A meta-analysis of genetic and phenotypic diversity of European local pig breeds reveals genomic regions associated with breed differentiation for production traits

Abstract

Background: Intense selection of modern pig breeds has resulted in genetic improvement of production traits while the performance of local pig breeds has remained lower. As local pig breeds have been bred in extensive systems, they have adapted to specific environmental conditions, resulting in a rich genotypic and phenotypic diversity. This study is based on European local pig breeds that have been genetically characterized using DNA-pool sequencing data and phenotypically characterized using breed level phenotypes related to stature, fatness, growth, and reproductive performance traits. These data were analyzed using a dedicated approach to detect signatures of selection linked to phenotypic traits in order to uncover potential candidate genes that may underlie adaptation to specific environments.

Results: Analysis of the genetic data of European pig breeds revealed four main axes of genetic variation represented by the Iberian and three modern breeds (i.e. Large White, Landrace, and Duroc). In addition, breeds clustered according to their geographical origin, for example French Gascon and Basque breeds, Italian Apulo Calabrese and Casertana breeds, Spanish Iberian, and Portuguese Alentejano breeds. Principal component analysis of the phenotypic data distinguished the larger and leaner breeds with better growth potential and reproductive performance from the smaller and fatter breeds with low growth and reproductive efficiency. Linking the signatures of selection with phenotype identified 16 significant genomic regions associated with stature, 24 with fatness, 2 with growth, and 192 with reproduction. Among them, several regions contained candidate genes with possible biological effects on stature, fatness, growth, and reproductive performance traits. For example, strong associations were found for stature in two regions containing, respectively, the ANXA4 and ANTXR1 genes, for fatness in a region containing the DNMT3A and POMC genes and for reproductive performance in a region containing the HSD17B7 gene.

Conclusions: In this study on European local pig breeds, we used a dedicated approach for detecting signatures of selection that were supported by phenotypic data at the breed level to identify potential candidate genes that may have adapted to different living environments and production systems.

Fig. 1

Principal component analysis of 24 pig breeds genotyped using a medium-density SNP array

Fig. 2

Population tree and admixture analysis of 23 pig breeds genotyped using a medium-density SNP array. The population tree constructed from pairwise genetic distances (Fst) is shown on the left, and the admixture component for all individuals belonging to the breed is shown on the right. The color levels follow the global axes of genetic variation, with populations most closely related to the Iberian type shown in shades of blue, to the Duroc in shades of red, to the Large White in shades of purple, and to the Landrace in shades of green. Heterogeneous populations, or those equidistant from these four clusters, are shown in orange. The Nero Siciliano breed exhibited extremely high heterogeneity and was, therefore, not included in the reconstruction of the population tree and is not shown

Fig. 3

Principal component analysis showing the relationship of breeds (a) with traits associated with stature (b) and the corresponding phenotypic breed scores (c). Breeds (a) colored in grey are the breeds with more than 50% of missing variables and, thus, their position on the PCA must be interpreted carefully. The variables (b) are colored according to quality of the representation, which is measured by squared cosine between the vector originating from the element and its projection on the axis. The variables that contribute most to the separation of the trait into PC1 and PC2 are colored black. Breeds (a and c) are colored according to their genetic similarity. Breeds (a and c) in green are genetically Landrace-like breeds, in purple Large White-like breeds, in blue Iberian-like breeds, in red Duroc-like breeds, and in light blue the Gascon and Basque breeds

Fig. 4

Global differences in production traits for 20 European local pig populations. Breeds are distributed according to breed scores for phenotypic traits and colored according to genetic similarity. Lower values for breed score growth represent lower average daily gain from weaning to 60 kg of live weight, while higher values represent higher average daily gain in the same growth period. Low values for breed score reproduction represent low reproductive performance, while high values represent breeds with higher reproductive performance. Low values for breed score stature represent lighter and smaller breeds, while high values represent heavier and larger breeds. Low values for the breed score fat represent leaner breeds, while high values represent fatter breeds. Breeds in green are genetically Landrace-like breeds, in purple Large White-like breeds, in blue Iberian-like breeds, in red Duroc-like breeds, and in light blue the Gascon and Basque breeds

Fig. 5

Manhattan plots for phenotypes associated with (a) stature, (b) fatness, (c) growth, and (d) reproduction and associated pp-plots

Fig. 6

Enrichment of SNPs associated with different traits into functional categories