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Randy Rotifers: Environmental Variation Prompts More Sex

Asexual reproduction is efficient and reliable in many small organisms, so why will some suddenly decide to mate? A rare lab experiment sheds light on the forces that drive the switch to sex
rotifers engage in more sex in varried environments



KUIPER/BECKS

Sex can be a costly endeavor—biologically, that is. Combining genetic material can of course bring beneficial new combinations, but even for tiny organisms that are barely visible to the naked eye, mating is fraught with all kinds of hazards, such as a long wait for offspring, sexually transmitted diseases, and the risk of getting eaten during or after sex. So why, if many of these bitty beasts can produce asexually, do some of them do it anyway?

Evolutionary theory has suggested that the nature of the environment might have something to do with the mode of reproduction. And a rare experiment has demonstrated that the idea holds true in a lab setting.

A team of researchers found that they could make one breed of rotifers (Brachionus calyciflorus)—microscopic or near-microscopic "pseudocoelomate" animals that can reproduce both sexually and asexually—more prone to sexual reproduction just by culturing the organisms in environments with different levels of food quality. The results are published in the October 14 issue of Nature. (Scientific American is part of Nature Publishing Group.)

"There are so many different theories about how sex evolved," says Lutz Becks, a postdoctoral researcher in evolutionary ecology at the University of Toronto and lead author of the study. "But almost none of those theories have been tested." The newly described experiments are a step toward uncovering "one of the enduring problems of evolutionary biology," the emergence of a practice that about 99.9 percent of known animals engage in at least sometimes, the researchers noted in their paper.

The implications of the work will likely bear fruit far beyond the rotifer world. "I think it's a really fantastic advance," says Sally Otto, a professor of evolutionary biology at the University of British Columbia, noting that there have been few experiments—and perhaps none in multicellular organisms—that document dynamics behind the emergence of sex. The study "provides good evidence that spatial complexity can favor sex" and a "gold mine of opportunity" to track down the molecular mechanisms that lead these organisms away from an asexual life, she notes.

Feast or famine
In a homogeneous lab environment this species of rotifer tends to go asexual. In the wild, however, B. calyciflorus engage in quite a bit more sex. What gives? One prevailing theory holds that in a more heterogeneous environment—as one would expect in nature—the advantages of sex would outweigh its costs.

To test this idea, researchers collected rotifers from the wild and split them into separate cell cultures of approximately 10,000 animals per population. One set of populations had a consistent exposure to only high-quality food, a second set only to low-quality food. Other populations were alternated each week between high- and low-quality food environments.

After 15 weeks (with about one new generation per day), the researchers found that rotifers in the homogeneous environments were better adapted to their respective food environments (than they were to the alternative environment), and about seven percent of these rotifers' eggs were created via sexual reproduction. The rotifers that had been transferred between the two food-quality environments, however, were reproducing sexually at more than double the rate (some 15 percent). The results "indicate that sex evolves differently in heterogeneous versus homogeneous environments," noted the researchers in their paper.

"I was surprised how rapidly the frequency of sex rose" in heterogeneous environments, Otto says. "It suggests that there's a really strong advantage, a strong force acting on the frequency of sex."

Risky business
With a perfectly homogeneous environment and stable population numbers, "there would almost certainly be no need for sex," noted Otto on a 2009 paper published in The American Naturalist.

In a dynamic world, however, sex seems to have won out. "It's easy to think that sex is beneficial, because with sex you shuffle your genes," Becks says. But despite the overall odds of optimal gene combinations winning out over time, for an individual rotifer—or generation of rotifers—the chances of a successful individual coming out ahead genetically are scant.

If a set of genes has worked well for a long line of asexually reproducing animals in a stable environment, the logic would say, why fix what is unbroken? After all, "you don't know what kinds of genes you get—you might get bad genes from your mate," thereby diluting your successful stock in your offspring," Becks explains.

Nevertheless, the experiment demonstrated that sex succeeded in "mixing and matching the best of the migrant alleles and the resident alleles," Otto explains. In a more heterogeneous environment some genes will be better for one type of habitat (high-quality food) and other genes will give the animals a little leg up in the second habitat (low-quality food), thus upping the appeal of swapping some genes via sex.

Another possible explanation for the shift to sex, which Otto notes is considerably "less interesting," is that it is simply an egg preservation strategy. When they reproduce sexually, this breed of rotifers produces so-called resting eggs, which can survive in a harsher environment than eggs generated asexually.

In that scenario, Otto explains, some rotifers would go, "Holy smokes, we're not very fit in this environment. Let's produce a resting egg to outlive this environment," in hopes that the surroundings will change back to one that better suits their genes by the time the egg hatches. Future research could help establish the true drivers behind the higher levels of sex.

A new model for sex

Sex likely did not emerge simply because of shifting levels of food quality, and many additional theories await experimentation. "There are other theories that we can test with these rotifers," Becks notes, hinting that there may be more sex studies in the works.

Otto, who works with yeast, was excited to see that these rotifers look to be a promising new model system that other researchers can now examine at the molecular level to study what prompts—and what is selected for in—sexual reproduction. "Even at the genetic level, we don't know if it's due to interaction of different genes or interactions of the same genes," that drives sex, she says. "It's going to be really super cool to dissect this."

The B. calyciflorus are also closely related to another group of rotifers that only produce asexually, providing scientists with a useful comparison to study slight differences that might allow for sex, Otto notes.

Becks hopes to test other organisms that have a capacity for both sexual and asexual reproduction to see if environmental cues could also spur more sex—in hopes of getting to the bottom of how these chancy encounters evolved in the first place.

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