A newly evolved gene is essential for efficient sperm entry into eggs inDrosophila melanogaster

Abstract

AbstractNew genes arise through a variety of evolutionary processes and provide raw material for adaptation in the face of both natural and sexual selection.De novoevolved genes emerge from previously non-protein-coding DNA sequences, and many such genes are expressed in male reproductive structures. InDrosophila melanogaster, several putativede novogenes have evolved essential roles in spermatogenesis, but whether such genes can also impact sperm function beyond the male has not been investigated. We identified a putativede novogene,katherine johnson(kj), that is required for high levels of male fertility. Males that do not expresskjproduce and transfer sperm that are stored normally in females, but sperm from these males enter eggs with severely reduced efficiency. Using a tagged transgenic rescue construct, we observed that KJ protein localizes to the nuclear periphery in various stages of spermatogenesis, but is not detectable in mature sperm. These data suggest thatkjexerts an effect on sperm development, the loss of which results in reduced fertilization ability. While previous bioinformatic analyses suggested thekjgene was restricted to themelanogastergroup ofDrosophila, we identified putative orthologs with conserved synteny, male-biased expression, and predicted protein features across the genus, as well as instances of gene loss in some lineages. Thus,kjpotentially arose in theDrosophilacommon ancestor and subsequently evolved an essential role inD. melanogaster. Our results demonstrate a new aspect of male reproduction that has been shaped by new gene evolution and provide a molecular foothold for further investigating the mechanism of sperm entry into eggs inDrosophila.Article SummaryHow fruit fly sperm enter eggs is poorly understood. Here, we identify a gene that potentially arose from non-protein-coding DNA and is required for efficient fertilization. Sperm from males lacking this gene’s function cannot enter eggs. The gene appears to act during sperm production, rather than in mature sperm. This study illustrates how newly evolved genes can affect important aspects of reproduction and provides insights into sperm-egg interactions.