Toxic stress-specific cytoprotective responses regulate learned behavioral decisions in C. elegans

Background Recognition of stress and mobilization of adequate “fight-or-flight” responses is key for survival and health. Previous studies have shown that exposure of Caenorhabditis elegans to pathogens or toxins simultaneously stimulates cellular stress and detoxification responses and aversive behavior. However, whether a coordinated regulation exists between cytoprotective stress responses and behavioral defenses remains unclear. Results Here, we show that exposure of C. elegans to high concentrations of naturally attractive food-derived odors, benzaldehyde and diacetyl, induces toxicity and food avoidance behavior. Benzaldehyde preconditioning activates systemic cytoprotective stress responses involving DAF-16/FOXO, SKN-1/Nrf2, and Hsp90 in non-neuronal cells, which confer both physiological (increased survival) and behavioral tolerance (reduced food avoidance) to benzaldehyde exposure. Benzaldehyde preconditioning also elicits behavioral cross-tolerance to the structurally similar methyl-salicylate, but not to the structurally unrelated diacetyl. In contrast, diacetyl preconditioning augments diacetyl avoidance, weakens physiological diacetyl tolerance, and does not induce apparent molecular defenses. The inter-tissue connection between cellular and behavioral defenses is mediated by JNK-like stress-activated protein kinases and the neuropeptide Y receptor NPR-1. Reinforcement of the stressful experiences using spaced training forms stable stress-specific memories. Memory retrieval by the olfactory cues leads to avoidance of food contaminated by diacetyl and context-dependent behavioral decision to avoid benzaldehyde only if there is an alternative, food-indicative odor. Conclusions Our study reveals a regulatory link between conserved cytoprotective stress responses and behavioral avoidance, which underlies “fight-or-flight” responses and facilitates self-protection in real and anticipated stresses. These findings imply that variations in the efficiency of physiological protection during past episodes of stress might shape current behavioral decisions. Graphical abstract

Experimental tests of bivalve shell shape reveal potential tradeoffs between mechanical and behavioral defenses

Bivalves protect themselves from predators using both mechanical and behavioral defenses. While their shells serve as mechanical armor, bivalve shells also enable evasive behaviors such as swimming and burrowing. Therefore, bivalve shell shape is a critical determinant of how successfully an organism can defend against attack. Shape is believed to be related to shell strength with bivalve shell shapes converging on a select few morphologies that correlate with life mode and motility. In this study, mathematical modeling and 3D printing were used to analyze the protective function of different shell shapes against vertebrate shell-crushing predators. Considering what life modes different shapes permit and analyzing the strength of these shapes in compression provides insight to evolutionary and ecological tradeoffs with respect to mechanical and behavioral defenses. These empirical tests are the first of their kind to isolate the influence of bivalve shell shape on strength and quantitatively demonstrate that shell strength is derived from multiple shape parameters. The findings of this theoretical study are consistent with examples of shell shapes that allow escape behaviors being mechanically weaker than those which do not. Additionally, shell elongation from the umbo, a metric often overlooked, is shown to have significant effects on shell strength.