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

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.