publications

2024

1. 

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

   Kathleen T Quach, Gillian A Hughes , and Sreekanth H Chalasani

   bioRxiv (under review at eLife), 2024

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   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.

2022

1. 

   Flexible reprogramming of Pristionchus pacificus motivation for attacking Caenorhabditis elegans in predator-prey competition

   Kathleen T Quach, and Sreekanth H Chalasani

   Current Biology, 2022

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   Animals with diverse diets must adapt their food priorities to a wide variety of environmental conditions. This diet optimization problem is especially complex for predators that compete with prey for food. Although predator-prey competition is widespread and ecologically critical, it remains difficult to disentangle predatory and competitive motivations for attacking competing prey. Here, we dissect the foraging decisions of the omnivorous nematode Pristionchus pacificus to reveal that its seemingly failed predatory attempts against Caenorhabditis elegans are actually motivated acts of efficacious territorial aggression. While P. pacificus easily kills and eats larval C. elegans with a single bite, adult C. elegans typically survives and escapes bites. However, non-fatal biting can provide competitive benefits by reducing access of adult C. elegans and its progeny to bacterial food that P. pacificus also eats. We show that the costs and benefits of both predatory and territorial outcomes influence how P. pacificus decides which food goal, prey or bacteria, should guide its motivation for biting. These predatory and territorial motivations impose different sets of rules for adjusting willingness to bite in response to changes in bacterial abundance. In addition to biting, predatory and territorial motivations also influence which search tactic P. pacificus uses to increase encounters with C. elegans. When treated with an octopamine receptor antagonist, P. pacificus switches from territorial to predatory motivation for both biting and search. Overall, we demonstrate that P. pacificus assesses alternate outcomes of attacking C. elegans and flexibly reprograms its foraging strategy to prioritize either prey or bacterial food.

2021

1. 

   State-dependent network interactions differentially gate sensory input at the motor and command neuron level in Caenorhabditis elegans

   Zachary T Cecere* , Kathleen T Quach*, Eviatar Yemini , and 4 more authors

   bioRxiv, 2021

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   Neural responses are influenced by both external stimuli and internal network states. While network states have been linked to behavioral and stimulus states, little is known about how sensory inputs are filtered by whole-brain activity to affect motor and command neurons. Here, we recorded whole-brain activity of Caenorhabditis elegans experiencing bacterial food stimuli, and modeled how sensory inputs affect motor and command neurons in a network state-dependent manner. First, we classified active neurons into six functional clusters: two sensory neuron clusters (ON, OFF), and four motor/command neuron clusters (AVA, RME, SMDD, SMDV). Using encoding models, we found that ON and OFF sensory neurons that respond to onset and removal of bacteria, respectively, employ different adaptation strategies. Next, we used decoding models to show that bacterial onset and removal differentially drive AVA and RME cluster activity. To explore state-dependent effects on AVA and RME clusters, we developed a model that identified network states and fitted submodels for each state to predict how each of the six functional clusters drive AVA and RME cluster activity. We also identified network states in which AVA and RME clusters were either largely unperturbed by or receptive to bacterial sensory input. Furthermore, this model allowed us to disentangle the state-dependent contributions of stimulus timescales and bacterial content to neural activity. Collectively, we present an interpretable approach for modeling network dynamics that goes beyond implication of neurons in particular states, and moves toward explicitly dissecting how neural populations work together to produce state dependence.

2020

1. 

   Intraguild predation between Pristionchus pacificus and Caenorhabditis elegans: a complex interaction with the potential for aggressive behaviour

   Kathleen T Quach, and Sreekanth H Chalasani

   Journal of Neurogenetics, 2020

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   The related nematodes Pristionchus pacificus and Caenorhabditis elegans both eat bacteria for nutrition and are therefore competitors when they exploit the same bacterial resource. In addition to competing with each other, P. pacificus is a predator of C. elegans larval prey. These two relationships together form intraguild predation, which is the killing and sometimes eating of potential competitors. In killing C. elegans, the intraguild predator P. pacificus may achieve dual benefits of immediate nutrition and reduced competition for bacteria. Recent studies of P. pacificus have characterized many aspects of its predatory biting behaviour as well as underlying molecular and genetic mechanisms. However, little has been explored regarding the potentially competitive aspect of P. pacificus biting C. elegans. Moreover, aggression may also be implicated if P. pacificus intentionally bites C. elegans with the goal of reducing competition for bacteria. The aim of this review is to broadly outline how aggression, predation, and intraguild predation relate to each other, as well as how these concepts may be applied to future studies of P. pacificus in its interactions with C. elegans.