Getting a head in the world: when the naidid worm reproduces, it grows a new front for its back half and a new tail for its front

Natural History, Oct, 2002 by Alexandra Bely, Gregory Wray

We peer down at the tiny worm wriggling under the lens of our microscope. Four black eyes peer up at us: two from the creature's head and two from its ... other head. Two-headed worms are common in our lab, and they're common outside the lab as well. If you've ever scratched the surface of a slimy rock in a pond or stream, you may even have taken one of these miniature beasts home with you, tucked away under your fingernail.

The bizarre worms we study are called naidids. They are members of the phylum Annelida, the group that includes segmented worms such as leeches, tube worms, and the familiar earthworm. Although naidids are widespread and abundant in ponds, streams, marshes, and other freshwater pools, we know relatively little about them, in part because of their size. Most are tiny; members of the largest species grow to about the size of a toothbrush bristle. A naidid's body is nearly transparent, allowing easy viewing of its inner workings: its bilobed brain, its pulsating blood vessels, its muscles and stomach, and even its lunch are plainly visible to anyone who cares to look. Also hard to miss, of course, are its two heads, complete with two pairs of eyes, two mouths, and two brains. One head is just where you would expect it, at the front end of the animal. The second head is right in the middle of its body.

Two-headed naidids are not abnormal mutants; rather, they are average worms that happen to be in the process of reproducing by a method known as paratomic fission (or paratomy). Growing a second head in the center of its body is a naidid's first step in propagating itself. Just in front of this head, new tail segments develop. The worm eventually splits into two complete animals (hence the term "fission"), one with the old head and a new tail, the other with the old tail and a new head. But why stop at two heads? Many naidids develop five or more at once, ultimately breaking up into an equivalent number of worms. This curious mode of reproduction has arisen in several groups of annelids. How such an unusual reproductive method may have evolved has been the subject of our research for several years.

Annelids are certainly not the only members of the animal kingdom with unconventional reproductive habits. Take Hydra, a genus of freshwater invertebrates that commonly inhabit lakes and ponds. With one end of its body attached to a rock or to submerged vegetation, a Hydra waves its tentacles in search of tiny aquatic prey, which it captures and stuffs into its mouth, located at the center of its ring of tentacles. To reproduce, a Hydra typically forms a bud that grows from the side of its body. The bud develops its own mouth and set of feeding tentacles but shares a gut, and hence its food, with its parent. Like a naidid, a Hydra eventually splits into two or more complete individuals that go their separate ways.

Sea anemones such as the pink-tipped surf anemone, which is common along the Pacific coast of North America, have a particularly dramatic mode of reproduction. Opposite ends of the anemone slowly crawl away from each other, creating a tug-of-war that ultimately causes the animal to tear itself in two. Each half then regenerates the part that was lost, making the behavior an efficient, if peculiar, way of procreating.

And the list continues--sea stars that split in half, marine ribbon worms that break up into dozens of small pieces, sponges that fragment. All these creatures propagate by all asexual method known as agametic reproduction: offspring are produced by a single parent, and no gametes (eggs or sperm) are involved in the process. Although certainly not common, this kind of reproduction has evolved numerous times and in disparate kinds of invertebrates.

With the ability to reproduce agametically, the would-be parent has no need to find a mate. Even a single naidid worm that makes its way to a new environment has the potential to quickly populate the entire body of water it inhabits. A well-fed naidid can reproduce every two or three days. Assuming that the average worm reproduces every three days, in just three months it could in theory be the proud progenitor of more than a billion offspring! Viewed another way, if that average one-centimeter worm did not split after consecutive rounds of fission, after three months it would be more than 6,000 miles long--roughly the distance from San Francisco to Paris. Given that reproduction is the currency of evolutionary success, naidids are clearly doing something right. But how does an animal become capable of reproducing this way? New molecular tools have made it possible to study the genes involved in this unorthodox manner of generating offspring.

The worm we have been studying is a delicate little naidid called Pristina leidyi. Rearing this species has proved to be surprisingly easy and inexpensive. Like most naidids, Pristina are detritivores that ingest fine sediments and scrape diatoms and algae from rocks and aquatic plants. In the laboratory, we housed worms in glass bowls filled with spring water and added a few paper towel pieces as a substrate for them to crawl on. For food, the worms were content with a century-old lab recipe (originally developed for growing organisms such as Paramecium) that consists of boiled hay and wheat grains. In this simple microcosm the worms flourished.