What are the mechanisms that drive evolutionary progress? The idea that the environment directly shapes the phenotype of the progeny has been heretic for centuries. While the classic Lamarckian ideas (inheritance of acquired traits) have been dismissed, recent observations suggest that certain acquired traits are heritable. We showed that worms inherit an acquired trait, antiviral resistance, through transgenerational transmission of antiviral small RNAs (viRNAs) that mediate RNA interference (RNAi). viRNAs transfer transgenerationally in a non-Mendelian, DNA-independent manner, to defend RNAi-deficient progeny. In addition, we discovered that maintenance of inherited RNA interference (iRNA), over the course of hundreds of generations, depends on the action of the RNA-dependent RNA polymerase (RDRP), RRF-1 (Cell, 2011), which amplifies the iRNA response in each generation. The transmission mechanism is progressively elucidated, and very recently it was shown that a nuclear argonaute, HRDE-1, is required for transgenerational transfer of small RNAs. We hypothesize that iRNA has had a major influence on nematodes’ evolution, and on evolution in general. We will examine if responses to different environmental pressures carry on to the next generations via iRNA, so that evolution is directed and accelerated. By performing dynamic and prolonged laboratory evolution experiments, massive parallel deep sequencing, and functional assays, we will test in real time the capacity of worms that differ in their ability to inherit acquired traits via small RNAs to evolve several major traits. To characterize the contribution of iRNA to the course of evolution, we will control the animal’s capacity to inherit small RNAs. This will be achieved by engineering the organism’s RRF-1 and HRDE-1 genes, which are required for iRNA. These experiments will be an important step towards elucidation of the role of iRNA in the evolutionary process.
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