GC-biased gene conversion conceals the prediction of the nearly neutral theory in avian genomes

Paulina Bolívar,Hans Ellegren,Laurent Guéguen,Carina F Mugal,Laurent Duret

doi:10.1186/s13059-018-1613-z

Abstract

BackgroundThe nearly neutral theory of molecular evolution predicts that the efficacy of natural selection increases with the effective population size. This prediction has been verified by independent observations in diverse taxa, which show that life-history traits are strongly correlated with measures of the efficacy of selection, such as the dN/dS ratio. Surprisingly, avian taxa are an exception to this theory because correlations between life-history traits and dN/dS are apparently absent. Here we explore the role of GC-biased gene conversion on estimates of substitution rates as a potential driver of these unexpected observations.ResultsWe analyze the relationship between dN/dS estimated from alignments of 47 avian genomes and several proxies for effective population size. To distinguish the impact of GC-biased gene conversion from selection, we use an approach that accounts for non-stationary base composition and estimate dN/dS separately for changes affected or unaffected by GC-biased gene conversion. This analysis shows that the impact of GC-biased gene conversion on substitution rates can explain the lack of correlations between life-history traits and dN/dS. Strong correlations between life-history traits and dN/dS are recovered after accounting for GC-biased gene conversion. The correlations are robust to variation in base composition and genomic location.ConclusionsOur study shows that gene sequence evolution across a wide range of avian lineages meets the prediction of the nearly neutral theory, the efficacy of selection increases with effective population size. Moreover, our study illustrates that accounting for GC-biased gene conversion is important to correctly estimate the strength of selection.

Highlights

The nearly neutral theory of molecular evolution predicts that the efficacy of natural selection increases with the effective population size
Results GC-biased gene conversion (gBGC) conceals the correlation between dN/dS and lifehistory traits in birds We explored the relationship between estimates of dN/ dS based on publicly available coding sequence alignments of 7986 genes in 47 avian species and three lifehistory traits
We have explored the role of gBGC behind the apparent lack of a positive correlation between life-history traits and dN/dS in birds, a correlation that would be expected based on the prediction of the nearly neutral theory of molecular evolution

Summary

Introduction

The nearly neutral theory of molecular evolution predicts that the efficacy of natural selection increases with the effective population size This prediction has been verified by independent observations in diverse taxa, which show that life-history traits are strongly correlated with measures of the efficacy of selection, such as the dN/dS ratio. The nearly neutral theory predicts that if Ne is small, the effect of genetic drift is strong, and slightly deleterious mutations are more likely to reach fixation than if Ne is large [5]. Species with small Ne will accumulate more slightly deleterious substitutions over time than species with large Ne. Here, comparison of the evolutionary rate at non-synonymous and synonymous sites allows assessment of the strength of natural selection acting on protein-coding genes, where low effectiveness of selection results in an elevated (but generally < 1), non-synonymous to synonymous substitution rate ratio (dN/dS). To test the validity of the nearly neutral theory, the relationship between Ne and dN/dS can be explored

Methods

Results

Discussion

Conclusion