Interspecific Y chromosome introgressions disrupt testis-specific gene expression and male reproductive phenotypes in Drosophila

Abstract

The Drosophila Y chromosome is a degenerated, heterochromatic chromosome with few functional genes. Nonetheless, natural variation on the Y chromosome in Drosophila melanogaster has substantial trans-acting effects on the regulation of X-linked and autosomal genes. However, the contribution of Y chromosome divergence to gene expression divergence between species is unknown. In this study, we constructed a series of Y chromosome introgression lines, in which Y chromosomes from either Drosophila sechellia or Drosophila simulans are introgressed into a common D. simulans genetic background. Using these lines, we compared genome-wide gene expression and male reproductive phenotypes between heterospecific and conspecific Y chromosomes. We find significant differences in expression for 122 genes, or 2.84% of all genes analyzed. Genes down-regulated in males with heterospecific Y chromosomes are significantly biased toward testis-specific expression patterns. These same lines show reduced fecundity and sperm competitive ability. Taken together, these results imply a significant role for Y/X and Y/autosome interactions in maintaining proper expression of male-specific genes, either directly or via indirect effects on male reproductive tissue development or function.evolution | regulatory divergence | male fitness T he Y chromosome in Drosophila melanogaster comprises ∼40 MB of sequence (∼20% of the male genome), but contains fewer than 20 protein-coding genes, most of which are specialized male reproductive genes (1-5). The vast bulk of the chromosome is comprised of large blocks of repetitive sequences, including large microsatellite repeats, transposable element-derived sequence, and bobbed, the Y-linked rDNA array (6). The heterochromatic and gene-poor nature of the Y chromosome is consistent with theoretical models that predict rapid degeneration and specialization for male-specific functions of Y chromosomes in the absence of recombination (7-9). Furthermore, the hemizygous nature of the Y chromosome, combined with the lack of recombination, makes it uniquely susceptible to population genetic processes that reduce genetic variation and limit adaptation (10-13).As predicted by theory, little or no SNP polymorphism exists in single-copy protein-coding sequences on the Y chromosome (7, 14-16). However, several cytological forms of the Y chromosome segregate in at least some species of Drosophila (17), and molecular evidence also suggests that the Y chromosome is not monomorphic. Variation exists for the size of repetitive DNA blocks (18,19), and Y-linked genetic variation associates with variation in organismal phenotypes, including thermal tolerance of spermatogenesis (20, 21) and male mating success (22). Nonetheless, direct tests of association between variation at the rDNA locus and phenotypes reveal no significant effect (18) and theoretical predictions suggest that nonneutral variation on the Y chromosome can only be maintained under very restrictive conditions (23,24). We have previously shown that Y-linked gen...

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

“…Albeit in a different hybrid species system, similar mechanisms might underlie earlier observations that Drosophila mojavensis males with a Y chromosome from Drosophila arizonae are sterile (Vigneault and Zouros, 1986;Pantazidis et al, 1993). Collectively, these results are in agreement with the notion that epistatic interactions between the Y chromosome and the genetic background are prevalent for components of male fitness (Johnson et al, 1992(Johnson et al, , 1993Chippindale and Rice, 2001;Sackton et al, 2011;Yee et al, 2015). Molecularly, a variety of mechanisms-involving both RNA mediators and non-coding DNA sequences-have been suggested for Y chromosome modulation of autosomal and X-linked gene expression that is, in turn, expected to modulate male fertility (reviewed in Francisco and Lemos, 2014).…”

“…Moreover, these studies support the expectation that Y-linked variation preferentially affects genes with male-biased expression and modifies male fertility. Interestingly, YRV affects genes with greater expression divergence between D. melanogaster and D. simulans and higher level of expression polymorphism within species (Lemos et al, 2008;Sackton et al, 2011). It is reasonable to expect that YRV will modulate the evolution of fast-evolving genes and contribute to speciation and hybrid incompatibility in Drosophila.…”

“…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 .…”

“…The construction of mixed-genotype lines in the laboratory provides an ideal system to test whether hybrid male fertility deficiency results from specific interactions among defined genomic regions. Intraspecific variation in the Y chromosome can be responsible for modulating hybrid phenotypes (Johnson et al, 1992(Johnson et al, , 1993Sackton et al, 2011;Cutter, 2012). However, subtle effects on fertility may go unnoticed and are particularly difficult to ascertain when single-species systems are investigated.…”

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

“…Possible biases introduced by using a D. melanogaster platform for a D. simulans genome are minimized because the probed genomes are essentially identical except for the Y chromosomes. The platform has been successfully used to profile gene expression variation in D. simulans when the probed genomes are isogenic for the sequences assayed (Araripe et al, 2010;Sackton et al, 2011). Here the probed genome is the SR1227 isogenic background.…”