The effects of sex-biased gene expression and X-linkage on rates of adaptive protein sequence evolution inDrosophila

Victoria Ávila,José L Campos,Brian Charlesworth

doi:10.1098/rsbl.2015.0117

Abstract

A faster rate of adaptive evolution of X-linked genes compared with autosomal genes may be caused by the fixation of new recessive or partially recessive advantageous mutations (the Faster-X effect). This effect is expected to be largest for mutations that affect only male fitness and absent for mutations that affect only female fitness. We tested these predictions in Drosophila melanogaster by using genes with different levels of sex-biased expression and by estimating the extent of adaptive evolution of non-synonymous mutations from polymorphism and divergence data. We detected both a Faster-X effect and an effect of male-biased gene expression. There was no evidence for a strong association between the two effects—modest levels of male-biased gene expression increased the rate of adaptive evolution on both the autosomes and the X chromosome, but a Faster-X effect occurred for both unbiased genes and female-biased genes. The rate of genetic recombination did not influence the magnitude of the Faster-X effect, ruling out the possibility that it reflects less Hill–Robertson interference for X-linked genes.

Highlights

The differences between the modes of inheritance of genes on the X chromosome and the autosomes are expected to affect their patterns of variation and evolution [1]
Our results show that the overall extent of adaptive evolution of protein sequences among D. melanogaster and D. yakuba is higher for male-biased genes than for female-biased or unbiased genes, with a clear pattern for va for the autosomes
When a and va are regressed against the recombination rate for bins of 80 genes, it is evident that, while the extent of adaptive evolution is positively correlated with the recombination rate, the differences between X and autosomes and the effect of male-biased gene expression are maintained across the range of recombination rates

Summary

Introduction

The differences between the modes of inheritance of genes on the X chromosome and the autosomes are expected to affect their patterns of variation and evolution [1]. If adaptive evolution is mostly caused by the fixation of new mutations, there may be a faster rate of substitution of beneficial X-linked mutations compared with autosomal mutations [1]. Such a difference in the rate of evolution is not expected for mutations with female-limited fitness effects and is most likely to occur for mutations with male-limited fitness effects. When adaptive evolution uses standing variation rather than new mutations, a Faster-X effect is less likely [1,2]

Methods

Results

Conclusion