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Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression.

Bosse M, Megens HJ, Frantz LA, Madsen O, Larson G, Paudel Y, Duijvesteijn N, Harlizius B, Hagemeijer Y, Crooijmans RP, Groenen MA - Nat Commun (2014)

Bottom Line: The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics.We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines.These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.

View Article: PubMed Central - PubMed

Affiliation: Animal Breeding and Genomics Centre, Wageningen University, Wageningen 6708 WD, The Netherlands.

ABSTRACT
The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics. During the Industrial Revolution, Chinese breeds were imported to Europe to improve commercial traits in European breeds. Here we demonstrate the presence of introgressed Asian haplotypes in European domestic pigs and selection signatures on some loci in these regions, using whole genome sequence data. The introgression signatures are widespread and the Asian haplotypes are rarely fixed. The Asian introgressed haplotypes are associated with regions harbouring genes involved in meat quality, development and fertility. We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines. These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.

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Levels of differentiation between LW and ASDom or EUWB in regions of introgression(a) Relative introgression fraction (rIBD) over the full length of chromosome 8 and 9. The longest regions of introgression are indicated with purple and blue. (b) Boxplot of D-statistics for the full genome (red) and the two longest regions of introgression as indicated in a on chr8 (purple) and chr9 (blue). The minimum, first quartile, median, third quartile and maximum are indicated with the box and whiskers with outliers >1.5*IQR. D-statistics are computed for each possible trio with LW=P1, ASDom=P2 and EUWB=P3, with the Sumatran S. scrofa as outgroup (O) resulting in 378 trios. (c–e) Distribution of Fst between LW-ASDom (blue) and LW-EUWB (red) in bins of 10 Kbp. The left histogram shows the Fst distributions based on the full genome (c), and the other two show the Fst distribution for the regions of introgression on chr8 (d) and chr9 (e).
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Figure 3: Levels of differentiation between LW and ASDom or EUWB in regions of introgression(a) Relative introgression fraction (rIBD) over the full length of chromosome 8 and 9. The longest regions of introgression are indicated with purple and blue. (b) Boxplot of D-statistics for the full genome (red) and the two longest regions of introgression as indicated in a on chr8 (purple) and chr9 (blue). The minimum, first quartile, median, third quartile and maximum are indicated with the box and whiskers with outliers >1.5*IQR. D-statistics are computed for each possible trio with LW=P1, ASDom=P2 and EUWB=P3, with the Sumatran S. scrofa as outgroup (O) resulting in 378 trios. (c–e) Distribution of Fst between LW-ASDom (blue) and LW-EUWB (red) in bins of 10 Kbp. The left histogram shows the Fst distributions based on the full genome (c), and the other two show the Fst distribution for the regions of introgression on chr8 (d) and chr9 (e).

Mentions: Chromosomes 8 and 9 contain the largest consecutive regions of inferred introgression in the LW genomes (defined as regions where rIBD>0). To check whether the extended haplotype homozygosity in the LW pool was specific for the breed or observed in more European breeds, we contrasted the LW signal with a reference pool of other European commercial pigs with the Rsb statistic27 (Supplementary Fig. 1b,c). This analysis demonstrates that the region of introgression on chromosome 8 contains a stronger extended haplotype homozygosity (EHH) signal in the reference panel, and that the region on chromosome 9 contains a particularly strong signal in the LW population. We used two independent methods, D-statistics and Fst, to support the detected introgression in these regions in the LW (Fig. 3a-e). To show that divergence between LW and ASDom was reduced in the introgressed regions, we calculated Fst for these regions separately. The Fst between ASDom and the LW was lower in both introgressed regions than between EUWB and LW (Fig. 3c-e), thereby supporting the signal of Asian introgression (high rIBD). The D-statisctics for the regions on chromosome 9 was lower than the genome-wide average, which corroborated our rIBD analysis (Fig. 3b). The region on chromosome 8 shows a wide distribution, indicating that some LW haplotypes contain the Asian signature, while others do not. Inconsistent clustering of European haplotypes within an Asian clade at this locus supports this hypothesis (Supplementary Fig. 2). Curiously, the ~4 Mb sequence shows a clear signal of introgression, although a large part of the region is devoid of annotated genes. As this part of the genome has a relatively low recombination frequency25, the region may extend considerably beyond the position of the actual favourable allele that has been selected for, due to genetic hitch-hiking and the short time since introgression. Alternatively, drift could have resulted in the presence of Asian haplotypes in this region. The PGRMC2 gene, coding for the progesterone receptor, lies within the highest peak of Asian haplotypes in that region. Progesterone is an important hormone involved in female reproduction and maternal behaviour28, traits that Asian pigs have been selected for extensively. Therefore, the Asian haplotype containing the PGRMC2 gene could be associated with higher reproductive success in LW pigs and may have been subjected to selection pressure as a result. The Rsb signal suggest that in other European breeds, the proportion of Asian haplotypes is even higher for this locus (Supplementary Fig. 1b,c). We used genotype data from the Illumina Porcine 60K iSelect beadchip29 for an additional 5,143 pigs from three European commercial lines to screen allele frequencies in this region. Two genetic lines have been selected for reproductive traits since the establishment of the lines (A and B), and one line for finishing traits (C). The SNP alleles in this 4-Mb region show a clear difference between the two reproduction-associated lines and the growth-associated line (Supplementary Fig. 3). These findings could indicate that the Asian haplotypes in this region are associated with fertility, but further analyses are needed to support this hypothesis.


Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression.

Bosse M, Megens HJ, Frantz LA, Madsen O, Larson G, Paudel Y, Duijvesteijn N, Harlizius B, Hagemeijer Y, Crooijmans RP, Groenen MA - Nat Commun (2014)

Levels of differentiation between LW and ASDom or EUWB in regions of introgression(a) Relative introgression fraction (rIBD) over the full length of chromosome 8 and 9. The longest regions of introgression are indicated with purple and blue. (b) Boxplot of D-statistics for the full genome (red) and the two longest regions of introgression as indicated in a on chr8 (purple) and chr9 (blue). The minimum, first quartile, median, third quartile and maximum are indicated with the box and whiskers with outliers >1.5*IQR. D-statistics are computed for each possible trio with LW=P1, ASDom=P2 and EUWB=P3, with the Sumatran S. scrofa as outgroup (O) resulting in 378 trios. (c–e) Distribution of Fst between LW-ASDom (blue) and LW-EUWB (red) in bins of 10 Kbp. The left histogram shows the Fst distributions based on the full genome (c), and the other two show the Fst distribution for the regions of introgression on chr8 (d) and chr9 (e).
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Figure 3: Levels of differentiation between LW and ASDom or EUWB in regions of introgression(a) Relative introgression fraction (rIBD) over the full length of chromosome 8 and 9. The longest regions of introgression are indicated with purple and blue. (b) Boxplot of D-statistics for the full genome (red) and the two longest regions of introgression as indicated in a on chr8 (purple) and chr9 (blue). The minimum, first quartile, median, third quartile and maximum are indicated with the box and whiskers with outliers >1.5*IQR. D-statistics are computed for each possible trio with LW=P1, ASDom=P2 and EUWB=P3, with the Sumatran S. scrofa as outgroup (O) resulting in 378 trios. (c–e) Distribution of Fst between LW-ASDom (blue) and LW-EUWB (red) in bins of 10 Kbp. The left histogram shows the Fst distributions based on the full genome (c), and the other two show the Fst distribution for the regions of introgression on chr8 (d) and chr9 (e).
Mentions: Chromosomes 8 and 9 contain the largest consecutive regions of inferred introgression in the LW genomes (defined as regions where rIBD>0). To check whether the extended haplotype homozygosity in the LW pool was specific for the breed or observed in more European breeds, we contrasted the LW signal with a reference pool of other European commercial pigs with the Rsb statistic27 (Supplementary Fig. 1b,c). This analysis demonstrates that the region of introgression on chromosome 8 contains a stronger extended haplotype homozygosity (EHH) signal in the reference panel, and that the region on chromosome 9 contains a particularly strong signal in the LW population. We used two independent methods, D-statistics and Fst, to support the detected introgression in these regions in the LW (Fig. 3a-e). To show that divergence between LW and ASDom was reduced in the introgressed regions, we calculated Fst for these regions separately. The Fst between ASDom and the LW was lower in both introgressed regions than between EUWB and LW (Fig. 3c-e), thereby supporting the signal of Asian introgression (high rIBD). The D-statisctics for the regions on chromosome 9 was lower than the genome-wide average, which corroborated our rIBD analysis (Fig. 3b). The region on chromosome 8 shows a wide distribution, indicating that some LW haplotypes contain the Asian signature, while others do not. Inconsistent clustering of European haplotypes within an Asian clade at this locus supports this hypothesis (Supplementary Fig. 2). Curiously, the ~4 Mb sequence shows a clear signal of introgression, although a large part of the region is devoid of annotated genes. As this part of the genome has a relatively low recombination frequency25, the region may extend considerably beyond the position of the actual favourable allele that has been selected for, due to genetic hitch-hiking and the short time since introgression. Alternatively, drift could have resulted in the presence of Asian haplotypes in this region. The PGRMC2 gene, coding for the progesterone receptor, lies within the highest peak of Asian haplotypes in that region. Progesterone is an important hormone involved in female reproduction and maternal behaviour28, traits that Asian pigs have been selected for extensively. Therefore, the Asian haplotype containing the PGRMC2 gene could be associated with higher reproductive success in LW pigs and may have been subjected to selection pressure as a result. The Rsb signal suggest that in other European breeds, the proportion of Asian haplotypes is even higher for this locus (Supplementary Fig. 1b,c). We used genotype data from the Illumina Porcine 60K iSelect beadchip29 for an additional 5,143 pigs from three European commercial lines to screen allele frequencies in this region. Two genetic lines have been selected for reproductive traits since the establishment of the lines (A and B), and one line for finishing traits (C). The SNP alleles in this 4-Mb region show a clear difference between the two reproduction-associated lines and the growth-associated line (Supplementary Fig. 3). These findings could indicate that the Asian haplotypes in this region are associated with fertility, but further analyses are needed to support this hypothesis.

Bottom Line: The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics.We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines.These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.

View Article: PubMed Central - PubMed

Affiliation: Animal Breeding and Genomics Centre, Wageningen University, Wageningen 6708 WD, The Netherlands.

ABSTRACT
The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics. During the Industrial Revolution, Chinese breeds were imported to Europe to improve commercial traits in European breeds. Here we demonstrate the presence of introgressed Asian haplotypes in European domestic pigs and selection signatures on some loci in these regions, using whole genome sequence data. The introgression signatures are widespread and the Asian haplotypes are rarely fixed. The Asian introgressed haplotypes are associated with regions harbouring genes involved in meat quality, development and fertility. We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines. These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.

Show MeSH
Related in: MedlinePlus