Abstract
In Drosophila melanogaster males, the expression of X-linked genes is regulated by mechanisms that operate on a chromosomal scale. One such mechanism, male-specific lethal complex-dependent X-linked dosage compensation, is thought to broadly enhance the expression of male X-linked genes through two-fold transcriptional upregulation. The evolutionary consequences of this form of dosage compensation are not well understood, particularly with regard to genes more highly expressed in males. It has been observed the X chromosome arrangement of these male-biased genes is non-random, consistent with what one might expect if there is a selective advantage for male-biased genes to avoid dosage compensation. Separately, it has been noted that the male-specific lethal complex and its dosage compensation mechanism appear absent in some male tissues, thus providing a control for the selection hypothesis. Here we utilized publicly available datasets to reassess the arrangement of X-linked male-biased expressed genes after accounting for expression in tissues not dosage compensated by the male-specific lethal complex. Our results do not corroborate previous observations supporting organismal-wide detrimental effects by dosage compensation on X-linked male-biased expressed genes. We instead find no evidence that dosage compensation has played a role in the arrangement of dosage compensated male-biased genes on the X chromosome.
Highlights
Phenotypic contrasts between Drosophila melanogaster males and females have revealed a vast number of traits to be sexually dimorphic
Previous work identified a depletion of X-linked male-biased expressed genes (MBGs) near chromatin entry site (CES) and found the degree of male bias to be greater for MBGs more distant from their nearest CES [18]
This result is supported by observations by Meisel and colleages [15] who were unable to find a depletion of larval expressed male-biased expressed genes on the X chromosome
Summary
Phenotypic contrasts between Drosophila melanogaster males and females have revealed a vast number of traits to be sexually dimorphic. A number of studies have sought to understand the role and evolutionary history of Drosophila sex-biased expressed genes, with an emphasis on X-linked male-biased expressed genes (MBGs) [4,5,6,7,8] Fundamental to these is an understanding of the sex-specific molecular mechanisms that globally regulate X-linked gene expression. The extent to which these operate remains a subject of debate [12,13,14] as do their evolutionary implications [5,8,15] It has been argued DC is selectively disadvanteous for some somatically expressed X-linked MBGs; likewise, many meiotically expressed X-linked MBGs are thought to be negatively impacted by MCSI. An association has been observed between the degree to which an MBG is malebiased and how far the gene resides from the nearest chromatin entry site (CES) in gonads, gonadectomized flies and whole flies [18]; this observation is relevant to DC because CESs are the primary binding targets for the MSL (Male-specific Lethal) complex, whose role in dosage compensation is discussed below [19,20]
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