Evolution of Generalists by Phenotypic Plasticity.

Adapting organisms face a tension between specializing their phenotypes for certain ecological tasks and developing generalist strategies that permit persistence in multiple environmental conditions. Understanding when and how generalists or specialists evolve is an important question in evolutionary dynamics. Here, we study the evolution of bacterial range expansions by selecting Escherichia coli for faster migration through porous media containing one of four different sugars supporting growth and chemotaxis. We find that selection in any one sugar drives the evolution of faster migration in all sugars. Measurements of growth and motility of all evolved lineages in all nutrient conditions reveal that the ubiquitous evolution of fast migration arises via phenotypic plasticity. Phenotypic plasticity permits evolved strains to exploit distinct strategies to achieve fast migration in each environment, irrespective of the environment in which they were evolved. Therefore, selection in a homogeneous environment drives phenotypic plasticity that improves performance in other environments.

Hitchhiking, collapse, and contingency in phage infections of migrating bacterial populations.

Natural bacterial populations are subjected to constant predation pressure by bacteriophages. Bacteria use a variety of molecular mechanisms to defend themselves from phage predation. However, since phages are nonmotile, perhaps the simplest defense against phage is for bacteria to move faster than phages. In particular, chemotaxis, the active migration of bacteria up attractant gradients, may help the bacteria escape slowly diffusing phages. Here we study phage infection dynamics in migrating bacterial populations driven by chemotaxis through low viscosity agar plates. We find that expanding phage-bacteria populations supports two moving fronts, an outermost bacterial front driven by nutrient uptake and chemotaxis and an inner phage front at which the bacterial population collapses due to phage predation. We show that with increasing adsorption rate and initial phage population, the speed of the moving phage front increases, eventually overtaking the bacterial front and driving the system across a transition from a regime where bacterial front speed exceeds that of the phage front to one where bacteria must evolve phage resistance to survive. Our data support the claim that this process requires phage to hitchhike with moving bacteria. A deterministic model recapitulates the transition under the assumption that phage virulence declines with host growth rate which we confirm experimentally. Finally, near the transition between regimes we observe macroscopic fluctuations in bacterial densities at the phage front. Our work opens a new, spatio-temporal, line of investigation into the eco-evolutionary struggle between bacteria and phage.

Biophysical constraints determine the selection of phenotypic fluctuations during directed evolution.

Phenotypes of individuals in a population of organisms are not fixed. Phenotypic fluctuations, which describe temporal variation of the phenotype of an individual or individual-to-individual variation across a population, are present in populations from microbes to higher animals. Phenotypic fluctuations can provide a basis for adaptation and be the target of selection. Here we present a theoretical and experimental investigation of the fate of phenotypic fluctuations in directed evolution experiments where phenotypes are subject to constraints. We show that selecting bacterial populations for fast migration through a porous environment drives a reduction in cell-to-cell variation across the population. Using sequencing and genetic engineering we study the genetic basis for this reduction in phenotypic fluctuations. We study the generality of this reduction by developing a simple, abstracted, numerical simulation model of the evolution of phenotypic fluctuations subject to constraints. Using this model we find that strong and weak selection generally lead respectively to increasing or decreasing cell-to-cell variation as a result of a bound on the selected phenotype under a wide range of parameters. However, other behaviors are also possible, and we describe the outcome of selection simulations for different model parameters and suggest future experiments. We analyze the mechanism of the observed reduction of phenotypic fluctuations in our experimental system, discuss the relevance of our abstract model to the experiment and explore its broader implications for evolution.

Environment determines evolutionary trajectory in a constrained phenotypic space.

Constraints on phenotypic variation limit the capacity of organisms to adapt to the multiple selection pressures encountered in natural environments. To better understand evolutionary dynamics in this context, we select Escherichia coli for faster migration through a porous environment, a process which depends on both motility and growth. We find that a trade-off between swimming speed and growth rate constrains the evolution of faster migration. Evolving faster migration in rich medium results in slow growth and fast swimming, while evolution in minimal medium results in fast growth and slow swimming. In each condition parallel genomic evolution drives adaptation through different mutations. We show that the trade-off is mediated by antagonistic pleiotropy through mutations that affect negative regulation. A model of the evolutionary process shows that the genetic capacity of an organism to vary traits can qualitatively depend on its environment, which in turn alters its evolutionary trajectory.