Chromosome-Wide Gene Silencing Initiates Y Degeneration in Drosophila

Y degeneration is characterized by pseudogenization of its gene content, an accumulation of repetitive DNA and transcriptional inactivation associated with changes in chromatin structure. The sequence of events leading to genetically inert Y chromosomes, however, is unknown. Does the accumulation of nonsense and missense mutations at protein-coding Y genes trigger their transcriptional downregulation, or does transcriptional silencing of genes precede and expedite the decay of Y-linked genes at the amino acid level? Here, we study patterns of gene expression of the recently formed neo-Y chromosome of Drosophila albomicans, which displays few signs of degeneration of protein-coding genes. We show that chromosome-wide downregulation initiates the processes of Y evolution. This implies that the massive degeneration of protein-coding genes observed at many evolving Y-chromosomes may have limited deleterious effects, and instead, decay of regulatory functions is the initial trigger reducing fitness of the Y.