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Weak selection on synonymous codons substantially inflates dN/dS estimates in bacteria.

Shakibur Rahman1, Sergei L Kosakovsky Pond2, Andrew Webb1

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Proceedings of the National Academy of Sciences of the United States of America
|May 11, 2021
PubMed
Summary
This summary is machine-generated.

Synonymous codon substitutions are not always neutral. A new multiclass model reveals that selection influences codon bias, suggesting traditional methods overestimate positive selection and underestimate purifying selection.

Keywords:
codon-substitution modelsdN/dSnatural selectionneutral model

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Area of Science:

  • Evolutionary Biology
  • Genomics
  • Molecular Biology

Background:

  • Synonymous codon substitutions are traditionally assumed to be selectively neutral.
  • However, codon usage patterns suggest some synonymous substitutions are under selection.
  • Previous analyses often overlook the complexity of selection acting on synonymous sites.

Purpose of the Study:

  • To develop a new model for estimating substitution rates that accounts for multiple classes of synonymous substitutions.
  • To re-evaluate the impact of selection on codon usage bias in bacterial genomes.
  • To investigate the strength of selection required to explain observed codon bias patterns.

Main Methods:

  • Analysis of codon usage in 13 bacterial genomes from the Enterobacterales order.
  • Development of a flexible multiclass synonymous substitution (MSS) model.
  • Comparison of substitution rates estimated by the MSS model versus the standard codon model.

Main Results:

  • The MSS model, which distinguishes between neutral and selected synonymous substitutions, yielded lower estimates of omega (ω) compared to the standard model.
  • On average, omega (ω) values were 80% lower under the MSS model.
  • Observed reductions in synonymous substitution rates can be explained by very weak selection (low Ne*s).

Conclusions:

  • Conventional omega (ω) analyses may overestimate positive diversifying selection and underestimate purifying selection.
  • Codon usage bias is influenced by weak selection, not solely by mutation bias or neutral processes.
  • The findings necessitate a refinement of evolutionary models to accurately assess selection pressures on synonymous sites.