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Transmissible cancer in Tasmanian devils: localized lineage replacement and host population response
Rodrigo K. Hamede Anne-Maree Pearse Kate Swift Leon A. Barmuta Elizabeth P. Murchison Menna E. Jones 《Proceedings. Biological sciences / The Royal Society》2015,282(1814)
Tasmanian devil facial tumour disease (DFTD) is a clonally transmissible cancer threatening the Tasmanian devil (Sarcophilus harrisii) with extinction. Live cancer cells are the infectious agent, transmitted to new hosts when individuals bite each other. Over the 18 years since DFTD was first observed, distinct genetic and karyotypic sublineages have evolved. In this longitudinal study, we investigate the associations between tumour karyotype, epidemic patterns and host demographic response to the disease. Reduced host population effects and low DFTD infection rates were associated with high prevalence of tetraploid tumours. Subsequent replacement by a diploid variant of DFTD coincided with a rapid increase in disease prevalence, population decline and reduced mean age of the population. Our results suggest a role for tumour genetics in DFTD transmission dynamics and epidemic outcome. Future research, for this and other highly pathogenic emerging infectious diseases, should focus on understanding the evolution of host and pathogen genotypes, their effects on susceptibility and tolerance to infection, and their implications for designing novel genetic management strategies. This study provides evidence for a rapid localized lineage replacement occurring within a transmissible cancer epidemic and highlights the possibility that distinct DFTD genetic lineages may harbour traits that influence pathogen fitness. 相似文献
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David G. Hamilton Menna E. Jones Elissa Z. Cameron Douglas H. Kerlin Hamish McCallum Andrew Storfer Paul A. Hohenlohe Rodrigo K. Hamede 《Proceedings. Biological sciences / The Royal Society》2020,287(1940)
Infectious diseases, including transmissible cancers, can have a broad range of impacts on host behaviour, particularly in the latter stages of disease progression. However, the difficulty of early diagnoses makes the study of behavioural influences of disease in wild animals a challenging task. Tasmanian devils (Sarcophilus harrisii) are affected by a transmissible cancer, devil facial tumour disease (DFTD), in which tumours are externally visible as they progress. Using telemetry and mark–recapture datasets, we quantify the impacts of cancer progression on the behaviour of wild devils by assessing how interaction patterns within the social network of a population change with increasing tumour load. The progression of DFTD negatively influences devils'' likelihood of interaction within their network. Infected devils were more active within their network late in the mating season, a pattern with repercussions for DFTD transmission. Our study provides a rare opportunity to quantify and understand the behavioural feedbacks of disease in wildlife and how they may affect transmission and population dynamics in general. 相似文献
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Olivia Bell Menna E. Jones Calum X. Cunningham Manuel RuizAravena David G. Hamilton Sebastien Comte Rodrigo K. Hamede Stuart Bearhop Robbie A. McDonald 《Ecology and evolution》2021,11(12):8038
Devil facial tumor disease (DFTD) is a transmissible cancer affecting Tasmanian devils Sarcophilus harrisii. The disease has caused severe population declines and is associated with demographic and behavioral changes, including earlier breeding, younger age structures, and reduced dispersal and social interactions. Devils are generally solitary, but social encounters are commonplace when feeding upon large carcasses. DFTD tumors can disfigure the jaw and mouth and so diseased individuals might alter their diets to enable ingestion of alternative foods, to avoid conspecific interactions, or to reduce competition. Using stable isotope analysis (δ13C and δ15N) of whiskers, we tested whether DFTD progression, measured as tumor volume, affected the isotope ratios and isotopic niches of 94 infected Tasmanian devils from six sites in Tasmania, comprising four eucalypt plantations, an area of smallholdings and a national park. Then, using tissue from 10 devils sampled before and after detection of tumors and 8 devils where no tumors were detected, we examined whether mean and standard deviation of δ13C and δ15N of the same individuals changed between healthy and diseased states. δ13C and δ15N values were generally not related to tumor volume in infected devils, though at one site, Freycinet National Park, δ15N values increased significantly as tumor volume increased. Infection with DFTD was not associated with significant changes in the mean or standard deviation of δ13C and δ15N values in individual devils sampled before and after detection of tumors. Our analysis suggests that devils tend to maintain their isotopic niche in the face of DFTD infection and progression, except where ecological conditions facilitate a shift in diets and feeding behaviors, demonstrating that ecological context, alongside disease severity, can modulate the behavioral responses of Tasmanian devils to DFTD. 相似文献
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Belov K 《BioEssays : news and reviews in molecular, cellular and developmental biology》2012,34(4):285-292
Cancer is generally defined as uncontrollable growth of cells caused by genetic aberrations and/or environmental factors. Yet contagious cancers also occur. The recent emergence of a contagious cancer in Tasmanian devils has reignited interest in transmissible cancers. Two naturally occurring transmissible cancers are known: devil facial tumour disease and canine transmissible venereal tumour. Both cancers evolved once and have then been transmitted from one individual to another as clonal cell lines. The dog cancer is ancient; having evolved more than 6,000 years ago, while the devil disease was first seen in 1996. In this review I will compare and contrast the two diseases focusing on the life histories of the clonal cell lines, their evolutionary trajectories and the mechanisms by which they have achieved immune tolerance. A greater understanding of these contagious cancers will provide unique insights into the role of the immune system in shaping tumour evolution and may uncover novel approaches for treating human cancer. 相似文献
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Abstract Devil facial tumour disease (DFTD), is an emerging infectious cancer thought to be spread by biting. It is causing ongoing, severe population decline of the Tasmanian devil (Sarcophilus harrisii), the largest surviving marsupial carnivore and there are concerns that DFTD may lead to extinction of the devil. Whether extinction is likely depends on contact rates and their relationship to host density. We investigated contact rates using two different datasets. The first consisted of field observations of contact and biting behaviour around prey carcasses and, the second was a 3‐year longitudinal series of injuries in a marked devil population. During feeding interactions at carcasses, contact rates were significantly positively associated with population density and subadults delivered more bites than adult males and females. Injuries from the marked devil population did not differ between adult males and females. In two of the three years, penetrating biting (resulting in injury) increased markedly during the mating season and was more frequent in adults than in subadults. Among injured devils with wounds penetrating the dermal layer, adults were more frequently bitten in the head (the location of primary tumours) in the mating season than in other seasons, and had more head bites than subadults. Our results suggest that the mating season may be the key period for disease transmission. If most penetrating bites occur during mating interactions, DFTD transmission is likely to be frequency dependent, which means that there would be no threshold host density for disease persistence, and disease‐induced extinction is possible. 相似文献
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1. We investigated the impact of a recently emerged disease, Devil Facial Tumour Disease (DFTD), on the survival and population growth rate of a population of Tasmanian devils, Sarcophilus harrisii, on the Freycinet Peninsula in eastern Tasmania. 2. Cormack-Jolly-Seber and multistate mark-recapture models were employed to investigate the impact of DFTD on age- and sex-specific apparent survival and transition rates. Disease impact on population growth rate was investigated using reverse-time mark-recapture models. 3. The arrival of DFTD triggered an immediate and steady decline in apparent survival rates of adults and subadults, the rate of which was predicted well by the increase in disease prevalence in the population over time. 4. Transitions from healthy to diseased state increased with disease prevalence suggesting that the force of infection in the population is increasing and that the epidemic is not subsiding. 5. The arrival of DFTD coincided with a marked, ongoing decline in the population growth rate of the previously stable population, which to date has not been offset by population compensatory responses. 相似文献
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Menna E. Jones Peter J. Jarman Caroline M. Lees Heather Hesterman Rodrigo K. Hamede Nick J. Mooney Dydee Mann Chrissy E. Pukk Jemma Bergfeld Hamish McCallum 《EcoHealth》2007,4(3):326-337
An emerging infectious facial cancer threatens Tasmanian devils with extinction. The disease is likely to occur across the
range of the devil within 5 years. This urgent time frame requires management options that can be implemented immediately:
the establishment of insurance populations, in captivity, wild-living on islands, and aiming for eradication in areas that
can be isolated. The long-term options of the spontaneous or assisted evolution of resistance or development of a field-deliverable
vaccine are unlikely to be available in time. The disease’s characteristic allograft transmission through intimate contact
simplifies isolation of insurance populations and breaking transmission in suppression trials. Better knowledge of contact
matrices in wild devils will help focus timing and demographic targets of removals. A metapopulation approach is needed that
integrates captive and wild-living island and peninsula (disease suppression) populations to minimize the loss of genetic
diversity over 50 years until either extinction and reintroduction can occur, resistance evolves or a field-deliverable vaccine
is developed. Given the importance of the insurance populations and the low genetic diversity of devils, a conservative target
for retention of 95% genetic diversity is recommended. Encouraging preliminary results of the first disease-suppression trial
on a large peninsula show fewer late stage tumors and no apparent population decline. Limiting geographic spread or suppressing
the disease on a broadscale are both unlikely to be feasible. Since the synergy of devil decline and impending fox establishment
could have devastating consequences for Tasmanian wildlife, it is crucial to manage the dynamics of new and old predator species
together. 相似文献
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The structure of the contact network between individuals has a profound effect on the transmission of infectious disease. Using a novel technology – proximity sensing radio collars – we described the contact network in a population of Tasmanian devils. This largest surviving marsupial carnivore is threatened by a novel infectious cancer. All devils were connected in a single giant component, which would permit disease to spread throughout the network from any single infected individual. Unlike the contact networks for many human diseases, the degree distribution was not highly aggregated. Nevertheless, the empirically derived networks differed from random networks. Contact networks differed between the mating and non-mating seasons, with more extended male–female associations in the mating season and a greater frequency of female–female associations outside the mating season. Our results suggest that there is limited potential to control the disease by targeting highly connected age or sex classes. 相似文献
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Tracey Hollings Hamish McCallum Kaely Kreger Nick Mooney Menna Jones 《Proceedings. Biological sciences / The Royal Society》2015,282(1810)
Apex predators structure ecosystems through lethal and non-lethal interactions with prey, and their global decline is causing loss of ecological function. Behavioural changes of prey are some of the most rapid responses to predator decline and may act as an early indicator of cascading effects. The Tasmanian devil (Sarcophilus harrisii), an apex predator, is undergoing progressive and extensive population decline, of more than 90% in long-diseased areas, caused by a novel disease. Time since local disease outbreak correlates with devil population declines and thus predation risk. We used hair traps and giving-up densities (GUDs) in food patches to test whether a major prey species of devils, the arboreal common brushtail possum (Trichosurus vulpecula), is responsive to the changing risk of predation when they forage on the ground. Possums spend more time on the ground, discover food patches faster and forage more to a lower GUD with increasing years since disease outbreak and greater devil population decline. Loss of top–down effects of devils with respect to predation risk was evident at 90% devil population decline, with possum behaviour indistinguishable from a devil-free island. Alternative predators may help to maintain risk-sensitive anti-predator behaviours in possums while devil populations remain low. 相似文献
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The Tasmanian devil (Sarcophilus laniarius), a medium‐sized predator/scavenger, is the largest member of the short‐lived carnivorous marsupial Family Dasyuridae. Now restricted to Tasmania, populations are impacted by habitat clearance and anthropogenic mortality and genetic studies could be of value in informing levels of genetic diversity, mating system, dispersal and the effects of natural and anthropogenic landscape features on gene flow. Microsatellite markers were isolated from a partial, size‐selected genomic library that was enriched for microsatellite sequences. Primer pairs were developed for 11 polymorphic dinucleotide microsatellite loci that conform with Hardy–Weinberg equilibrium and reveal moderate genetic variability across the species range. 相似文献
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Hamish McCallum Daniel M. Tompkins Menna Jones Shelly Lachish Steve Marvanek Billie Lazenby Greg Hocking Jason Wiersma Clare E. Hawkins 《EcoHealth》2007,4(3):318-325
The Tasmanian devil, Sarcophilus harrisii, is the largest extant marsupial carnivore. In 1996, a debilitating facial tumor was reported. It is now clear that this
is an invariably lethal infectious cancer. The disease has now spread across the majority of the range of the species and
is likely to occur across the entire range within 5 to 10 years. The disease has lead to continuing declines of up to 90%
and virtual disappearance of older age classes. Mark-recapture analysis and a preliminary epidemiological model developed
for the population with the best longitudinal data both project local extinction in that area over a timeframe of 10 to 15
years from disease emergence. However, the prediction of extinction from the model is sensitive to the estimate of the latent
period, which is poorly known. As transmission appears to occur by biting, much of which happens during sexual encounters,
the dynamics of the disease may be typical of sexually transmitted diseases. This means that transmission is likely to be
frequency-dependent with no threshold density for disease maintenance. Extinction over the entire current range of the devil
is therefore a real possibility and an unacceptable risk. 相似文献
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Yoshikazu Furusawa Shinji Yamada Shunsuke Itai Takuro Nakamura Junko Takei Masato Sano Hiroyuki Harada Masato Fukui Mika K. Kaneko Yukinari Kato 《Biochemistry and Biophysics Reports》2019
Monoclonal antibodies (mAbs) against not only human, mouse, and rat but also rabbit, dog, cat, bovine, pig, and horse podoplanins (PDPNs) have been established in our previous studies. PDPN is used as a lymphatic endothelial cell marker in pathological diagnoses. However, mAbs against Tasmanian devil PDPN (tasPDPN), which are useful for immunohistochemical analysis, remain to be developed. Herein, mice were immunized with tasPDPN-overexpressing Chinese hamster ovary (CHO)-K1 (CHO/tasPDPN) cells, and hybridomas producing mAbs against tasPDPN were screened using flow cytometry. One of the mAbs, PMab-233 (IgG1, kappa), specifically detected CHO/tasPDPN cells by flow cytometry and recognized tasPDPN protein by western blotting. Furthermore, PMab-233 strongly detected CHO/tasPDPN cells by immunohistochemistry. These findings suggest that PMab-233 may be useful as a lymphatic endothelial cell marker of the Tasmanian devil. 相似文献
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The Tasmanian devil (Sarcophilus harrisii) is currently threatened by an emerging wildlife disease, devil facial tumour disease. The disease is decreasing devil numbers dramatically and may lead to the extinction of the species. At present, nothing is known about the immune genes or basic immunology of the devil. In this study, we report the construction of the first genetic library for the Tasmanian devil, a spleen cDNA library, and the isolation of full-length MHC Class I and Class II genes. We describe six unique Class II beta chain sequences from at least three loci, which belong to the marsupial Class II DA gene family. We have isolated 13 unique devil Class I sequences, representing at least seven Class I loci, two of which are most likely non-classical genes. The MHC Class I sequences from the devil have little heterogeneity, indicating recent divergence. The MHC genes described here are most likely involved in antigen presentation and are an important first step for studying MHC diversity and immune response in the devil. 相似文献
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In a number of marsupial species, females exhibit characteristic, stereotyped parturient behavior that facilitates the passage of the neonates to the pouch. In macropodids, this parturient behavior can be induced in non-pregnant females and males by treatment with either prostaglandin F2alpha (PGF2alpha) or oxytocin (OT). This study investigated the effects of PGF2alpha and OT on behavior of Tasmanian devils. Animals tended to sit or lie down quickly, with little vocalization, after treatment with PGF2alpha or OT, while after saline, the animals remained alert, seldom sat, and frequently vocalized. Hormone treatment caused increased respiration. Urogenital and pouch grooming, a characteristic element of parturient behavior in macropodids, was seen in only one devil after hormone treatment. However, no pouch or urogenital grooming was seen in videotape of a devil giving birth, so this may not be a feature of parturient behavior in this species. Overall behavior of males and females was very similar suggesting that the behavioral effects observed may be due to direct neural action of PGF2alpha or OT, rather than an indirect response to uterine or vaginal contractions caused by the hormones. This study is the first to demonstrate that OT results in PGF2alpha secretion as PGFM levels rose after OT injection. 相似文献
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Infectious disease has been shown to be a major cause of population declines in wild animals. However, there remains little empirical evidence on the genetic consequences of disease-mediated population declines, or how such perturbations might affect demographic processes such as dispersal. Devil facial tumour disease (DFTD) has resulted in the rapid decline of the Tasmanian devil, Sarcophilus harrisii, and threatens to cause extinction. Using 10 microsatellite DNA markers, we compared genetic diversity and structure before and after DFTD outbreaks in three Tasmanian devil populations to assess the genetic consequences of disease-induced population decline. We also used both genetic and demographic data to investigate dispersal patterns in Tasmanian devils along the east coast of Tasmania. We observed a significant increase in inbreeding (FIS pre/post-disease −0.030/0.012, P<0.05; relatedness pre/post-disease 0.011/0.038, P=0.06) in devil populations after just 2–3 generations of disease arrival, but no detectable change in genetic diversity. Furthermore, although there was no subdivision apparent among pre-disease populations (θ=0.005, 95% confidence interval (CI) −0.003 to 0.017), we found significant genetic differentiation among populations post-disease (θ=0.020, 0.010–0.027), apparently driven by a combination of selection and altered dispersal patterns of females in disease-affected populations. We also show that dispersal is male-biased in devils and that dispersal distances follow a typical leptokurtic distribution. Our results show that disease can result in genetic and demographic changes in host populations over few generations and short time scales. Ongoing management of Tasmanian devils must now attempt to maintain genetic variability in this species through actions designed to reverse the detrimental effects of inbreeding and subdivision in disease-affected populations. 相似文献
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Olivia Bell Menna E. Jones Manuel Ruiz‐Aravena Rodrigo K. Hamede Stuart Bearhop Robbie A. McDonald 《Ecology and evolution》2020,10(14):7861-7871
Age‐related changes in diet have implications for competitive interactions and for predator–prey dynamics, affecting individuals and groups at different life stages. To quantify patterns of variation and ontogenetic change in the diets of Tasmanian devils Sarcophilus harrisii, a threatened marsupial carnivore, we analyzed variation in the stable isotope composition of whisker tissue samples taken from 91 individual devils from Wilmot, Tasmania from December 2014 to February 2017. Both δ13C and δ15N decreased with increasing age in weaned Tasmanian devils, indicating that as they age devils rely less on small mammals and birds, and more on large herbivores. Devils <12 months old had broader group isotopic niches, as estimated by Bayesian standard ellipses (SEAB mode = 1.042) than devils from 12 to 23 months old (mode = 0.541) and devils ≥24 months old (mode = 0.532). Devils <24 months old had broader individual isotopic niches (SEAB mode range 0.492–1.083) than devils ≥24 months old (mode range 0.092–0.240). A decrease in δ15N from the older whisker sections to the more recently grown sections in devils <24 months old likely reflects the period of weaning in this species, as this pattern was not observed in devils ≥24 months old. Our data reveal changes in the isotopic composition of devil whiskers with increasing age, accompanied by a reduction in isotopic variation both among population age classes and within individuals, reflecting the effect of weaning in early life, and a likely shift from an initially diverse diet of small mammals, birds, and invertebrates towards increasing consumption of larger herbivores in adulthood. 相似文献