Intergenomic signatures of coevolution between Tasmanian devils and an infectious cancer.

Coevolution is common and frequently governs host-pathogen interaction outcomes. Phenotypes underlying these interactions often manifest as the combined products of the genomes of interacting species, yet traditional quantitative trait mapping approaches ignore these intergenomic interactions. Devil facial tumor disease (DFTD), an infectious cancer afflicting Tasmanian devils (Sarcophilus harrisii), has decimated devil populations due to universal host susceptibility and a fatality rate approaching 100%. Here, we used a recently developed joint genome-wide association study (i.e., co-GWAS) approach, 15 y of mark-recapture data, and 960 genomes to identify intergenomic signatures of coevolution between devils and DFTD. Using a traditional GWA approach, we found that both devil and DFTD genomes explained a substantial proportion of variance in how quickly susceptible devils became infected, although genomic architectures differed across devils and DFTD; the devil genome had fewer loci of large effect whereas the DFTD genome had a more polygenic architecture. Using a co-GWA approach, devil-DFTD intergenomic interactions explained ~3× more variation in how quickly susceptible devils became infected than either genome alone, and the top genotype-by-genotype interactions were significantly enriched for cancer genes and signatures of selection. A devil regulatory mutation was associated with differential expression of a candidate cancer gene and showed putative allele matching effects with two DFTD coding sequence variants. Our results highlight the need to account for intergenomic interactions when investigating host-pathogen (co)evolution and emphasize the importance of such interactions when considering devil management strategies.

Adaptive potential in the face of a transmissible cancer in Tasmanian devils.

Emerging infectious diseases (EIDs) not only cause catastrophic declines in wildlife populations but also generate selective pressures that may result in rapid evolutionary responses. One such EID is devil facial tumour disease (DFTD) in the Tasmanian devil. DFTD is almost always fatal and has reduced the average lifespan of individuals by around 2 years, likely causing strong selection for traits that reduce susceptibility to the disease, but population decline has also left Tasmanian devils vulnerable to inbreeding depression. We analysed 22 years of data from an ongoing study of a population of Tasmanian devils on Freycinet Peninsula, Tasmania, to (1) identify whether DFTD may be causing selection on body size, by estimating phenotypic and genetic correlations between DFTD and size traits, (2) estimate the additive genetic variance of susceptibility to DFTD, and (3) investigate whether size traits or susceptibility to DFTD were under inbreeding depression. We found a positive phenotypic relationship between head width and susceptibility to DFTD, but this was not underpinned by a genetic correlation. Conversely, we found a negative phenotypic relationship between body weight and susceptibility to DFTD, and there was evidence for a negative genetic correlation between susceptibility to DFTD and body weight. There was additive genetic variance in susceptibility to DFTD, head width and body weight, but there was no evidence for inbreeding depression in any of these traits. These results suggest that Tasmanian devils have the potential to respond adaptively to DFTD, although the realised evolutionary response will critically further depend on the evolution of DFTD itself.

Do Tasmanian devil declines impact ecosystem function?

Tasmanian eucalypt forests are among the most carbon-dense in the world, but projected climate change could destabilize this critical carbon sink. While the impact of abiotic factors on forest ecosystem carbon dynamics have received considerable attention, biotic factors such as the input of animal scat are less understood. Tasmanian devils (Sarcophilus harrisii)-an osteophageous scavenger that can ingest and solubilize nutrients locked in bone material-may subsidize plant and microbial productivity by concentrating bioavailable nutrients (e.g., nitrogen and phosphorus) in scat latrines. However, dramatic declines in devil population densities, driven by the spread of a transmissible cancer, may have underappreciated consequences for soil organic carbon (SOC) storage and forest productivity by altering nutrient cycling. Here, we fuse experimental data and modeling to quantify and predict future changes to forest productivity and SOC under various climate and scat-quality futures. We find that devil scat significantly increases concentrations of nitrogen, ammonium, phosphorus, and phosphate in the soil and shifts soil microbial communities toward those dominated by r-selected (e.g., fast-growing) phyla. Further, under expected increases in temperature and changes in precipitation, devil scat inputs are projected to increase above- and below-ground net primary productivity and microbial biomass carbon through 2100. In contrast, when devil scat is replaced by lower-quality scat (e.g., from non-osteophageous scavengers and herbivores), forest carbon pools are likely to increase more slowly, or in some cases, decline. Together, our results suggest often overlooked biotic factors will interact with climate change to drive current and future carbon pool dynamics in Tasmanian forests.

Human habitat modification, not apex scavenger decline, drives isotopic niche variation in a carnivore community.

Top carnivores can influence the structure of ecological communities, primarily through competition and predation; however, communities are also influenced by bottom-up forces such as anthropogenic habitat disturbance. Top carnivore declines will likely alter competitive dynamics within and amongst sympatric carnivore species. Increasing intraspecific competition is generally predicted to drive niche expansion and/or individual specialisation, while interspecific competition tends to constrain niches. Using stable isotope analysis of whiskers, we studied the effects of Tasmanian devil Sarcophilus harrisii declines upon the population- and individual-level isotopic niches of Tasmanian devils and sympatric spotted-tailed quolls Dasyurus maculatus subsp. maculatus. We investigated whether time since the onset of devil decline (a proxy for severity of decline) and landscape characteristics affected the isotopic niche breadth and overlap of devil and quoll populations. We quantified individual isotopic niche breadth for a subset of Tasmanian devils and spotted-tailed quolls and assessed whether between-site population niche variation was driven by individual-level specialisation. Tasmanian devils and spotted-tailed quolls demonstrated smaller population-level isotopic niche breadths with increasing human-modified habitat, while time since the onset of devil decline had no effect on population-level niche breadth or interspecific niche overlap. Individual isotopic niche breadths of Tasmanian devils and spotted-tailed quolls were narrower in human-modified landscapes, likely driving population isotopic niche contraction, however, the degree of individuals' specialisation relative to one another remained constant. Our results suggest that across varied landscapes, mammalian carnivore niches can be more sensitive to the bottom-up forces of anthropogenic habitat disturbance than to the top-down effects of top carnivore decline.

Over-eruption in marsupial carnivore teeth: compensation for a constraint.

Pronounced over-eruption of the canine teeth, causing the cervical enamel margin to extend beyond the alveolar bone and exposing the root, occurs with age and growth in Australian marsupial carnivores, much more than in eco-morphologically equivalent placental carnivores. Suppression of functional tooth replacement is characteristic of marsupials, where most placentals have the primitive diphyodont pattern of two generations of incisor, canine and premolar teeth. Canine and molar tooth dimensions of four species of marsupial carnivores (thylacine Thylacinus cynocephalus, Tasmanian devil Sarcophilus harrisii and two quolls Dasyurus spp.) and canine dimensions of seven eco-morphologically equivalent placental carnivore species were measured from museum specimens. Canine dimensions were measured in a time series on live wild-living individual devils and quolls. The canine teeth and to a lesser extent the molar teeth of marsupial carnivores continue to erupt through life, resulting in a net increase in tooth height and diameter, a phenomenon not evident in placental carnivores. Potential mechanisms causing over-eruption include tooth wear and gradual release of occlusal pressure as the individual grows. Over-eruption in marsupial carnivores may be a compensatory response for tooth size limits imposed by monophyodont tooth replacement, ensuring that animal's teeth are scaled to jaw size from juvenile to adulthood.

Top predator restricts the niche breadth of prey: effects of assisted colonization of Tasmanian devils on a widespread omnivorous prey.

Few landscape-scale experiments test the effects of predators on the abundance and distribution of prey across habitat gradients. We use the assisted colonization of a top predator, the Tasmanian devil (Sarcophilus harrisii), to test the impacts of predation on the abundance, habitat use and temporal activity of a widespread prey species, the omnivorous common brushtail possum (Trichosurus vulpecula). Before introduction of devils to Maria Island, Tasmania, Australia, in 2012, possums were abundant in open grasslands as well as forests. Predation by devils caused high mortality of possums in grasslands, but individuals with access to trees had a higher survival probability. Possum abundance declined across the whole island from 2012-2016, as possums disappeared almost completely from grasslands and declined in drier forests with more open understorey. Abundance remained stable in wet forests, which are not preferred habitat for possums but provide better refuge from devils. Abundance and habitat use of possums remained unchanged at a control site on the adjacent Tasmanian mainland, where the devil population was low and stable. This study demonstrates how spatial variation in predator-caused mortality can limit both abundance and habitat breadth in generalist prey species, excluding them entirely from certain habitats.

Evolution and lineage dynamics of a transmissible cancer in Tasmanian devils.

Devil facial tumour 1 (DFT1) is a transmissible cancer clone endangering the Tasmanian devil. The expansion of DFT1 across Tasmania has been documented, but little is known of its evolutionary history. We analysed genomes of 648 DFT1 tumours collected throughout the disease range between 2003 and 2018. DFT1 diverged early into five clades, three spreading widely and two failing to persist. One clade has replaced others at several sites, and rates of DFT1 coinfection are high. DFT1 gradually accumulates copy number variants (CNVs), and its telomere lengths are short but constant. Recurrent CNVs reveal genes under positive selection, sites of genome instability, and repeated loss of a small derived chromosome. Cultured DFT1 cell lines have increased CNV frequency and undergo highly reproducible convergent evolution. Overall, DFT1 is a remarkably stable lineage whose genome illustrates how cancer cells adapt to diverse environments and persist in a parasitic niche.

Dominant carnivore loss benefits native avian and invasive mammalian scavengers.

Scavenging by large carnivores is integral for ecosystem functioning by limiting the build-up of carrion and facilitating widespread energy flows. However, top carnivores have declined across the world, triggering trophic shifts within ecosystems. Here, we compare findings from previous work on predator decline against areas with recent native mammalian carnivore loss. Specifically, we investigate top-down control on utilization of experimentally placed carcasses by two mesoscavengers-the invasive feral cat and native forest raven. Ravens profited most from carnivore loss, scavenging for five times longer in the absence of native mammalian carnivores. Cats scavenged on half of all carcasses in the region without dominant native carnivores. This was eight times more than in areas where other carnivores were at high densities. All carcasses persisted longer than the three-week monitoring period in the absence of native mammalian carnivores, while in areas with high carnivore abundance, all carcasses were fully consumed. Our results reveal that top-carnivore loss amplifies impacts associated with carnivore decline-increased carcass persistence and carrion access for smaller scavengers. This suggests that even at low densities, native mammalian carnivores can fulfil their ecological functions, demonstrating the significance of global carnivore conservation and supporting management approaches, such as trophic rewilding.

Extracellular vesicle proteomes of two transmissible cancers of Tasmanian devils reveal tenascin-C as a serum-based differential diagnostic biomarker.

The iconic Tasmanian devil (Sarcophilus harrisii) is endangered due to the transmissible cancer Devil Facial Tumour Disease (DFTD), of which there are two genetically independent subtypes (DFT1 and DFT2). While DFT1 and DFT2 can be differentially diagnosed using tumour biopsies, there is an urgent need to develop less-invasive biomarkers that can detect DFTD and distinguish between subtypes. Extracellular vesicles (EVs), the nano-sized membrane-enclosed vesicles present in most biofluids, represent a valuable resource for biomarker discovery. Here, we characterized the proteome of EVs from cultured DFTD cells using data-independent acquisition-mass spectrometry and an in-house spectral library of > 1500 proteins. EVs from both DFT1 and DFT2 cell lines expressed higher levels of proteins associated with focal adhesion functions. Furthermore, hallmark proteins of epithelial-mesenchymal transition were enriched in DFT2 EVs relative to DFT1 EVs. These findings were validated in EVs derived from serum samples, revealing that the mesenchymal marker tenascin-C was also enriched in EVs derived from the serum of devils infected with DFT2 relative to those infected with DFT1 and healthy controls. This first EV-based investigation of DFTD increases our understanding of the cancers' EVs and their possible involvement in DFTD progression, such as metastasis. Finally, we demonstrated the potential of EVs to differentiate between DFT1 and DFT2, highlighting their potential use as less-invasive liquid biopsies for the Tasmanian devil.

Spatial variation in gene expression of Tasmanian devil facial tumors despite minimal host transcriptomic response to infection.

BACKGROUND: Transmissible cancers lie at the intersection of oncology and infectious disease, two traditionally divergent fields for which gene expression studies are particularly useful for identifying the molecular basis of phenotypic variation. In oncology, transcriptomics studies, which characterize the expression of thousands of genes, have identified processes leading to heterogeneity in cancer phenotypes and individual prognoses. More generally, transcriptomics studies of infectious diseases characterize interactions between host, pathogen, and environment to better predict population-level outcomes. Tasmanian devils have been impacted dramatically by a transmissible cancer (devil facial tumor disease; DFTD) that has led to widespread population declines. Despite initial predictions of extinction, populations have persisted at low levels, due in part to heterogeneity in host responses, particularly between sexes. However, the processes underlying this variation remain unknown. RESULTS: We sequenced transcriptomes from healthy and DFTD-infected devils, as well as DFTD tumors, to characterize host responses to DFTD infection, identify differing host-tumor molecular interactions between sexes, and investigate the extent to which tumor gene expression varies among host populations. We found minimal variation in gene expression of devil lip tissues, either with respect to DFTD infection status or sex. However, 4088 genes were differentially expressed in tumors among our sampling localities. Pathways that were up- or downregulated in DFTD tumors relative to normal tissues exhibited the same patterns of expression with greater intensity in tumors from localities that experienced DFTD for longer. No mRNA sequence variants were associated with expression variation. CONCLUSIONS: Expression variation among localities may reflect morphological differences in tumors that alter ratios of normal-to-tumor cells within biopsies. Phenotypic variation in tumors may arise from environmental variation or differences in host immune response that were undetectable in lip biopsies, potentially reflecting variation in host-tumor coevolutionary relationships among sites that differ in the time since DFTD arrival.

A triple threat: high population density, high foraging intensity and flexible habitat preferences explain high impact of feral cats on prey.

Alien mammalian carnivores have contributed disproportionately to global loss of biodiversity. In Australia, predation by the feral cat and red fox is one of the most significant causes of the decline of native vertebrates. To discover why cats have greater impacts on prey than native predators, we compared the ecology of the feral cat to a marsupial counterpart, the spotted-tailed quoll. Individual prey are 20-200 times more likely to encounter feral cats, because of the combined effects of cats' higher population densities, greater intensity of home-range use and broader habitat preferences. These characteristics also mean that the costs to the prey of adopting anti-predator behaviours against feral cats are likely to be much higher than adopting such behaviours in response to spotted-tailed quolls, due to the reliability and ubiquity of feral cat cues. These results help explain the devastating impacts of cats on wildlife in Australia and other parts of the world.

Contemporary and historical selection in Tasmanian devils (Sarcophilus harrisii) support novel, polygenic response to transmissible cancer.

Tasmanian devils (Sarcophilus harrisii) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. Here, we compared signatures of selection across temporal scales to determine whether genes or gene pathways under contemporary selection (six to eight generations) have also been subject to historical selection (65-85 Myr). First, we used targeted sequencing, RAD-capture, in approximately 2500 devils in six populations to identify genomic regions subject to rapid evolution. We documented genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. Then we used a molecular evolution approach to identify historical positive selection in devils compared to other marsupials and found evidence of selection in 1773 genes. However, we found limited overlap across time scales, with only 16 shared candidate genes, and no overlap in enriched functional gene sets. Our results are consistent with a novel, multi-locus evolutionary response of devils to DFTD. Our results can inform conservation by identifying high priority targets for genetic monitoring and guiding maintenance of adaptive potential in managed populations.

The effects of weather variability on patterns of genetic diversity in Tasmanian bettongs.

While the effects of climate (long-term, prevailing weather) on species abundance, range and genetic diversity have been widely studied, short-term, localized variations in atmospheric conditions (i.e., weather) can also rapidly alter species' geographical ranges and population sizes, but little is known about how they affect genetic diversity. We investigated the relationship between weather and range-wide genetic diversity in a marsupial, Bettongia gaimardi, using dynamic species distribution models (SDMs). Genetic diversity was lower in parts of the range where the weather-based SDM predicted high variability in probability of B. gaimardi occurrence during 1950-2009. This is probably an effect of lower population sizes and extinction-recolonization cycles in places with highly variable weather. Spatial variation in genetic diversity was also better predicted by mean probabilities of B. gaimardi occurrence from weather- than climate-based SDMs. Our results illustrate the importance of weather in driving population dynamics and species distributions on decadal timescales and thereby in affecting genetic diversity. Modelling the links between changing weather patterns, species distributions and genetic diversity will allow researchers to better forecast biological impacts of climate change.

A native apex predator limits an invasive mesopredator and protects native prey: Tasmanian devils protecting bandicoots from cats.

Apex predators can limit the abundance and behaviour of mesopredators, thereby reducing predation on smaller species. We know less about whether native apex predators are effective in suppressing invasive mesopredators, a major global driver of vertebrate extinctions. We use the severe disease-induced decline of an apex predator, the Tasmanian devil, as a natural experiment to test whether devils limit abundance of invasive feral cats and in turn protect smaller native prey. Cat abundance was c. 58% higher where devils had declined, which in turn negatively affected a smaller native prey species. Devils had a stronger limiting effect on cats than on a native mesopredator, suggesting apex predators may have stronger suppressive effects on evolutionarily naive species than coevolved species. Our results highlight how disease in one species can affect the broader ecosystem. We show that apex predators not only regulate native species but can also confer resistance to the impacts of invasive populations. Apex predators could therefore be a powerful but underutilised tool to prevent biodiversity loss.

Contemporary Demographic Reconstruction Methods Are Robust to Genome Assembly Quality: A Case Study in Tasmanian Devils.

Reconstructing species' demographic histories is a central focus of molecular ecology and evolution. Recently, an expanding suite of methods leveraging either the sequentially Markovian coalescent (SMC) or the site-frequency spectrum has been developed to reconstruct population size histories from genomic sequence data. However, few studies have investigated the robustness of these methods to genome assemblies of varying quality. In this study, we first present an improved genome assembly for the Tasmanian devil using the Chicago library method. Compared with the original reference genome, our new assembly reduces the number of scaffolds (from 35,975 to 10,010) and increases the scaffold N90 (from 0.101 to 2.164 Mb). Second, we assess the performance of four contemporary genomic methods for inferring population size history (PSMC, MSMC, SMC++, Stairway Plot), using the two devil genome assemblies as well as simulated, artificially fragmented genomes that approximate the hypothesized demographic history of Tasmanian devils. We demonstrate that each method is robust to assembly quality, producing similar estimates of Ne when simulated genomes were fragmented into up to 5,000 scaffolds. Overall, methods reliant on the SMC are most reliable between ∼300 generations before present (gbp) and 100 kgbp, whereas methods exclusively reliant on the site-frequency spectrum are most reliable between the present and 30 gbp. Our results suggest that when used in concert, genomic methods for reconstructing species' effective population size histories 1) can be applied to nonmodel organisms without highly contiguous reference genomes, and 2) are capable of detecting independently documented effects of historical geological events.

Infectious disease and sickness behaviour: tumour progression affects interaction patterns and social network structure in wild Tasmanian devils.

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.

Comparative landscape genetics reveals differential effects of environment on host and pathogen genetic structure in Tasmanian devils (Sarcophilus harrisii) and their transmissible tumour.

Genetic structure in host species is often used to predict disease spread. However, host and pathogen genetic variation may be incongruent. Understanding landscape factors that have either concordant or divergent influence on host and pathogen genetic structure is crucial for wildlife disease management. Devil facial tumour disease (DFTD) was first observed in 1996 and has spread throughout almost the entire Tasmanian devil geographic range, causing dramatic population declines. Whereas DFTD is predominantly spread via biting among adults, devils typically disperse as juveniles, which experience low DFTD prevalence. Thus, we predicted little association between devil and tumour population structure and that environmental factors influencing gene flow differ between devils and tumours. We employed a comparative landscape genetics framework to test the influence of environmental factors on patterns of isolation by resistance (IBR) and isolation by environment (IBE) in devils and DFTD. Although we found evidence for broad-scale costructuring between devils and tumours, we found no relationship between host and tumour individual genetic distances. Further, the factors driving the spatial distribution of genetic variation differed for each. Devils exhibited a strong IBR pattern driven by major roads, with no evidence of IBE. By contrast, tumours showed little evidence for IBR and a weak IBE pattern with respect to elevation in one of two tumour clusters we identify herein. Our results warrant caution when inferring pathogen spread using host population genetic structure and suggest that reliance on environmental barriers to host connectivity may be ineffective for managing the spread of wildlife diseases. Our findings demonstrate the utility of comparative landscape genetics for identifying differential factors driving host dispersal and pathogen transmission.

Individual and temporal variation in pathogen load predicts long-term impacts of an emerging infectious disease.

Emerging infectious diseases increasingly threaten wildlife populations. Most studies focus on managing short-term epidemic properties, such as controlling early outbreaks. Predicting long-term endemic characteristics with limited retrospective data is more challenging. We used individual-based modeling informed by individual variation in pathogen load and transmissibility to predict long-term impacts of a lethal, transmissible cancer on Tasmanian devil (Sarcophilus harrisii) populations. For this, we employed approximate Bayesian computation to identify model scenarios that best matched known epidemiological and demographic system properties derived from 10 yr of data after disease emergence, enabling us to forecast future system dynamics. We show that the dramatic devil population declines observed thus far are likely attributable to transient dynamics (initial dynamics after disease emergence). Only 21% of matching scenarios led to devil extinction within 100 yr following devil facial tumor disease (DFTD) introduction, whereas DFTD faded out in 57% of simulations. In the remaining 22% of simulations, disease and host coexisted for at least 100 yr, usually with long-period oscillations. Our findings show that pathogen extirpation or host-pathogen coexistence are much more likely than the DFTD-induced devil extinction, with crucial management ramifications. Accounting for individual-level disease progression and the long-term outcome of devil-DFTD interactions at the population-level, our findings suggest that immediate management interventions are unlikely to be necessary to ensure the persistence of Tasmanian devil populations. This is because strong population declines of devils after disease emergence do not necessarily translate into long-term population declines at equilibria. Our modeling approach is widely applicable to other host-pathogen systems to predict disease impact beyond transient dynamics.

An Australian perspective on rewilding.

Rewilding is increasingly recognized as a conservation tool but is often context specific, which inhibits broad application. Rewilding in Australia seeks to enhance ecosystem function and promote self-sustaining ecosystems. An absence of large-bodied native herbivores means trophic rewilding in mainland Australia has focused on the restoration of functions provided by apex predators and small mammals. Because of the pervasive influence of introduced mesopredators, predator-proof fences, and establishment of populations on predator-free islands are common rewilding approaches. This sets Australian rewilding apart from most jurisdictions and provides globally relevant insights but presents challenges to restoring function to broader landscapes. Passive rewilding is of limited utility in arid zones. Although increasing habitat extent and quality in mesic coastal areas may work, it will likely be necessary to undertake active management. Because much of Australia's population is in urban areas, rewilding efforts must include urban areas to maximize effectiveness. Thus rewilding is not synonymous with wilderness and can occur over multiple scales. Rewilding efforts must recognize human effects on other species and benefit both nature and humans. Rewilding in Australia requires development of a shared vision and strategy and proof-of-concept projects to demonstrate the benefits. The repackaging of existing conservation activities as rewilding may confuse and undermine the success of rewilding programs and should be avoided. As elsewhere, rewilding in Australia should be viewed as an important conservation tool.

Una Perspectiva Australiana del Proceso de Resilvestrar Resumen El proceso de resilvestrar es reconocido cada vez más como una herramienta de conservación, pero con frecuencia depende del contexto ambiental, lo que inhibe su aplicación generalizada. En Australia, el proceso de resilvestrar busca mejorar la función ambiental y promover los ecosistemas auto-sustentables. Una ausencia de herbívoros nativos corpulentos significa que el resilvestreo trófico en la isla principal de Australia se ha enfocado en la restauración de las funciones que proporcionan los superdepredadores y los mamíferos pequeños. Debido a la influencia generalizada de los mesodepredadores introducidos, los cercos contra depredadores y el establecimiento de poblaciones en islas libres de depredadores son estrategias comunes de resilvestreo. Esto coloca al resilvestreo australiano aparte del que ocurre en muchas jurisdicciones y proporciona información relevante a nivel mundial, pero presenta retos para la restauración de la función en paisajes más amplios. El resilvestreo pasivo es de utilidad limitada en las zonas áridas. Aunque el aumento de la extensión del hábitat y la calidad en las áreas meso-costeras puede funcionar, probablemente sea necesario emprender un manejo activo. Ya que la mayoría de la población de Australia se encuentra en áreas urbanas, los esfuerzos de resilvestreo deben incluir a las áreas urbanas para maximizar su efectividad. Por lo tanto, el resilvestreo no es sinónimo de la naturaleza y puede ocurrir en múltiples escalas. Los esfuerzos de resilvestreo deben reconocer los efectos que los humanos tienen sobre otras especies y deben beneficiar a la naturaleza y a las personas. El resilvestreo en Australia requiere del desarrollo de una visión compartida y de proyectos con prueba de concepto para demostrar sus beneficios. La reinvención de las actividades de conservación existentes como resilvestreo podría confundir y debilitar el éxito de los programas de resilvestreo, por lo que debería evitarse. Como en todos lados, el proceso de resilvestrar en Australia debería verse como una herramienta importante de conservación.

Conserving adaptive potential: lessons from Tasmanian devils and their transmissible cancer.

Maintenance of adaptive genetic variation has long been a goal of management of natural populations, but only recently have genomic tools allowed identification of specific loci associated with fitness-related traits in species of conservation concern. This raises the possibility of managing for genetic variation directly relevant to specific threats, such as those due to climate change or emerging infectious disease. Tasmanian devils (Sarcophilus harrisii) face the threat of a transmissible cancer, devil facial tumor disease (DFTD), that has decimated wild populations and led to intensive management efforts. Recent discoveries from genomic and modeling studies reveal how natural devil populations are responding to DFTD, and can inform management of both captive and wild devil populations. Notably, recent studies have documented genetic variation for disease-related traits and rapid evolution in response to DFTD, as well as potential mechanisms for disease resistance such as immune response and tumor regression in wild devils. Recent models predict dynamic persistence of devils with or without DFTD under a variety of modeling scenarios, although at much lower population densities than before DFTD emerged, contrary to previous predictions of extinction. As a result, current management that focuses on captive breeding and release for maintaining genome-wide genetic diversity or demographic supplementation of populations could have negative consequences. Translocations of captive devils into wild populations evolving with DFTD can cause outbreeding depression and/or increases in the force of infection and thereby the severity of the epidemic, and we argue that these risks outweigh any benefits of demographic supplementation in wild populations. We also argue that genetic variation at loci associated with DFTD should be monitored in both captive and wild populations, and that as our understanding of DFTD-related genetic variation improves, considering genetic management approaches to target this variation is warranted in developing conservation strategies for Tasmanian devils.