Experiences have been shown to modulate behavior and physiology of future generations in some contexts, but there is limited evidence for inheritance of associative memory in different species. Here, we trained C. elegans nematodes to associate an attractive odorant with stressful starvation conditions and revealed that this associative memory was transmitted to the F1 progeny who showed odor-evoked avoidance behavior. Moreover, the F1 and the F2 descendants of trained animals exhibited odor-evoked cellular stress responses, manifested by the translocation of DAF-16/FOXO to cells’ nuclei. Sperm, but not oocytes, transmitted these odor-evoked cellular stress responses which involved H3K9 and H3K36 methylations, the small RNA pathway machinery, and intact neuropeptide secretion. Activation of a single chemosensory neuron sufficed to induce a serotonin-mediated systemic stress response in both the parental trained generation and in its progeny. Moreover, inheritance of the cellular stress responses increased survival chances of the progeny as exposure to the training odorant allowed the animals to prepare in advance for an impending adversity. These findings suggest that in C. elegans associative memories and cellular changes may be transferred across generations.

在某些情况下，经验已被证明可以调节后代的行为和生理机能，但有关不同物种联想记忆遗传的证据有限。在这里，我们训练秀丽隐杆线虫线虫将有吸引力的气味与压力性饥饿条件联系起来，并发现这种联想记忆被传递给表现出气味诱发回避行为的 F1 后代。此外，经过训练的动物的 F1 和 F2 后代表现出气味诱发的细胞应激反应，表现为 DAF-16/FOXO 易位到细胞核。精子（而非卵母细胞）传递这些气味诱发的细胞应激反应，其中涉及 H3K9 和 H3K36 甲基化、小 RNA 途径机制和完整的神经肽分泌。单个化学感应神经元的激活足以在受过父母训练的一代及其后代中诱导血清素介导的全身应激反应。此外，细胞应激反应的遗传增加了后代的生存机会，因为接触训练气味使动物能够提前为即将到来的逆境做好准备。这些发现表明，在线虫中，联想记忆和细胞变化可能会代代相传。