Abstract
BackgroundThe ratio of the rates of non-synonymous and synonymous substitution (dN/dS) is commonly used to estimate selection in coding sequences. It is often suggested that, all else being equal, dN/dS should be lower in populations with large effective size (Ne) due to increased efficacy of purifying selection. As Ne is difficult to measure directly, life history traits such as body mass, which is typically negatively associated with population size, have commonly been used as proxies in empirical tests of this hypothesis. However, evidence of whether the expected positive correlation between body mass and dN/dS is consistently observed is conflicting.ResultsEmploying whole genome sequence data from 48 avian species, we assess the relationship between rates of molecular evolution and life history in birds. We find a negative correlation between dN/dS and body mass, contrary to nearly neutral expectation. This raises the question whether the correlation might be a method artefact. We therefore in turn consider non-stationary base composition, divergence time and saturation as possible explanations, but find no clear patterns. However, in striking contrast to dN/dS, the ratio of radical to conservative amino acid substitutions (Kr/Kc) correlates positively with body mass.ConclusionsOur results in principle accord with the notion that non-synonymous substitutions causing radical amino acid changes are more efficiently removed by selection in large populations, consistent with nearly neutral theory. These findings have implications for the use of dN/dS and suggest that caution is warranted when drawing conclusions about lineage-specific modes of protein evolution using this metric.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-014-0542-8) contains supplementary material, which is available to authorized users.
Highlights
The ratio of the rates of non-synonymous and synonymous substitution is commonly used to estimate selection in coding sequences
The time required for this effect to decay has been suggested to depend on Ne [47], which could be potentially problematic for our data given that we find a positive correlation between body mass and time since divergence from the most recent ancestor (ρ = 0.406, P = 0.0127; calibration points with confidence intervals in the upper quintile were excluded), indicating shorter times for birds with larger populations
Conclusions branch-specific estimates of dN /dS show no evidence for more efficient selection in large bird populations, Kr/Kc estimates appear to conform to the predictions of nearly neutral theory in birds, with smallbodied birds tending to have fewer radical amino acid changes
Summary
The ratio of the rates of non-synonymous and synonymous substitution (dN/dS) is commonly used to estimate selection in coding sequences. It has long been established that different lineages evolve at heterogeneous rates [1,2] and that differences in organismal life history are reflected by rates of molecular evolution This is readily observed in terms of lineagespecific nucleotide divergence, with small-bodied species with shorter generations tending to evolve more quickly than their larger relatives [3,4,5,6,7,8,9,10]. Empirical studies on mammals employing body mass as a proxy for Ne in absence of actual census counts [21] present a similar pattern, with smaller-bodied species tending to have lower dN /dS ratios than their larger counterparts [22,23,24,25,26,27] (though not all authors report a significant relationship; see [9]). It does not follow that an increase in dN /dS, if at all present, need necessarily be owing to a reduction in population size
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