Survival of the simplest: the cost of complexity in microbial evolution

TL;DR

This paper demonstrates that phenotypic interference in microbial evolution constrains genetic complexity, favoring simpler genomes, and suggests that the evolution of sex can mitigate these constraints.

Contribution

It introduces a biophysically grounded model showing how phenotypic interference limits genome complexity and proposes a transition to sexual reproduction as a solution.

Findings

Phenotypic interference couples gene stability to evolutionary speed.

Selection against genome complexity increases with gene number.

Recombination can reduce the cost of complexity and promote sex.

Abstract

The evolution of microbial and viral organisms often generates clonal interference, a mode of competition between genetic clades within a population. In this paper, we show that interference strongly constrains the genetic and phenotypic complexity of evolving systems. Our analysis uses biophysically grounded evolutionary models for an organism's quantitative molecular phenotypes, such as fold stability and enzymatic activity of genes. We find a generic mode of asexual evolution called phenotypic interference with strong implications for systems biology: it couples the stability and function of individual genes to the population's global speed of evolution. This mode occurs over a wide range of evolutionary parameters appropriate for microbial populations. It generates selection against genome complexity, because the fitness cost of mutations increases faster than linearly with the number of genes. Recombination can generate a distinct mode of sexual evolution that eliminates the superlinear cost. We show that positive selection can drive a transition from asexual to facultative sexual evolution, providing a specific, biophysically grounded scenario for the evolution of sex. In a broader context, our analysis suggests that the systems biology of microbial organisms is strongly intertwined with their mode of evolution.