Abstract

As populations spread into new territory, environmental heterogeneities can shape the population front and genetic composition. We focus here on the effects of an important building block of heterogeneous environments, isolated obstacles. With a combination of experiments, theory, and simulation, we show how isolated obstacles both create long-lived distortions of the front shape and amplify the effect of genetic drift. A system of bacteriophage T7 spreading on a spatially heterogeneous Escherichia coli lawn serves as an experimental model system to study population expansions. Using an inkjet printer, we create well-defined replicates of the lawn and quantitatively study the population expansion of phage T7. The transient perturbations of the population front found in the experiments are well described by a model in which the front moves with constant speed. Independent of the precise details of the expansion, we show that obstacles create a kink in the front that persists over large distances and is insensitive to the details of the obstacle’s shape. The small deviations between experimental findings and the predictions of the constant speed model can be understood with a more general reaction-diffusion model, which reduces to the constant speed model when the obstacle size is large compared to the front width. Using this framework, we demonstrate that frontier genotypes just grazing the side of an isolated obstacle increase in abundance, a phenomenon we call ‘geometry-enhanced genetic drift’, complementary to the founder effect associated with spatial bottlenecks. Bacterial range expansions around nutrient-poor barriers and stochastic simulations confirm this prediction. The effect of the obstacle on the genealogy of individuals at the front is characterized by simulations and rationalized using the constant speed model. Lastly, we consider the effect of two obstacles on front shape and genetic composition of the population illuminating the effects expected from complex environments with many obstacles.

Highlights

  • Populations expand into new territory on all length and time scales

  • Geographical structure influences the dynamics of the expansion of populations into new habitats and the relative importance of the evolutionary forces of mutation, selection, PLOS Computational Biology | DOI:10.1371/journal.pcbi

  • To explore the effects of obstacles on the population front dynamics, we employed a microbial model system, bacteriophage T7 spreading on a lawn of E. coli cells

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Summary

Introduction

Populations expand into new territory on all length and time scales. Examples include the migration of humans out of Africa [1], the recent invasion of cane toads in Australia [2], and the growth of colonies of microbes. Populations often persist long after invading [3], events during their spread can have long-lasting effects on their genetic diversity [4, 5]. Considerable effort has been undertaken to understand the role of the invasion process on the evolutionary path of the population: The small population size at the edge of the advancing population wave amplifies genetic drift, reducing genetic diversity, which can culminate in the formation of monoclonal regions [4]. While the genetic consequences of such range expansions have been studied in the field [11, 12], the complexity of natural populations makes it difficult to draw general conclusions. Laboratory expansions of microbes have become a useful tool to illustrate, test, and inspire theoretical predictions [13,14,15,16]

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