Transposable elements are major components of most eukaryotic genomes. Such sequences are generally defective for transposition and have little or no coding capacity. Because transposition can be highly mutagenic, mobile elements that remain functional are tightly repressed in all living species. Drosophila pericentromeric heterochromatin naturally contains transposition-defective, non-coding derivatives of a LINE retrotransposon related to the I-factor. The I-factor is a good model to study the regulation of transposition in vivo because, under specific conditions, current functional copies of this mobile element can transpose at high frequency, specifically in female germ cells, with deleterious effects including female sterility. However, this high transpositional activity becomes spontaneously repressed upon ageing or heat treatment, by a maternally transmitted, transgenerational epigenetic mechanism of unknown nature. We have analyzed, by quantitative real time RT-PCR, the RNA profile of the transposition-defective I-related sequences, in the Drosophila ovary during ageing and upon heat treatment, and also in female somatic tissues and in males, which are not permissive for I-factor transposition. We found evidence for a role of transcripts from these ancestral remnants in the natural epigenetic protection of the Drosophila melanogaster genome against the deleterious effects of new invasions by functional I-factors. These results provide a molecular basis for a probably widespread natural protection against transposable elements by persisting vestiges of ancient invasions.