Intrastrain variability in memory formation of freshly collected Lymnaea stagnalis: The influence of stressor type on memory.

Abstract

Understanding how environmental stressors influence memory formation is essential for evaluating the ecological and toxicological impacts of pollution on animal behavior. Using Lymnaea stagnalis snails collected from a pollutant-exposed freshwater creek in Canada, we investigated how distinct stressors affect learning and memory abilities and their underlying molecular mechanisms. In one procedure, pairing an appetitive cue with a predator-mimicking mechanical stressor (shell clip) revealed intra-strain variability in memory formation: only a subset of snails formed aversive memory, evidenced by reduced feeding upon cue re-exposure. This behavioral divergence correlated with increased expression of oxidative stress markers and plasticity-related genes in the central nervous system. In contrast, pairing the same cue with acute heat shock, known to induce a sickness-like state, resulted in long-term memory formation only in snails showing upregulation of cellular stress, immune-related, and neuroplasticity genes. Thus, both the nature of the stressor and individual physiological state shape memory outcomes, with Lymnaea engaging stressor-specific molecular programs to support learning. Importantly, this work positions Lymnaea as a valuable sentinel species in behavioral ecotoxicology. The transcriptional markers identified, such as LymHSP70, LymTLR4, and LymP2X, may serve as sensitive indicators of learning and memory disruption by environmental contaminants. By integrating behavioral and gene expression analyses, this study offers a promising framework for investigating how natural and anthropogenic stressors affect cognition, with broad applications for environmental monitoring, toxicology, and conservation biology.