The evolution of genetic drift over 50,000 generations

Abstract

Random variation in reproductive success-genetic drift-profoundly shapes genetic diversity and evolutionary trajectories. The strength of drift depends on the variance in descendant number, [Formula], which governs key evolutionary outcomes: for instance, the establishment probability of a beneficial mutation scales inversely with [Formula]. However, whether [Formula] itself evolves over long timescales has remained unclear, because allele-frequency fluctuations depend on drift only through the effective population size, [Formula], which blends census population size with descendant-number variance. Here, we disentangle these components by using model-based Bayesian inference combined with joint tracking of (i) frequency fluctuations of neutrally barcoded lineages and (ii) census population sizes across growth cycles in theE. coliLong-Term Evolution Experiment (LTEE). Analyzing 33 clones spanning the ancestor through 50,000 generations in two replicate populations (Ara-2 and Ara+2), we find that the strength of genetic drift evolved markedly-and divergently-between the two replicate populations. Both census size and [Formula] changed substantially through time, with most variation in Ne driven by shifts in [Formula] rather than census size. After approximately 2,000 generations, the [Formula] of the two populations diverged sharply: Ara+2 generally remained close to a bottleneck-only null expectation, whereas Ara-2 exhibited 1.5-5x stronger drift, consistent with an evolved increase in stochasticity during growth. These results imply that mutations can alter both the mean and the variance of the descendant-number distribution, and we show that the joint distribution of mutational effects on fitness and on [Formula] can substantially modulate the rate of adaptation. The key parameter governing genetic drift can therefore itself evolve in the LTEE, with direct consequences for adaptation.