Population genetics of polymorphism and divergence in rapidly evolving populations

• Published in: Genetics (Austin) 2022-07, Vol.221 (4)
• Main Authors: Melissa, Matthew J, Good, Benjamin H, Fisher, Daniel S, Desai, Michael M
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Biological Evolution; Divergence; Dynamics; Evolution; Fitness; Frequency spectrum; Gene polymorphism; Genetic diversity; Genetics; Genetics, Population; Investigation; Models, Genetic; Mutation; Polymorphism; Population; Population genetics; Populations; Reproductive fitness; Selection, Genetic; Time; Traveling waves
• ISSN: 1943-2631; 0016-6731; 1943-2631
• DOI: 10.1093/genetics/iyac053

Abstract In rapidly evolving populations, numerous beneficial and deleterious mutations can arise and segregate within a population at the same time. In this regime, evolutionary dynamics cannot be analyzed using traditional population genetic approaches that assume that sites evolve independently. Instead, the dynamics of many loci must be analyzed simultaneously. Recent work has made progress by first analyzing the fitness variation within a population, and then studying how individual lineages interact with this traveling fitness wave. However, these “traveling wave” models have previously been restricted to extreme cases where selection on individual mutations is either much faster or much slower than the typical coalescent timescale Tc. In this work, we show how the traveling wave framework can be extended to intermediate regimes in which the scaled fitness effects of mutations (Tcs) are neither large nor small compared to one. This enables us to describe the dynamics of populations subject to a wide range of fitness effects, and in particular, in cases where it is not immediately clear which mutations are most important in shaping the dynamics and statistics of genetic diversity. We use this approach to derive new expressions for the fixation probabilities and site frequency spectra of mutations as a function of their scaled fitness effects, along with related results for the coalescent timescale Tc and the rate of adaptation or Muller’s ratchet. We find that competition between linked mutations can have a dramatic impact on the proportions of neutral and selected polymorphisms, which is not simply summarized by the scaled selection coefficient Tcs. We conclude by discussing the implications of these results for population genetic inferences. In rapidly evolving populations, multiple beneficial and deleterious mutations are often present simultaneously in a variety of linked combinations, and natural selection cannot act on each locus individually. Thus, classical population genetic theory, which treats each mutation independently, cannot be applied. Here, Melissa et al. present a general framework for calculating statistics of genetic diversity and divergence in these rapidly evolving populations. Their work expands on previous theory, connecting disparate parameter regimes from earlier studies into a more general analysis.