Evolution of Drift Robustness in Small Populations of Digital Organisms

Most mutations are deleterious and cause a reduction in population mean fitness known as the mutational load. In small populations, weakened selection against slightly-deleterious mutations results in an additional reduction in fitness: the drift load. Many studies have established that populations can evolve a reduced mutational load by evolving mutational robustness, but it is uncertain whether populations can evolve a reduced drift load. Here, using digital experimental evolution, we show that small populations do evolve reduced drift loads, that is, they evolve robustness to genetic drift, or “drift robustness”. We find that, compared to genotypes from large populations, genotypes from small populations have a decreased likelihood of small-effect deleterious mutations, thus causing small-population genotypes to be drift-robust. We further show that drift robustness is not under direct selection, but instead arises because small populations preferentially adapt to drift-robust fitness peaks. These results have implications for genome evolution in organisms with small effective population sizes. One consequence of the power of adaptation is that the majority of mutations reduce their bearer’s fitness [1]. The recurring nature of these deleterious mutations results in an equilibrium reduction of population fitness at mutation-selection balance. At the population level, this reduction in fitness is known as the genetic or mutational load [2–5]. As selection generally acts to increase a population’s mean fitness, one avenue for selection to increase mean fitness is to reduce the mutational load by altering mutation-selection balance and increasing mutational robustness [6, 7]. The evolution of mutational robustness has been demonstrated using theoretical modeling [8–11], digital experimental evolution [12–14], and microbial experimental evolution [15–17]. Recurring deleterious mutations are not the only strain on fitness. In small populations, genetic drift leads to the fixation of slightly-deleterious mutations that bring about a reduction in fitness called the drift load [18, 19]. Over time, genetic drift can lead to continual fitness declines and ultimately population extinction [20, 21]. In asexual populations, this