Menna E. Jones

Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease

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.

Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore

Genetic diversity and population structure were investigated across the core range of Tasmanian devils (Sarcophilus laniarius; Dasyuridae), a wide‐ranging marsupial carnivore restricted to the island of Tasmania. Heterozygosity (0.386–0.467) and allelic diversity (2.7–3.3) were low in all subpopulations and allelic size ranges were small and almost continuous, consistent with a founder effect. Island effects and repeated periods of low population density may also have contributed to the low variation. Within continuous habitat, gene flow appears extensive up to 50 km (high assignment rates to source or close neighbour populations; nonsignificant values of pairwise FST), in agreement with movement data. At larger scales (150–250 km), gene flow is reduced (significant pairwise FST) but there is no evidence for isolation by distance. The most substantial genetic structuring was observed for comparisons spanning unsuitable habitat, implying limited dispersal of devils between the well‐connected, eastern populations and a smaller northwestern population. The genetic distinctiveness of the northwestern population was reflected in all analyses: unique alleles; multivariate analyses of gene frequency (multidimensional scaling, minimum spanning tree, nearest neighbour); high self‐assignment (95%); two distinct populations for Tasmania were detected in isolation by distance and in Bayesian model‐based clustering analyses. Marsupial carnivores appear to have stronger population subdivisions than their placental counterparts.

Distribution and Impacts of Tasmanian Devil Facial Tumor Disease

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.

Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil)

The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction because of a contagious cancer known as Devil Facial Tumor Disease. The inability to mount an immune response and to reject these tumors might be caused by a lack of genetic diversity within a dwindling population. Here we report a whole-genome analysis of two animals originating from extreme northwest and southeast Tasmania, the maximal geographic spread, together with the genome from a tumor taken from one of them. A 3.3-Gb de novo assembly of the sequence data from two complementary next-generation sequencing platforms was used to identify 1 million polymorphic genomic positions, roughly one-quarter of the number observed between two genetically distant human genomes. Analysis of 14 complete mitochondrial genomes from current and museum specimens, as well as mitochondrial and nuclear SNP markers in 175 animals, suggests that the observed low genetic diversity in todays population preceded the Devil Facial Tumor Disease disease outbreak by at least 100 y. Using a genetically characterized breeding stock based on the genome sequence will enable preservation of the extant genetic diversity in future Tasmanian devil populations.

Road upgrade, road mortality and remedial measures: impacts on a population of eastern quolls and Tasmanian devils

The impact of road mortality on local populations of wildlife has rarely been quantified. In June 1991, the access road into the northern end of the Cradle Mountain – Lake St Clair National Park in Tasmania was widened and sealed. This occurred part-way through an ecological study of the dasyurid carnivore guild, during which populations were being monitored. In 17 months, the resident population of 19 eastern quolls became extinct and the devil population, of 39 individuals, halved. Concurrently, there was a dramatic increase in the number of road-kills. The main causal factor was probably an increase in modal speed of about 20 km h–1 and a greater increase in maximum speed. Measures were implemented to reduce the incidence of vehicle/wildlife collisions. Measures directed at people included physically slowing traffic speed (using ‘slow points’) and increasing driver awareness (signs and pamphlets). Those directed at wildlife included deterring wildlife from crossing the road in the path of approaching vehicles (wildlife reflectors), and encouraging escape off the road (ramps across gutters and banks, and pipes for shelter). The ‘slow points’ were effective in reducing vehicle speeds by 20 km h–1. Wildlife used the ramps and pipes. The eastern quoll population was re-establishing within six months, and after two years, had recovered to 50% of its former level. There was some indication that devil populations were recovering.

Life-history change in disease-ravaged Tasmanian devil populations

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 disease-induced 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.

The role of connectivity in Australian conservation

The existing system of nature reserves in Australia is inadequate for the long-term conservation and restoration of native biological diversity because it fails to accommodate, among other elements, large scale and long-term ecological processes and change, including physical and biotic transport in the landscape. This paper is an overview of the connectivity elements that inform a scientific framework for significantly improving the prospects for the long-term conservation of Australias biodiversity. The framework forms the basis for the WildCountry programme. This programme has identified connectivity at landscape, regional and continental scales as a critical component of an effective conservation system. Seven categories of ecological phenomena are reviewed that require landscape permeability and that must be considered when planning for the maintenance of biological diversity and ecological resilience in Australia: (1) trophic relations at regional scales; (2) animal migration, dispersal, and other large scale movements of individuals and propagules; (3) fire and other forms of disturbance at regional scales; (4) climate variability in space and time and human forced rapid climate change; (5) hydroecological relations and flows at all scales; (6) coastal zone fluxes of organisms, matter, and energy; and, (7) spatially-dependent evolutionary processes at all scales. Finally, we mention eight cross-cutting themes that further illuminate the interactions and implications of the seven connectivity-related phenomena for conservation assessment, planning, research, and management, and we suggest how the results might be applied by analysts, planners, scientists, and community conservationists.

MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer

Tasmanian devils face extinction owing to the emergence of a contagious cancer. Devil facial tumour disease (DFTD) is a clonal cancer spread owing to a lack of major histocompatibility complex (MHC) barriers in Tasmanian devil populations. We present a comprehensive screen of MHC diversity in devils and identify 25 MHC types and 53 novel sequences, but conclude that overall levels of MHC diversity at the sequence level are low. The majority of MHC Class I variation can be explained by allelic copy number variation with two to seven sequence variants identified per individual. MHC sequences are divided into two distinct groups based on sequence similarity. DFTD cells and most devils have sequences from both groups. Twenty per cent of individuals have a restricted MHC repertoire and contain only group I or only group II sequences. Counterintuitively, we postulate that the immune system of individuals with a restricted MHC repertoire may recognize foreign MHC antigens on the surface of the DFTD cell. The implication of these results for management of DFTD and this endangered species are discussed.

Reversible epigenetic down-regulation of MHC molecules by devil facial tumour disease illustrates immune escape by a contagious cancer

Contagious cancers that pass between individuals as an infectious cell line are highly unusual pathogens. Devil facial tumor disease (DFTD) is one such contagious cancer that emerged 16 y ago and is driving the Tasmanian devil to extinction. As both a pathogen and an allograft, DFTD cells should be rejected by the host–immune response, yet DFTD causes 100% mortality among infected devils with no apparent rejection of tumor cells. Why DFTD cells are not rejected has been a question of considerable confusion. Here, we show that DFTD cells do not express cell surface MHC molecules in vitro or in vivo, due to down-regulation of genes essential to the antigen-processing pathway, such as β2-microglobulin and transporters associated with antigen processing. Loss of gene expression is not due to structural mutations, but to regulatory changes including epigenetic deacetylation of histones. Consequently, MHC class I molecules can be restored to the surface of DFTD cells in vitro by using recombinant devil IFN-γ, which is associated with up-regulation of the MHC class II transactivator, a key transcription factor with deacetylase activity. Further, expression of MHC class I molecules by DFTD cells can occur in vivo during lymphocyte infiltration. These results explain why T cells do not target DFTD cells. We propose that MHC-positive or epigenetically modified DFTD cells may provide a vaccine to DFTD. In addition, we suggest that down-regulation of MHC molecules using regulatory mechanisms allows evolvability of transmissible cancers and could affect the evolutionary trajectory of DFTD.

Landscape Management of Fire and Grazing Regimes Alters the Fine-Scale Habitat Utilisation by Feral Cats

Intensification of fires and grazing by large herbivores has caused population declines in small vertebrates in many ecosystems worldwide. Impacts are rarely direct, and usually appear driven via indirect pathways, such as changes to predator-prey dynamics. Fire events and grazing may improve habitat and/or hunting success for the predators of small mammals, however, such impacts have not been documented. To test for such an interaction, we investigated fine-scale habitat selection by feral cats in relation to fire, grazing and small-mammal abundance. Our study was conducted in north-western Australia, where small mammal populations are sensitive to changes in fire and grazing management. We deployed GPS collars on 32 cats in landscapes with contrasting fire and grazing treatments. Fine-scale habitat selection was determined using discrete choice modelling of cat movements. We found that cats selected areas with open grass cover, including heavily-grazed areas. They strongly selected for areas recently burnt by intense fires, but only in habitats that typically support high abundance of small mammals. Intense fires and grazing by introduced herbivores created conditions that are favoured by cats, probably because their hunting success is improved. This mechanism could explain why, in northern Australia, impacts of feral cats on small mammals might have increased. Our results suggest the impact of feral cats could be reduced in most ecosystems by maximising grass cover, minimising the incidence of intense fires, and reducing grazing by large herbivores.