Caenorhabditis elegans male sensory-motor neurons and dopaminergic support cells couple ejaculation and post-ejaculatory behaviors

The nematode worm, C. elegans, is roughly 1 mm long, made up of around 1000 cells and has two sexes: male and hermaphrodite. Hermaphrodite worms produce both eggs and sperm and can self-fertilize to generate around 300 offspring each time. Fertilization by a male, on the other hand, results in three times as many progeny and introduces genetic diversity into the population. However, it also reduces the lifespan of the hermaphrodite. Mating also incurs a cost for males: it requires a lot of energy, which prevents male works from engaging in other activities, such as feeding, and it also increases their risk of predation. In many species, including C. elegans, the frequency with which a male can mate is limited by a period of reduced mating drive and ability that follows each instance of successful mating. However, the molecular and cellular basis of this ‘refractory period’ remains largely unclear. Using a range of techniques, LeBoeuf et al. have now identified the circuits that regulate male mating behavior in C. elegans. When male worms were introduced into a Petri dish containing 15 hermaphrodites, most males initiated mating within about 2 min. The length of the refractory period varied between worms, but averaged roughly 12 min. This consisted of a period of disinterest, in which males did not approach hermaphrodites, followed by a period in which males attempted mating but were slower and less efficient, suggesting that the neural circuits controlling mating behaviors had yet to recover completely. Males with longer refractory periods produced more progeny in their second mating than those with shorter refractory periods, suggesting that the interval also enables males to replenish their sperm levels. Further experiments revealed that a chemical transmitter called dopamine promotes ejaculation and then immediately reduces the worm's activity levels, giving rise to the refractory period. By enforcing a delay between matings, the refractory period may also increase the likelihood that successive matings will be with different hermaphrodites, helping to maximize the number and diversity of offspring. Some aspects of the neural circuitry that controls the refractory period in C. elegans resemble those seen in mammals, suggesting that insights gained from an animal with 1000 cells could also be relevant to more complex species.