Environmental heterogeneity can tip the population genetics of range expansions.

Matti Gralka,Oskar Hallatschek

doi:10.7554/elife.44359

Abstract

The population genetics of most range expansions is thought to be shaped by the competition between Darwinian selection and random genetic drift at the range margins. Here, we show that the evolutionary dynamics during range expansions is highly sensitive to additional fluctuations induced by environmental heterogeneities. Tracking mutant clones with a tunable fitness effect in bacterial colonies grown on randomly patterned surfaces we found that environmental heterogeneity can dramatically reduce the efficacy of selection. Time-lapse microscopy and computer simulations suggest that this effect arises generically from a local 'pinning' of the expansion front, whereby stretches of the front are slowed down on a length scale that depends on the structure of the environmental heterogeneity. This pinning focuses the range expansion into a small number of 'lucky' individuals with access to expansion paths, altering the neutral evolutionary dynamics and increasing the importance of chance relative to selection.

Highlights

Stochasticity and its competition with deterministic forces plays an integral role in biology, such as in stochastic gene expression, cellular decision making, and cell differentiation (Balazsi et al, 2011)
Genetic drift is strong at the front of range expansions, where only a relatively small number of individuals at the front of the expansion contributes to future growth and has any influence on the future genotypic composition of the population
The neutral diversity and adaptation in spatially expanding populations has been studied in computer simulations (Edmonds et al, 2004; Klopfstein et al, 2006; Kuhr et al, 2011; Kuhr and Stark, 2015; Lavrentovich and Nelson, 2014; Otwinowski and Krug, 2014), in the field (Ramachandran et al, 2005; White et al, 2013; Louppe et al, 2017), and in microbial colonies (Hallatschek et al, 2007; Fusco et al, 2016; Gralka et al, 2016b; Korolev et al, 2011), which can serve as a useful model system because short generation times and ease of handling allow for quantitative investigations of the evolutionary dynamics of range expansions

Summary

Introduction

Stochasticity and its competition with deterministic forces plays an integral role in biology, such as in stochastic gene expression, cellular decision making, and cell differentiation (Balazsi et al, 2011). Genetic drift is strong at the front of range expansions, where only a relatively small number of individuals at the front of the expansion contributes to future growth and has any influence on the future genotypic composition of the population. Nutrient gradients and mechanical effects limit the number of proliferating individuals to a small region close to the colony perimeter called the growth layer (Grant et al, 2014; Gralka et al, 2016b; Warren et al, 2019). For mutations occurring inside the growth layer, most mutant offspring are concentrated in a relatively small number of enormously successful lineages that manage to remain at the front and ’surf’ on the expanding population wave (Excoffier and Ray, 2008). The evolutionary dynamics is different in microbial colonies compared with well-mixed

Methods

Results

Conclusion