Why Madagascar's Tapeworms Matter–To You

tapewormEverything is connected. And when I say everything, I include you, dear reader, and the tapeworms of Madagascar. They carry a hidden history of our entire species.

I’m sure we’d all prefer that there was no such connection. Tapeworm are not just gross, but they are pretty much the polar opposite of the human existence. They have no brain. They have no eyes. They lack mouths and guts, having turned their body inside out, absorbing food through its surface. Most of their hideously long body is made up of segments, each of which contains its own supply of both eggs and sperm. To reproduce, the tapeworm fertilizes its eggs, either with its own sperm or another tapeworm’s, and then sheds its segments. Once out of the body, those segments can crawl around on the ground on their own.

But, like it or not, tapeworms–or at least the pork tapeworm Taenia solium–has an intimate relationship with us. After all, it can only live in our guts as an adult, where it will dwell for years and grow over 20 feet long. Without us, these tapeworms would simply not exist. From the safety of our guts, they can shed six egg-loaded segments a day, each of which contains 50,000 eggs. If a pig swallows one of these eggs, it hatches in the animal’s instestines, drills its way into the abdominal cavity, and finds a muscle to infect. There it dwells in a barely visible cyst, for years if need be. In order to complete its life cycle, it must get into another human, which it does if a human eats a piece of infected, undercooked pork.

Carrying an adult tapeworm around in your gut may be disturbing, but it’s not the worst thing a tapeworm can do to you. Sometimes people get infected with the eggs of pork tapeworms, rather than the cysts. Instead of developing into an adult, the tapeworm treats you like a pig. It invades your muscles, where it makes a cyst. Sometimes the tapeworms can get into people’s brains. These cysts can trigger dangerous reactions from our immune systems, and can sometimes be fatal. This disease, known as cysticercosis, is relatively rare in the United States. Only 221 people died of it between 1990 and 2002. But in other parts of the world, it’s a lot worse, with ten percent or so of the population of many countries showing signs of having had the disease.

Madagascar is one of those countries. In the highlands, over 20% of people have antibodies to cysticercosis. To get a better handle on the epidemiology of the disease, medical researchers at the Pasteur Institute of Madagascar have traveled around the country, gathering tapeworm from different regions. They isolated DNA from 13 of the samples and then compared their genetic sequences to see how they were related to one another, and to tapeworms from other parts of the world.

The family tree of tapeworms they got was strangely ancient and alien. In many cases, the closest relatives of tapeworms on Madagascar are not other tapeworms on Madagascar. The tapeworms that live in the southwest part of the island are closely related to tapeworms hundreds of miles away, in Africa. The tapeworms in other parts of the island are more closely related to tapeworms thousands of miles away, in south Asia.

The scientists then tallied up the mutations in each lineage of tapeworm to figure out how long ago they had split off from a common ancestor. All the T. solium tapeworms the scientists studied descend from a common ancestor that lived about 680,000 years ago. The southwest Madagascar tapeworms and the tapeworms of Africa share a common ancestor that lived 235,000 years ago. All of the Madagascar and Asian tapeworms share a common ancestor that lived about 260,000 years ago. The Madagascar tapeworms and their very closest Asian relatives share an ancestor that lived 85,000 years ago.

So how on Earth did one remote island end up with two such deeply split lineages of tapeworms in their pigs? The answer is like a guided tour thorugh the evolution of our species, rolling right on through the history of civilization.

Along with pork tapeworms, there are two other species of Taenia that live in humans. One, T. asiatica, also cycles between people and pigs, but only in Asia as the name suggests. The other, T. saginata, moves between people and cows. Both of these human tapeworms use domesticated hoofed mammals (known as ungulates) as their intermediate hosts. Pigs and cows were only domesticated within the past 11,000 years or so. The best way to find clues to how these tapeworms colonized us is to compare them to the 39 species of Taenia tapeworms that infect wild animals. Eric Hoberg, a parasitologist at the U.S. Department of Agriculture, and his colleagues have found that most Taenia tapeworms form cysts in wild ungulates, such as antelopes, and then become adults in the carnivores that eat their intermediate hosts. The closest relatives of all three human tapeworms live in Africa. Hyenas are the hosts of the closest relatives of pork tapeworms, while lions are the hosts of the closest relative to the other two species, T. saginata and T. asiatica. Hoberg and his colleagues compared the mutations in the DNA of T. saginata and T. asiatica and found that their common ancestor lived somewhere between 780,000 and 1.71 million years ago.

The new results from Madagascar fit in nicely with Hoberg’s results. Hundreds of thousands of years ago, our ancestors lived in Africa, where they scavenged meat from ungulates. In so doing, it appears, they stepped into the life cycle of Taenia tapeworms. Tapeworms that might have ended up in the gut of a hyena or a lion ended up in the gut of our ancestors instead. Over thousands of years, some populations of these tapeworms adapted to our scavenger ancestors. These were the common ancestors of today’s human tapeworms, whose great antiquity is now recorded in the DNA of living tapeworms.

As hominins expanded their ranges both within Africa and beyond it, they carried their tapeworms along for the ride. As hominins scavenged new game, the tapeworms adapted to new intermediate hosts. Hominins gradually developed the skills and weapons to hunt game, offering still more opportunities for their tapeworms. Neanderthals and other hominins hunted wild boar as well, and it’s likely that we infected them with the ancestors of today’s pork tapeworms.

Starting about 11,000 years ago, humans domesticated pigs many times over, both in East Asia and in the Near East. Now the trip from host to host became riduclously easy for the tapeworms. Instead of waiting for its wild boar host getting speared by a hunter, it could make the journey on the dinner plate. Judging from the deep split in the evolution of pork tapeworms, the parasites must have made two separate shifts from wild boar to domesticated pigs, in both East Asia and the Near East.

The genealogy of the tapeworms also matches up nicely with the human history of Madagascar. People only arrived on the island 2000 years ago. They came from two directions. Bantu farmers sailed from the west from Africa across the Mozambique channel. Asians came from the east, traveling thousands of miles across the Indian Ocean from Indonesia. Malagasy culture emerged from the mingling of these two origins. That culture also includes the livestock that the Bantu and Indonesians brought to the island. And those animals brought parasites with them that had been separated for almost 700,000 years, reaching back to a time when our ancestors had yet to invent fire or spoken language.

[Image: Chiang Mai University]

10 thoughts on “Why Madagascar's Tapeworms Matter–To You

  1. Great article!

    Am I a Luddite if I hate the word “hominins”?

    (Also: You might fix “riduclously” in the next to last graf, and then delete this part of this comment.)

  2. Should the last sentence actually say “… when our ancestors had YET to invent fire or spoken language.”?

  3. This is the first time I’ve heard the claim that the Bantu settled Madagascar, as well as Asians. How solid is that information? From genetic studies, perhaps?

    I had understood that Madagascar was settled in the past 1500-2000 years or so from what is now Indonesian Borneo. The Malagasy language of the island is most closely related to the language of the Barito area in southern Borneo. This is part of the most widespread (pre-modern) language group in the world, the Austronesian group, stretching from Madagascar to Easter Island.

  4. In reply to zackoz, you are correct that the Malagasy language is an austronesian language, particularly closely related to languages spoken in present-day Borneo. However, genetic evidence of contemporary Malagasy people shows that they are roughly half-African and half-Asian. There are other clues that point to their dual origin in Asia and Africa — the prevalence of cultural customs with ties to both areas, as well as a fair about of Bantu-derived words in the Malagasy language.

    From my understanding, most would claim that the people who arrived in Madagascar starting around 2000 years ago were probably a combination of the two BEFORE arrival, rather than arriving in two distinct waves as this article suggests. In other words, some folks from the Indonesia area traveled westward along the coast, past India, to Eastern Africa, and their mixed descendants then headed east to Madagascar. But it is really hard to say how Madagascar was settled, given the lack of archaeological evidence.

    Fascinating article nevertheless! Thanks!

  5. Thanks Laura, I had not heard of that twist to the story, esp the genetic side of it. In pre-modern times, trade routes certainly existed between modern Indonesia and India, and then down the African coast. That may make more sense than an Austronesian voyage straight across the Indian Ocean. Despite the ethnic mixture, I think it is true to say that the dominant strain is Austronesian?

    As an Indonesian speaker, I have Madagascar on my list of places to visit, but unfortunately the list is a theoretical if-only-I-could one!

  6. I’ve read that some of the African settlers didn’t come there voluntarily, but as slaves. Re Laura’s idea that the mixing happened beforehand arrival, that’s probably true in part, but there are differences in appearance and I believe gene expression in different parts of the island that suggest the mixing was not complete.

    My question – how does the tapeworm history fit with the bottleneck theory for human populations? If humans went through a bottleneck of very small populations, especially for an extended period as has been suggested by some, like Sarah Hrdy, it seems unlikely that the LCA for tapeworms would be hundreds of thousands of years earlier.

  7. To add to the discussion of the colonisation of Madagascar –

    I had understood that the Asian people arrived first, and the Africans joined them about 1000 years later. I think there is archaeological evidence supporting this. The Africans introduced cattle, which the Asians did not have. I had also assumed that the Asians got there more or less directly by boat, but I have never understood how they managed it.

    1. Here’s a 2005 paper on the topic you can read for free:

      “The Dual Origin of the Malagasy in Island Southeast Asia and East Africa: Evidence from Maternal and Paternal Lineages”

      Linguistic and archaeological evidence about the origins of the Malagasy, the indigenous peoples of Madagascar, points to mixed African and Indonesian ancestry. By contrast, genetic evidence about the origins of the Malagasy has hitherto remained partial and imprecise. We defined 26 Y-chromosomal lineages by typing 44 Y-chromosomal polymorphisms in 362 males from four different ethnic groups from Madagascar and 10 potential ancestral populations in Island Southeast Asia and the Pacific. We also compared mitochondrial sequence diversity in the Malagasy with a manually curated database of 19,371 hypervariable segment I sequences, incorporating both published and unpublished data. We could attribute every maternal and paternal lineage found in the Malagasy to a likely geographic origin. Here, we demonstrate approximately equal African and Indonesian contributions to both paternal and maternal Malagasy lineages. The most likely origin of the Asia-derived paternal lineages found in the Malagasy is Borneo. This agrees strikingly with the linguistic evidence that the languages spoken around the Barito River in southern Borneo are the closest extant relatives of Malagasy languages. As a result of their equally balanced admixed ancestry, the Malagasy may represent an ideal population in which to identify loci underlying complex traits of both anthropological and medical interest.

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