A Theory of Heterosis

Abstract Heterosis refers to the superior performance of a hybrid over its parents. It is the basis for hybrid breeding particularly for maize and rice. Genetically it is due to interactions between alleles of quantitative trait loci (QTL) (dominance and epistasis). Despite enormous interest and efforts to study the genetic basis of heterosis, the relative contribution of dominance vs. epistasis to heterosis is still not clear. This is because most published studies estimate QTL effects in pieces, not able to put them together to assess the overall pattern adequately. We propose a theoretical framework that focuses on the inference of the relationship between genome and traits that includes the identification of multiple QTL and estimation of the whole set of QTL (additive, dominant, and epistatic) effects. Used for heterosis, it gives a clear genetic definition and interpretation of heterosis. We applied the theory and methods to a large maize dataset with a factorial design of many male and female inbred lines and their hybrid crosses. Heterosis of ear weight in maize is primarily due to QTL dominant effects, many are over-dominant. The contribution to heterosis due to epistasis is small and diffused. For comparison, we also analyzed a rice dataset that is an F2-type population derived from a cross between two inbred lines. The result indicates that dominance is still the main contributor to heterosis, and epistasis contribution is small. Article Summary We propose a general theoretical framework to analyze and interpret quantitative trait genetic variation in a population through the identification of quantitative trait loci (QTL) and the estimation of QTL effects including interactions. Applied to a large genomic study in maize, we produce direct estimation of genetic contribution to heterosis—QTL dominance and epistasis and compare them to the observed heterosis. The evidence is clear that the heterosis of ear weight in maize is primarily due to QTL dominance. The contribution to heterosis due to QTL epistasis is relatively small and diffused.