Polygenic dynamics underlying the response of quantitative traits to directional selection

• Published in: Theoretical population biology Vol. 158; pp. 21 - 59
• Main Authors: Götsch, Hannah, Bürger, Reinhard
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.08.2024
• Subjects: Galton–Watson branching process; Infinite-sites model; Mutation; Polygenic adaptation; Wright–Fisher model; Wright–Fisher model; Infinite-sites model; Mutation; Polygenic adaptation; Galton–Watson branching process; Galton-Watson branching process; Wright-Fisher mode
• ISSN: 0040-5809; 1096-0325; 1096-0325
• DOI: 10.1016/j.tpb.2024.04.006

We study the response of a quantitative trait to exponential directional selection in a finite haploid population, both at the genetic and the phenotypic level. We assume an infinite sites model, in which the number of new mutations per generation in the population follows a Poisson distribution (with mean Θ) and each mutation occurs at a new, previously monomorphic site. Mutation effects are beneficial and drawn from a distribution. Sites are unlinked and contribute additively to the trait. Assuming that selection is stronger than random genetic drift, we model the initial phase of the dynamics by a supercritical Galton–Watson process. This enables us to obtain time-dependent results. We show that the copy-number distribution of the mutant in generation n, conditioned on non-extinction until n, is described accurately by the deterministic increase from an initial distribution with mean 1. This distribution is related to the absolutely continuous part W+ of the random variable, typically denoted W, that characterizes the stochasticity accumulating during the mutant’s sweep. A suitable transformation yields the approximate dynamics of the mutant frequency distribution in a Wright–Fisher population of size N. Our expression provides a very accurate approximation except when mutant frequencies are close to 1. On this basis, we derive explicitly the (approximate) time dependence of the expected mean and variance of the trait and of the expected number of segregating sites. Unexpectedly, we obtain highly accurate approximations for all times, even for the quasi-stationary phase when the expected per-generation response and the trait variance have equilibrated. The latter refine classical results. In addition, we find that Θ is the main determinant of the pattern of adaptation at the genetic level, i.e., whether the initial allele-frequency dynamics are best described by sweep-like patterns at few loci or small allele-frequency shifts at many. The number of segregating sites is an appropriate indicator for these patterns. The selection strength determines primarily the rate of adaptation. The accuracy of our results is tested by comprehensive simulations in a Wright–Fisher framework. We argue that our results apply to more complex forms of directional selection. •Accurate and tractable time-dependent results at genetic and phenotypic level.•Explicit approximations for the initial phase of polygenic adaptation.•Refined classical, quantitative genetics results for the stationary phase.•Population-wide mutation rate characterizes genetic pattern of adaptation.•Number of segregating sites is an indicator of the pattern of adaptation.