C. elegans aversive olfactory learning generates diverse intergenerational effects

Abstract

Parental experience can modulate the behavior of their progeny. While the molecular mechanisms underlying parental effects or inheritance of behavioral traits have been studied under several environmental conditions, it remains largely unexplored how the nature of parental experience affects the information transferred to the next generation. To address this question, we used C. elegans, a nematode that feeds on bacteria in its habitat. Some of these bacteria are pathogenic and the worm learns to avoid them after a brief exposure. We found, unexpectedly, that a short parental experience increased the preference for the pathogen in the progeny. Furthermore, increasing the duration of parental exposure switched the response of the progeny from attraction to avoidance. To characterize the underlying molecular mechanisms, we found that the RNA-dependent RNA Polymerase (RdRP) RRF-3, required for the biogenesis of 26 G endo-siRNAs, regulated both types of intergenerational effects. Together, we show that different parental experiences with the same environmental stimulus generate different effects on the behavior of the progeny through small RNA-mediated regulation of gene expression.

Keywords:

• Intergeneration
• epigenetics
• learning
• olfaction
• C. elegans

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

A.P., X.G., K.K. and Y.Z. designed the experiments, interpreted the results and wrote the manuscript. A.P., X.G. and K.K. performed the experiments and analyzed the data.

Data availability statement

The data and codes supporting this study are accessible in the Harvard Dataverse repository, https://doi.org/10.7910/DVN/UQAYAK

Additional information

Funding

We thank Caenorhabditis Genetics Center, funded by NIH Office of Research Infrastructure Programs [P40 OD010440], for strains. Ana Pereira was funded by the Dean’s Competitive Fund for Promising Scholarship, Harvard University. Y.Z. is funded by NIH [DC009852].