Most pathogens threatening to cause extinction of a host species are maintained on one or more reservoir hosts, in addition to the species that is threatened by disease. Further, most conventional host-pathogen theory assumes that transmission is related to host density, and therefore a pathogen should become extinct before its sole host. Tasmanian devil facial tumor disease is a recently emerged infectious cancer that has led to massive population declines and grave concerns for the future persistence of this largest surviving marsupial carnivore. Here we report the results of mark-recapture studies at six sites and use these data to estimate epidemiological parameters critical to both accurately assessing the risk of extinction from this disease and effectively managing this disease threat. Three sites were monitored from before or close to the time of disease arrival, and at three others disease was well established when trapping began, in one site for at least 10 years. We found no evidence for sex-specific differences in disease prevalence and little evidence of consistent seasonal variation in the force of infection. At all sites, the disease was maintained at high levels of prevalence (>50% in 2-3-year-old animals), despite causing major population declines. We also provide the first estimates of the basic reproductive rate R0 for this disease. Using a simple age-structured deterministic model, we show that our results are not consistent with transmission being proportional to the density of infected hosts but are consistent with frequency-dependent transmission. This conclusion is further supported by the observation that local disease prevalence in 2-3-year-olds still exceeds 50% at a site where population density has been reduced by up to 90% in the past 12 years. These findings lend considerable weight to concerns that this host-specific pathogen will cause the extinction of the Tasmanian devil. Our study highlights the importance of rapidly implementing monitoring programs to determine how transmission depends on host density and emphasizes the need for ongoing management strategies involving a disease-free "insurance population," along with ongoing field monitoring programs to confirm whether local population extinction occurs.
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
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.
Summary 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.
In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.
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