A dynamical limit to evolutionary adaptation

Proc Natl Acad Sci U S A. 2024 Jan 23;121(4):e2312845121. doi: 10.1073/pnas.2312845121. Epub 2024 Jan 19.

Abstract

Natural selection makes evolutionary adaptation possible even if the overwhelming majority of new mutations are deleterious. However, in rapidly evolving populations where numerous linked mutations occur and segregate simultaneously, clonal interference and genetic hitchhiking can limit the efficiency of selection, allowing deleterious mutations to accumulate over time. This can in principle overwhelm the fitness increases provided by beneficial mutations, leading to an overall fitness decline. Here, we analyze the conditions under which evolution will tend to drive populations to higher versus lower fitness. Our analysis focuses on quantifying the boundary between these two regimes, as a function of parameters such as population size, mutation rates, and selection pressures. This boundary represents a state in which adaptation is precisely balanced by Muller's ratchet, and we show that it can be characterized by rapid molecular evolution without any net fitness change. Finally, we consider the implications of global fitness-mediated epistasis and find that under some circumstances, this can drive populations toward the boundary state, which can thus represent a long-term evolutionary attractor.

Keywords: Muller’s ratchet; evolutionary attractor; fitness-mediated epistasis; rapid evolution.

MeSH terms

  • Evolution, Molecular
  • Models, Genetic
  • Mutation
  • Mutation Rate*
  • Population Density
  • Selection, Genetic*