Nematode sperm go rogue

When nematodes have sex with the wrong species, sperm can turn into rampaging killers.

In the worst mixed-up couplings between tiny, eyeless worms of the genus Caenorhabditis, the sperm of males from more sexually competitive species can be so aggressive they reduce the fertility of, or eventually kill, the receiving partner. The marauding sperm push beyond normal receptacles for sperm and storm into ovaries and the rest of the partner’s reproductive tract, says Eric Haag of the University of Maryland, College Park.

That premature contact with sperm can ruin eggs that have not developed enough for fertilization. Then aggressive sperm can “bust out of the ovary and start crawling around the body cavity,” Haag says. He’s even found sperm barging around in a partner’s head.

While gruesome, such mating mayhem gives clues to which worm species have long-standing conflicts between the sexes that would be hard to detect otherwise, the researchers say July 29 in PLOS Biology. The cross-species mating result “is a kind of gross, weird thing,” Haag says, but it sheds light on same-species mating too, too. “What it’s telling us is that within a species the world is much rougher than it looks.”

The perils involved in mixed mating “surprised a lot of us when we first saw the preliminary data,” says Diane Shakes of the College of William & Mary in Williamsburg, Va. She learned of  the sperm violence last year   at an international meeting of specialists studying C. elegans. The worm is a familiar workhorse in labs worldwide, but the way it gets trashed by the sperm of other species with livelier sex lives was startling.

The contrasts between the nematode species’ mating habits lie at the heart of the experiment. In C. elegans and several other species, male worms turn up now and then, but most individuals are self-fertilizing hermaphrodites. Nematode gonads don’t form elaborate specialized structures, so it’s not a big deal for individuals to start out life producing and storing sperm and later to switch to making eggs for the dollops of stored sperm to fertilize.

These minimalist hermaphrodites don’t have the right anatomy to deliver sperm to another worm but they can receive sperm from the occasional males of their species. Using their own stored sperm, “they go generations without mating at all,”” Haag says. Over evolutionary time the sperm of these species become weak competitors.

In contrast, species of Caenorhabditis with full-time males and females often mate with multiple partners. In such a promiscuous arena, evolution favors barnstorming aggression that lets sperm reach an egg first. For females of these species, “their body is the battleground upon which these males are fighting,” Haag says. Evolution also favors females that “make sure these pushy, aggressive sperm that are good at fertilizing eggs don’t get too pushy and harm them,” he adds. As long the sexes’ countermeasures balance, this escalating conflict between the sexes causes little visible harm and can be difficult for a scientist to detect.

Signs of the hidden evolutionary arms races reveal themselves when worm species mix. The ferocious aggression showed up when researchers paired males from various competitive species with partners from any of three self-fertilizing hermaphrodite species, including C. elegans. The competitive alien species’ sperm not only goes on rampages but can actually push aside the smaller sperm from males of  the mostly hermaphroditic species. (Nematode sperm can’t swim but are powerful, amoeba-like crawlers.)

In one set of doomed pairings, a population of mild-mannered C. briggsae hermaphrodites started dying after only  one encounter with males of C. nigoni. These pairings also yielded only about 25 young on average instead of the 225 or more from hermaphrodites left to fertilize themselves.

These nematodes, so useful for other research, may become revealing organisms for studying how battles of the sexes play out over evolutionary time, says Ronald E. Ellis of Rowan University School of Osteopathic Medicine in Stratford, N.J. Other animals routinely injure their partners during sex. These nematodes, Ellis points out, inflict harm after mating; partners have already gone their separate ways when the sperm left behind break bad.