A global search reveals epistatic interaction between QTL for early growth in the chicken

Abstract

We have identified quantitative trait loci (QTL) explaining a large proportion of the variation in body weights at different ages and growth between chronological ages in an F(2) intercross between red junglefowl and White Leghorn chickens. QTL were mapped using forward selection for loci with significant marginal genetic effects and with a simultaneous search for epistatic QTL pairs. We found 22 significant loci contributing to these traits, nine of these were only found by the simultaneous two-dimensional search, which demonstrates the power of this approach for detecting loci affecting complex traits. We have also estimated the relative contribution of additive, dominance, and epistasis effects to growth and the contribution of epistasis was more pronounced prior to 46 days of age, whereas additive genetic effects explained the major portion of the genetic variance later in life. Several of the detected loci affected either early or late growth but not both. Very few loci affected the entire growth process, which points out that early and late growth, at least to some extent, have different genetic regulation.

Figure 1.

The number of quantitative trait loci affecting one to nine of the traits in the study at a 5% and 20% genome-wide threshold as determined by randomization testing.

Figure 2.

All quantitative trait loci (QTL) for body weight at 112 days of age detected by forward selection and SIM. The QTL detected using a forward selection search are presented on the diagonal (F). All QTL pairs that were detected by SIM (S) or both forward selection and SIM (FS) are presented above the diagonal. QTL pairs where the epistatic model was selected by a randomization test are presented below the diagonal (E). The results are given for a 5%, 10%, and 20% genome-wide significance threshold. The full designation of linkage group E47 is E47W24.

Figure 3.

Least square means for the nine possible genotypes for the interacting quantitative trait loci pair affecting weight at hatch. Each locus was assumed to segregate for two alleles inherited from the red junglefowl (J) and the White Leghorn (L) founders, respectively.

Figure 4.

The residual variance explained by the marginal effects of the quantitative trait loci (QTL) mapped using forward selection and by the marginal and epistatic effects of the QTL mapped by SIM at a 5% genome-wide significance level. A, additive effect; D, dominance effect; I, interaction; Bw1, body weight at day 1; Bw8, body weight at day 8; Bw46, body weight at day 46; Bw112, body weight at day 112; Bw200, body weight at day 200; Gr18, growth from day 1 to day 8; Gr846, growth from day 8 to day 46; Gr46112, growth from day 46 to day 112; Gr112200, growth from day 112 to day 200.

Figure 5.

Partitioning of the total phenotypic (P) and the genetic (G) variance explained by the quantitative trait loci mapped by SIM at a 20% genome-wide significance level in the F₂ generation of a red junglefowl × White Leghorn intercross. Vr, residual variance; Vg, genetic variance; Vb, variance explained by batch effects; Vs, variance explained by sex effects; Vdd, dominance-by-dominance genetic interaction variance; Vad, additive-by-dominance and dominance-by-additive genetic interaction variance; Vaa, additive-by-additive genetic interaction variance; Vd, dominance genetic variance; Va, additive genetic variance. Abbreviations for traits are explained in the legend of Figure 4.

Figure 6.

Additive and dominance genetic effects for the quantitative trait loci affecting body weight at 112 days that were mapped by SIM using a 20% genome-wide significance threshold, sorted by size of the additive effect.