Asymmetrical Damage Partitioning in Bacteria: A Model for the Evolution of Stochasticity, Determinism, and Genetic Assimilation.

Lin Chao,Camilla Ulla Rang,Jasper Ubirajara Chao,Audrey Menegaz Proenca,Mark M Tanaka

doi:10.1371/journal.pcbi.1004700

Abstract

Non-genetic phenotypic variation is common in biological organisms. The variation is potentially beneficial if the environment is changing. If the benefit is large, selection can favor the evolution of genetic assimilation, the process by which the expression of a trait is transferred from environmental to genetic control. Genetic assimilation is an important evolutionary transition, but it is poorly understood because the fitness costs and benefits of variation are often unknown. Here we show that the partitioning of damage by a mother bacterium to its two daughters can evolve through genetic assimilation. Bacterial phenotypes are also highly variable. Because gene-regulating elements can have low copy numbers, the variation is attributed to stochastic sampling. Extant Escherichia coli partition asymmetrically and deterministically more damage to the old daughter, the one receiving the mother’s old pole. By modeling in silico damage partitioning in a population, we show that deterministic asymmetry is advantageous because it increases fitness variance and hence the efficiency of natural selection. However, we find that symmetrical but stochastic partitioning can be similarly beneficial. To examine why bacteria evolved deterministic asymmetry, we modeled the effect of damage anchored to the mother’s old pole. While anchored damage strengthens selection for asymmetry by creating additional fitness variance, it has the opposite effect on symmetry. The difference results because anchored damage reinforces the polarization of partitioning in asymmetric bacteria. In symmetric bacteria, it dilutes the polarization. Thus, stochasticity alone may have protected early bacteria from damage, but deterministic asymmetry has evolved to be equally important in extant bacteria. We estimate that 47% of damage partitioning is deterministic in E. coli. We suggest that the evolution of deterministic asymmetry from stochasticity offers an example of Waddington’s genetic assimilation. Our model is able to quantify the evolution of the assimilation because it characterizes the fitness consequences of variation.

Highlights

The costs and benefits of non-genetic phenotypic variation are a long-standing topic of interest in evolutionary biology [1,2,3]
We show that the partitioning of damage by a mother bacterium to its two daughters is a variable trait that provides an advantage by generating fitness variation
By modeling damage partitioning in a population, we find that the asymmetry is advantageous because it increases fitness variation and the efficiency of natural selection

Summary

Introduction

The costs and benefits of non-genetic phenotypic variation are a long-standing topic of interest in evolutionary biology [1,2,3]. The variation is non-genetic because it results from stochasticity or noise in the expression of genes or developmental pathways controlling the phenotype. If the new conditions become long term, natural selection shifts to favor genetic modifications in which the initial trait evolves from being stochastically determined to become genetically controlled. The phenotype was initially determined by environmental factors because wild type flies, which were not CVL under normal conditions, expressed the gap after their pupae were exposed to a brief heat shock. Waddington selected for the CVL phenotype after heat shock by using flies expressing the gap as the parents for the generation.

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