Inheritance of associative memories and acquired cellular changes in C. elegans

Area of Science:

• Epigenetics
• Neurobiology
• Genetics

Background:

• Inheritance of learned information across generations is poorly understood.
• Associative memory and its transgenerational epigenetic inheritance require further investigation in model organisms.

Purpose of the Study:

• To investigate the transgenerational inheritance of associative memory and cellular stress responses in *C. elegans*.
• To identify the mechanisms underlying the inheritance of environmentally induced traits.

Main Methods:

• Training *C. elegans* nematodes to associate an odorant with starvation.
• Analyzing behavioral responses (odor-evoked avoidance) in F1 and F2 progeny.
• Investigating cellular stress responses (DAF-16/FOXO translocation) and epigenetic modifications (H3K9/H3K36 methylation).
• Examining the role of sperm versus oocytes in transmission.
• Assessing the impact of inherited stress responses on survival.

Main Results:

• Associative memory of odor-starvation was transmitted to F1 progeny, inducing odor-evoked avoidance.
• F1 and F2 descendants exhibited odor-evoked cellular stress responses, including DAF-16/FOXO nuclear translocation.
• Sperm, not oocytes, transmitted these stress responses, involving specific epigenetic marks and small RNA pathways.
• Activation of a single chemosensory neuron triggered systemic stress responses in parents and progeny.
• Inherited cellular stress responses improved progeny survival upon exposure to the training odorant.

Conclusions:

• Associative memories and cellular stress responses can be epigenetically transferred across generations in *C. elegans*.
• Sperm-mediated epigenetic inheritance plays a crucial role in transmitting learned stress responses.
• Transgenerational inheritance of stress responses enhances offspring adaptation and survival to environmental adversity.