The Epigenetic Memory Nexus: encoding, maintenance, and inheritance of insect diapause

The classical neuroendocrine-circadian paradigm for insect diapause faces a fundamental memory crisis: it cannot explain how insects accumulate environmental signals, maintain a stable diapause state for months, or transmit this adaptive information across generations. To resolve this, we propose a unifying framework called the Epigenetic Memory Nexus. It provides a putative mechanistic basis for encoding, stabilizing, and heritably transmitting environmental information. We define the Nexus as a dynamic hub comprising three epigenetic pillars: DNA methylation, histone modifications, and non-coding RNAs (ncRNAs). This review delineates the Nexus’s molecular architecture and its three core functions. First, it acts as a signal-translation bridge, converting circadian-decoded inputs into stable chromatin states, which in turn orchestrate neuroendocrine output to establish the diapause phenotype. Second, it serves as a master regulator of biological time: diapause reprograms a DNA methylation-based epigenetic clock that slows adult aging, linking a short-term seasonal adaptation to a long-term life-history strategy. Third, it functions as a vehicle for evolutionary adaptation, transmitting diapause memory through heritable histone marks, enabling non-genetic pre-adaptation. By integrating these findings, we propose that the Nexus extends our conceptualization of diapause from a simple hormonal switch to a programmable, heritable memory state anchored in chromatin-level regulation. This integrative framework offers a potential resolution to long-standing contradictions in diapause biology while providing a roadmap for predicting and managing insect populations in an era of rapid climate change.