Divergent evolution peaks under intermediate population bottlenecks during bacterial experimental evolution

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.

Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

“…Our study addresses a complex selective agent (a multihazard alpine environment 57 ) in order to provide insights into an ecologically realistic scenario relevant for adaptation in natural environments 14,53,54 .. Results might differ in systems with a high degree of self-fertilization or recent bottlenecks, as these might decrease the probability of gene reuse even among closely related lineages by reducing the pool of shared standing variation 58,59 . Although this is not the case in our Arabidopsis outcrossers, encompassing highly variable and demographically stable populations, drift might have contributed to the low number of overlaps in comparisons involving the lessvariable selfer Arabidopsis thaliana 38 in our meta-analysis ( Fig.…”

Ecology and molecular targets of hypermutation in the global microbiome

“…laboratory incubations. There, both the observed diversity and amino acid change frequency were much lower for all types of DGRs, probably due to the population bottlenecks 25,26 , lack of various environmental stress, and/or shorter time frames of these experiments ( Fig. 3F).…”

Gene expression noise can promote the fixation of beneficial mutations in fluctuating environments

“…Fluctuations in 410 population size are known to reduce the fixation probability of beneficial 411 mutations [2,62,63], especially because reductions in population size can lead to an 412 increase in the power of drift and rapid elimination of genetic variation [64]. Empirical 413 work regularly shows faster adaptation in populations that undergo less severe 414 bottlenecks [65][66][67]. Although many theoretical studies consider the effect of population 415 bottlenecks on the fate of mutations [62], most assume that these fluctuations in 416 population size are caused by factors outside the control of the organism [63,64], 417 although there are exceptions [22,68,69].…”