Review
Population size and the rate of evolution

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Highlights

  • The relationship between population size and the rate of evolution is important

  • Many factors affect this relationship, sometimes in counterintuitive ways

  • We synthesise the theoretical and empirical studies of this relationship.

Does evolution proceed faster in larger or smaller populations? The relationship between effective population size (Ne) and the rate of evolution has consequences for our ability to understand and interpret genomic variation, and is central to many aspects of evolution and ecology. Many factors affect the relationship between Ne and the rate of evolution, and recent theoretical and empirical studies have shown some surprising and sometimes counterintuitive results. Some mechanisms tend to make the relationship positive, others negative, and they can act simultaneously. The relationship also depends on whether one is interested in the rate of neutral, adaptive, or deleterious evolution. Here, we synthesize theoretical and empirical approaches to understanding the relationship and highlight areas that remain poorly understood.

Section snippets

Does population size limit evolution?

Do small populations evolve faster or slower than large populations? When and why does population size limit adaptation? Answering these questions is important for understanding present-day diversity and the evolutionary past and future of life on Earth 1, 2, 3. A quantitative answer requires one to measure the ‘rate of evolution’, and link it to population size.

Although there are many ways to measure the rate of evolution, in this review we specifically focus on the relationship between

The neutral substitution rate reflects the mutation rate

Neutral and effectively neutral mutations have fitness effects at or very close to zero (s ≈ 0, Ne|s|<<1, Box 2); therefore, their fate is dominated by genetic drift and largely unaffected by selection. Genetic drift is the stochastic fluctuation in allele frequencies caused by random differences in the fecundity and survival of individuals. As Ne increases, genetic drift becomes weaker because the larger the population, the smaller the proportional impact of each random event that concerns

The shape of the NeRR depends on the fitness effects of mutations

For mutations on which natural selection can act (i.e., those with s ≠ 0, Box 2), the NeRR depends on the fitness effects of mutations (s, Figure 1). As Ne increases, natural selection becomes more effective at fixing advantageous mutations and removing deleterious mutations, but larger populations also produce more of both types of mutation. Theory suggests that as Ne increases the power of natural selection increases faster than the production of new mutations (see [5] for a recent review).

The distribution of fitness effects

The NeRR of all mutations (i.e., combining substitutions from mutations of all fitness effects) is of particular interest because it describes how the overall substitution rate is related to Ne. Because mutations of different fitness effects have different NeRRs (Figure 1), the distribution of fitness effects of new mutations (DFE) is important for predicting the NeRR for all mutations. In general, we expect the NeRR for all mutations to have a ‘U’ shape: resembling the NeRR for deleterious

Empirical studies of the NeRR

Most empirical studies of the NeRR use a comparative approach in which substitution rates are estimated for two or more species [4] or regions of the genome (Box 4), and compared to estimates of Ne. The biggest challenge for these studies is obtaining estimates of Ne (Box 1); most comparative studies rely on crude proxies of Ne, which can limit the inferences that can be made about the NeRR. It is also possible to use experimental approaches to study the NeRR [58], although relatively few such

Concluding remarks and future perspectives

Existing studies of the NeRR tend to fit our expectations that most mutations are deleterious, and that drift and selection are the most important forces determining the NeRR. Some more recent studies hint at more complex effects, but in order to make progress we need to focus on obtaining more accurate estimates of Ne. We currently rely heavily on proxies of Ne that are highly imperfect, and tell us little or nothing about population structure or historical variation in Ne 45, 46. Luckily, the

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