The Evolution of Natural Competence: Disentangling Costs and Benefits of Sex in Bacteria

Abstract

One of the most challenging questions in evolutionary biology is how sex has evolved in the face of substantial fitness costs. In this study, we focus on the evolution of bacterial sex in the form of natural transformation, where cells take up exogenous DNA and integrate it into the genome. Besides the physiological cost of producing a DNA uptake system, transformation can potentially impose a genetic cost as a result of an overrepresentation of deleterious mutations in the extracellular DNA pool. On the other hand, the uptake of DNA can be beneficial not only because of genetic effects but also because of the immediate nutritional value of the DNA. To disentangle these fitness costs and benefits, we developed a mathematical model and competed three bacterial types during adaptation to a new environment: competent cells capable of DNA import and digestion; competent cells capable of DNA import, digestion, and recombination; and noncompetent cells. Our results indicate a complex interplay between several physiological and ecological factors, including the rate at which DNA is taken up, the rate of DNA decay in the medium, and the nutritional value of DNA. In finite populations, the recombining type is often favored through the Fisher-Muller effect.