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Directional Selection Rather than Functional Constraints Can Shape the G Matrix in Rapidly Adapting Asexuals.

Genetics 2018 December 18
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 phenotypic curve 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 far less stable than has previously been found, fluctuating over the timescale of selective sweeps. However, its orientation is relatively stable, corresponding to high genetic variance in fitness-associated traits and strong negative covariance - the same pattern often interpreted in terms of pleiotropic constraints but caused instead by linkage disequilibrium. We find that different mechanisms drive the instabilities along versus perpendicular to the fitness gradient. 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.

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