PgmNr D1399: De novo evolved genes are essential for spermatogenesis in D. melanogaster.

Authors:
Geoffrey Findlay; Anna Gubala; Tery Vinh; Michael Kearns; Purva Rumde


Institutes
College of the Holy Cross, Worcester, MA.


Keyword: genome evolution

Abstract:

Gene duplication has long been considered the major evolutionary process that gives rise to new, lineage-specific genes.  However, recent research in Drosophila and other taxa suggests that de novo evolved genes are also an important source of evolutionary novelty.  De novo genes arise from non-protein-coding DNA at a surprisingly high rate, and their expression is often restricted to the male germline.  Previous studies have attempted to use organism-wide RNA interference to infer the function of these genes, but interpretation of these results has been impaired by technical issues with the RNAi library that was used.  By using tissue-specific knockdown in the testes, we have identified two de novo evolved genes, saturn and goddard, that have become essential for spermatogenesis and sperm function in D. melanogaster.  RNAi depletion of saturn leads to a 60 percent reduction in sperm production and transfer and a near-complete inability of sperm to be stored in the female reproductive tract.  Depletion of goddard prevents production of mature sperm by the testes.  Molecular evolutionary analyses showed that saturn arose near the base of the Drosophila phylogeny and has a dynamic evolutionary history that includes gene duplication, gene loss, and positive selection in D. melanogaster and its closest relatives.  In contrast, goddard is present only in the melanogaster group of species and has evolved under purifying selection.  While males of all Drosophila species produce sperm, there is extensive interspecific variation in the type, size and number of sperm produced in males and in the patterns of sperm storage in females.  Our data suggest that lineage-specific de novo genes may play a previously unappreciated role in boosting male fitness by shaping the critical process of spermatogenesis.