Should I Stay or Should I Go?

Crawling C. elegans hermaphrodite worm

Crawling C. elegans hermaphrodite worm (Photo credit: Wikipedia)

             Should I stay or should I go? Well, how much food do you have? In some organisms, sexual desire is expressed by leaving, that is, by bidding adieu to a delicious pile of food and wandering off in search of a mate. But not just any mate, a mate with food! Lipton et al., at  Albert Einstein College of Medicine, use the “leaving assay” to measure male sexual desire. Their subject is the elegant, rod-like worm, Caenorhabditis elegans.*  They start by placing males on their preferred food source; then they measure how often males exit in search of mating partners. You can see the trails they leave in the substrate in this video of C. elegans appropriating Harlem art and culture.

              How do the researchers know “leaving” is a sex behavior? Context. Leaving a food source occurs only in a sexual context, and the leaving assay is being used to tease apart the threads that control the appetites for food and sex.

            First, a quick lesson in the fascinating sexuality of C. elegans. Males are not interested in other males, but they search intensely for a mating partner of the other sex. Note that I said “other sex” not “opposite sex.” There are no female C. elegans.  Males of this species mate enthusiastically with hermaphrodites. Hermaphrodites can, of course, self-fertilize, but sexual unions between males and hermaphrodites are far more fruitful than selfing. For hermaphrodites, mating with a male will produce more offspring, and for males, hermaphrodites are the only crying game in town.

            In the leaving assay, C. elegans males are placed on a preferred food source with or without hermaphrodites. Sexually mature males tend to linger when dining with hermaphrodites but leave readily when no hermaphrodites are present at the food source. They wander off searching for mates. The predilection is specific to sexually mature C. elegans, not to juveniles or males that have had their gonads removed.  It’s the gonads that put the lust in wanderlust. As sexy males’ bodies move through the substrate, they leave their snakey imprint, a permanent record of their search for the ideal dining experience. What is the ideal? A cozy little bistro with not only delicious cuisine but hermaphrodite companionship. What’s more, the hermaphrodites alone are not enough. Males prefer to stay and mate with hermaphrodites, but only hermaphrodites positioned at an abundant food source.

            The leaving assay in C. elegans is being used to tease apart the intricate threads that control the appetites for food and sex. Like our own appetites, those of C. elegans are sensitive to prior experience. Males that have been previously food-deprived have a longer latency to leave a food source. Hungry males will stay longer on a lonely, hermaphrodite-free food source before finally wandering off in search of a companion. The longer the food deprivation, the longer the males delay their wanderlust. These changes in the hunger for food and desire for sex may be mediated by some of the same hormones at work in our own species. Other researchers have shown that when members of C. elegans eat food, there is an increase in the secretion of serotonin. You’ve heard of it. Drugs prescribed for human depression target serotonin action. Prozac, for example, increases serotonin levels by blocking the reuptake of serotonin by the cells that secreted it in the first place. We have long known that depletion of serotonin is associated with anxiety and depression, and more recently it has been suggested that overeating foods that promote serotonin synthesis is a form of self-medication. Getting back to C. elegans, Lipton et al., found that mutations in the genes that encode serotonin receptors render the males insensitive to serotonin action. Mutant males that are insensitive to serotonin act like food-deprived males in that they fail to leave a food source in search of mating partners. There’s more. Mutations or other manipulations that inhibit gonadal function also act like food deprivation, i.e., they prevent wanderlust. Mutation of the fog-1 gene transformed males to females, that is, fog-1 mutants produced oocytes instead of sperm. Those males so transformed did not show the leaving behavior, but instead remained on food! This suggest that the chemical pathways that determine whether a young nematode develops into an adult male or a hermaphrodite also determine the leaving response to a food source.

            As I have noted in recent a review article (Schneider et al., 2012), most of the chemical messengers that increase the hunger for food inhibit sexual desire and ability. The reverse is also true. Chemical messengers that inhibit eating tend to increase sexual desire and ability.  The sheer number of these chemical messengers is mind boggling. The thought of unraveling the complexity of motivated behavior in vertebrates is overwhelming. On the other hand, the nervous system of C. elegans, a nematode worm, is comprised of only a few hundred neurons. The fact that they show quantifiable, goal-oriented decisions regarding food and sex is remarkable.

            Most investigators study food intake in animals (usually rats or mice) that are singly-housed and have little or no opportunity to move, let alone interact with potential mating partners. Most investigators that study reproduction do not observe their experimental subjects in the presence of food. The entire pharmaceutical-industrial complex is driven by theories derived from studying animals in these artificial environments. The knee-jerk assumption in obesity research is that chemical messengers like serotonin, leptin, and others function to keep body weight within some fashionable and “healthy” limit, and that this system has failed in over 60% of the population.  The work of Lipton is more in line with the idea that these chemical messengers function to orchestrate the appetites for food and sex in environments where energy availability fluctuates. For testing this idea, what system could be more elegant than that of C. elegans?

*its name is actually Greek and Latin for “recent, rod-like, elegant”

This is my favorite

C. elegans parody of that awful Harlem Shake video.

Lipton, J. Kleemann, G., Ghosh, R. Lints, R., Emmons, S. W. Journal of Neuroscience, 24 (34) pp. 7427, 2004.

Schneider J. E., Klingerman C. M. and Abdulhay A. (2012) Sense and nonsense in metabolic control of reproduction. Front. Endocrin. 3:26. doi: 10.3389/fendo.2012.00026.

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