The distribution of fitness effects during adaptive walks using a simple genetic network

PLoS Genet. 2024 May 24;20(5):e1011289. doi: 10.1371/journal.pgen.1011289. eCollection 2024 May.

Abstract

The tempo and mode of adaptation depends on the availability of beneficial alleles. Genetic interactions arising from gene networks can restrict this availability. However, the extent to which networks affect adaptation remains largely unknown. Current models of evolution consider additive genotype-phenotype relationships while often ignoring the contribution of gene interactions to phenotypic variance. In this study, we model a quantitative trait as the product of a simple gene regulatory network, the negative autoregulation motif. Using forward-time genetic simulations, we measure adaptive walks towards a phenotypic optimum in both additive and network models. A key expectation from adaptive walk theory is that the distribution of fitness effects of new beneficial mutations is exponential. We found that both models instead harbored distributions with fewer large-effect beneficial alleles than expected. The network model also had a complex and bimodal distribution of fitness effects among all mutations, with a considerable density at deleterious selection coefficients. This behavior is reminiscent of the cost of complexity, where correlations among traits constrain adaptation. Our results suggest that the interactions emerging from genetic networks can generate complex and multimodal distributions of fitness effects.

MeSH terms

  • Adaptation, Physiological / genetics
  • Alleles
  • Computer Simulation
  • Evolution, Molecular
  • Gene Regulatory Networks*
  • Genetic Fitness*
  • Genotype
  • Models, Genetic*
  • Mutation*
  • Phenotype
  • Selection, Genetic* / genetics

Grants and funding

This work was supported by an Australian Research Council grant awarded to DO (FT200100169) and the Australian Research Council Centre of Excellence for Plant Success in Nature and Agriculture (CE200100015). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.