Search for: All records

Abstract Emerging infectious diseases threaten natural populations, and data-driven modeling is critical for predicting population dynamics. Despite the importance of integrating ecology and evolution in models of host–pathogen dynamics, there are few wild populations for which long-term ecological datasets have been coupled with genome-scale data. Tasmanian devil (Sarcophilus harrisii) populations have declined range wide due to devil facial tumor disease (DFTD), a fatal transmissible cancer. Although early ecological models predicted imminent devil extinction, diseased devil populations persist at low densities, and recent ecological models predict long-term devil persistence. Substantial evidence supports the evolution of both devils and DFTD, suggesting coevolution may also influence continued devil persistence. Thus, we developed an individual-based, eco-evolutionary model of devil–DFTD coevolution parameterized with nearly 2 decades of devil demography, DFTD epidemiology, and genome-wide association studies. We characterized potential devil–DFTD coevolutionary outcomes and predicted the effects of coevolution on devil persistence and devil–DFTD coexistence. We found a high probability of devil persistence over 50 devil generations (100 years) and a higher likelihood of devil–DFTD coexistence, with greater devil recovery than predicted by previous ecological models. These novel results add to growing evidence for long-term devil persistence and highlight the importance of eco-evolutionary modeling for emerging infectious diseases. 

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. 

Abstract Forest disturbance has well-characterized effects on soil microbial communities in tropical and northern hemisphere ecosystems, but little is known regarding effects of disturbance in temperate forests of the southern hemisphere. To address this question, we collected soils from intact and degraded Eucalyptus forests along an east–west transect across Tasmania, Australia, and characterized prokaryotic and fungal communities using amplicon sequencing. Forest degradation altered soil microbial community composition and function, with consistent patterns across soil horizons and regions of Tasmania. Responses of prokaryotic communities included decreased relative abundance of Acidobacteriota, nitrifying archaea, and methane-oxidizing prokaryotes in the degraded forest sites, while fungal responses included decreased relative abundance of some saprotrophic taxa (e.g. litter saprotrophs). Forest degradation also reduced network connectivity in prokaryotic communities and increased the importance of dispersal limitation in assembling both prokaryotic and fungal communities, suggesting recolonization dynamics drive microbial composition following disturbance. Further, changes in microbial functional groups reflected changes in soil chemical properties—reductions in nitrifying microorganisms corresponded with reduced NO3-N pools in the degraded soils. Overall, our results show that soil microbiota are highly responsive to forest degradation in eucalypt forests and demonstrate that microbial responses to degradation will drive changes in key forest ecosystem functions. 

Abstract 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 byr‐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. 

Abstract 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. 

Emerging infectious diseases pose one of the greatest threats to human health and biodiversity. Phylodynamics is often used to infer epidemiological parameters essential for guiding intervention strategies for human viruses such as severe acute respiratory syndrome coronavirus 2 (SARS-Cov-2). Here, we applied phylodynamics to elucidate the epidemiological dynamics of Tasmanian devil facial tumor disease (DFTD), a fatal, transmissible cancer with a genome thousands of times larger than that of any virus. Despite prior predictions of devil extinction, transmission rates have declined precipitously from ~3.5 secondary infections per infected individual to ~1 at present. Thus, DFTD appears to be transitioning from emergence to endemism, lending hope for the continued survival of the endangered Tasmanian devil. More generally, our study demonstrates a new phylodynamic analytical framework that can be applied to virtually any pathogen. 

Abstract Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective processes. Phylodynamics is a robust framework to understand the interaction of pathogen evolutionary processes with epidemiological dynamics, providing a powerful tool to evaluate disease control strategies. Tasmanian devils have been threatened by a fatal transmissible cancer, devil facial tumour disease (DFTD), for more than two decades. Here we employ a phylodynamic approach using tumour mitochondrial genomes to assess the role of tumour genetic diversity in epidemiological and population dynamics in a devil population subject to 12 years of intensive monitoring, since the beginning of the epidemic outbreak. DFTD molecular clock estimates of disease introduction mirrored observed estimates in the field, and DFTD genetic diversity was positively correlated with estimates of devil population size. However, prevalence and force of infection were the lowest when devil population size and tumour genetic diversity was the highest. This could be due to either differential virulence or transmissibility in tumour lineages or the development of host defence strategies against infection. Our results support the view that evolutionary processes and epidemiological trade‐offs can drive host‐pathogen coexistence, even when disease‐induced mortality is extremely high. We highlight the importance of integrating pathogen and population evolutionary interactions to better understand long‐term epidemic dynamics and evaluating disease control strategies.