The neuroethology of C. elegans escape

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Escape behaviors are crucial to survive predator encounters. Touch to the head of Caenorhabditis elegans induces an escape response where the animal rapidly backs away from the stimulus and suppresses foraging head movements. The coordination of head and body movements facilitates escape from predacious fungi that cohabitate with nematodes in organic debris. An appreciation of the natural habitat of laboratory organisms, like C. elegans, enables a comprehensive neuroethological analysis of behavior. In this review we discuss the neuronal mechanisms and the ecological significance of the C. elegans touch response.

Highlights

► C. elegans coordinates head and body movements during a touch induced escape response. ► The complete sensory-motor circuit that controls the C. elegans escape response is known. ► Predacious fungi catch nematodes using hyphal trapping devices. ► The C. elegans escape response increases its odds of surviving encounters with predacious fungi. ► Study of the natural habitat of genetic model organisms allows for a comprehensive neuroetholigical analysis of behavior.

Introduction

‘Eat but don’t get eaten’ is a prevailing motto that guides animal behavior. However, this principle presents a dilemma since foraging often increases the risk of predation. Animals can offset part of these risks by trying to survive a confrontation with a predator. Run, dart, jump, fly, burrow and hide can all improve the prey's odds in these life or death encounters. Time is of the essence so the animal needs to quickly translate sensory information into action. As a consequence, these escape responses are typically robust, use dedicated neuronal structures and have a clear evolutionary purpose, making them favorite subjects for laboratory study [1]. The tail-flip escape in the crayfish [2], the C-start escape in goldfish [3] and the mollusk withdrawal response [4] have provided crucial insights into fundamental neuronal processes as diverse as synaptic transmission, sensory transduction, decision making, and learning and memory. The study of these relatively simple circuits has provided some of the rare examples where we know the complete path from sensory input to a motor output. However, genetic analyses in these organisms are difficult, leaving the molecular coding of these behaviors relatively unexplored. Studies in genetically tractable organisms, like the fruit fly Drosophila melanogatser and the roundworm Caenorhabditis elegans, have provided some insight into the molecular basis of escape behaviors. In the fly, the giant fiber (GF) neurons coordinate leg extension and wing depression, which are critical for fast flight initiation when a fly is startled by a strong visual stimulus [5] (see review G. Card, this issue). A number of genes have been identified from genetic screens which play a role in the development of the giant fiber circuit, identifying molecular mechanisms that control outgrowth of GF axons, and the formation and maturation of synapses [6]. The neuronal pathway from the GF to motor neurons is well defined, but relatively little is known about its sensory inputs.

Section snippets

The C. elegans touch response

The complete wiring diagram of the C. elegans nervous system is known [7]. This framework is a tremendous asset for understanding sensory processing, including the escape response. C. elegans moves on its side by propagating a sinusoidal wave of dorsal–ventral flexures along the length of its body [8]. Locomotion is accompanied by exploratory head movements, where the head of the animal sways rapidly from side to side (Figure 1). Head and body movements are controlled independently by distinct

The neural circuit of escape

In the worm, gentle touch to the body is sensed by six mechanosensory neurons; the ALM and AVM neurons sense touch to the anterior half, while the PLM and PVM neurons sense touch to the posterior half (Figure 2) [11]. Optogenetic activation of the ALM/AVM or PLM/PVM neurons in transgenic animals that express a light activated channelrhodopsin in the mechanosensory neurons induces a reversal or a forward acceleration, respectively [12, 13]. All six neurons send anteriorly directed processes that

C. elegans ecology

What does C. elegans need to escape from? Natural populations of C. elegans are found world wide in decomposing organic material such as compost, decaying leaves and rotting fruit [23, 24••]. C. elegans can survive less favorable conditions as a dauer larvae, an alternative developmental stage that is long lived. Dauer larvae can climb onto protrusions, stand on their tail and wave in the air, a process known as nicatation. This behavior may promote dispersal to new more favorable habitats.

Out of the jaws of death

Since the C. elegans mechanosensory neurons are very sensitive, the touch of a mite, a sticky hyphae or a tightening fungal noose could provide enough force to trigger an escape response. An acceleration or quick reversal may allow the worm to survive such an encounter with a predator. The wide array of available mutants in C. elegans provides unique opportunities to directly test if behavioral traits contribute to the odds of surviving predator encounters. Studies of predator–prey

Conclusions

While escape responses have been a favorite subject for neuroethological studies of behavior, it has been hard to unify the analysis of proximate and ultimate causes of behavior. A renewed appreciation for the natural history of laboratory animals may allow us to bridge a gap between the molecular ‘how’ and behavioral ‘why’. Furthermore, even though genomic approaches have been instrumental in studies of genotypic selection, our understanding is largely correlative. The experimental

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We would like to thank Claire Benard and Scott Waddell for comments on the manuscript. This work is supported by a grant from the National Institutes of Health grant GM084491.

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