Abstract

How new traits originate in evolution is a fundamental question of evolutionary biology. When such traits arise, they can either be immediately beneficial in their environment of origin, or they may become beneficial only in a future environment. Compared to immediately beneficial novel traits, novel traits without immediate benefits remain poorly studied. Here we use experimental evolution to study novel traits that are not immediately beneficial but that allow bacteria to survive in new environments. Specifically, we evolved multiple E. coli populations in five antibiotics with different mechanisms of action, and then determined their ability to grow in more than 200 environments that are different from the environment in which they evolved. Our populations evolved viability in multiple environments that contain not just clinically relevant antibiotics, but a broad range of antimicrobial molecules, such as surfactants, organic and inorganic salts, nucleotide analogues and pyridine derivatives. Genome sequencing of multiple evolved clones shows that pleiotropic mutations are important for the origin of these novel traits. Our experiments, which lasted fewer than 250 generations, demonstrate that evolution can readily create an enormous reservoir of latent traits in microbial populations. These traits can facilitate adaptive evolution in a changing world.

Highlights

  • How novel traits evolve is a central question in evolutionary biology (Bock 1959; Pigliucci 2008; Wagner and Lynch 2010; Wagner 2011, Erwin 2021)

  • Nalidixic acid is a quinolone antibiotic that inhibits the activity of DNA gyrase, an enzyme that is essential for DNA synthesis

  • Our work shows that phenotyping evolving populations in multiple environments can be crucial to identify novel traits that may become not just adaptive but essential for survival in some environments

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Summary

Introduction

How novel traits evolve is a central question in evolutionary biology (Bock 1959; Pigliucci 2008; Wagner and Lynch 2010; Wagner 2011, Erwin 2021). Some novel traits comprise new and beneficial structures, such as wings in birds (Wagner and Lynch 2010). Microorganisms are highly suitable to study novel physiological traits, because their large population sizes and short generation times can make the evolutionary origin of such traits observable on laboratory time scales. Microbial genomes are small, and genomic changes that bring forth novel traits can be studied by genome sequencing (Bennett and Hughes 2009; Toll-Riera et al 2016)

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