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Planet Earth

Fatal Cancer Threatens Tasmanian Devil Population

A voracious cancer threatens to wipe out an iconic Tasmanian species and destabilize the island's ecosystem. Can biologists trick the disease into taming itself?

Tas-opener

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Menna Jones peered into a trap, and a Tasmanian devil peered back at her. Its gaze was somehow off. The devil’s face seemed misshapen, and its jaw was raw and red. Perhaps, she thought, the swelling was an infected wound. Many devils are torn up by the end of the breeding season, after a month of winning and defending mates.

Jones, a biologist at the University of Tasmania, was trying to decipher the social structure of the island’s iconic creature, the largest meat-eating marsupial in existence. Were the devils promiscuous, as many researchers suspected? Which ones were studly and prolific, and which ones were losing the reproductive race? This fellow was one of many helping Jones answer those questions in June 2001 at her study site on the Freycinet Peninsula, a crooked finger of land in eastern Tasmania.

Jones reached for a canvas sack, tipped the cage gently and shook the black, beagle-size animal into the bag. Then she sat on the ground, legs wrapped around the bagged animal. Gripping him firmly, she pulled the bag back to measure his head. It was a dance she’d performed hundreds of times, moving smoothly and predictably so the devils knew what to expect.

Sometimes after she released a devil, it stayed in her lap and sniffed the sunscreen on her arm or buried its furry face in her armpit to hide from the sun. Although this devil was new to her — he was at the neck of the peninsula, which she visited only once a year — she often trapped the same devils dozens of times over the years, watching them grow from tiny imps in their mothers’ pouches to the grizzled old age of about 5.

When she pulled the bag back from this devil’s face, her soothing ritual faltered. A mass obliterated his right eye and erupted into an oozing, red-and-black cauliflower across his cheek. Another swelling deformed his left cheek into a deceptive chipmunk-chubbiness.

These facial growths were ominously familiar to Jones, though few others had ever seen one. Two years earlier, she’d observed strange tumors on a third of the devils she’d trapped 100 miles to the north. At the time, she thought perhaps they’d been exposed to some toxin.

Lacking a camera, she could take only measurements and descriptions to a wildlife veterinarian. He told her the only way he could figure out what ailed her devils would be if she were to euthanize one and bring it to him. “I was horrified at the thought that you’d euthanize a devil just to find out what it was sick with,” Jones told me, sitting in her office in the port town of Hobart. “Interesting to think back on that now that tens of thousands have died.”

Over the remainder of Jones’ 2001 trip to Freycinet, two more strapping 3-year-old males appeared in her traps with tumors on their faces. One of these tumors spread across the devil’s jaw and then dissolved, leaving a gaping hole. He could no longer eat. With no qualms about putting this doomed creature out of his misery, Jones brought him to a veterinary pathologist. Cancer, the veterinarian confirmed, but he wasn’t sure what kind.

Menna-Jones
Biologist Menna Jones of the University of Tasmania has led the charge to thwart the contagious cancer that threatens Tasmanian devils.University of Tasmania

The following January, Jones spotted tumors blooming on the faces of devils five miles farther down the peninsula — devils she’d known for years. When she returned in April 2002, the blight had marched still farther. By June, when she returned to the neck of Freycinet, she caught only 14 devils, rather than her usual 50. A third of them had tumors.

The disease was spreading. Somehow, it seemed, this cancer had evolved to become contagious.

Now, more than a decade later, the tumor is finally beginning to reveal its tricks. These devils are suffering from a malady so odd many researchers scarcely thought it possible: One devil’s cancer has learned how to survive in other devils’ bodies, and that one tumor is now threatening to wipe out an entire species. This would undermine the Tasmanian ecosystem and likely cause the extinction of many other marsupials that survive only in Tasmania, an island state off the southern coast of mainland Australia.

Fearing such a calamity, the Tasmanian government, working with a network of biologists, has begun quarantining healthy devils in zoos and on isolated islands. If the cancer kills off all other wild devils, this “insurance population” could, in theory, help reboot the species. (See “A Tasmanian Devil Insurance Policy” below.) Meanwhile, some of Jones’ colleagues are trying to decipher how the cancer evolved in hopes of using the information to create a vaccine. But Jones puts better odds on figuring out how to hack evolution itself, so the tumor can coexist with the devil.

The big question is whether researchers can do that before the disease wipes out wild Tasmanian devils altogether.

Unraveling the mystery will do more than save a few furry creatures at the bottom of the world. The tragedy has given researchers a backstage pass to see the evolution of cancer itself. No ordinary cancer can live as long or divide as many times as that of the “immortal devil,” the long-dead animal that spawned the current plague. All cancers are products of natural selection played out on the level of cells rather than species. So understanding the strange tricks that devil facial tumor disease, or DFTD, has evolved to ensure its survival should shed new light on cancer writ large.

Life Raft

Sick-Tas
An estimated 5,000 devils are infected with devil facial tumor disease, which typically causes death within six months of the appearance of a tumor.Menna Jones

Watching the Freycinet devil population crash in 2001 and 2002, Jones worried the survival of the species might be at risk. It seemed almost unimaginable. After all, devils were so common many considered them pests. Their nighttime screeches (frightening enough to have inspired the name the early Tasmanian settlers gave the small, shy creatures) startled people awake. Dead devils littered the roads, having fed on roadkill until meeting the same fate as their dinner. Farmers complained the devils ate their chickens and lambs. Most rural Tasmanians viewed devils like Americans tend to regard raccoons or squirrels: ubiquitous, occasionally annoying, worthy of little thought.

But the devils’ ubiquity was no guarantee of their survival. Biologists believe a new and virulent disease can eradicate even a well-established species if the pathogen continues spreading after the population becomes sparse. So in late 2002, Jones sounded the alarm to the state government.

Conducting a quick-and-dirty survey of devil populations, officials found that devils in the northeast, where Jones first saw the disease, were nearly wiped out. Of the few survivors, many were already infected. The disease seemed to spread during mating season, when female devils fight off suitors and males compete for females. Devils bite each other on the face as they scrabble, and malignant cells can crumble off tumors like feta cheese, dropping into bite wounds.

Over the next several years, Jones watched the populations at her study sites fall by 50 percent a year. She kept feeding the new data into mathematical models that factored in the animals’ age, migration patterns and disease prevalence in the population, among other things. The models’ predictions were bleak: Once the disease arrived in an area, devils there would vanish within 10 to 15 years.

Grim as the outlook was for the devils themselves, Jones’ deepest concern was that if the Tasmanian devil vanished from the wild, it could take a big chunk of Australia’s dwindling biodiversity with it.

Sick-Tas
Like the Tasmanian devil, the Tasmanian tiger, or thylacine (Thylacinus cynocephalus), survived in the wild only in Tasmania after being wiped out from mainland Australia. But by the 1930s, Tasmanian sheep farmers slaughtered thylacines to extinction in an effort to prevent them from preying on lambs. In a 2006 article contemplating the fate of the Tasmanian devils, Menna Jones riffed on Oscar Wilde: “To lose one large marsupial carnivore may be regarded as a misfortune; to lose both would look like carelessness.”Zoological Society of London

More mammals have gone extinct from Australia than from any other continent. Nineteen mammal species have disappeared over the past 200 years, and more than a hundred more are threatened or endangered. Tasmania is Australia’s one exception. Since it was settled in 1803, the island has lost only one mammal, the Tasmanian tiger (or thylacine) — a wolfish, striped, carnivorous marsupial. And the island state serves as a life raft: Four Australian species survive only here, having been completely or nearly wiped out from the mainland. Tasmania also offers a safe haven for nine more species that are threatened on the mainland. Many of these creatures’ names sound as if they’ve leapt from children’s fables: the eastern barred bandicoot, the Tasmanian pademelon, the eastern quoll, the long-nosed potoroo, the eastern bettong.

The devil, which went extinct on the mainland about 5,000 years ago, is one of these Tasmanian survivors. And it is the thumb in the dam, preventing many other creatures from being swept from the Tasmanian landscape into extinction. Devils suppress feral cats and foxes (repeatedly and illegally introduced to the island) by preying on their young and competing for habitat and resources. If populations of cats and foxes were to spread, as they did long ago on the mainland, they would slash a hole in the marsupials’ life raft. “It’s just like taking wolves out of Yellowstone,” Jones says. “Losing the top predator sends the ecosystem out of balance.”

The Spread of a Killer Cancer

Since its first recorded sighting in 1996, devil facial tumor disease (DFTD) has maintained a steady westward march in Tasmania, depleting devil populations by as much as 90 percent in some areas.

DSC-Devils-Map
Kellie Jaeger/Discover

Cancer as a Parasite

Jones’ warning spurred the Tasmanian government to action, leading to the 2003 formation of the Save the Tasmanian Devil (STTD) program, with Jones as an adviser. The program’s goals were to suss out the threat and find a way to address it.

News reports about the devils’ plight sprang up around the globe. Anne-Maree Pearse, a retired cancer researcher living in Launceston, Tasmania, heard a radio story about the disease and called the Save the Tasmanian Devil program offering to help.

Pearse was uniquely qualified: Decades earlier, she began her scientific career studying the genetic makeup of a species of flea that had a special taste for the Tasmanian devil. Then she applied her expertise to humans, studying chromosomal rearrangements in leukemia cells. As a result, Pearse was perhaps the only person in the world with expertise in both cancer and devils — and, though the relevance was not yet apparent, in parasites as well.

The STTD program jumped at Pearse’s offer and gave her devil cancer cells to analyze. When Pearse put the first one under her microscope, she found that, as is common in cancer, its chromosomes were mangled: One pair of chromosomes was missing entirely, one lacked a partner, one was chomped off, and some leftover bits were jammed together into extra chromosomes.

When she looked at a cancer cell from another devil, she saw the same pattern — chromosomes that had shattered and reformed in precisely the same way. The third, too. The chromosomes from all 11 devils she studied had the same deletions and the same extra bits put together in the same exact way.

The similarity could mean only one thing: These cells were clones of one another. Later, a different group found that the sex chromosomes in the jammed-together leftovers were always of the XX variety — female — regardless of the devil host’s gender. That confirmed the cancer cells weren’t mutations from the sickened devil, the way cancer ordinarily works. They had come from another devil entirely, a female undoubtedly dead for years. Her cells, though, lived on. The cancer cell line had become an organism that survived by sucking nutrients from other devils’ bodies. It was, in other words, a parasite.

Chromosomes
A healthy male devil has 14 chromosomes, including an XY (male) chromosome (top). All the diseased devils Anne-Maree Pearse first studied had the same pattern of missing and mangled chromosomes; other researchers found they also all had XX (female) genetic material (bottom). A.M. Pearse and K. Swift/Adapted by permission from Macmillan Publishers Ltd. Nature 439, 549 (2 February 2006)

A healthy male devil has 14 chromosomes, including an XY (male) chromosome (top). All the diseased devils Anne-Maree Pearse first studied had the same pattern of missing and mangled chromosomes; other researchers found they also all had XX (female) genetic material (bottom).A.M. Pearse and K. Swift/Adapted by permission from Macmillan Publishers Ltd. Nature 439, 549 (2 February 2006)

News of Pearse’s discovery quickly spread to the Australian mainland, where it reached University of Sydney immunologist Kathy Belov. Belov had just earned her Ph.D. showing that marsupial immune systems were vigorous, much like humans’. So it seemed shocking that devil immune systems would fail to recognize and stomp out something as obviously foreign as another devil’s cancer cells.

She wouldn’t have been so surprised if the cancer were spread by a virus, since viruses (such as the papillomavirus, which turns human cervical cells cancerous) have had millions of years to evolve ways of evading the immune system. But Pearse had shown that no virus was involved; the cancer cells had transferred directly from one animal to the next. So why hadn’t the devils’ cytotoxic (or “killer”) T cells, their immune systems’ designated cancer assassins, detected the invasion?

One plausible explanation was that over the course of successive population crashes, the devils had become so inbred that their cells look identical — at least to the animals’ immune systems. Belov knew how to check this. An animal’s immune system detects foreign cells by scanning for proteins, called antigens, that stick out from the surface of each cell. These molecular identity cards are produced by a set of genes collectively known as the major histocompatibility complex, or MHC. That’s why identical twins make perfect organ donors for each other: Only they have perfectly matched MHC genes.

Perhaps, Belov reasoned, all devils were like identical twins. If so, then different devils’ perfectly matched “identity cards” would prevent their killer T cells from recognizing each other’s tissues as foreign.

Fellow Island Survivors

Like the devil, the eastern quoll (left), Tasmanian pademelon (center) and Tasmanian bettong (right) have all gone extinct from mainland Australia. They exist only in Tasmania, where the devil helps protect them from feral cats and foxes.

Island-survivors
Left to right: Dave Watts/naturepl.com (2); Peter Oxford/naturepl.com

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