A theory of oligogenic adaptation of a quantitative trait

Abstract

Rapid phenotypic adaptation is widespread in nature, but the underlying genetic dynamics remain controversial. Whereas population genetics envisages sequential beneficial substitutions, quantitative genetics assumes a collective response through subtle shifts in allele frequencies. This dichotomy of a monogenic and a highly polygenic view of adaptation raises the question of a middle ground, as well as the factors controlling the transition. Here, we consider an additive quantitative trait with equal locus effects under Gaussian stabilizing selection that adapts to a new trait optimum after an environmental change. We present an analytical framework based on Yule branching processes to describe how phenotypic adaptation is achieved by collective changes in allele frequencies at the underlying loci. In particular, we derive an approximation for the joint allele-frequency distribution at threshold levels of the trait mean as a comprehensive descriptor of the adaptive architecture. Depending on the model parameters, this architecture reproduces the well-known patterns of sequential, monogenic sweeps, or of subtle, polygenic frequency shifts. Between these endpoints, we observe oligogenic architecture types that exhibit characteristic patterns of partial sweeps. We find that a single compound parameter, the population-scaled background mutation ratebg, is the most important predictor of the type of adaptation, while selection strength, the number of loci in the genetic basis, and linkage only play a minor role.