High rate of translocation-based gene birth on the Drosophila Y chromosome

The Y chromosome is a unique genetic environment defined by a lack of recombination and male-limited inheritance. The Drosophila Y chromosome has been gradually acquiring genes from the rest of the genome, with only seven Y-linked genes being gained over the past 63 million years (0.12 gene gains/Myrs). Using a novel NGS-powered genomic scan, we show that gene transfers to the Y chromosome are much more common than previously suspected: at least 25 have arisen across three Drosophila species over the past 5.4 million years (1.67/Myrs for each lineage). The gene transfer rate is significantly lower in D. melanogaster than in the D. simulans clade, primarily due to Y-linked retrotranspositions being significantly more common in the latter. Despite all Y-linked gene transfers being evolutionarily recent (=1Myrs old), only three showed evidence for purifying selection (? =0.14). Thus, while the resulting Y-linked functional gene acquisition rate (0.25 new genes/Myrs) is double the longer-term estimate, the fate of most new Y-linked genes is defined by rapid degeneration and pseudogenization. Our results show that Y-linked gene traffic, and the molecular mechanisms governing these transfers, can diverge rapidly between species, revealing the Drosophila Y chromosome to be more dynamic than previously appreciated. Our analytical method provides a powerful means to identify Y-linked gene transfers, and will help illuminate the evolutionary dynamics of the Y chromosome in Drosophila and other species.