And now for something completely different—a worm with three sexes

January 18, 2018 by Joseph Mcclain, The College of William & Mary
And now for something completely different — a worm with three sexes
Diane Shakes is one of the authors on a paper examining the odd genetics of a nematode species, knowledge that has important human-health implications. Credit: Joseph McClain

Diane Shakes shakes her head. A trisexual arrangement is really not so different. Three sexes—male, female and hermaphrodite—are "part of the plan" for many organisms. There's even a word for it: trioecious.

And Shakes points out that hermaphroditism has a rich, varied and distinguished place in natural history.

"It's pretty common among invertebrates," she said. "What's not quite so common are self-fertile hermaphrodites. Think about earthworms: They're hermaphrodites, but it still takes two, because of the way the sex works, they're not self-fertile."

Other organisms display sequential hermaphroditism, she said. Oysters and other shellfish change from male to female as they age. "And in some organisms, when the 'leader of the pack' dies, another changes sex to be the new leader," she explained.

Shakes is a professor in William & Mary's Department of Biology. She and her collaborators have been examining Auanema rhodensis, a species of nematode that brings a completely different take to hermaphroditism. She is co-author on a paper in Current Biology that examines the genetics behind the worm's curious trisexual reproductive strategy.

"We're talking about three sexes, here," she explained. "There's males and females—and also hermaphrodites. Their bodies look like a female, but they make both eggs and sperm."

Like most animals, human reproduction relies on sex labeled X and Y. Human females are XX and males are XY. Males produce a 50:50 mix of X and Y sperm, and the winning sperm ultimately determines the sex of the children.

Shakes explained that consistent with Mendelian genetics, individual families may not have a 50:50 ratio of boys and girls—but the overall human population stays right at this mark. In A. rhodensis, both the females and hermaphrodites are XX, whereas the males have a single X and no Y. This species not only manages three sexes, but its inheritance patterns confound the predictions of Mendelian genetics.

"What we've figured out is that A. rhodensis has developed ways to stray from the genetics rulebook—specifically in regards to how it handles its X chromosome," she said.

Shakes is one of the authors of "Sex- and Gamete-Specific Patterns of X Chromosome Segregation in a Trioecious Nematode," published in the journal Current Biology.

In previous studies, Shakes and colleagues discovered that the sperm-producing cells in A. rhodensis males have hijacked a cellular program normally used to streamline sperm in order to produce exclusively X-bearing sperm. Thus, when males cross with females, they produce only female offspring.

"If that wasn't crazy enough, in this new study, we've found that the hermaphrodites are also manipulating the genetic dice," she said.

Shakes explained that standard genetic rules predict that XX hermaphrodites should produce 1X eggs and 1X sperm. They found that A. rhodensis hermaphrodites break these rules by producing sperm with two X chromosomes and eggs with none.

"We are still figuring how exactly they do this, but this setup yields pretty interesting genetics," she said.

Shakes explained that A. rhodensis is fully and truly a trisexual species. The hermaphrodites may be self-fertile, but they also are sexually versatile, happy to breed with males and females of the species.

"When hermaphrodites produce offspring through self-fertilization, they produce mostly XX females and XX hermaphrodites," she said. "However, when hermaphrodite cross with males, the joining of 1X male sperm with no-X eggs yields a jackpot of male offspring!"

The trisexual A. rhodensis is an interesting animal in its own right, but the scientists' exploration of oddities in nematode has important human-health implications.

"Chromosome segregation" refers to the tango of DNA strands in both meiosis (which produces egg and sperm cells) as well as mitosis (which produces new body cells). When the dance of chromosome segregation gets out of step, bad things can happen.

"Abnormalities in chromosome segregation, in most cases, cause an embryo to be spontaneously aborted in the first couple of weeks," Shakes explained. "The ones we hear about are the ones that survive to term. The most famous, of course, is Down's syndrome, where there's one extra copy of one tiny chromosome."

In addition to missteps in embryo development, Shakes points out that chromosome segregation errors raise their ugly heads in the development of many cancers.

"If you look at a cancer cell, there's going to be weird numbers of chromosomes. You will have broken and reattached chromosomes, those sort of things," she said. "When you go from a benign tumor into malignant cancer, it's really common to find defects in chromosome segregation."

Nematodes offer an excellent proxy for the study of human genetics. Both humans and the model nematode C. elegans have roughly the same number of genes, and many of these genes are functionally identical.

However, Shakes noted that the C. elegans genome is much more compact, with less DNA per cell. Nematodes have only six or seven chromosomes, whereas humans have 23. The relative compactness of the nematode genome led to C. elegans being the first multicellular organism to have its genome sequenced.

"It became the working model for the Human Genome Project," she said. "C. elegans has about 20,000 genes. Learning that was a sort of humbling experience because it's got about the same number of genes as a human."

But there is a difference in the two nematode species. C. elegans has two, not three, sexes—males and hermaphrodites. For A. rhodensis, having three sexes gives it additional reproductive tactics. In A. rhodensis, being a hermaphrodite with the ability to make both eggs and sperm is coupled with passage through a specialized, developmentally rugged larval stage.

"These hermaphrodites are the explorers," Shakes said. "They go find a new food patch and when they get there, they can reproduce all by themselves. During their rugged larval stage, they have features that help them resist environmental stressors, and they exhibit behaviors that maximize their dispersal."

The adaptive advantages of being a self-fertilizing hermaphrodite are obvious. There's none of that tedious mate-selection and courtship nonsense. If you're a hermaphrodite A. rhodensis all alone on a desert island, you won't be for long. And the DNA of the offspring is all pure you, of course.

But there is a price to pay for those advantages. Self-fertilizing hermaphrodites don't endow their offspring with the genetic diversity that come from male-female breeding and that benefits progeny in the long run.

Another disadvantage of their self-service sex life is that for hermaphrodites, passage through that rugged larval stage delays the onset of sexual maturity. Whereas males and females grow from embryo to sexual maturity in three to four days, the larval program of a adds a whole day to the nematode's maturation, Shakes explained.

"One day, in the context of three or four days, is significant," she said. "So if you make males and females, they're going to produce grandchildren for you faster."

Shakes says her hypothesis on the reproductive strategy of the three-sexed A. rhodensis can be summed up as canny evolutionary hedge-betting.

"I think of the species as a gambler," she said. "It's always placing bets on if life is going to get bad or if it's going to get good."

Those bets take the form of the mix of offspring sexes, Shakes explained: "The ultimate goal is to make as many great-grandchildren as possible."

A good life for a colony of nematodes is pretty basic. Shakes sums it up: "I've got plenty of bacteria to chew on and my progeny will have the same—but the environment could change very quickly."

When life is good, a male-female mix will pay off. When things begin to change for the worse, a worm will want to breed a lot of tough little hermaphrodites who will go out into the wider world to explore new food patches and start new colonies.

"The curious thing is that we don't actually know that much about what they are doing in the wild," she said. "There's not a lot of research on that, but there are a lot of features that suggests that in the wild, there are a lots of hermaphrodites."

A. rhodensis was found only twice in the wild, Shakes said. One was in Connecticut and another was in Appalachian Virginia. Both specimens were found associated with other animals, a dead tick and a beetle. She says the tough, exploring nematodes were probably interested in transportation.

"They're probably not infecting those beetles or ticks, but they'll actually sit there and flail in the air. They're trying to get picked up by an insect. They want to ride. they're only a millimeter long—they can only crawl so far," Shakes explained. "If they can get picked up by a beetle or a tick or something, they can move much further."

Explore further: Researchers document the biology behind a sex oddity

More information: Sophie Tandonnet et al. Sex- and Gamete-Specific Patterns of X Chromosome Segregation in a Trioecious Nematode, Current Biology (2017). DOI: 10.1016/j.cub.2017.11.037

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