Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

Abstract

X-linked sex-ratio distorters that disrupt spermatogenesis can cause a deficiency in functional Y-bearing sperm and a femalebiased sex ratio. Y-linked modifiers that restore a normal sex ratio might be abundant and favored when a X-linked distorter is present. Here we investigated natural variation of Y-linked suppressors of sex-ratio in the Winters systems and the ability of these chromosomes to modulate gene expression in Drosophila simulans. Seventy-eight Y chromosomes of worldwide origin were assayed for their resistance to the X-linked sex-ratio distorter gene Dox. Y chromosome diversity caused males to sire B63% to B98% female progeny. Genome-wide gene expression analysis revealed hundreds of genes differentially expressed between isogenic males with sensitive (high sex ratio) and resistant (low sex ratio) Y chromosomes from the same population. Although the expression of about 75% of all testis-specific genes remained unchanged across Y chromosomes, a subset of post-meiotic genes was upregulated by resistant Y chromosomes. Conversely, a set of accessory gland-specific genes and mitochondrial genes were downregulated in males with resistant Y chromosomes. The D. simulans Y chromosome also modulated gene expression in XXY females in which the Y-linked protein-coding genes are not transcribed. The data suggest that the Y chromosome might exert its regulatory functions through epigenetic mechanisms that do not require the expression of protein-coding genes. The gene network that modulates sex ratio distortion by the Y chromosome is poorly understood, other than that it might include interactions with mitochondria and enriched for genes expressed in post-meiotic stages of spermatogenesis.

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

“…Moreover, analyses of Y chromosome variation in wild-type backgrounds and in genotypes with loss-of-function mutations revealed that the manifestation of YRV is exquisitely sensitive to the genomic background (Jiang et al, 2010;Branco et al, 2013a, b). Moreover, these studies support the expectation that Y-linked variation preferentially affects genes with male-biased expression and modifies male fertility.…”

“…These data suggest that the genotype Dox/nmy (Dox distorter/nmy lack-offunction suppressor) has a predominant effect on fertility regardless of the Y chromosome. Interestingly, Branco et al (2013a) have shown that the D. simulans Y chromosome is polymorphic for its capacity to modulate sex ratio distortion in genotype SR12-2-7. These authors used the same stock SR12-2-7 as a background for the introgression of 78 Y chromosomes from several D. simulans populations and found that there is significant diversity in Y chromosome resistance to sexratio distortion: some Y chromosomes carry YRV that overrides the effects of the distorter Dox, while other Y chromosomes are even more sensitive to Dox than the original Y chromosome present in SR12-2-7.…”

“…These include changes in the expression level of genes involved with functions as varied as metabolism, cell division, immune response and chromatin structure. In D. simulans, Branco et al (2013a) observed a range of sex ratios in Y chromosome substitution lines of the Winter's sex-ratio system. The data indicate that polymorphic variation residing in the Y chromosome causes resistance to an X-linked distorter.…”

“…Genome-wide gene expression in genotypes differing only in Y chromosome origin revealed cryptic Y chromosome diversity (Lemos et al, 2008;Lemos et al, 2010;Jiang et al, 2010;Branco et al, 2013a). These include changes in the expression level of genes involved with functions as varied as metabolism, cell division, immune response and chromatin structure.…”

“…Instead, most if not all of the~14 protein-coding genes present on the Y chromosomes of Drosophila melanogaster, D. simulans and other closely related species have male-specific functions and are exclusively expressed in the testis (Gepner and Hays, 1993;Carvalho et al, 2000;Carvalho et al, 2001;Vibranovski et al, 2008). Nevertheless, a suite of studies have shown that genetic variation present on the Y of Drosophila underlie phenotypic variation in male fitness (Chippindale and Rice, 2001;Yee et al, 2015), sex ratio distortion (Carvalho et al, 1997;Montchamp-Moreau et al, 2001;Branco et al, 2013a, b), tolerance to temperature extremes (Rohmer et al, 2004;David et al, 2005), behavior (Stoltenberg and Hirsch, 1997;Huttunen and Aspi, 2003), gene expression (Lemos et al, 2008;Sackton et al, 2011;Branco et al, 2013a, b) and chromatin states in somatic tissues .…”