NEW YORK (GenomeWeb) – By sequencing nearly 70 pigs from different parts of China, a Jiangxi Agricultural University-led team identified a number of variants that appear to have enabled the various breeds to adapt to their local environments.
As they reported in Nature Genetics today, the researchers also found a large selective sweep on the X chromosome that harbored two haplotypes, one present in pigs living at high latitudes and one in pigs from low latitudes. The adaptive haplotype, the researchers reported, appears to have originated from a now-extinct pig species.
"We identified a genome-wide set of candidate targets of natural selection for local adaptation to environments at varying latitudes in the diverse Chinese pig breeds," said Jiangxi's Lusheng Huang and colleagues in their paper.
Pigs (Sus scrofa) were domesticated in the Near East and China some 10,000 years ago, and there are now about a hundred different breeds living in and adapted to various parts of China. Pigs from southern and northern China have developed different thermoregulatory control mechanisms to cope with the differences in temperature in the regions, the researchers noted.
Huang and colleagues selected 69 pigs from 11 diverse breeds from both warm and cold regions of China for sequencing on the Illumina HiSeq2000 platform. Using the Wuzhishan pig sequence as a reference, they identified more than 40 million SNPs in those 69 pig genomes. These SNP calls, they noted, were largely consistent with those found using the Illumina 60K porcine BeadChip array. About half of the SNPs the researchers found were not in the dbSNP database.
Each breed had an average of nearly 800 putative loss-of-function mutations, though only three mutations appeared to be breed-specific.
The researchers also compared the genomes they generated to a set of publicly available genomes from European and Asian pigs. Population genetics analysis of the two sets showed a clear split between Chinese and European pigs, the researchers said.
Using a locus-specific branch-length analysis of the SNPs they identified, the researchers uncovered 774 possible selective sweeps within the pigs' genomes. Most were about 51 kilobases large, but one on the X chromosome was some 14 megabases large.
Huang and colleagues found 219 genes that corresponded to the autosomal selective sweeps. According to a Gene Ontology analysis, this set was overrepresented with genes involved in regulating body heat. For instance, they uncovered genes enriched in hair cell differentiation, forebrain neuron differentiation, and kidney development, all of which are involved in temperature adaptation.
The most pronounced signal from their locus-specific branch-length analysis traced to a region of chromosome 15 harboring DCAF17, a gene that's been linked to human Woodhouse-Sakati syndrome, which is marked by hair loss among other symptoms. The top SNP in this gene, the researchers said, exhibited allelic imbalance between northern and southern Chinese pigs.
Two nonsynonymous variants the researchers found that also showed differences in allelic frequency between northern and southern pigs corresponded to the VPS13A gene. This gene encodes a blood-platelet regulator, which could affect platelet counts and blood viscosity in southern Chinese pigs, allowing them to better withstand the hot environment, the researchers said.
The X chromosome, meanwhile, had a strong, 14 megabase selective sweep signal, which Huang and colleagues noted was also present in European pigs.
This signal of strong selection, the researchers said, was shared by all northern Chinese breeds, including Tibetan pigs, and had a core haplotype that was distinct from what southern breeds had. Additionally, in both northern and southern breeds, this region showed unusually low heterozygosity. It appears, the researchers said, that more than one selective sweep affected this region to reduce variability, though affecting different haplotypes in the northern and southern pigs.
This region also has a low rate of recombination, the researchers added, arguing that that low rate is likely not due to structural variations, but to an enrichment of poly(T) sequences.
Using a molecular clock model, Huang and colleagues traced these two northern and southern haplotypes back some 8.5 million years ago — a time that far predates the average coalescence time in the pig genome.
Rather, they hypothesized that this sweep was introgressed from a closely related species. They constructed a phylogenetic tree that included four additional Sus species and an African warthog. While the tree for the autosomal region reflected the known Sus evolutionary history, it differed for this 14-Mb region — European and northern Chinese pigs formed their own clade. The African warthog, they noted, remained a divergent outgroup.
This, Huang and colleagues said, suggests that the northern haplotype was introgressed from another, likely extinct Sus species that is an outgroup to S. scrofa and the four additional Sus species in the tree. That haplotype then spread through northern Chinese and European wild boars.
The researchers speculated that this spread might have occurred before Chinese and European boars split some 1.2 million years ago or during the Pleistocene after they diverged.
"Surprisingly, the adaptive haplotype in the northern Chinese populations was likely introduced from another divergent Sus species, providing the first evidence, to our knowledge, that inter-species introgression has driven adaptation in a mammal," Huang and colleagues said.
"The results of this study suggest that introgression between very divergent species might be more important in understanding evolutionary adaptation than previously thought," they added.