On the origin and evolution of Drosophila new genes during spermatogenesis

Abstract

Origin of functional new genes is a basic biological process that has a 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 meitoic sex chromosome inactivation (MSCI). Here we analyse 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 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 expression pattern from their progenitors for future functional studies.

Functional Diversity and Evolution of the Drosophila Sperm Proteome

“…A variety of mechanisms drive genomic and protein diversity including gene duplication and retroposition (5,37) resulting in unique, lineage-specific patterns of gene age (47)(48)(49). Newly evolved genes frequently acquire testis-biased gene expression (50) and it was therefore of interest to query the gene age landscape of the DmSP3.…”