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This worm's sperm invades and kills females of another species

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An 'unprecedented' means of avoiding reproduction between species

Gavin Woodruff

When it comes to sex, animals have developed a plethora of tricks to avoid mixups with other species. They use sight, smell, and even feel to tell each other apart. But in certain cases, the similarities between species are just too strong, so internal processes, such as a female’s ability to detect sperm from another species and select those that belong to her own, have to pick up the slack. This is what tends to happen with Caenorhabditis worms, a type of roundworm. Unfortunately, this doesn’t always work — sometimes the sperm cells are just too quick, and things can go terribly wrong.

"What we found was that female gonads can instead get overrun by sperm from foreign males, leading to their permanent sterility," and sometimes death, said Asher Cutter, an evolutionary biologist at the University of Toronto, in an email to The Verge.

"female gonads can instead get overrun by sperm from foreign males."

Cutter is part of a team of researchers that published a study in PLOS Biology today describing how they went from observing the mechanism that Caenorhabditis worms use to prevent mixing genes with different species — often using mismatched reproductive cells and organs — to observing females of the Caenorhabditis briggsae species being "overrun by sperm."

"We were fascinated by the idea that 'mating with the wrong species' in many organisms often does not have much long-term consequence, in that there is often no exchange of genes between the species," Cutter said. So, "we started out trying to make genetic hybrids between species."

One of the things they did was mate C. briggsae females — this species is mostly made up of females that fertilize themselves using sperm they’ve produced on their own, so the researchers refer to them as "hermaphrodites" — with males of a different species called C. nigoni. These two species are very closely related, so they can actually produce viable and fertile offspring. But as the researchers observed for the first time, when this pairing does produce eggs, there are far fewer offspring than would normally be the case. "Instead of the 300 or so offspring they would normally make, they would make 10 or 20," Cutter said. "This was very unexpected."

To understand what was actually happening inside these translucent worms, the researchers used fluorescent dye and watched the sperm migrate inside the worms’ bodies after mating. "This showed us that the sperm derived from males of the 'wrong species' often migrated into inappropriate parts of the bodies of their mates," Cutter said, "sometimes leaving the reproductive organs entirely."

The sperm invasion also "induced early death."

This phenomenon — which the researchers called a "sperm invasion" dynamic — was "quite shocking," Cutter said, because in extreme cases, the overwhelming quantity of sperm migrated around the entire body cavity, instead of just around the reproductive organs. "This led to sterility of the hermaphrodites that males had mated with," he said, "and also induced early death." And when the hermaphrodites did manage to produce hybrid embryos, they were "not laid through the vulva," the researchers write, and got stuck in the oviduct instead. "This is one of several ways in which nigoni sperm sterilize briggsae hermaphrodites," said Eric Haag, a biologist at the University of Maryland and the co-author of the study, in an email.

Yet mating the C. briggsae males, which are rare, with the non-hermaphroditic C. nigoni females didn’t cause the females to die early. It still led to sterilization, however, when the females mated with these males more than once.

"Despite being a bit grotesque, an intriguing feature of [the hermaphrodites'] serious problem of having mated to males of another species is that it still precludes exchange of genes between the species," Cutter said, much like when females ignore foreign sperm during fertilization. So, one can still look at this and think of it as a successful — albeit rather drastic — iteration of an inter-species breeding avoidance mechanism.

Because this phenomenon hasn’t been described before, the researchers call it "unprecedented" in the paper. But some aspects of these observations aren’t altogether novel, given that there are other animal species where sperm cells move through the body cavity before fertilizing egg cells. This happens in flatworms and bed bugs, for instance. But usually this migration is a precursor to fertilization, which means it doesn’t cause infertility or death.

Hybrid embryos weren't laid through the vulva. They got stuck inside instead.

"We don't yet know what allows sperm to migrate beyond the spermatheca," Cutter said, referencing the female organ where fertilization takes place. Under normal circumstances, having sperm that can migrate quickly up the reproductive tract is advantageous for males who compete with other males for the best spot for their sperm inside the spermatheca. But in this case, the signals that keep the sperm inside the organ appear to have gone haywire.

"It could be that the seminal fluid contains a compound that the sperm cells release" and that causes the oviduct muscles to relax, Cutter said. As a result, the sperm would be able to crawl up the body cavity (the use of the word "crawl" is important because these sperm are amoeboid, meaning that they use protrusions of the cell body to push themselves forward, instead of "swimming" with a tail). Yet another possibility is that there could be some sort of short-circuiting of signals involving the prostaglandin mixture, a chemical cue that usually serves to attract sperm to the site of fertilization.

"hermaphrodites are especially vulnerable because they rarely mate."

But even after researchers figure this out, a number of questions will remain. For example, the scientists don’t know how widespread this phenomenon is, or what biological features make female reproductive organs more resistant to invasive sperm.

"We believe hermaphrodites are especially vulnerable because they rarely mate, and when they do it is generally with a single male," Haag said. This means that male competition is "more or less non-existent," he said, and over time their bodies and their sperm evolved to become more benign. That might have caused hermaphrodites to biologically "let their guard down" over evolutionary time. "This works fine as long as they only mate with their own males," Hagg said, "but clearly problems arise when they mate with males from outcrossing species."

And, of course, there's still the question of what the sperm are doing to kill C. briggsae hermaphrodites. "We imagine that to get out of the gonad, [the sperm] must puncture the membrane that surrounds it," Haag said. "This would cause leakage of material from one compartment to another, and this could directly hurt them." Another possibility, he said, is that the sperm damage delicate body structures outside of the gonad, like neurons. "We do see them all the way up in the head area, where most neurons are." But for now, Cutter said, "the biochemistry and genetic details controlling these mismatches are still a black box to us."