Divergent evolution peaks under intermediate population bottlenecks during bacterial experimental evolution.

Tom Vogwill,Danna R Gifford,Robyn L Phillips,R Craig Maclean

doi:10.1098/rspb.2016.0749

Abstract

There is growing evidence that parallel molecular evolution is common, but its causes remain poorly understood. Demographic parameters such as population bottlenecks are predicted to be major determinants of parallelism. Here, we test the hypothesis that bottleneck intensity shapes parallel evolution by elucidating the genomic basis of adaptation to antibiotic-supplemented media in hundreds of populations of the bacterium Pseudomonas fluorescens Pf0-1. As expected, bottlenecking decreased the rate of phenotypic and molecular adaptation. Surprisingly, bottlenecking had no impact on the likelihood of parallel adaptive molecular evolution at a genome-wide scale. However, bottlenecking had a profound impact on the genes involved in antibiotic resistance. Specifically, under either intense or weak bottlenecking, resistance predominantly evolved by strongly beneficial mutations which provide high levels of antibiotic resistance. In contrast with intermediate bottlenecking regimes, resistance evolved by a greater diversity of genetic mechanisms, significantly reducing the observed levels of parallel genetic evolution. Our results demonstrate that population bottlenecking can be a major predictor of parallel evolution, but precisely how may be more complex than many simple theoretical predictions.

Highlights

Parallel evolution, where the same beneficial mutations are fixed in independent populations or lineages, has been documented in a wide range of organisms and in response to a range of selection pressures [1,2,3]
Some degree of parallel genetic evolution is commonly observed during host specialization in pathogens [4,5,6] and in endosymbionts [7,8,9], and parallel evolution in antibiotic resistance genes occurs across highly divergent bacteria [4,5,10,11]
In large populations that experience weak bottlenecking, independently derived beneficial mutations can compete with each other, which has the potential to eliminate weakly beneficial mutations. The consequence of this effect, known as Hill–Robertson [22] or clonal interference [23], is that adaptation in large populations will be driven by strongly beneficial mutations in a subset of genes that are under strong selection, resulting in a high probability of parallel evolution

Summary

Introduction

Parallel evolution, where the same beneficial mutations are fixed in independent populations or lineages, has been documented in a wide range of organisms and in response to a range of selection pressures [1,2,3]. In large populations that experience weak bottlenecking, independently derived beneficial mutations can compete with each other, which has the potential to eliminate weakly beneficial mutations The consequence of this effect, known as Hill–Robertson [22] or clonal interference [23], is that adaptation in large populations will be driven by strongly beneficial mutations in a subset of genes that are under strong selection, resulting in a high probability of parallel evolution. This argument is based on classical concepts from population genetics, and is solely based on differences in relative fitness between competing genotypes. The inoculum levels of these assays did not affect the maximum rate of growth, at least at the bottleneck sizes used here

Results

Findings

Discussion