Stable inheritance of an acquired behavior in Caenorhabditis elegans

Sensory imprinting produces life-long attachment to environmental features experienced during a critical period of early development. Imprinting of this kind is highly conserved in evolution and is an important form of adaptive behavioral plasticity [1]. The nematode Caenorhabditis elegans undergoes such adaptation to new environments through imprinting: attractive odorants, when present during the first larval stage, produce life-long olfactory imprints that enhance attraction and egg-laying rates in the adults [2]. Here I report evidence that the olfactory imprint can be transmitted to the next generation. If the imprint is generated successively over more than four generations, it is not just transmitted through one further generation, but rather, it is stably inherited through many following generations. While the transient nature of the inheritance suggests the existence of resetting mechanisms, stable transgenerational inheritance of the kind reported here raises the possibility that a behavioral alteration produced by an environmental change might be genetically assimilated after a limited number of generations. Behavioral plasticity is the ability of an animal to modify its behavior so as to respond to an environmental change. C. elegans adapts to novel olfactory environments by imprinting: worms exposed to odorants during the critical first larval stage of development (L1) keep life-long imprints that shape their behavior when they encounter the olfactory cues again as adults. In C. elegans, olfactory imprinting increases attraction to imprinted odorants and enhances odorant-induced egg-laying rates [2]. Such long-term memory of favorable conditions might be useful to subsequent generations, so we therefore tested whether a non-imprinted animal would have an improved attraction to olfactory cues if its parent was imprinted. Intriguingly, this appears to be the case: as shown in Figure 1A, a parental imprint was inherited by F1 worms, but not transmitted to F2 worms. Oliver Hobert and I [2] have previously reported that olfactory imprinting involves at least two classes of neurons, the chemosensory neurons AWC and the interneurons AIY. Imprinting inheritance suggests that neuronal