Decoding Lamarck—transgenerational control of metabolism by noncoding RNAs

The concept of epigenetic transgenerational inheritance (ETI) posits that lifetime experiences in parents, particularly fathers, alter the phenotypic trajectory of their progeny independently of Mendelian genetics. Based on evidence from population studies and laboratory-controlled studies in syngenic animals, this long-term discredited so-called Lamarckian inheritance gained prominent attention. This article aims to summarize the current knowledge about ETI in lower and in higher organisms as well as in human cohorts and elaborates on epigenetic principles potentially underlying this nongenetic mode of heredity. Special attention is given to—small and long—noncoding RNAs in male gametes that recently emerged as a molecular sensor of organismal metabolic states which can ultimately relay information across the germline barrier by translating environmental cues into (epigenetic) changes in zygotic gene expression.