By: Helen Beilinson
Caenorhabditis elegans, or simply C. elegans, are small nematodes (worms) that are one of the most popular organisms used to study animal biology. There are many reasons for this: they replicate quickly and they are easy and inexpensive to care for. But the most fascinating fact is that each individual worm has a set number of cells that each has a specific position and function. Each of the cells can be followed from its conception to its final location. In the 1980’s, Sir John Sultson was one of the first scientists to track each of the worm’s cells throughout development to create one of the first maps of cell lineage. Since then, many researchers have continued to follow up on Sultson’s studies, leading to the belief that C. elegans’ cell lineage map had been completed. So, it came as a big surprise to the field when a group out of London discovered two new neuronal cells in the male worms.
Although C. elegans are sexually dimorphic, like humans, they are not divided into males and females. Instead, they are made up of hermaphrodites that can self-fertilize and males that can only fertilize the hermaphrodites. Males and hermaphrodites have different reproductive behaviors to reflect their reproductive patterns. Male worms need to learn how to optimally locate mating partners, which they accomplish through a process called sexual conditioning. It was previously known that males are attracted to hermaphrodites by sensing their pheromones or by directly sensing them with their tails. A recent study in the journal Nature identified two previously undescribed male-specific neurons that are necessary for sexual maturation.
This finding came as a surprise. Because they are self-perpetuating, hermaphroditic worms are easy to maintain, and are consequently more widely studied than male worms. When studying males, most scientists have focused on physically obvious attributes, such as the worms’ tails, not their brains. However, when these authors looked more closely at male worms’ brains, which had been thought to contain 383 neurons, they found that they contained 385. They called these neurons mystery cells of the male, or MCMs. To identify the function of MCMs, the authors explored other cells that the MCMs interact with. They found that these cells are a component in a loop of interactions between neurons that function in regulating mating experiences by modulating behavior. Specifically, the MCMs are necessary for a male-specific switch in puberty, in which they respond to chemical signals differently after sexual conditioning. This sexual conditioning functions to make the males suppress cues from the environment that indicates presence or absence of food in favor of sex. While hermaphrodites will always migrate towards areas with good food and migrate away from dangerous areas without food, sexual conditioning causes males to go away from areas with good food or go towards areas with bad food if there are potential mates in those locations. In effect, males prioritize sex over food.
To test this hypothesis, the authors set up the following experiment. C. elegans tend to avoid salt-rich environments, because high salt is usually an indication of food scarcity. The authors placed potential mates into a salt-rich environment and placed either hermaphrodites or males outside of this salt-rich location. They found that hermaphrodites, before and after sexual conditioning, will always avoid salt locations. However, the males will avoid the salt location before sexual conditioning, and will enter the salt-rich area after sexual conditioning. If the authors remove the MCMs from sexually conditioned males, they no longer enter the salt-rich area after sexual conditioning. The authors conclude that male C. elegans suppress their knowledge of the risk of no food for the benefit of potentially mating.
This phenomenon makes sense. Hermaphrodites are capable of self-fertilization, so in order to procreate, they need any other worms around and need to prioritize their health to be good parents. Males, on the other hand, absolutely need another partner to reproduce. The health of the male is not as critical in producing viable children as is their partners, the hermaphrodites. Thus, they can risk putting sex before food.
When the authors tried to find the origin of the MCMs during C. elegans’ development, they found that they arise from glial cells. Glia are cells that reside next to neurons and provide structural and functional support to neurons with which they are associated. However, during sexual maturation, some of the worms’ glial cells begin to start expressing neuronal proteins and develop into MCMs. Hermaphrodites do not have the glial precursors of the MCMs, so these cells, from the beginning of the male worms’ lives, are male-specific. This is the first case found in non-vertebrates where neurons develop from glial cells.
The discovery of these new neurons links developmental and anatomical differences between males and hermaphrodites to their sex-specific behaviors. It’s fascinating that the behavioral patterns of these worms is quite literally hard-wired in their minds, as opposed to something they have learned and apply to a situation. These findings are also a testament to how many new discoveries are happenstance and often come from re-observing something that’s right under your own nose.