On the origin and evolution of Drosophila new genes during spermatogenesis

Origin of functional new genes is a basic biological process that has significant contribution to organismal diversity. Previous studies in both Drosophila and mammals showed that new genes tend to be expressed in testis, and avoid the X chromosome presumably because meiotic sex chromosome inactivation (MSCI). Here we analyze the published single-cell transcriptome data of Drosophila adult testis and find an enrichment of male germline mitotic genes, but an underrepresentation of meiotic genes on the X chromosome. This can be attributed to an excess of autosomal meiotic genes that were derived from their X-linked mitotic progenitors, which provides direct cell-level evidence for MSCI in Drosophila. We reveal that new genes, particularly those produced by retrotransposition, tend to exhibit an expression shift toward late spermatogenesis compared to their parental copies, probably due to the more intensive sperm competition or sexual conflict. Our results dissect the complex factors including the age, the origination mechanisms and the chromosomal locations that influence the new gene origination and evolution in testis, and identify new gene cases that show divergent cell-level expression pattern from their progenitors for future functional studies.