Abstract
Pleiotropic effects of mutations underlie diverse biological phenomena such as ageing and specialization. In particular, antagonistic pleiotropy (“AP”: when a mutation has opposite fitness effects in different environments) generates tradeoffs, which may constrain adaptation. Models of adaptation typically assume that AP is common ‐ especially among large‐effect mutations ‐ and that pleiotropic effect sizes are positively correlated. Empirical tests of these assumptions have focused on de novo beneficial mutations arising under strong selection. However, most mutations are actually deleterious or neutral, and may contribute to standing genetic variation that can subsequently drive adaptation. We quantified the incidence, nature, and effect size of pleiotropy for carbon utilization across 80 single mutations in Escherichia coli that arose under mutation accumulation (i.e., weak selection). Although ∼46% of the mutations were pleiotropic, only 11% showed AP; among beneficial mutations, only ∼4% showed AP. In some environments, AP was more common in large‐effect mutations; and AP effect sizes across environments were often negatively correlated. Thus, AP for carbon use is generally rare (especially among beneficial mutations); is not consistently enriched in large‐effect mutations; and often involves weakly deleterious antagonistic effects. Our unbiased quantification of mutational effects therefore suggests that antagonistic pleiotropy may be unlikely to cause maladaptive tradeoffs.
Highlights
Biologists have long observed that organisms maximize resource allocation to one trait while compromising allocation to another trait (Goethe)(Lenoir 1984)
To estimate the incidence of pleiotropy, we measured the fitness effect of single mutations obtained during an Mutation Accumulation (MA) experiment, on 11 different carbon sources (Fig. 1)
The distribution of fitness effects (DFEs) observed for each resource showed that on average, ~49% of all sampled mutations were deleterious, and would have been missed if we focused only on beneficial mutations (Fig. S2)
Summary
Biologists have long observed that organisms maximize resource allocation to one trait while compromising allocation to another trait (Goethe)(Lenoir 1984) Such tradeoffs manifest as negative correlations between traits, and may constrain evolution by limiting the breadth of phenotypes available to organisms (Rees 1993). Tradeoffs can occur when multiple neutral or deleterious mutations accumulate and degrade traits under weak selection, leading to a negative correlation with other traits evolving under positive selection (Elena and Lenski 2003). Tradeoffs may occur when a single mutation increases fitness in a specific environment (or trait), simultaneously reducing fitness in alternate environments (or a second trait) (Cooper and Lenski 2000). Such mutations are antagonistically pleiotropic for the two traits or environments, and the phenomenon is called antagonistic pleiotropy ( “AP”)
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