Chemotaxis is a behavior used to alter the direction of motion towards or away from chemical stimuli employed by a number of simple organisms. Prokaryotes such as E. coli use a “run” and “tumble” approach towards chemotaxis. They move forward for 1-2 seconds (“run”) and then reorient themselves in a random direction (“tumble”) for less than 1 second. By modulating the number of tumbles based on the chemical environment, the organism can avoid or approach various stimuli (Maki et al, 2000). Eukaryotes such as C. elegans also use stochastically determined chemotaxis in order to move towards and away from stimulants, although their model has some modifications. Instead of periodically stopping, C. elegans randomly changes its direction of motion through pirouettes, which are suppressed when the current environment is attractive (Pierce-Shimomura et al, 1999). Nuttley et al (2002) examine the chemotaxis behavior of C. elegans when exposed to benzaldehyde in an associative learning paradigm. The researchers argue that the effects of the unconditioned and conditioned stimuli in their study can only be explained in an associative learning framework. This paper will review the evolutionary and ecological explanations for the proposed behavioral plasticity and evaluate the empirical evidence offered as support.
Like all Caenorhabditis species, C. elegans feed and live in soil filled with nutrients and microbacterial organic material. The natural habitat of C. elegans itself has not yet been discovered, although it is well known to thrive in man-made environments such as compost and garden soil (Kiontke and Sudhaus, 2006). Males represent less than 0.5% of the population under normal conditions, but sperm is used with 100% efficiency. Their reproductive mode favors early over large broods, typically produces about 300 progeny, and is optimized for rapid population growth (Hodgkin and Barnes, 1991). Under these competitive conditions, even a slight fitness advantage in survival would be very likely to be selected for.
Food is a strong unconditioned stimulus and motivator for behavior in C. elegans. Cassada and Russell (1975) showed that by limiting the supply of the food supply bacteria, the worms can be induced into regressing to the dauer larva stage, indicating that they have incentive to feed in addition to avoiding starvation. Additionally, there is evidence that different bacteria in the environment release different amounts of volatile aromas (Sondergaard and Stahnke, 2002), and that C. elegans’s bacterial food choices display variance in quality (Shtonda and Avery, 2006). C. elegans are initially responsive to at least 40 of the odors released by these bacteria (Nuttley et al, 2002), but after prolonged exposure they begin to suppress their attraction in a process known as olfactory adaptation. Worms with an ability to suppress this adaptation when exposed to odors that are associated with high-quality food will have a fitness advantage over worms without this ability. That is because those with the ability will be more likely to be exposed to more and better food sources, making them less likely to either die or enter the dauer larva stage and thus making them more likely to pass on their genes for associative learning to the next generation.
Nuttley et al (2002) posit that C. elegans have such a propensity for associative learning. C. elegans have a natural attraction to the odor benzaldehyde, although this is suppressed by olfactory adaptation to the stimulus for 1 hour, as shown by a chemotactic index (CI). If this adaptation is a result of associative learning, then it should be reversed either when benzaldehyde is subsequently presented with food, or when the lack of food is shown to be independent of benzaldehyde. The researchers test for both of these conditions, as well as a number of other controls, and summarize their results in their Figure 3. The naïve CI is above 0.9, indicating that on average more than 95% of the worms travelled to the benzaldehyde as opposed to the ethanol control. When the worms were exposed to benzaldehyde for 1 hour the CI dropped to less than 0, indicating olfactory adaptation. The researchers then measured groups exposed to an additional hour of benzaldehyde without food, which increased the olfactory adaptation (an even lower CI), and food without odorant, which decreased the adaptation due to faulty short-term memory (a slightly higher CI). But the most important trials were when the researchers exposed the worms to a second hour of either benzaldehyde and food, or no odorant and no food. As a result of both of these conditions the worms reversed their olfactory adaptation and returned to CI levels just below naïve. Both of these results are key conditions of the associative learning paradigm and lend support for that conclusion.
Why do C. elegans show such a strong initial preference for volatile odors such as benzaldehyde? One hypothesis is that C. elegans have a novelty-seeking adaptation that serves to guide the worms to food sources. Their chemoreceptors retain a natural affinity towards novel odors until the worms can learn its associations with food. If the odor is not a sufficient indicator of high-quality food, then the worms will undergo olfactory adaptation. However, if it is a good indicator of food, then the olfactory adaptation will be suppressed, and the worms will continue to be attracted to the scent. This hypothesis is consistent with the evidence from Nuttley et al that olfactory adaptation to the odor is suppressed by exposure to a food source in a dose-dependent manner, and that initial olfactory adaptation can be reversed by subsequent pairing of the odor with food. Chemoreception is the most complex genetic system of C. elegans and probably constitutes the majority of its signal transduction (Robertson and Thomas, 2006), so the ability to learn associatively within this behavior would be highly adaptive in an evolutionary sense.
Cassada RC, Russell RL. 1975 The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Developmental Biology 46:326-342.
Sondergaard AK, Stahnke LH. 2002 Growth and aroma production by Staphylococcus xylosus, S. carnosus and S. equorum—a comparative study in model systems. International Journal of Food Microbiology 75:99-109.
Kiontke K, Sudhaus W. 2006 Ecology of Caenorhabditis species, WormBook, ed. The C. elegans Research Community, WormBook. doi/10.1895/wormbook.1.37.1.
Torayama I, Ishihara T, Katsura I. 2007 Caenorhabditis elegans integrates the signals of butanone and food to enhance chemotaxis to butanone. Journal of Neuroscience 27:741-750.
Robertson HM, Thomas JH. 2006 The putative chemoreceptor families of C. elegans. WormBook, ed. The C. elegans Research Community, WormBook.
Shtonda BB, Avery L. 2006 Dietary choice behavior in Caenorhabditis elegans. Journal of Experimental Biology 209:89-102.
Hodgkin J, Barnes TM. 1991 More is not better: Brood size and population growth in a self-fertilizing nematode. Proc Biol Sci 246:19-24.
Pierce-Shimomura, JT, Morse TM, Lockery SR. 1999 The fundamental role of pirouettes in Caenorhaditis elegans chemotaxis. Journal of Neuroscience 19:9557-9569.
Nuttley WM, Atkinson-Leadbeater KP, van der Kooy D. 2002 Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. PNAS 99:12499-12454.