Evolutionary dynamics in microbial colonies

Traditionally, evolutionary biology has mostly taken a retrospective view, looking backwards in time to infer past evolutionary dynamics. Over the past 30 years, evolution experiments in the laboratory have become a valuable complementary technique to study evolution in real time. Microbial populations in shaken flasks are an ideal model system to do this, because their short generation times and easy reproducibility allow for the study of dozens to hundreds of replicates. Our understanding of microbial evolution in these simple laboratory environments has dramatically improved in recent years./nMicrobial populations in the wild face vastly more complex conditions: they grow as spatially structured communities called microbial biofilms, often consisting of interacting mixtures of different species fulfilling different purposes, subject to various, potentially self-generated, biophysicochemical gradients of, e.g., oxygen or nutrients, which are in turn altered by the physical structure of the community. In short, natural population are subject to a vast variety of ecological interactions, and it has remained unclear how much can be learned from well-mixed liquid culture experiments about how ecology affects evolution in more complex scenarios./nIn this dissertation, I approach this question using one of the simplest possible ecological aspects: the fact that most populations grow in spatially structured communities. Using microbial colonies as an experimental model system, I examine the effect of spatial structure on evolutionary dynamics in a variety of ways. First, Chapters 2-4 investigate the fates of neutral mutations and the dynamics of beneficial mutations in microbial colonies to find that both the neutral diversity resulting from spontaneous mutations and the strength of adaptation is increased in colonies compared to microbial populations grown in shaken flasks. The second half of the thesis is concerned with the effects of environmental heterogeneity on evolutionary dynamics. In Chapter 5, randomly disordered environments are used to examine the competition of selection and extrinsic noise in a model system for spontaneous beneficial and deleterious mutations. In these experiments, extrinsic noise can almost entirely overpower selection such that beneficial variants cannot leverage their advantage to further their evolutionary success. Chapter 6 discusses the effects of gradients on the emergence of antibiotic resistance and how convective flow can shape the trade-off between selection for resistance and the efficacy of treatment./nOverall, the results presented in this thesis suggest that spatial structure can have a momentous influence on the evolutionary dynamics of many dense cellular populations like biofilms and tumors: not only do the dynamics of adaptation change quantitatively in spatially structured populations, but qualitatively different patterns of evolutionary dynamics emerge that cannot arise in well-mixed population. Environmental heterogeneity can also have a strong influence on the speed and the direction of adaptation: whereas random heterogeneity in the environment prevents the spread of beneficial variants, the presence of antibiotic gradients can facilitate the rapid emergence of resistance. This work thus offers a glimpse into the profound and complex ways in which ecology can impact evolution even in simple model systems.

Advisor: Hallatschek, Oskar