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Life-history trade-offs can mediate population declines following perturbations, and early reproduction should be favoured when adult survival is impacted more than juvenile survival. In Tasmanian devils (Sarcophilus harrisii), following the emergence of a transmissible cancer that caused steep population declines, females started to breed precocially (i.e. at age 1 instead of 2 years old). Here, using 18 years of mark–recapture data from a site where the disease was present (Freycinet Peninsula, Tasmania, Australia), we tested whether: (i) the probability of 1-yea-old females breeding continued to increase over time; (ii) there was a relationship between body size and breeding success for either 1-year-old or adult females; and (iii) there was inbreeding depression in breeding success for either age category. We show that the probability of 1-year-old females breeding did not increase between 2003 and 2021, and that the proportion of precocially breeding females remains at around 40%. We also show that there was no effect of skeletal body size on the probability of breeding, but heavier females were always more likely to breed. Finally, we found no evidence for inbreeding depression in breeding success. We discuss our results in the context of possible constraints by way of limitations to growth in the offspring of precocially breeding females. 

Abstract Herein, we rebut the critique of Patton et al. (2020), entitled, “No evidence that a transmissible cancer has shifted from emergence to endemism”, by Stammnitz et al. (2024). First and foremost, the authors do not conduct any phylogenetic or epidemiological analyses to rebut the inferences from the main results of the Patton et al. (2020) article, rendering the title of their rebuttal without evidence or merit. Additionally, Stammnitz et al. (2024) present a phylogenetic tree based on only 32 copy number variants (not typically used in phylogenetic analyses and evolve in a completely different way than DNA sequences) to “rebut” our tree that was inferred from 436.1 kb of sequence data and nearly two orders of magnitude more parsimony-informative sites (2520 SNPs). As such it is not surprising that their phylogeny did not have a similar branching pattern to ours, given that support for each branch of their tree was weak and the essentially formed a polytomy. That is, one could rotate their resulting tree in any direction and by nature, it would not match ours. While the authors are correct that we used suboptimal filtering of our raw whole genome sequencing data, re-analyses of the data with 30X coverage, as suggested, resulted in a mutation rate similar to that reported in Stammnitz et al. (2024). Most importantly, when we re-analyzed our data, as well as Stammnitz et al.’s own data, the results of the Patton et al. (2020) article are supported with both datasets. That is, the effective transmission rate of DFTD has transitioned over time to approach one, suggesting endemism; and, the spread of DFTD is rapid and omnidirectional despite the observed east-to-west wave of spread. Overall, Stammnitz et al. (2024) not only fail to provide evidence to contradict the findings of Patton et al. (2020), but rather help support the results with their own data. 

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. 

Apex consumers are declining worldwide. While the effects of apex predator declines on ecosystems are widely documented, the cascading effects of apex scavenger declines are poorly understood. We evaluated whether disease‐induced declines of an apex scavenger, the Tasmanian devil (Sarcophilus harrisii), increased carrion use by invertebrate scavengers. We manipulated devil access to 36 carcasses across a gradient of devil density from east to west Tasmania and measured carcass use by invertebrates. We found the amount of carcass removed within 5 days was 3.58 times lower at sites with the lowest devil densities. Adult carrion beetle (Ptomaphila lacrymosa) and blow fly (Calliphoridae) larvae abundances were two times higher at open‐access carcasses at low‐density sites than at intermediate‐ and high‐density sites. Adult beetles persisted for 10 days at the low‐density site but declined after 5 days when devils had access to carcasses in intermediate‐ and high‐density sites. Blow fly larvae abundance was not affected by devils in the low‐density site but decreased with devil access in intermediate‐ and high‐density sites. Our results suggest that apex scavenger declines may increase invertebrate scavenger abundance and their contribution to carrion decomposition, with potential cascading effects on nutrient cycling and ecosystems. 

Global apex scavenger declines strongly alter food web dynamics, but studies rarely test whether trophic downgrading impacts ecosystem functions. Here, we leverage a unique, disease‐induced gradient in Tasmanian devil (Sarcophilus harrisi) population densities to assess feedbacks between carcass persistence, subordinate scavenger guilds, and biogeochemical cycling. We further explored interkingdom and seasonal interactions by manipulating carcass access and replicating experiments in warmer, drier summer versus cooler, wetter winter periods. We show Tasmanian devil declines significantly extend carcass persistence and increase the flux of carcass‐derived nutrients belowground (e.g., by 18–134‐fold for ammonium). Greater nutrient availability reduces soil microbiome diversity by up to 26%, increasing the relative abundance of putative zoonotic pathogens. Nutrient subsidies also shift microbial communities toward faster‐growing taxa that invest less energy in resource acquisition, with implications for soil carbon sequestration. Rates of carcass decomposition were reduced in the winter, dampening soil biogeochemical responses and interkingdom competition. Notably, while less efficient scavenger guilds clearly facilitate carcass consumption, they were not able to fill the functional role of apex scavengers. Our study illustrates how trophic downgrading effects can ripple across all levels of ecological organization. 

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 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. 

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.