals from 5 Tibetan geographic populations and 34 lowland breeds.

Results: Using a series of population genetic analyses, we show that Tibetan pig populations have marked genetic differentiations. Tibetan pigs appear to be 3 independent populations corresponding to the Tibetan, Gansu and Sichuan & Yunnan locations. Each population is more genetically similar to its geographic neighbors than to any of the other Tibetan populations. By applying a locus-specific branch length test, we identified both population-specific and -shared candidate genes under selection in Tibetan pigs. These genes, such as PLA2G12A, RGCC, C9ORF3, GRIN2B, GRID1 and EPAS1, are involved in high-altitude physiology including angiogenesis, pulmonary hypertension, oxygen intake, defense response and erythropoiesis. A majority of these genes have not been implicated in previous studies of highlanders and high-altitude animals.

Conclusion: Tibetan pig populations have experienced substantial genetic differentiation. Historically, Tibetan pigs likely had admixture with neighboring lowland breeds. During the long history of colonization in the Plateau, Tibetan pigs have developed a complex biological adaptation mechanism that could be different from that of Tibetans and other animals. Different Tibetan pig populations appear to have both distinct and convergent adaptive loci for the harsh environment of the Plateau.

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Related in: MedlinePlus

Population split and historical mixture for Tibetan pigs in a context of Chinese diverse breeds. Arrows indicate migration events among Chinese indigenous breeds. A spectrum of heat colors indicates different migration weights at the migration event.
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Fig2: Population split and historical mixture for Tibetan pigs in a context of Chinese diverse breeds. Arrows indicate migration events among Chinese indigenous breeds. A spectrum of heat colors indicates different migration weights at the migration event.

Mentions: To further infer population splits and mixtures of Tibetan pigs, we used a recently developed approach, Treemix [21], to construct a maximum-likelihood tree of the 5 Tibetan populations, 21 Chinese lowland breeds and 1 Chinese wild boar population. A close examination of residuals from the inferred tree without migration events (Additional file 5: Figure S4) revealed that 6 pairs of populations were apparently not compatible with the best-fit tree, suggestive of gene flow events. Indeed, the tree model without migration events only explained 89.9% of the variance in the relatedness between populations. We sequentially added migration events to the maximum-likelihood tree (Figure 2). The new tree model allowing 6 major migration events explained higher percentage (96.0%) of the variance in the relatedness between populations. In the inferred graph (Figure 2), the regional populations from Tibet, Yunnan and Sichuan provinces were grouped into one of the two major groupings, whereas the Gansu Tibetan population clusters with the other major grouping consisting of Bamei and Hetao pigs. An ancestral edge further divided Tibet and Yunnan/Sichuan populations into different subgroups. Again, Yunan and Sichuan Tibetan populations clustered with their geographic neighbors Neijiang and Rongchang. Of the six migration events, the strongest signal suggests a genetic contribution from the ancestry of Tongcheng, Shaziling and Ganxi breeds to Dongshan pigs (migration weight (w) = 49.9%). Another visually apparent event is a gene flow from the ancestry of Wuzhishan and Luchuan pigs into Diannan pigs (w = 49.2%). We also inferred a significant admixture event from Meishan to Hetao individuals (w = 33.8%). For Tibetan pigs, we found a gene flow event from the early Gansu Tibetan population into the ancestry of the other four Tibetan populations with a migration weight of 38.8%.Figure 2


Population history and genomic signatures for high-altitude adaptation in Tibetan pigs.

Ai H, Yang B, Li J, Xie X, Chen H, Ren J - BMC Genomics (2014)

Population split and historical mixture for Tibetan pigs in a context of Chinese diverse breeds. Arrows indicate migration events among Chinese indigenous breeds. A spectrum of heat colors indicates different migration weights at the migration event.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4197311&req=5

Fig2: Population split and historical mixture for Tibetan pigs in a context of Chinese diverse breeds. Arrows indicate migration events among Chinese indigenous breeds. A spectrum of heat colors indicates different migration weights at the migration event.
Mentions: To further infer population splits and mixtures of Tibetan pigs, we used a recently developed approach, Treemix [21], to construct a maximum-likelihood tree of the 5 Tibetan populations, 21 Chinese lowland breeds and 1 Chinese wild boar population. A close examination of residuals from the inferred tree without migration events (Additional file 5: Figure S4) revealed that 6 pairs of populations were apparently not compatible with the best-fit tree, suggestive of gene flow events. Indeed, the tree model without migration events only explained 89.9% of the variance in the relatedness between populations. We sequentially added migration events to the maximum-likelihood tree (Figure 2). The new tree model allowing 6 major migration events explained higher percentage (96.0%) of the variance in the relatedness between populations. In the inferred graph (Figure 2), the regional populations from Tibet, Yunnan and Sichuan provinces were grouped into one of the two major groupings, whereas the Gansu Tibetan population clusters with the other major grouping consisting of Bamei and Hetao pigs. An ancestral edge further divided Tibet and Yunnan/Sichuan populations into different subgroups. Again, Yunan and Sichuan Tibetan populations clustered with their geographic neighbors Neijiang and Rongchang. Of the six migration events, the strongest signal suggests a genetic contribution from the ancestry of Tongcheng, Shaziling and Ganxi breeds to Dongshan pigs (migration weight (w) = 49.9%). Another visually apparent event is a gene flow from the ancestry of Wuzhishan and Luchuan pigs into Diannan pigs (w = 49.2%). We also inferred a significant admixture event from Meishan to Hetao individuals (w = 33.8%). For Tibetan pigs, we found a gene flow event from the early Gansu Tibetan population into the ancestry of the other four Tibetan populations with a migration weight of 38.8%.Figure 2

Bottom Line: Several geographically isolated pig populations are distributed throughout the Plateau.Tibetan pig populations have experienced substantial genetic differentiation.Different Tibetan pig populations appear to have both distinct and convergent adaptive loci for the harsh environment of the Plateau.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory for Animal Biotechnology of Jiangxi Province and the Ministry of Agriculture of China, Jiangxi Agricultural University, Nanchang 330045, P, R China. renjunjxau@hotmail.com.

ABSTRACT

Background: The Tibetan pig is one of domestic animals indigenous to the Qinghai-Tibet Plateau. Several geographically isolated pig populations are distributed throughout the Plateau. It remained an open question if these populations have experienced different demographic histories and have evolved independent adaptive loci for the harsh environment of the Plateau. To address these questions, we herein investigated ~ 40,000 genetic variants across the pig genome in a broad panel of 678 individuals from 5 Tibetan geographic populations and 34 lowland breeds.

Results: Using a series of population genetic analyses, we show that Tibetan pig populations have marked genetic differentiations. Tibetan pigs appear to be 3 independent populations corresponding to the Tibetan, Gansu and Sichuan & Yunnan locations. Each population is more genetically similar to its geographic neighbors than to any of the other Tibetan populations. By applying a locus-specific branch length test, we identified both population-specific and -shared candidate genes under selection in Tibetan pigs. These genes, such as PLA2G12A, RGCC, C9ORF3, GRIN2B, GRID1 and EPAS1, are involved in high-altitude physiology including angiogenesis, pulmonary hypertension, oxygen intake, defense response and erythropoiesis. A majority of these genes have not been implicated in previous studies of highlanders and high-altitude animals.

Conclusion: Tibetan pig populations have experienced substantial genetic differentiation. Historically, Tibetan pigs likely had admixture with neighboring lowland breeds. During the long history of colonization in the Plateau, Tibetan pigs have developed a complex biological adaptation mechanism that could be different from that of Tibetans and other animals. Different Tibetan pig populations appear to have both distinct and convergent adaptive loci for the harsh environment of the Plateau.

Show MeSH
Related in: MedlinePlus