NYU biologist Matthew Rockman and his colleagues have made a discovery that points to a previously unknown dynamic among certain types of worms: Natural variation in a single gene produces males with excretory pores that attract the sexual attentions of other males.
For tiny nematode worms of the species Caenorhabditis elegans, males are rare and generally irrelevant in nature. That’s because the vast majority of C. elegans individuals are self-fertilizing hermaphrodites. But NYU biologist Matthew Rockman and his colleagues have made a discovery that points to a previously unknown dynamic among these worms: Natural variation in a single gene produces males with excretory pores that attract the sexual attentions of other males.
“We found that variation in a single gene makes male worms attractive to other male worms, at least under very controlled and defined conditions in the lab,” Rockman says of the study, which appears in the journal Current Biology. “Given how rare males are, this attraction is probably never manifested in nature. But the findings still point to the way that sexual attraction in these worms is mediated by molecular biology and shaped by simple genetic differences among individuals.”
Scientists had known that some C. elegans males are attracted to other males. Rockman and his co-authors were intrigued based on a general interest in understanding how and why individuals differ from one another when it comes to sexual behaviors as well as other traits.
They’ve now traced much of the variation in this behavior to a single gene known as plep-1. Males carrying two copies of a plep-1 mutation attract other males for reasons that remain mysterious. When males mate with the excretory pore of another male, they leave an injurious plug behind. Males with plugged excretory pores have trouble in mating and they don’t live as long as either.
When the researchers asked where this gene is active, they made another remarkable find.
“Of the 1000 cells in a C. elegans male, the gene turns out to be active in one: the excretory cell!” Rockman said.
The researchers say that the persistence of this gene--despite its detrimental effects on the individuals who carry it--may be explained by the distinctive reproductive mode in this species. Most of these worms have only one parent, a self-fertile hermaphrodite. Because matings between males and hermaphrodites are rare, sex has little chance to generate new combinations of genes—unlike in species with males and females. With few genetic combinations circulating in the population, natural selection has little ability to precisely weed out harmful mutations, particularly if they happen to occur on otherwise healthy chromosomes.
This isn’t the first study to show that worms’ behavior can be “surprisingly modular,” explains Luke Noble, the paper’s lead author and an NYU postdoctoral fellow.
“In some cases, the activity of single genes is required to specify single neurons, which are in turn required for components of behaviors such as locomotion and environmental sensing, at least under very restricted conditions in the lab,” he observes.
Still, most of their behaviors, including mating, are more complex, involving multiple genes and genetic networks. As a result, the new findings come as something of a surprise.
The researchers say they’d like to figure out how this one mutation in one gene makes males attractive to other males. They’d also like to explore male-male excretory pore plugging in the closely related species C. briggsae and the function of the gene plep-1 in worms and other species.
“These genes have been conserved across a huge swath of evolutionary history, and their functions are unknown,” Rockman said.
The research was supported, in part, by grants from the National Institutes of Health (R01 GM089972, F32 HD065442).