How an infectious tumor in Tasmanian demons evolved as it spread

Communicable cancer in the Tasmanian devil has evolved over the past two decades, with some lineages spreading and replacing others, according to a new study published in the open access journal PLOS Biology by Young Mi Kwon, Kevin Gori and Elizabeth Murchison of the University of Cambridge (UK) and their colleagues. The evolutionary dynamics of cancer help explain how this Australian marsupial became endangered so quickly and may inform the evolution of other forms of cancer.

The Tasmanian Devil is a carnivorous marsupial, the size of a small dog, found only in Tasmania, an island state off the southern coast of eastern Australia. Devil’s facial tumor 1 (DFT1) was first observed in the mid-1990s and has since spread to demons across much of the island, passed from animal to animal through bite, a current social behavior. Remarkably, the tumor cells transferred in this way, rather than being eliminated by the immune system of the new host, survive and establish a new tumor. The infection is usually fatal.

To better understand the spread of the disease, the authors analyzed the genomes of 648 DFT1 tumors collected between 2003 and 2018. They found that when the tumor began to spread, DFT1 split into five clades, or sub-lineages. Two of them became extinct, while three continued to spread. One, clade A, broke up again. The authors mapped the distribution of each clade, which revealed how diseased demons spread cancer in the environment; their findings support those of epidemiological research and emphasize the importance of geography in influencing the movements of demons and their disease.

The effects of human attempts to prevent the spread were also reflected in the data – a pilot program to eliminate infected animals was likely responsible for a series of sublineage replacements in an isolated region. The authors also identified several types of genomic instability in the DFT1 genome, including the duplication and loss of genes and the gain or loss of whole chromosomes; they further described the frequency of duplication of the whole genome leading to tetraploid tumors. Nonetheless, the degree of genomic diversity within the devil’s tumor population was low compared to that often found even in a single human tumor, the authors noted.

Largely due to the spread of DFT1, and now exacerbated by the emergence of a second communicable cancer, DFT2, the Tasmanian devil population has plummeted and the species is now endangered. “The results of this study may be useful for epidemiological modeling and prediction of the benefits of management interventions,” Murchison said.