Signatures of diversifying selection in European pig breeds

Abstract

Following domestication, livestock breeds have experienced intense selection pressures for the development of desirable traits. This has resulted in a large diversity of breeds that display variation in many phenotypic traits, such as coat colour, muscle composition, early maturity, growth rate, body size, reproduction, and behaviour. To better understand the relationship between genomic composition and phenotypic diversity arising from breed development, the genomes of 13 traditional and commercial European pig breeds were scanned for signatures of diversifying selection using the Porcine60K SNP chip, applying a between-population (differentiation) approach. Signatures of diversifying selection between breeds were found in genomic regions associated with traits related to breed standard criteria, such as coat colour and ear morphology. Amino acid differences in the EDNRB gene appear to be associated with one of these signatures, and variation in the KITLG gene may be associated with another. Other selection signals were found in genomic regions including QTLs and genes associated with production traits such as reproduction, growth, and fat deposition. Some selection signatures were associated with regions showing evidence of introgression from Asian breeds. When the European breeds were compared with wild boar, genomic regions with high levels of differentiation harboured genes related to bone formation, growth, and fat deposition.

Figure 1. Patterns of genetic variation within regions showing strong signals of diversifying selection in Gloucestershire Old Spots (SSC11) and Berkshire (SSC5).

The top-left panel shows the allele frequencies for Gloucestershire Old Spots and the other pig breeds, with F_ST-windows for Gloucestershire Old Spots shown in blue. The bottom-left panel shows the position of the coat colour gene EDNRB. The top-right panel shows the allele frequencies for Berkshire, Meishan and the other pig breeds, with F_ST-windows for Berkshire shown in blue. The bottom-right panel shows the position of the coat colour gene KITLG.

Figure 2. Patterns of genetic variation associated with pig ear phenotypes.

A. Genomic distribution of signatures of diversifying selection as measured by genetic differentiation. The top panel shows prick-eared breeds against flat-eared breeds. The second panel shows prick-eared breeds against intermediate-eared breeds. The third panel shows intermediate-eared breeds against flat-eared breeds. B. Variation in breed allele frequencies of SNPs at the candidate region for ear morphology on SSC5. The top panel shows the allele frequencies for each of the European breeds (colour coded by the ear morphology class to which they belong) and Meishan. The second panel shows the positions of biologically interesting genes in that region.

Figure 3. Summary of genetic variation between wild boar and the European pig breeds.

A. Genomic distribution of signatures of diversifying selection in pig breeds when contrasted against wild boar. The dashed grey line denotes the 99^th percentile. B. Variation in allele frequencies of SNPs compared between wild boar and certain pig breeds on a 2-Mb region on SSC1. The top panel shows the allele frequencies for wild boar (black) versus the Landrace (blue), Welsh (orange) and Tamworth (brown). C. Variation in allele frequencies of SNPs compared between wild boar and certain pig breeds on an 8-Mb region on SSC7. The top panel shows the allele frequencies for wild boar (black) versus the Duroc (red), Landrace (blue) and Large Black (green). For both SSC1 (B) and SSC7 (C), the second panels show the level of genetic differentiation estimated between pig breeds and wild boar and the bottom panels show the positions of biologically interesting genes in these regions.

Figure 4. Multiple sequence alignment for the signal peptide and N-terminal extracellular domain of the EDNRB protein.

Dots indicate identities to the porcine reference sequence. Accession numbers of sequences used in the alignment: Reference Pig: ENSSSCP00000010120, Microbat: ENSMLUP00000005042, Tarsier: ENSTSYP00000001754, Hedgehog: ENSEEUP00000005222, Panda: ENSAMEP00000005967, Mouse: ENSMUSP00000022718, Tasmanian Devil: ENSSHAP00000009143, Cow: ENSBTAP00000006979, Human: ENSP00000366416.