This Worm Can Express Three Sexes Simultaneously

It might look simple, but a nematode species’ chromosomal gymnastics could shine a light for humans, too.

Sinclair Stammers/Science Photo Library

Hermaphrodites are a wild concept for most people to understand, but for scientists, they’re sort of passé. Case in point: nematodes, who have had us beat for millions of years. In a new paper published in Current Biology, Diane Shakes, a biologist at the University of William & Mary, and her colleagues describe a species of nematode that has three sexes—male, female, and hermaphrodite—and how they’ve managed to hack into a unique mechanism of reproductive biology that’s unlike anything scientists have ever seen before.

Many animal species utilize hermaphroditism as a way to enable sexual reproduction more widely across the species and make all individuals potential partners. Some hermaphrodites are actually self-fertilizing, and confer what Shakes likes to call a “boom in a bust” situation. “If things are really bad,” she told The Daily Beast, “a single worm can go off and find a new food source, and establish a whole new population.”

In nematode species, hermaphrodites are certainly not new. “The model nematode that everyone has been studying since the middle of the ’70s, Caenorhabditis elegans, has hermaphrodites and males,” said Shakes.

But trisex species found in nature are extremely rare. In 2004, a researcher named Marie-Anne Felix published a paper outlining a free-living nematode called SB347 (later named Auanema rhodensis) that produced not one, not two, but three sexes: males, females, and hermaphrodites. The females only produce eggs and can only reproduce by mating with males, while hermaphrodites produce eggs and sperm, and are capable of mating with males or self-fertilizing their own eggs with their own sperm. The males only produce sperm and are capable of mating with both other sexes.

How exactly this “trioecious” species operated, however, was a mystery. Shakes and her colleagues have been trying to investigate this among other questions, and the result was entirely unexpected.

“The actual paper, to tell you the truth, is more of a ‘gee-whiz, genetics!’ paper,” Shakes said. “We’re breaking the laws of Gregor Mendel and our fundamental assumptions of how genetics is supposed to work.” Mendelian genetics generally dictates that a sexually-reproducing species will be a roughly even split of males and females. In humans, this is determined by the fact that females possess two X chromosomes (XX), and males are XY. Sex cells work by contributing a chromosome each upon fertilization, so all eggs produced by females carry a single X, while male sperm are generated with a 50:50 mix of X or Y. As a result, each pregnancy has an equal chance of being male or female, and so the population as a whole skews to an even gender ratio.

A. rhodensis upends these rules not just by having three sexes, but by using only one sex chromosome (X) to determine that sex. Unlike in humans, these nematodes don’t have a Y sex chromosome. Females and hermaphrodites are XX, while males are single X.

Even with just X chromosomes to play around with, classical genetics would presume half the nematode sperm (in males and hermaphrodites) would have an X chromosome and half would not. It would also presume all female and hermaphrodite eggs have one X chromosome. Mating in any sense would produce half XX progeny (females and hermaphrodites) and half X progeny (males). But previous studies show that A. rhodensis males only produce single X sperm. So when males breed with females, they only produce female offspring.

That already warps things, but this new paper takes things to a more absurd level: Shakes and her team found that, while the females are making single X eggs, most hermaphrodites eggs have no X chromosomes, and almost all the sperm are XX. Thus, the hermaphrodites, when they self-fertilize, produce mostly XX offspring (females and hermaphrodites), although still a few males. When they breed with males, the result is mostly male (single X) offspring.

To tell you the truth, it’s more of a ‘gee-whiz, genetics!’ paper. We’re breaking the laws of Gregor Mendel and our fundamental assumptions of how genetics is supposed to work.
Diane Shakes

“This was a huge surprise,” said Shakes. “We really didn’t expect this.” But it actually makes sense from an evolutionary standpoint. Cross-mating is more ideal because it produces more genetic diversity, but self-fertilization gives the species an opportunity to venture off as individuals and sire offspring elsewhere. Hermaphrodites, Shakes explained, are “explorers” able to seek new food patches and survive tougher conditions.

In addition, shirking the skew towards 50:50 male:female representation is also advantageous. A population in any species actually grows faster with fewer males mating with more females, so a distribution like this with three different sexes actually helps ensure there are more egg-producing members and less sperm-producing ones. Ultimately, three sexes gives A. rhodensis a remarkable ability to adapt to changing conditions and funnel resources to population growth more efficiently than other species.

But what determines whether XX progeny will be female or hermaphrodite? Shakes’ co-author, Andre Pires-da Silva from the University of Warwick in the U.K., has found that larval exposure to a particular pheromone (and another undetermined factor controlled by the mother) can affect what sex the nematode grows up to be.

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This is quite a far ways away from the standard XX and XY distribution we see in humans, although there is a bit of shared experience between nematodes and the human species. Chromosomal abnormalities in humans sometimes results in an individual possessing an irregular number of sex chromosomes. Triple X syndrome (also known as trisomy) is when a female individual has three X chromosomes; symptoms include learning difficulties, decreased muscle tone, and some issues with the kidneys. Klinefelter syndrome in males is the result of an XXY distribution, and primarily results in sterility and small testicles, with other less pronounced symptoms sometimes manifesting. Turner syndrome occurs in females with only one X chromosome, and confers a shorter and webbed neck, shorter stature, and swollen hands and feet.

The main difference, obviously, is that irregular sex chromosome segregation is a purposeful, evolutionary-advantageous phenomena in nematodes. “This species is manipulating the X in a way that’s actually helpful for the worm, and it’s doing so with accuracy and precision,” Shakes said. That’s certainly not the case in humans, although modern medicine has certainly made great strides into making those afflicted by genetic disorders live easier, more normal lives.

That doesn’t mean we can’t apply what we learn from A. rhodensis to human genetics. “This is a very extreme system of chromosomal segregation,” she said. “If you’re an examining an extreme segregation, you can start to learn why it is that only the X chromosome behaves in a certain way as opposed to other chromosomes. If you start to understand how and why this happening, that could apply to what’s going on in abnormal situations in humans where the chromosomes aren’t separating properly.”

Another biomedical benefit goes back to dealing with parasitic nematode species, some which affect humans, and many which are devastating to agricultural plants grown by farmers. “One question we have is whether this extreme trisexual mechanism is happening out in the wild,” Shakes pointed out. Understanding those dynamics in depth means we could learn something about how to better combat those pest species and develop interventions that could keep people and crops safer. Rather than, say, genetically engineering a nematode-resistant crop, we could develop a poison that targets nematode reproductive mechanisms directly, with its male, female, or hermaphrodite.

Those implications, however, won’t augur into something practical until much later on. For now, Shakes and her colleagues still have a ton of outstanding questions they’d like to answer. She’s excited they finally have evidence that this crazy reproductive behavior is really happening, but she and her team also want to know more about the molecular factors that allow for this occur, as well as determine whether related species are exhibiting the same or similar mechanisms in their own biology.