Sensory systems: their impact on C. elegans survival

Abstract

An animal's survival strongly depends on a nervous system that can rapidly process and integrate the changing quality of its environment and promote the most appropriate physiological responses. This is amply demonstrated in the nematode worm Caenorhabditis elegans, where its sensory system has been shown to impact multiple physiological traits that range from behavior and developmental plasticity to longevity. Because of the accessibility of its nervous system and the number of tools available to study and manipulate its neural circuitry, C. elegans has thus become an important model organism in dissecting the mechanisms through which the nervous system promotes survival. Here we review our current understanding of how the C. elegans sensory system affects diverse physiological traits, whose coordination would be essential for survival under fluctuating environments. The knowledge we derive from the C. elegans studies should provide testable hypotheses in discovering similar mechanisms in higher animals.

Keywords: C. elegans; developmental plasticity; insulin-like peptides; learning; lifespan; sensory system.

Figure 1

A schematic diagram of the C. elegans anatomy. The nervous system of the animal is shown, which consists of the head ganglia, the nerve ring, the dorsal and ventral nerve cords, a few lateral neurons and the tail ganglia. Many of the animals’ sensory neurons are found in the head and tail ganglia. A few of the sensory neurons are also found throughout the length of the animal. This diagram is drawn according to www.wormatlas.org.

Figure 2

The C. elegans hermaphrodite life cycle. C. elegans development progresses through four larval stages (L1-L4) prior to reproductive adulthood under favorable conditions, i.e., abundant availability of bacterial food sources, low population density and ideal temperatures. When presented with harsh conditions, C. elegans L1 larvae undergo an alternate developmental program, known as dauer. When conditions improve, dauer larvae, which are developmentally arrested, can exit into L4 to become a reproductive adult.

Figure 3

Context-dependent sensory effects on C. elegans lifespan. (A) Chemosensory neurons detect food type-derived cues that inhibit or promote longevity. (B) A decrease in food intake levels, also commonly known as dietary restriction, increases the lifespan of C. elegans through the chemosensory neuron ASI, which involves skn-1 signaling. (C) Male C. elegans secrete pheromone(s) that shorten the lifespan of hermaphrodites. (D) C. elegans thrive under temperatures ranging from 15 to 25°C, which requires the activities of thermosensory neurons. See text for references.

Figure 4

Sensory influences on developmental plasticity in C. elegans. Throughout their lives, C. elegans secrete a pheromone mixture, known as dauer pheromone, whose environmental concentration reflects population density. (A) A combination of low dauer pheromone and abundant food is detected by specific chemosensory neurons that ensure reproductive growth, i.e., C. elegans develops from L1-L4 to become a reproductive adult. (B) In contrast, a combination of high pheromone and low food is detected by other chemosensory neurons that promote dauer developmental arrest. (C) Once in the dauer stage, environmental conditions are sensed by other neurons that either inhibit or promote exit from arrest. See text for references.