Dissection of the genetic architecture of body weight in chicken reveals the impact of epistasis on domestication traits

Abstract

In this contribution, we study the genetic mechanisms leading to differences in the observed growth patterns of domesticated White Leghorn chickens and their wild ancestor the red jungle fowl. An epistatic QTL analysis for several body-weight measures from hatch to adulthood confirms earlier findings that polymorphisms at >15 loci contribute to body-weight determination in an F(2) intercross between these populations and that many loci are involved in complex genetic interactions. Here, we use a new genetic model to decompose the genetic effects of this multilocus epistatic genetic network. The results show how the functional modeling of genetic effects provides new insights into how genetic interactions in a large set of loci jointly contribute to phenotypic expression. By exploring the functional effects of QTL alleles, we show that some alleles can display temporal shifts in the expression of genetic effects due to their dependencies on the genetic background. Our results demonstrate that the effects of many genes are dependent on genetic interactions with other loci and how their involvement in the domestication process relies on these interactions.

Figure 1.—

Graphic illustration of growth pattern features described by the principal components. The mean phenotype of the F₂ population (dotted curve) is taken as a reference to describe the effects of the three first principal components. All PCs are set to 0, except one (top, PC1; middle, PC2; and bottom, PC3) that is varied from −3 (solid thin line) to 3 (solid thick line). The values −3 and 3 roughly represent the maximum and minimum values for the PCs in the population (see supplemental Figure 2).

Figure 2.—

Genetic effects of individual loci in wild and domestic genetic backgrounds. The estimated phenotypic effect of “2” (“Leghorn” or “domestic”) alleles at each of the 8 loci included in the regression analysis in the “wild” (left plots) and “domestic” genetic backgrounds (right plots). The reference is always the “11” (homozygote wild) genotype (solid thin line) in both backgrounds, and plots are scaled according to the residual variance at each age. Additive and dominance effects can be extracted in each plot from the dotted and thick solid lines representing the heterozygote (“12”) and the homozygote domestic (“22”) genotypes, respectively. Epistasis is evident in the comparison of the genetic effects in the alternative genetic backgrounds (if there was no epistasis, right and left plots should be identical). For instance, being 22 instead of 11 at locus 1A increases the body weight at 200 days by ∼1.2σ_P in the “jungle fowl” background (11 genotype at all other loci) and by about 2σ_P in the “Leghorn” background (22 genotype at all other loci).