Interdependence between SEB-3 and NLP-49 peptides shifts across predator-induced defensive behavioral modes in Caenorhabditis elegans

Abstract

Prey must balance the need to avoid predators with the need to feed, a dilemma central to prey refuge theory. Additionally, prey must also assess predatory imminence, or how close predator threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes--pre-encounter, post-encounter, and circa-strike--each corresponding to increasing levels of predatory imminence--suspecting a predator, detecting a predator, and contact with a predatory attack. Although prey often simultaneously face variations in predatory imminence and spatial distribution of predation risks, research on how these factors intersect to influence defensive behaviors has been limited. Integrating these factors into a complex, naturalistic environment could enable comprehensive analysis of multiple defense modes in consistent conditions within the same study, unlike laboratory tests designed to examine only one mode at a time. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. We show that C. elegans innately exhibits circa-strike behaviors in a foraging environment comprised of a food-rich, high-risk patch and a food-poor, predator-free refuge. However, after extended experience in this environment, C. elegans acquires post- and pre-encounter behaviors that proactively anticipate threats rather than merely reacting to attacks. We also demonstrate that these defense modes are potentiated by increasingly harmful predators, with only life-threatening predators capable of eliciting all three defense modes. Finally, our model system reveals that SEB-3 receptors and NLP-49 peptides, key to stress response regulation, vary in their impact and interdependence across defense modes. We find that SEB-3 has a greater impact on the highest-imminence defense mode, while NLP-49 peptides have a stronger effect on the lowest-imminence defense mode. Overall, our model system reveals detailed and comprehensive insights into how stress-related molecular signaling affects behavioral responses to threats.