For decades, it was thought that the only heritable information transmitted from one individual to another was that encoded in the DNA sequence. However, it has become increasingly clear that this is not the case and that the transmission of molecules from within the cytoplasm of the gamete also plays a significant role in heritability. The roundworm, Caenorhabditis elegans, has emerged as one of the leading model organisms in which to study the mechanisms of transgenerational epigenetic inheritance (TEI). Collaborative efforts over the past few years have revealed that RNA molecules play a critical role in transmitting transgenerational responses, but precisely how they do so is as yet uncertain. In addition, the role of histone modifications in epigenetic inheritance is increasingly apparent, and RNA and histones interact in a way that we do not yet fully understand. Furthermore, both exogenous and endogenous RNA molecules, as well as other environmental triggers, are able to induce heritable epigenetic changes that affect transcription across the genome. In most cases, these epigenetic changes last only for a handful of generations, but occasionally can be maintained much longer: perhaps indefinitely. In this review, we discuss the current understanding of the role of RNA and histones in TEI, as well as making clear the gaps in our knowledge. We also speculate on the evolutionary implications of epigenetic inheritance, particularly in the context of a short-lived, clonally propagating species. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

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