Build Me A Tapeworm

i-23e06f2250a4ce34cdc3ad046827568d-shark tapeworm.jpgDarwin gave a lot of thought to the strangest creatures on this planet, wondering how they had evolved from less strange ancestors. Whales today might be fish-like warm-blooded beasts with blowholes and flukes, but long ago, Darwin argued, their ancestors were ordinary mammals that walked on land with legs. His suggestion was greeted with shock and disbelief; neverthless, scientists have found bones from ancient walking whales. Humans, Darwin argued, evolved from apes, most likely in Africa where chimpanzees and gorillas are found today. And today scientists have found about twenty different species of hominids, from chimp-like creatures that lived six million years ago to not-quite humans that lived alongside our own species. Darwin also pondered the origins of barnacles, orchids, and many other strange creatures. But for some reason--perhaps thanks to his famously weak stomach--Darwin didn't write a single word about tapeworms. It's a pity, because tapeworms are as strange as animals can get...

These flat, ribbon-like creatures live inside the digestive tracts of vertebrates. The tapeworms that live in humans can get up to sixty feet long. They feed on our food, despite the fact that they have neither a mouth nor a digestive tract. Their bodies are like a kind of inside-out intestine, rippling with finger-like projections that absorb nutrients. Once inside us, tapeworms can live for decades, deftly escaping the notice of the immune system despite their being as long as an anaconda. Some tapeworms have hooks or suckers on their front end ("head" is too generous a term), which they use to anchor themselves in place. They can also swim upstream to meet food coming out of the stomach and drift back down the intestines to feed, releasing chemicals to slow down their host's peristalsis so that they don't get swept away.

Most of a tapeworm's body is taken up with the equipment for making more tapeworms. Except for its anchoring front end, it is made up of repeating segments, each loaded with male and female sex organs. While the mating habits of tapeworms are a profound mystery, it's clear that these segments can each produce millions of fertilized eggs. Those eggs have to leave their host to continue the life cycle of the tapeworm; they do so when the segments at the back end of the tapeworm break off and get passed out of the body. The eggs can then be taken up by pigs or cows, where they develop into cysts in their muscle. Eat cyst-infected meat, and you get a tapeworm in your gut. Despite the legends of tapeworm-induced anorexia, most people have no symptoms if they are host to an adult tapeworm. Get a tapeworm egg in you, and you're in for a totally different experience. The tapeworm may wander through your body and end up in a strange place like your brain, where it grows like a tumor.

We humans are host to 54 species of tapeworms. That's actually only a tiny fraction of the full diversity of tapeworms, which now stands at about six thousand species. Some live in mammals, others in birds, reptiles, amphibians, and fish. Most tapeworms have elaborate life cycles that take them through an invertebrate, such as a beetle or a crustacean, before passing into a vertebrate. Some travel through three species or more. And along the way, they can manipulate their hosts to ease their path through life. The rat tapeworm develops first in beetles, which they make easier targets for rats. Infected beetles lose the ability to make the toxic chemicals that keep rats at bay, and the beetles become slow to flee from danger. A tapeworm known as Schistocephalus solidus does much the same thing, but underwater. It first infects invertebrates called copepods, which it causes to swim around more, making them easier prey for stickleback fish. Once in the stickleback fish, the tapeworm develops further, getting so big that the fish's belly swells. Once the tapeworm is ready to move to host number three, the sticklebacks turn bright white and swim boldly, becoming easier prey for water birds. The birds then become hosts to the tapeworms and shed their eggs with their droppings.

Tapeworms are so unlike other animals, so exquisitely adapted to their own way of life, that it can be hard to imagine how they were anything other than tapeworms. In fact, as I described here, the life cycle of tapeworms was discovered by a particularly devout nineteenth-century parasitologist who wanted to demonstrate that God made nothing in vain. As I write in my book Parasite Rex, the evolution of parasites poses a challenge to scientists because they generally don't leave behind fossils. But they do carry DNA, which scientists can compare to that of other animals. Scientists have been studying the molecular evidence of tapeworm origins for a little over a decade, and a rough picture is emerging. The work is slow, in part because many species of tapeworms and their relatives have yet to be discovered, and scientists have yet to make a careful study of many of the species they have found.

The newest analysis of tapeworms and their relatives has now been published in the journal BMC Evolutionary Biology. It's the work of Tim Littlewood of the Natural History Museum in London and colleagues in South Korea. The take-home message of the paper is actually a picture, which I've reprinted at the bottom of this post. It's the evolutionary tree of tapeworms and their relatives that emerges from the DNA of these animals. If you follow the tree from its base to the tapeworm branch at the top ("Cestoda"), you are taking the path the ancestors of tapeworms apparently took from free-living animals to superb parasites.

The ancestors of tapeworms were free-living flatworms (platyhelminths). Many flatworms live in the ocean or in fresh water. The transition to parasitism was, not surprisingly, gradual. A group of flatworms called monogeneans are among the closest relatives of tapeworms, and instead of living inside their hosts, they mostly live on the outside. Monogeneans use suckers and hooks to clamp onto a fish. Some grab the gills, other the eyes, others the scales. They then use their mouths to feed on the mucus or blood of their hosts. It appears the monogeneans move from fish to fish, each species of parasite living on a single species of fish host. (Here's a digression but a good one: some monogeneans give birth to offspring without releasing them from their bodies. Their offspring mature inside them and give birth as well. Like a hideous Russian doll, a monogenean may contain twenty generations of descendents inside its body! ["Kids, it's time you found a place of your own..."])

While monogeneans are close kin to tapeworms, they are not the closest. That dubious honor goes to another group of parasitic flatworms, known as trematodes. They're commonly called flukes. Many flukes are shaped like leaves, with flat, oval bodies. Like monogeneans, they have powerful suckers for moving around and grasping their hosts, as well as a muscular mouth and throat for feeding.

But instead of living on their hosts, flukes live in them. Blood flukes (schistosomes) live in the blood vessels behind the intestines or bladder of humans. Other flukes set up house in the liver, brain, and other organs of various animals. Another difference between monogenans and flukes are their hosts. Monogeneans have one; flukes generally have two or more. Blood flukes insert their eggs into the human bladder or intestines. Once they reach the outer world, the eggs can infect snails, where they develop into missile shaped forms that then seek out new human flesh. The magnificently grotesque lancet fluke also lives in snails, only to be coughed up by their hosts and then devoured by ants. The ants later crawl up blades of grass, where they are eaten by grazing mammals.

This tree indicates that flukes and tapeworms descend from a flatworm that moved from the outside of its hosts to their inside. This happened a long time ago, judging from the fact that monogeneans, flukes, and tapeworms are found on all sorts of vertebrates except for the oldest lineages represented today by the jawless lampreys and hagfish. When jawed fish first emerged about 450 million years ago, flatworms began their invasion. This ancestral tapefluke may have only needed one host species to complete its life cycle, but afterwards the tapeworms and flukes began to add other species. The tapeworms added arthropods (such as copepods and insects) while the flukes added mollusks such as snails.

It's possible that the earliest tapeworms were a lot like flukes. Only after they branched off did they lose the sucker found on flukes and monogeneans, for example. Only then did their skin turn into a way to eat. A few clues to the early stages of tapeworm evolution can be gleaned from the oldest lineages of living tapeworms. These tapeworms don't have repeating segments with male and female organs. Instead, the tapeworms have a single compartment in their body with the sex organs jumbled up inside it. Only after those tapeworms branched off did the sex organs begin to get organized into groups. And only after they were organized into groups, did they get divided into segments.

These "true tapeworms" (known as eucestodes) are the most successful of the group. They've thrived by taking advantage of their evolving hosts. They moved ashore with our relatives and infected many species of land vertebrates. Dinosaurs probably had tapeworms too, and we can only wonder how long they got. When whales and other vertebrates returned to the water, they took tapeworms with them. In the evolutionary trees of tapeworms, scientists can see the collisions of continents, the openings of oceans. Tapeworms shuffled between host species as well. Our own ancestors may have acquired the most common human tapeworm (Taenia solium) from the carcasses that hominids scavenged with stone tools a million years ago.

This tree is different in some important ways from previous versions, which isn't surprising since it is based on more data. Littlewood and other researchers will be testing it with still more data--other species, other genes. And while this tree offers a series of steps from free-living flatworm to gut-dwelling tapeworm, many steps in between remain to be documented. Of course, that's the case with any evolutionary transition, whether it's whales moving to sea or hominids becoming human. In this case, perhaps some of those steps will be filled in with the discovery of new species of tapeworms and their relatives. Perhaps down in some unexplored chasm in the deep sea there's some fish swimming around with a parasite that's not quite tapeworm, not quite fluke: a living piece of history.

i-18e00812d0f0dd19b6e53e9d0f7c79ac-tapeworm tree.jpg

Top image courtesy of Darlyne Murawski


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Parasites have proved so clever (-- you know what I mean --) that they make Hannibal Lecter look unimaginative and, frankly, dull as dishwater.

The Human [and many other animals] may even display remnants of evolution from Porifera.

The Gastrointestinal tract could be a series of multifunctional, direct links to Porifera if sphincters evolved from the holdfast.
See bottom, left of Figure 2: The calcareous syconoid sponge, Scypha . Porifera58L.gif

Fascinating creatures - and just thinking about them makes me queasy. 8P I had trouble watching "House" last week.

Give me a king cobra to milk, a saltwater crocodile to handle or even a free ride on the back of a hammershark but an egg of a tapeworm? Hell no!

By Marlene S. J. (not verified) on 19 Feb 2007 #permalink

That's actually only a tiny fraction of the full diversity of tapeworms, which now stands at about six thousand species.

If memory serves, there are somewhat fewer than six thousand species of mammals presently alive. Just for proportion ...

Kind of makes you regret missing your annual full body MRI.

By Michael B (not verified) on 20 Feb 2007 #permalink

Nice one - I always thought we had the Protestants to thank for these 'orrible creatures, but no longer will I curse Martin Luther and his Diet of Worms.

Hat's off to you, Doug - it's so seldom I find anyone who makes even worse puns than I do.

Curse you, Zimmer, for scrolling this past me just after I'd eaten dinner (raw pig brains). However, what intrigues me most is not the exciting lives of parasites, interesting though these are, but the cladogram. Cestodes, Trematodes and Turbellaria are a natural group snuck next to Lophotrochozoan outgroups ... does this mean that 'higher' flatworms are now Lophotrochozoa, and that the lowest (and cuddliest) flatworms, the acoels, have at last been Hurled Headlong, to coin a phrase, from the Aetheral Sky? Fascinating. Pass the sweetbreads.

By Henry Gee (not verified) on 21 Feb 2007 #permalink

Henry: Let your intestinal parasites finish up dinner, and then get thee to the paper. There's some fairly high-level discussion of acoels etc. in there.

Thank you Jud - it was no mere fluke, you know.

Thanks Carl, I shall. Or I would, were I not so darned hungry. And an aside which I just know I shall regret. When I stumble across hellfire evangelism my mind cheekily adopts the lisp of a child and whispers "Jesus Wants Me For A Tapeworm". There, the triumph of Evolution over Creation in just six words. So help me.

By Henry Gee (not verified) on 22 Feb 2007 #permalink

Interesting facts about tapeworms. Thank you for bringing such information to light.

One question springs to mind, reading that, though: could tapeworms return to being external parasites, or even free-swimming animals? Or have they specialized to such a degree that they can't (easily) move to other niches?

Just curious.

have nice days.

Anthony [13]--There's no evidence I know of of tapeworms evolving into free-living forms. Hard to imagine them doing so, but it's never good to rely on one's own sense of incredulity when it comes to biology.

I agree with Carl. Evloutionary change of parasitic life style back to free-living mode does not seem to be highly likely, once it was successfully established in their life cycle. There is one paper I recommend to read about this issue.
Siddal, M. Brooks, M.E., Desser, S.S. (1993). Phylogeny and the reversibility of parasitism. Evolution, 47(1):308-313.

Thanks, Dr. Park. (FYI, Dr. Park is one of the authors of the tapeworm paper that was the seed of this post.)

The funniest, most disgusting, horrifying tale of a tapeworm experience. Follow link at your own risk. It takes guts...

By Doug Jones (not verified) on 23 Feb 2008 #permalink

Some species of tapeworm secrete a molecule that is phosphorylated by the human TGF-beta type I receptor. TGF-beta activates foxp3 in human T cells which has been suspected in the transformation to regulatory T cells (Tregs). Cannot help but speculate that is how some tapeworms evades the host immune system. And since the lack of Tregs is suspected in a handful of human diseases, one wonders if the lack of tapeworms could be partially responsible for some of those diseases.

The murine model of chemically induced colitis is reversed by inoculation with a murine tapeworm. This mechanism is block by neutralizing IL-10. Tregs secrete lots of Il-10.

There are several phase II trials testing hookworm and pig whipworm for the treatment of human colitis, asthma and multiple sclerosis. Doubt anyone will ever conduct a tapeworm trial. Seems there is no getting over the "ick" factor with this one...

Poor Dr. Fujita.