The genomic distribution of sex-biased genes in drosophila serrata: X chromosome demasculinization, feminization, and hyperexpression in both sexes

Abstract

The chromosomal distribution of genes with sex-biased expression is often nonrandom, and in species with XY sex chromosome systems, it is common to observe a deficit of X-linked male-biased genes and an excess of X-linked female-biased genes. One explanation for this pattern is that sex-specific selection has shaped the gene content of the X. Alternatively, the deficit of male-biased and excess of female-biased genes could be an artifact of differences between the sexes in the global expression level of their X chromosome(s), perhaps brought about by a lack of dosage compensation in males and hyperexpression in females. In the montium fruit fly, Drosophila serrata, both these explanations can account for a deficit of male-biased and excess of female-biased X-linked genes. Using genome-wide expression data from multiple male and female tissues (n = 176 hybridizations), we found that testis- and accessory gland-specific genes are underrepresented whereas female ovary-specific genes are overrepresented on the X chromosome, suggesting that X-linkage is disfavored for male function genes but favored for female function genes. However, genes with such sex-specific functions did not fully account for the deficit of male-biased and excess of female-biased X-linked genes. We did, however, observe sex differences in the global expression level of the X chromosome and autosomes. Surprisingly, and in contrast to other species where a lack of dosage compensation in males is responsible, we found that hyperexpression of X-linked genes in both sexes leads to this imbalance in D. serrata. Our results highlight how common genomic distributions of sex-biased genes, even among closely related species, may arise via quite different evolutionary processes.

Keywords: Drosophila; X chromosome; dosage compensation; sex-biased gene expression.

Fig. 1.—

Sex-biased expression of 11,631 genes of D. serrata: (A) whole-body (n = 71 hybridizations per sex), (B) gonads (n_female = 3, n_male = 4), (C) gonadectomized abdomen (n_female = 4, n_male = 4), (D) head (n_female = 4, n_male = 4), (E) thorax (n_female = 3, n_male = 4), and (F) whole-body excluding sex-specific genes (n = 71 per sex). Red represents female-biased genes, blue are male-biased genes, and black are unbiased genes (Welch’s t-test, FDR < 0.05).

Fig. 2.—

The genomic distribution of sex-biased genes in D. serrata: (A) male-biased and (B) female-biased. The dotted line is the expected percentage of sex-biased genes per chromosome from 1,000 random permutations of the data; numbers above chromosome labels indicate the number of genes in each bar, and asterisk indicates probablilty that observed value does not differ from expected: ***P < 0.001, **P < 0.01, *P < 0.05.

Fig. 3.—

The X chromosome of D. serrata is lacking in male-biased and enriched for female-biased genes. Male-specific tissues are shown in blue and female-specific in red. The number of sex-specific genes per tissue is shown in table 1. The dotted line is the random expectation for the percentage of biased genes per chromosome estimated from 1,000 permutations; numbers above chromosome labels indicate the number of genes in each bar, and asterisk indicates probablilty that observed value does not differ from expected: ***P < 0.001, **P < 0.01, *P < 0.05.

Fig. 4.—

Dosage compensation via hyperexpression in both sexes. (A) Boxplots showing mean expression of X-linked genes (red) and autosomal genes (blue) for males. Plots are shown for all genes on the microarray (All Genes) and subsets containing either genes expressed in both sexes (Co-expressed) or genes expressed in one sex only (sex-specific). P values are from Mann–Whitney U tests comparing expression on the X chromosome versus the autosomes (see Materials and Methods). (B) As in (A) but for females. Numbers above chromosome labels indicate the number of genes.