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Out of Africa: The Origins
of the Tapeworms
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Adult specimen of the pork tapeworm,
Taenia solium, from the intestine
of a human.
(K9453-1)
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Tapeworms are among the most
disgusting but intriguing parasites of humans and other animals. They occur
worldwide, causing malnutrition, sickness, and occasionally the death of their
hosts. Yet, despite their economic significance, little has been known about
how and when these parasites first attacked humans.
Now, ARS zoologist Eric P. Hoberg, who
is in the Biosystematics Unit of the Parasite Biology, Epidemiology, and
Systematics Laboratory at Beltsville, Maryland, has made a remarkable
discovery—one that contradicts long-held theories. |
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Specimens and information databases of
the U.S. National Parasite Collection
are a unique and irreplaceable resource
for parasite biodiversity research.
Zoologist Eric Hoberg examines a specimen.
(K9429-1)
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"Traditionally, scientists
believed that about 10,000 years ago—coincidental with the domestication
of intermediate hosts such as cattle, swine, and companion carnivores like
dogs—three species of taeniid tapeworms became associated with
humans," Hoberg says.
But he and colleagues Alan de Queiroz and Nancy L. Alkire at the University of
Colorado-Boulder and Arlene Jones at The Natural History Museum in London have
uncovered new genealogical evidence that contradicts the traditional theory
that humans got these parasites from domesticated animals. Their work is based
on comparative morphology and DNA sequence analyses of parasites.
By studying the present-day ecology and geographic distribution of these
parasites and their hosts, the researchers have uncovered new information about
a long ancestry reflecting millions of years of host associations. |
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Hoberg examines a specimen of a Taenia
tapeworm from a North American lynx.
(K9432-2)
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Hoberg curates the U.S. National
Parasite Collection at Beltsville. It is one of the world's largest collections
of parasites of humans and animals—containing several million specimens.
One of his roles as curator is as a systematist—that is, discovering,
describing, and developing concepts for the evolution and biodiversity of
parasites.
"Pathogenic macroparasites, like tapeworms, have parasitized the world's
vertebrates and invertebrates for millions of years," says Hoberg.
"And although they remain a constant threat to economically important
fisheries, livestock, and wildlife, only about one-third have been described or
named.
"Our incomplete knowledge and understanding of taxonomy and species-level
relationships of these parasites has hindered our full understanding of their
host associations—final and intermediate—and their potential for
causing disease," says Hoberg. |
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Hoberg reviews phylogenetic trees with
information about carnivorous final hosts,
herbivorous intermediate hosts, and
geographic distribution.
(K9431-2)
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The disease caused by tapeworms is
known as cestodiasis. As a systematist, Hoberg carefully examines living
species of tapeworms and other parasites and describes them by meticulously
detailing their distinguishing characteristics—morphological, biochemical,
and molecular. (See "Searching for
Parasitic ‘Roots,’" Agricultural Research, December
1996, pp. 4-7.)
"Systematists deal with taxonomy, phylogeny—that is, recognizing
evolutionary relationships among species—and ultimately, classification,
in which organisms are grouped hierarchically based on their evolutionary
relationships," says Hoberg. "These classifications represent
everything we know about the relationships among these organisms.
"More importantly," he says, "these classifications help predict
species behavior. If we know which order, family, or genus a parasite is in, we
can predict—with some certainty—patterns of life history and what
effect it will have on hosts within the same or related families.
"Parasites have characteristic host and geographic distribution, as well
as predictable life cycles and transmission patterns," says Hoberg. He's
one of just a few U.S. systematic parasitologists who also examine where
parasites are distributed geographically and how they co-evolve with their
hosts.
Looking at Clues From the Past
Hoberg uses the vast U.S. National Parasite Collection and his expertise in
parasite systematics to examine evolutionary relationships between hosts and
parasites. This research, called cospeciation analysis, includes studies of
where hosts and parasites occur now and where they originated.
"The past is the key to the present," Hoberg says. "Historical
studies involving tapeworms contribute to a predictive foundation for
understanding today's environments and communities of living things. Besides
telling us something about their hosts, parasites can tell us about their
geographical links to long ago. They're both the products of a current
environment and, at the same time, of a long ancestry reflecting millions of
years of association with their hosts."
Hoberg's past research includes studies of the systematics and evolution of
tapeworms of seabirds, seals, and sea lions. This expertise has helped him to
examine tapeworm cospeciation and to perform biogeographic analysis—the
study of their geographic distribution.
Based on their analysis, Hoberg's team showed that 12 named genera of taeniid
tapeworms belong to 1 genus, Taenia. Recently, they completed the first
phylogenetic study of Taenia species based on analyses of morphological
characteristics of adult and larval parasites. Their study "provides
information that will enhance our ability to predict and understand the life
history and geographic distribution for this large genus," Hoberg says.
Basic Life Cycle of the Parasite
"Taenia tapeworms can range in size from about 0.04 inch to over 50
feet," says Hoberg. "They're internal parasites, infecting all types
of mammals—including humans and domestic animals. Their life cycles are
very complex. They require one intermediate host—always an
herbivore—and a final or definitive host—always a carnivore—in
which to reproduce." The final host is the host in which the adult
tapeworm lives.
Taeniid tapeworms have a global economic impact because of the sickness
and death they can cause in humans and the production losses in domestic stock,
including cattle and swine. Hoberg says, "Three species of these taeniid
worms—T. solium, T. saginata, and T. asiatica—infect
only humans. Their life cycles depend on domesticated cattle and swine as
intermediate hosts."
The pork tapeworm, T. solium—often found wherever raw or
undercooked pork is eaten—lives in the human intestine in its adult stage.
Each segment, or proglottid, may contain as many as 40,000 eggs.
"Like most tapeworms, T. solium are hermaphroditic. That means that
functional reproductive organs of both sexes occur in the same
individual," Hoberg says, "and they're often self-fertilizing."
If the embryos, which pass out with the host's feces, are then eaten by a pig,
the larvae emerge in the pig's digestive tract. They bore through the
intestinal wall into a blood vessel and are carried to muscle tissue where they
encyst, or form a protective capsule. The larval parasite that develops is then
called a cysticercus, or bladder worm.
"If the cysticercus is eaten alive in raw or undercooked meat or a
visceral organ like the liver, it attaches itself to the final host's intestine
and develops directly into a mature adult," Hoberg says. This completes
the T. solium life cycle.
"T. solium is unique in having a broad range of intermediate hosts
such as domestic and wild swine, dogs, and primates including humans. But only
humans serve as final hosts," Hoberg says.
The life cycle of the beef tapeworm, T. saginata, which occurs worldwide
where beef is eaten raw or improperly cooked, resembles that of the pork
tapeworm. With this species, cattle serve as the intermediate host, while
humans are the final host.
Humans Got Tapeworms First!
Hoberg and his colleagues have evidence—phylogenetic, geographic,
ecological, and molecular—indicating that, well over 10,000 years ago,
ancestors of modern humans, living on the savannas of Africa, became hosts for
Taenia.
"This occurred before the origin of modern humans and substantially
earlier than the domestication of swine and cattle and the development of
agriculture," he says. This conclusion was inferred from an examination of
evolutionary histories for hosts and parasites and from evidence for the rate
of molecular evolution between T. saginata and T. asiatica.
About 2 million years ago, Hoberg believes, African hominids (our early
ancestors), who scavenged for food or preyed on antelope and other bovids, were
exposed to colonization by these tapeworms. "The worms were using hyena
and large cats as definitive hosts and bovids as intermediate hosts."
Hoberg says that species of Taenia tapeworms are historical ecological
indicators of the foraging behavior and food habits of our early ancestors
during the diversification of Homo sapiens, or humans. "These
tapeworms tell a story about the ecological linkage between hominids and large
carnivores that shared prey on the savannas of Africa."
Hoberg says, "Surprisingly, rather than humans' acquiring Taenia
from cattle and pigs, we believe man gave tapeworms to these domestic animals,
because the association between Taenia and hominids was established
before the domestication of these food animals."
In fact, transmission from humans, he says, has occurred at least three times,
represented by T. saginata in cattle and T. asiatica and T.
solium in swine. "This means that the spread of T. solium among
humans may have been enhanced by cannibalism or by humans eating dogs."
Hoberg's team did DNA studies that gave more evidence for the idea that
prehumans acquired these tapeworms before cattle and swine were domesticated
about 10,000 years ago. When the team studied the DNA of these worms, they
estimated—based on a molecular clock—that divergence between the
human-parasitic sister species T. saginata and T. asiatica
occurred at least 160,000 years ago. "These sister species may have
diverged coincidental with the migration of early humans from Africa to
Asia," says Hoberg. "There, the worms continued to parasitize their
hosts, and an isolated group evolved to become T. asiatica."
Hoberg's team's research provides new information for understanding the
association between taeniid tapeworms and humans. It indicates that these
parasites' origins are not linked to the "recent" domestication of
food animals.
This discovery can also serve as collateral evidence for understanding the
ecological setting for human evolution that can now be applied to detailed
historical and anthropological studies.—By
Hank Becker,
Agricultural Research Service Information Staff.
This research is part of Animal Production, Product Value, and Safety, an
ARS National Program (#103) described on the World Wide Web at
http://www.nps.ars.usda.gov.
Eric P. Hoberg is in the
USDA-ARS Biosystematics and
National Parasite Collection Unit, 10300 Baltimore Ave., Bldg. 1180,
Beltsville, MD 20705-2350; phone (301) 504-8588, fax (301) 504-8979. |
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"Out of Africa: The Origins of the
Tapeworms" was published in the
May 2001
issue of Agricultural Research magazine.
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