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

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.

Keywords: Drosophila; Faster-X effect; recombination; sex-biased gene expression; sexual selection.

Figure 1.

Boxplots of (a) α and (b) ω_a for female-biased (F), male-biased (M) and unbiased (U) genes on the autosomes (A) and on the X chromosome (X). * and *** denote p values of 0.05 and 0.001, respectively, from Mann–Whitney U-tests; n.s. denotes lack of significance.

Figure 2.

Plots of α and ω_a against the mean effective recombination rates of bins of 80 genes (least-squares regression lines are shown), for female-biased (F), male-biased (M) and unbiased (U) genes. ρ denotes the Spearman's rank correlation coefficients for each expression group. * , ** and *** indicate p values of 0.05, 0.01 and 0.001, respectively.