The Worm’s Altruistic Suicide

Caenorhabditis elegans, a millimeter-long nematode or roundworm, has been poked and prodded, dissected and inspected. Every cell in its body has been mapped, the circuitry of its neurons traced, and its entire genome sequenced. For the past 50 years, it has been the experimental animal of choice, the subject of over 15,000 articles on everything from genetics to drug development. Biologically speaking, we know more about this animal than any other in the world—including ourselves.

But for all that we know about C. elegans, one aspect remains a mystery. In an abnormal birth process called matricide, the offspring eat and kill their mother. Researchers have shown that this unusual phenomenon may in fact be an evolutionary adaptation. By committing suicide for the sake of her young, the mother provides them the opportunity to become dauers, larvae that are incredibly stress-resistant.

The C. elegans‘ transparent body contains exactly 959 cells.
From J.E. Sulston and H.R. Horvitz, Dev. Biol. 56:110-156, 1977.

Sydney Brenner, a biologist at Oxford, first saw the nematode’s potential in the 1960’s. C. elegans, he realized, is the ideal multicellular organism to study in the lab—simple yet possessing the basic tissues common to all animals. Almost all C. elegans are hermaphrodites, essentially female bodies capable of producing and self-fertilizing with their own sperm. About four days after birth, the worm reaches maturity and self-breeds, laying up to three hundred eggs, which hatch outside its body. In a defective worm that is unable to form a vulva or opening necessary to expel the eggs from its body, the eggs hatch inside. As biologists Diana McCulloch and David Gems from the University College London described, “eggs eventually hatch within the uterus, and the emerging larvae devour the mother.”

Such a worm is often called a “bag of worms,” because under the microscope it looks like a bloated worm. (Watch the “bag of worms” in action here.) The eggs hatch inside and, with nowhere else to go, the offspring writhe frantically about and eat their mother’s insides until they pierce their way out of her body. Once they escape, many of the larvae who have inherited the genes involved in matricide will encounter the same fate as their mother.

In the underbelly of the worm, a special cell called the anchor cell signals three precursor cells to form the vulva in preparation for breeding. In a worm carrying the genetic mutation, however, the anchor cell breaks down in relaying its messages to the precursor cells. The worm is unable to form a vulva and is then fated to become a bag of worms.

While matricide has often been cast as a defect, emerging research has shed light on its evolutionary value. In 2003, Jianjun Chen and Edward P. Caswell-Chen, scientists in the department of nematology at the University of California, Davis, found that far from being a rare phenomenon of the laboratory, matricide occurs in nematodes living in the wild as well.

In the lab or the wild, severe stress can cause matricide, even in worms that do not carry the mutation. Starve a pregnant C. elegans, expose it to toxic substances, or transfer it from a solid to a liquid environment, and it is likely to develop into a bag of worms. In their experiment, the researchers starved batches of C. elegans and watched their response under the microscope for several hours. They found that when starved, the mother “sacrifices its body” to provide nutrition to its offspring. Interestingly, they also discovered that matricide is reversible: feeding a starving mother allows it to lay its eggs normally, assuming offspring that already hatched inside did not cause too much damage already.

Most importantly, the researchers found that in matricide, the mother provides her offspring with a mechanism for coping with stress through the dauer stage, a larval stage that is a kind of emergency survival mode. When the mother’s body has been consumed and food is still not available, the larva can enter developmental arrest, reducing its metabolism and increasing its capacity to withstand stress. Compared to the typical two- to three-week lifespan of C. elegans, dauer larvae can survive months without food. In particular, the researchers found that the longer they starved the mother, the fewer the offspring that survived (due to competition for resources), but a higher proportion of those survivors were able to reach the dauer stage.

Leaving behind even a single dauer is an evolutionary fitness advantage for C. elegans. By sacrificing herself, the mother is able to ensure that her young live on. In the survival of the fittest, dog eat dog does not always win the game. Sometimes, altruism goes a long way—even if it means being the one that gets eaten.