Background: Gene-poor, degenerate Y chromosomes have evolved repeatedly from ordinary autosomes, but little is known about the processes that silence most genes on an evolving Y.
Results: Here, I quantify relative expression levels of 58 gene pairs on the recently formed neo-sex chromosomes of Drosophila miranda, in order to test competing models of gene inactivation on its newly evolving Y chromosome (the neo-Y). Although the neo-Y of D. miranda still contains the majority of its original genes, most exhibit an accelerated rate of protein evolution, and many contain frameshift or nonsense mutations. All but three of these genes show significantly different levels of expression from the neo-X and neo-Y chromosome, with approximately 80% of all genes being expressed at lower levels from the neo-Y. The downregulation of many genes on the neo-Y appears to occur randomly, regardless of the level of accumulation of amino acid substitutions or whether the gene produces a functional protein. In addition, adjacent genes show considerable heterogeneity in levels of gene expression, an observation that argues against chromatin-structure-mediated changes in gene expression levels.
Conclusions: My results suggest that transcriptional inactivation of degenerating Y linked genes is an accidental by-product of mutation accumulation, and not driven by selection to either maintain expression at functional loci or downregulate maladapted genes from the neo-Y. Thus, most mutations observed on the neo-Y are likely to have deleterious effects on fitness and accumulate as a result of the reduced efficiency of natural selection on a nonrecombining chromosome, rather than neutrally or adaptively.