Abstract
Dosage compensation, the process whereby expression of sex-linked genes remains similar between sexes (despite heterogamety) and balanced with autosomal expression, was long believed to be essential. However, recent research has shown that several lineages, including birds, butterflies, monotremes and sticklebacks, lack chromosome-wide dosage compensation mechanisms and do not completely balance the expression of sex-linked and autosomal genes. To obtain further understanding of avian sex-biased gene expression, we studied Z-linked gene expression in the brain of two songbirds of different genera (zebra finch, Taeniopygia guttata, and common whitethroat, Sylvia communis) using microarray technology. In both species, the male-bias in gene expression was significantly higher for Z than for autosomes, although the ratio of Z-linked to autosomal expression (Z:A) was relatively close to one in both sexes (range: 0.89–1.01). Interestingly, the Z-linked male-bias in gene expression increased with expression level, and genes with low expression showed the lowest degree of sex-bias. These results support the view that the heterogametic females have up-regulated their single Z-linked homologues to a high extent when the W-chromosome degraded and thereby managed to largely balance their Z:A expression with the exception of highly expressed genes. The male-bias in highly expressed genes points towards male-driven selection on Z-linked loci, and this and other possible hypotheses are discussed.
Highlights
Many mammals and birds, and several important genetic model organisms, e.g. Drosophila spp. and Caenorhabditis elegans, have sex chromosomes that differ in gene content
We have previously studied the extent of sex-biased gene expression in two passerine birds, the zebra finch (Taeniopygia guttata) and the common whitethroat (Sylvia communis) [29]
As in the zebra finch, female intensity in the common whitethroat was significantly lower for Zlinked (6.1460.048) than autosomal genes (6.9060.013; F1, 19623 = 181.4, p,0.0001) (Figure 1B)
Summary
Several important genetic model organisms, e.g. Drosophila spp. and Caenorhabditis elegans, have sex chromosomes that differ in gene content. Despite unequal sex chromosome copy numbers in males and females, the expression of X-linked genes is not much lower in the heterogametic males than in homogametic females in some species, including in Drosophila melanogaster, C. elegans, Anopheles gambiae, Tribolium castaneum, and possibly in mammals [5,6,7,8,9,10,11,12,13] (see [10,14] for a contrasting view in mammals). Dosage compensation was long believed to be essential recent research in e.g. birds, butterflies, sticklebacks and platypus, clearly show that the sex chromosome to autosomal expression ratios (X:A or Z:A) of less than one can frequently be tolerated in the heterogametic sex [23,24,25,26,27,28,29,30] [reviewed in 19]
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