In rapidly adapting asexuals, the orientation of G can reflect selection rather than functional constraints

Abstract

Genetic covariances represent a combination of pleiotropy and linkage disequilibrium, shaped by the population's history. Observed genetic covariance is most often interpreted in pleiotropic terms. In particular, functional constraints restricting which phenotypes are physically possible can lead to a stable G matrix with high genetic variance in fitness-associated traits and high pleiotropic negative covariance along the Pareto front of constraint. In contrast, population genetic models of relative fitness assume endless adaptation without constraint, through a series of selective sweeps that are well described by recent traveling wave models. We describe the implications of such population genetic models for the G matrix when pleiotropy is excluded by design, such that all covariance comes from linkage disequilibrium. The G matrix is highly unstable over the timescale of selective sweeps, covering a greater range of values than predicted by previous models. However, its orientation is relatively stable, corresponding to high genetic variance in fitness-associated traits and strong negative covariance caused by linkage disequilibrium rather than pleiotropy - the same pattern often interpreted in terms of pleiotropic constraints. Different mechanisms drive the instabilities of the two eigenvalues. The origin of linkage disequilibrium is not drift, but small amounts of linkage disequilibrium are instead introduced by mutation and then amplified during competing selective sweeps. This illustrates the need to integrate a broader range of population genetic phenomena into quantitative genetics.