Bottlenecks can constrain and channel evolutionary paths

Abstract

Population bottlenecks are commonplace in experimental evolution, specifically in serial passaging experiments where microbial populations alternate between growth and dilution. Natural populations also experience such fluctuations caused by seasonality, resource limitation, or host-to-host transmission for pathogens. Yet, how unlimited growth with periodic bottlenecks influence the adaptation of populations is not fully understood. Here we study theoretically the effects of bottlenecks on the accessibility of evolutionary paths and on the rate of evolution. We model an asexual population evolving on a minimal fitness landscape consisting of two types of beneficial mutations with the empirically supported trade-off between mutation rate and fitness advantage, in the regime where multiple beneficial mutations may segregate simultaneously. In the limit of large population sizes and small mutation rates, we show the existence of a unique most likely evolutionary scenario, determined by the size of the wild-type population at the beginning and at the end of each cycle. These two key demographic parameters determine which adaptive paths may be taken by the evolving population by controlling the supply of mutants during growth and the loss of mutants at the bottleneck. We do not only show that bottlenecks act as a deterministic control of evolutionary paths but also that each possible evolutionary scenario can be forced to occur by tuning demographic parameters. This work unveils the effects of demography on adaptation of periodically bottlenecked populations and can guide the design of evolution experiments.