Paucity of genes on the Drosophila X chromosome showing male-biased expression

Abstract

Sex chromosomes are primary determinants of sexual dimorphism in many organisms. These chromosomes are thought to arise via the divergence of an ancestral autosome pair and are almost certainly influenced by differing selection in males and females. Exploring how sex chromosomes differ from autosomes is highly amenable to genomic analysis. We examined global gene expression in Drosophila melanogaster and report a dramatic underrepresentation of X-chromosome genes showing high relative expression in males. Using comparative genomics, we find that these same X-chromosome genes are exceptionally poorly conserved in the mosquito Anopheles gambiae. These data indicate that the X chromosome is a disfavored location for genes selectively expressed in males.

Fig. 1.

Gene expression profiles. Control experiments performed with split samples (A). The twofold cutoff is indicated (red). Adult male versus female (B), testes versus ovaries (C) and gonadectomized male versus gonadectomized females (D). Intensities greater than twofold are indicated by blue (male-biased) and red (female-biased). The average of eight ratios is shown (B to D).

Fig. 2.

Gene expression for major chromosome arms. Columns are male-biased (A, D, G), female-biased (B, E, H), or nonsex-differentially expressed (C, F, I). Rows represent comparing testes versus ovaries (A to C), whole adult males versus females (D to F) and gonadectomized males versus gonadectomized females (G to I). The percentage of genes with male, female, or non-biased expression are shown: less than twofold (open), greater than twofold (light), greater than fourfold (dark), and > 10-fold (black). Remaining genes were not reliably detected. Significant deviations (chi-square) are indicated for greater than twofold (**P < 0.0001; *P < 0.005).

Fig. 3.

Expression parsed into chromosome arms (A and B). The relative distribution between the X chromosome (A) and a typical autosome arm (B) is shown. Expression of X-chromosome (red) and autosomal (black) genes encoding 38 ribosomal proteins: gonads (C), gonadectomized (D). No significant differences in regression lines (C). The difference in intercept is significant, but is well within the twofold range (D).

Fig. 4.

Drosophila/Anopheles homology correlates expression and location. Percentage of Drosophila: X-chromosome genes with X chromosome (A), autosomal genes with X chromosome (B), X-chromosome genes with autosomal (C), and autosomal genes with autosomal (D) Anopheles homologs.