We exploited mutants that become progressively sterile to study telomerase-mediated telomere repeat addition, deficiency for which in humans results in transgenerational telomere erosion accompanied by lethal diseases anemia or pulmonary fibrosis. Moreover, telomere erosion may be broadly relevant to human cellular aging because telomerase is silenced in human somatic cells. We recently identified a novel class of small RNAs composed of (TTAGGC)n telomere repeats that are exceptionally rare in mammals and C. elegans but are abundant in the closely related nematodes, C. briggsae and C. remanei. This indicates a dramatic change in telomeric small RNA biogenesis in recent evolution. Telomeric small RNAs may regulate expression of the TElomere Repeat containing RnA (TERRA), which is created at the 5′ ends of telemeres. TERRA expression increases in older people with short somatic telomeres and in astronauts who experience telomere lengthening. TERRA has recently been shown to be translated in dipeptide repeat proteins based on RAN translation. We are studying the biogenesis and functional significance of TERRA.