Mechanisms of gene death in the Red Queen race revealed by the analysis ofde novomicroRNAs

Abstract

AbstractThe prevalence ofde novocoding genes is controversial due to the length and coding constraints. Non-coding genes, especially small ones, are freer to evolvede novoby comparison. The best examples are microRNAs (miRNAs), a large class of regulatory molecules ~22 nt in length. Here, we study 6de novomiRNAs inDrosophilawhich, like most new genes, are testis-specific. We ask how and whyde novogenes die because gene death must be sufficiently frequent to balance the many new births. By knocking out each miRNA gene, we could analyze their contributions to each of the 9 components of male fitness (sperm production, length, competitiveness etc.). To our surprise, the knockout mutants often perform better in some components, and slightly worse in others, than the wildtype. When two of the younger miRNAs are assayed in long-term laboratory populations, their total fitness contributions are found to be essentially zero. These results collectively suggest that adaptivede novogenes die regularly, not due to the loss of functionality, but due to the canceling-out of positive and negative fitness effects, which may be characterized as “quasi-neutrality”. Sincede novogenes often emerge adaptively and become lost later, they reveal ongoing period-specific adaptations, reminiscent of the “Red-Queen” metaphor for long term evolution.