By Marlene Cimons, National Science Foundation
Evolutionary biologist Ronald Fisher (1890-1962) predicted that most species would produce equal numbers of male and female offspring. He believed such reproductive behavior was a stable strategy of evolution, and his model became known as Fisher’s Principle.
But Fisher’s Principle turned out to be far too simplistic, and, in some cases, wrong.
Take the nematode, for example, more commonly known as the roundworm. Most species of nematodes do make equal numbers of male and female progeny. But certain species of roundworms defy Fisher’s Principle by producing dramatically small numbers of males, typically fewer than 5 percent. They also produce hermaphrodites, worms with female characteristics that can make both eggs and sperm and thus propagate all by themselves.
“I was curious about how this ability evolved to produce three different genders,’’ says André Pires da Silva, assistant professor of biology at the University of Texas at Arlington, of his interest in studying their complicated reproduction, specifically the reasons behind the roundworms’ mysteriously low number of male offspring. “Also, I wanted to know: what does it take for a hermaphrodite to produce sperm?"
Three years ago, da Silva, an evolutionary geneticist, contacted Diane Shakes, associate professor of biology at William & Mary and cell biology expert, and a new scientific collaboration was born.
“André and I bring very different strengths and experiences to the project,’’ Shakes says. “It’s so integrative. He asks the classic questions of evolution, for example, what kind of ecology do they live in that would foster this kind of reproductive mode? I understand how cells work, so I ask, how can you tweak the dynamics at the level of cell division? We know so little about the cellular mechanisms of how sex ratios change from 50/50 to something different. People have reported similarly unequal sex ratios in a wide variety of organisms, but haven’t gotten down to the cellular mechanisms. We’re getting pretty close."
Understanding the basic science behind their reproductive behavior, in particular how these species skew their gender ratios, could lead to new methods of roundworm population control. Ultimately, this could have an impact on pest management, as well as on new drug development for treating roundworm- related diseases, a problem in developing nations. New information about cell behavior also could provide new insights into the behavior of stem cells, and even cancer.
“This also could be applied to other species with a normal ratio population of genders," da Silva says. Shakes agrees. “Potentially, we could tinker even with the 50/50," she says.
The two scientists are studying roundworm behavior, specifically the species Rhabditis, under a three-year grant from the National Science Foundation. The combined grant totals nearly $443,000.
Another expert in nematode evolution, Marie-Anne Félix, currently at the Institut de Biologie de l’école Normale Supérieure (IBENS) in Paris, first reported the unusual gender ratios in the roundworm species Rhabditis in 2004. She discovered that mating between males and females yielded a very small number of male offspring, but couldn’t explain it. Shakes and da Silva decided to take a closer look.
In many species, males make two kinds of sperm, X and Y. An X sperm results in a female, while the Y brings a male. During the usual process of sperm production, early stage sperm cells divide twice to produce four sperm with the two X-bearing sperm contributing to the production of daughters and two Y-bearing sperm contributing to the production of sons. Nematode males represent a variation on this theme; producing X-bearing sperm that contribute to the production of daughters and non-X bearing sperm that contribute to the production of sons.
“Normally the mother cell divides twice to form four cells, all of which develop into sperm, ’’ da Silva explains. “In our worms, we found that, during the second division, the mother cell does not give the same stuff to the two daughter cells. Instead, the mother cell, just before it divides, puts all the things needed for sperm to become functional into just one cell – while the sister cell gets trash. It turns out that the X-bearing sperm gets all the good stuff while the non-X bearing sperm end up with cellular trash.’’
Hence, the disproportionately large number of females and small number of males.
“In this species, the X-bearing sperm receives all of the proteins that sperm need to be viable while the other sperm are duds,’’ Shakes says. “The cells that would produce sons fail to receive the goods. So, they can’t move, they can’t fertilize an egg, and are presumably discarded. These males produce only daughters, because the sperm that could have contributed to the production of sons is no good.”
In the context of evolution, this is not necessarily a bad thing, since the species also produces female-like worms that make both eggs and sperm and thus can propagate on their own, without help from males. The hermaphrodites “go through a dispersive stage where they go out and explore new territories,’’ Shakes says. “If they go exploring and find a new food source, hermaphrodites can start a new population all by themselves."
The researchers now are trying to figure out how the mother cell does it. “How is she able to separate stuff so you have one cell having trash, and one cell having the good stuff,’’ da Silva says. “If we could find the mechanism that controls this, we could find ways to have her put trash in both. That would mess up the male so it could no longer reproduce."
They also hope to decipher the story of the hermaphrodites and females, “and how the decision is made to produce a hermaphrodite,’’ he adds.
Their findings, published in the journal Nature Communications in January 2011, are significant because “similar examples of unequal cell divisions occur all the time during development in all kinds of organisms," da Silva says. “One mother cell dividing to become two different cells is very common.
“We don’t know yet exactly how this happens, but it has important implications for health, for example, in studying stem cells and, when something goes wrong in cell division, even cancer,’’ he adds. “We are working with a funny little worm that could answer some of the most fundamental questions in biology."
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