The Properties of Adaptive Walks in Evolving Populations of Fungus

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Abstract
The rarity of beneficial mutations has frustrated efforts to develop a quantitative theory of adaptation. Recent models of adaptive walks, the sequential substitution of beneficial mutations by selection, make two compelling predictions: adaptive walks should be short, and fitness increases should become exponentially smaller as successive mutations fix. We estimated the number and fitness effects of beneficial mutations in each of 118 replicate lineages of Aspergillus nidulans evolving for approximately 800 generations at two population sizes using a novel maximum likelihood framework, the results of which were confirmed experimentally using sexual crosses. We find that adaptive walks do indeed tend to be short, and fitness increases become smaller as successive mutations fix. Moreover, we show that these patterns are associated with a decreasing supply of beneficial mutations as the population adapts. We also provide empirical distributions of fitness effects among mutations fixed at each step. Our results provide a first glimpse into the properties of multiple steps in an adaptive walk in asexual populations and lend empirical support to models of adaptation involving selection towards a single optimum phenotype. In practical terms, our results suggest that the bulk of adaptation is likely to be accomplished within the first few steps. Adaptation is one of the least understood processes in biology because it relies on beneficial mutations, which are often too rare to study. We developed a method to infer the number and size of beneficial mutations substituted during adaptation, a process called an adaptive walk, and used this to test predictions about the properties of adaptive walks in experimental populations of fungus. Our work shows that, in contrast to the gradualist view of adaptation dominant since the 1930s, adaptive walks tend to be fast and short, with beneficial mutations of large effect substituted first, followed by those of smaller effect.

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