Clonally transmissible cancers are somatic cell lineages that are spread between individuals via the transfer of living cancer cells. There are only three known naturally occurring transmissible cancers, and these affect dogs, soft-shell clams, and Tasmanian devils, respectively. The Tasmanian devil transmissible facial cancer was first observed in 1996, and is threatening its host species with extinction. Until now, this disease has been consistently associated with a single aneuploid cancer cell lineage that we refer to as DFT1. Here we describe a second transmissible cancer, DFT2, in five devils located in southern Tasmania in 2014 and 2015. DFT2 causes facial tumors that are grossly indistinguishable but histologically distinct from those caused by DFT1. DFT2 bears no detectable cytogenetic similarity to DFT1 and carries a Y chromosome, which contrasts with the female origin of DFT1. DFT2 shows different alleles to both its hosts and DFT1 at microsatellite, structural variant, and major histocompatibility complex (MHC) loci, confirming that it is a second cancer that can be transmitted between devils as an allogeneic, MHC-discordant graft. These findings indicate that Tasmanian devils have spawned at least two distinct transmissible cancer lineages and suggest that transmissible cancers may arise more frequently in nature than previously considered. The discovery of DFT2 presents important challenges for the conservation of Tasmanian devils and raises the possibility that this species is particularly prone to the emergence of transmissible cancers. More generally, our findings highlight the potential for cancer cells to depart from their hosts and become dangerous transmissible pathogens.
Changes in life history are expected when new sources of extrinsic mortality impact on natural populations. We report a new disease, devil facial tumor disease, causing an abrupt transition from iteroparity toward single breeding in the largest extant carnivorous marsupial, the Tasmanian devil (Sarcophilus harrisii), in which males can weigh as much as 14 kg and females 9 kg. This change in life history is associated with almost complete mortality of individuals from this infectious cancer past their first year of adult life. Devils have shown their capacity to respond to this diseaseinduced increased adult mortality with a 16-fold increase in the proportion of individuals exhibiting precocious sexual maturity. These patterns are documented in five populations where there are data from before and after disease arrival and subsequent population impacts. To our knowledge, this is the first known case of infectious disease leading to increased early reproduction in a mammal. The persistence of both this disease and the associated life-history changes pose questions about longer-term evolutionary responses and conservation prospects for this iconic species.carnivorous marsupial ͉ infectious cancer ͉ wildlife disease ͉ precocious breeding ͉ semelparity
1. Monitoring the response of wild mammal populations to threatening processes is fundamental to effective conservation management. This is especially true for infectious diseases, which may have dynamic and therefore unpredictable interactions with their host. 2. We investigate the long-term impact of a transmissible cancer, devil facial tumour disease (DFTD), on the endemic Tasmanian devil. We analyse trends in devil spot-light counts and density across the area impacted by the disease. We investigate the demographic parameters which might be driving these trends, and use spatial capture-recapture models to examine whether DFTD has affected home range size. 3. We found that devils have declined by an average of 77% in areas affected by DFTD, and that there is a congruent trend of ongoing small decline in spotlight counts and density estimates. Despite this, devils have persisted to date within each of nine monitoring sites. One site is showing as yet unexplained small increases in density 8–10 years after the emergence of DFTD. 4. We also found the prevalence of DFTD has not abated despite large declines in density and that diseased sites continue to be dominated by young devils. The long-term impact of the disease has been partially offset by increased fecundity in the form of precocial breeding in 1-year-old females, and more pouch young per female in diseased sites. The lower densities resulting from DFTD did not affect home range size. 5. Synthesis and applications. Transmission of devil facial tumour disease continues despite large declines in devil density over multiple generations. Plasticity in life history traits has ameliorated the impact of devil facial tumour disease, however broad-scale trends in density show ongoing decline. In light of this, devil facial tumour disease and the impact of stochastic events on the reduced densities wrought by the disease, continue to threaten devils. In the absence of methods to manage disease in wild populations, we advocate managing the low population densities resulting from disease rather than disease per se.
BackgroundThe Tasmanian devil, the world’s largest carnivorous marsupial, is at risk of extinction due to devil facial tumour disease (DFTD), a fatal contagious cancer. The Save the Tasmanian Devil Program has established an insurance population, which currently holds over 600 devils in captive facilities across Australia. Microbes are known to play a crucial role in the health and well-being of humans and other animals, and increasing evidence suggests that changes in the microbiota can influence various aspects of host physiology and development. To improve our understanding of devils and facilitate management and conservation of the species, we characterised the microbiome of wild devils and investigated differences in the composition of microbial community between captive and wild individuals.ResultsA total of 1,223,550 bacterial 16S ribosomal RNA (rRNA) sequences were generated via Roche 454 sequencing from 56 samples, including 17 gut, 15 skin, 18 pouch and 6 oral samples. The devil’s gut microbiome was dominated by Firmicutes and showed a high Firmicutes-to-Bacteroidetes ratio, which appears to be a common feature of many carnivorous mammals. Metabolisms of carbohydrates, amino acids, energy, cofactors and vitamins, nucleotides and lipids were predicted as the most prominent metabolic pathways that the devil's gut flora contributed to. The microbiota inside the female’s pouch outside lactation was highly similar to that of the skin, both co-dominated by Firmicutes and Proteobacteria. The oral microbiome had similar proportions of Proteobacteria, Bacteroidetes, Firmicutes and Fusobacteria.ConclusionsCompositional differences were observed in all four types of microbiota between devils from captive and wild populations. Certain captive devils had significantly lower levels of gut bacterial diversity than wild individuals, and the two groups differed in the proportion of gut bacteria accounting for the metabolism of glycan, amino acids and cofactors and vitamins. Further studies are underway to investigate whether alterations in the microbiome of captive devils can have impacts on their ability to adapt and survive following re-introduction to the wild.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0143-0) contains supplementary material, which is available to authorized users.
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