Rapid evolution of male-biased gene expression in Drosophila

Abstract

A number of genes associated with sexual traits and reproduction evolve at the sequence level faster than the majority of genes coding for non-sex-related traits. Whole genome analyses allow this observation to be extended beyond the limited set of genes that have been studied thus far. We use cDNA microarrays to demonstrate that this pattern holds in Drosophila for the phenotype of gene expression as well, but in one sex only. Genes that are male-biased in their expression show more variation in relative expression levels between conspecific populations and two closely related species than do female-biased genes or genes with sexually monomorphic expression patterns. Additionally, elevated ratios of interspecific expression divergence to intraspecific expression variation among male-biased genes suggest that differences in rates of evolution may be due in part to natural selection. This finding has implications for our understanding of the importance of sexual dimorphism for speciation and rates of phenotypic evolution.

Fig. 1.

Frequency distributions of gene expression states for male-enriched, female-enriched, and non-sex-biased genes. Relative gene expression levels were coded into discrete expression states as described in Materials and Methods.

Fig. 2.

S_e and D_e for male-biased, female-biased, and unbiased genes. The product moment correlation coefficients for each class are all significantly different from zero (MBG, r = 0.273, P < 0.001; FBG, r = 0.064, P = 0.013; UBG, r = 0.162, P < 0.001) and from each other (MBG vs. UBG, z = 2.717, P = 0.007; UBG vs. FBG, z = 2.674, P = 0.008). Both S_e and D_e were log-transformed before graphing.