Abstract
Experimental evolution with microbes is often highly repeatable under identical conditions, suggesting the possibility to predict short-term evolution. However, it is not clear to what degree evolutionary forecasts can be extended to related species in non-identical environments, which would allow testing of general predictive models and fundamental biological assumptions. To develop an extended model system for evolutionary forecasting, we used previous data and models of the genotype-to-phenotype map from the wrinkly spreader system in Pseudomonas fluorescens SBW25 to make predictions of evolutionary outcomes on different biological levels for Pseudomonas protegens Pf-5. In addition to sequence divergence (78% amino acid and 81% nucleotide identity) for the genes targeted by mutations, these species also differ in the inability of Pf-5 to make cellulose, which is the main structural basis for the adaptive phenotype in SBW25. The experimental conditions were changed compared to the SBW25 system to test if forecasts were extendable to a non-identical environment. Forty-three mutants with increased ability to colonize the air-liquid interface were isolated, and the majority had reduced motility and was partly dependent on the Pel exopolysaccharide as a structural component. Most (38/43) mutations are expected to disrupt negative regulation of the same three diguanylate cyclases as in SBW25, with a smaller number of mutations in promoter regions, including an uncharacterized polysaccharide synthase operon. A mathematical model developed for SBW25 predicted the order of the three main pathways and the genes targeted by mutations, but differences in fitness between mutants and mutational biases also appear to influence outcomes. Mutated regions in proteins could be predicted in most cases (16/22), but parallelism at the nucleotide level was low and mutational hot spot sites were not conserved. This study demonstrates the potential of short-term evolutionary forecasting in experimental populations and provides testable predictions for evolutionary outcomes in other Pseudomonas species.
Highlights
An increasing number of experimental evolution studies, primarily using microbes, have provided insights into many fundamental questions in evolutionary biology including the repeatability of evolutionary processes [1,2,3,4,5,6]
We showed that a well-characterized bacterial experimental evolution system, based on biofilm formation by Pseudomonas fluorescens at the surface of static growth tubes, can be extended to the related species Pseudomonas protegens
Given the ability to control environmental conditions, population size, as well as the use of a single asexual organism, such studies could provide an opportunity to predict evolutionary outcomes in simplified model systems. High repeatability on both phenotypic and genetic levels have been observed in a large number of experimental evolution studies, but it has become clear that high repeatability alone is not sufficient for testing evolutionary predictability beyond the prediction that under identical conditions the same evolutionary outcome is probable
Summary
An increasing number of experimental evolution studies, primarily using microbes, have provided insights into many fundamental questions in evolutionary biology including the repeatability of evolutionary processes [1,2,3,4,5,6]. Given the ability to control environmental conditions, population size, as well as the use of a single asexual organism, such studies could provide an opportunity to predict evolutionary outcomes in simplified model systems. High repeatability on both phenotypic and genetic levels have been observed in a large number of experimental evolution studies (reviewed in [5]), but it has become clear that high repeatability alone is not sufficient for testing evolutionary predictability beyond the prediction that under identical conditions the same evolutionary outcome is probable. The most useful model systems for testing and developing our ability to predict evolution, at least at this point, are likely to be of intermediate complexity with several beforehand recognizable phenotypic and genetic solutions to combine ample opportunities for failure with a decent chance of success
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