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. U NDERSTANDING the impact of epistasis on the evolution of multifactorial traits remains a major challenge in complex-trait genetics. Epistasis is more complicated to model, detect, and interpret than marginal (i.e., additive and dominance) genetic effects since the effect of specific alleles at a locus depends on allelic frequencies at other loci. In a population under natural or artificial selection, allele frequencies will change over time and, as a result of this, so will the genetic effects. Explorations of the impact of genetic interactions on phenotypic evolution thus rely on the study of populations in which both genetic and phenotypic information is available. This requires models that are able to decouple the effect of genetic interactions on the displayed genetic variance and to estimate the effect of allele substitutions in different genetic backgrounds.Domestication of animals and plants provides outstanding examples of rapid evolution. The genetic architecture (i.e., the number of genes and alleles, as well as the nature of interactions among them) that underlies a trait of agricultural interest determines how fast and how far a domesticated species is able to respond to long-term directional selection (Le Rouzic et al. 2007;Le Rouzic and Carlborg 2008). Dissecting the genetic differences between domesticated strains and the corresponding wild populations is a particularly relevant approach to unravel mechanisms involved in the domestication process. Wild and domestic populations normally display large phenotypic differences for a wide range of traits and as domestication has been a rapid process in an evolutionary perspective, a reasonably low number of major genetic factors are expected to contribute to these differences. As wild and domestic populations for agricultural traits produce viable offspring, quantitative trait loci (QTL) detecti...

Genotype-Phenotype Maps Maximizing Evolvability: Modularity Revisited

“…The B matrix represents a linear genotype-phenotype map. Nevertheless, epistasis is a common finding in empirical studies across species (e.g., Wolf et al 2000;Cheverud et al 2001;Bradshaw et al 2005;Brem and Kruglyak 2005;Malmberg et al 2005;West et al 2007;Le Rouzic et al 2008;Pavlicev et al 2010). So far modeling the effects of epistasis on evolvability has been restricted to the univariate case (Hermisson et al 2003;Carter et al 2005;Hansen et al 2006; but see Hansen and Wagner 2001).…”

Estimation of Genetic Effects and Genotype-Phenotype Maps

“…This so-called ‘functional modeling of genetic effects’ enables researchers to use real data to study interesting aspects of evolution such as hybrid incompatibilities and domestication processes (e.g. Le Rouzic et al 2008). …”

Characteristics of Egg-related Traits in the Onagadori (Japanese Extremely Long Tail) Breed of Chickens

“…The plural traits in the same principal component might be controlled partially by the same genetic basis. Thus, genetic analysis with principal components will reveal new insights to understand the mechanism of the genetic control of egg quality traits, as shown in the growth curve trait of chickens (Le Rouzic et al, 2008) and the postnatal growth trait of mice (Ishikawa and Namikawa, 2004).…”