Faster Evolving Primate Genes Are More Likely to Duplicate.

Áine N O’Toole,Aoife Mclysaght,Laurence D Hurst

doi:10.1093/molbev/msx270

Áine N O’Toole, Aoife Mclysaght + Show 1 more

Open Access

https://doi.org/10.1093/molbev/msx270

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Abstract

An attractive and long-standing hypothesis regarding the evolution of genes after duplication posits that the duplication event creates new evolutionary possibilities by releasing a copy of the gene from constraint. Apparent support was found in numerous analyses, particularly, the observation of higher rates of evolution in duplicated as compared with singleton genes. Could it, instead, be that more duplicable genes (owing to mutation, fixation, or retention biases) are intrinsically faster evolving? To uncouple the measurement of rates of evolution from the determination of duplicate or singleton status, we measure the rates of evolution in singleton genes in outgroup primate lineages but classify these genes as to whether they have duplicated or not in a crown group of great apes. We find that rates of evolution are higher in duplicable genes prior to the duplication event. In part this is owing to a negative correlation between coding sequence length and rate of evolution, coupled with a bias toward smaller genes being more duplicable. The effect is masked by difference in expression rate between duplicable genes and singletons. Additionally, in contradiction to the classical assumption, we find no convincing evidence for an increase in after duplication, nor for rate asymmetry between duplicates. We conclude that high rates of evolution of duplicated genes are not solely a consequence of the duplication event, but are rather a predictor of duplicability. These results are consistent with a model in which successful gene duplication events in mammals are skewed toward events of minimal phenotypic impact.

Highlights

It is commonly reported that recently duplicated genes have higher rates of evolution than singleton genes (Lynch and Conery 2000; Van de Peer et al 2001; Pegueroles et al 2013)
We find that genes that duplicated in the great apes have higher rates of evolution in their closely related outgroup, supporting the alternative model of greater duplicability of fast evolving genes
We performed a systematic search for genes that were singletons at the base of the primate tree and remain singletons in macaque and gibbon, and classified these as either singleton or duplicable based on their duplication status in the great apes inferred from gene tree analysis

Summary

Introduction

It is commonly reported that recently duplicated genes have higher rates of evolution than singleton genes (Lynch and Conery 2000; Van de Peer et al 2001; Pegueroles et al 2013). An alternative scenario, involving positive selection after gene duplication, arises when there is conflict between separate functions of a singleton gene such that neither function can be improved without compromising the other This restriction of the singleton gene to be a “jack of all trades, master of none” is released by gene duplication which provides an escape from adaptive conflict, as seen in an anthocyanin pathway gene in morning glory plants (Des Marais and Rausher 2008). The latter is an example of a phenomenon first proposed by Hughes and known as “subfunctionalization,” where functions of a multi-functional ancestral singleton gene get shared out between the daughter paralogs (Hughes 1994). Subfunctionalization may occur as a passive process involving degenerative mutations, but this is considered more likely for regulatory sequence evolution as opposed to coding sequence evolution (Hughes 1994; Force et al 1999)

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