Chytrid fungus infection in alpine tree frogs is associated with individual heterozygosity and population isolation but not population-genetic diversity

Chytridiomycosis, a disease caused by the emerging fungus Batrachochytrium dendrobatidis (Bd), has been implicated in the decline of over 500 amphibian species. Population declines could have important genetic consequences, including reduced genetic diversity. We contrasted genetic diversity among both long-Bd-exposed and unexposed populations of the south-east Australian alpine tree frog (Litoria verreauxii alpina) across its range. At the population level, we found no significant differences in genetic diversity between Bd-exposed and unexposed populations. Encouragingly, even Bd-infected remnant populations that are now highly isolated maintain genetic diversity comparable to populations in which Bd is absent. Spatial genetic structure among populations followed an isolation-by-distance pattern, suggesting restricted movement among remnant populations. At the individual level, greater heterozygosity was associated with reduced probability of infection. Loss of genetic diversity in remnant populations that survived chytridiomycosis epidemics does not appear to be a threat to L. v. alpina. We suggest several factors underpinning maintenance of genetic diversity: (1) remnant populations have remained large enough to avoid losses of genetic diversity; (2) many individuals in the population are able to breed once before succumbing to disease; and (3) juveniles in the terrestrial environment have low exposure to Bd, providing an annual ‘reservoir’ of genetic diversity. The association between individual heterozygosity and infection status suggests that, while other work has shown all breeding adults are typically killed by Bd, males with greater heterozygosity may survive longer and obtain fitness benefits through extended breeding opportunities. Our results highlight the critical role of life history in mitigating the impacts of Bd infection for some amphibian species, but we infer that increased isolation as a result of disease-induced population extirpations will enhance population differentiation and thus biogeographic structure

Response to comment on 'Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity'

Lambert et al. question our retrospective and holistic epidemiological assessment of the role of chytridiomycosis in amphibian declines. Their alternative assessment is narrow and provides an incomplete evaluation of evidence. Adopting this approach limits understanding of infectious disease impacts and hampers conservation efforts. We reaffirm that our study provides unambiguous evidence that chytridiomycosis has affected at least 501 amphibian species

High adult mortality in disease-challenged frog populations increases vulnerability to drought

Pathogen emergence can drive major changes in host population demography, with implications for population dynamics and sensitivity to environmental fluctuations. The amphibian disease chytridiomycosis, caused by infection with the fungal pathogen Batrachochytrium dendrobatidis (Bd), is implicated in the severe decline of over 200 amphibian species. In species that have declined but not become extinct, Bd persists and can cause substantial ongoing mortality. High rates of mortality associated with Bd may drive major changes in host demography, but this process is poorly understood. Here, we compared population age structure of Bd-infected populations, Bd-free populations, and museum specimens collected prior to Bd emergence for the endangered Australian frog, Litoria verreauxii alpina (alpine tree frog). We then used population simulations to investigate how pathogen-associated demographic shifts affect the ability of populations to persist in stochastic environments. We found that Bd-infected populations have a severely truncated age structure associated with very high rates of annual adult mortality. Near-complete annual adult turnover in Bd-infected populations means that individuals breed once, compared with Bd-free populations where adults may breed across multiple years. Our simulations showed that truncated age structure erodes the capacity of populations to withstand periodic recruitment failure; a common challenge for species reproducing in uncertain environments. We document previously undescribed demographic shifts associated with a globally emerging pathogen and demonstrate how these shifts alter host ecology. Truncation of age structure associated with Bd effectively reduces host niche width, and can help explain the contraction of L. v. alpina to perennial waterbodies where the risk of drought-induced recruitment failure is low. Reduced capacity to tolerate other sources of mortality may explain variation in decline severity among other chytridiomycosis-challenged species and highlights the potential to mitigate disease impacts through minimising other sources of mortality

Evolution of resistance to chytridiomycosis is associated with a robust early immune response

Potentiating the evolution of immunity is a promising strategy for addressing biodiversity diseases. Assisted selection for infection resistance may enable the recovery and persistence of amphibians threatened by chytridiomycosis, a devastating fungal skin disease threatening hundreds of species globally. However, knowledge of the mechanisms involved in the natural evolution of immunity to chytridiomycosis is limited. Understanding the mechanisms of such resistance may help speed-assisted selection. Using a transcriptomics approach, we examined gene expression responses of endangered alpine tree frogs (Litoria verreauxii alpina) to subclinical infection, comparing two long-exposed populations with a naïve population. We performed a blinded, randomized and controlled exposure experiment, collecting skin, liver and spleen tissues at 4, 8 and 14\ua0days postexposure from 51 wild-caught captively reared infection-naïve adult frogs for transcriptome assembly and differential gene expression analyses. We analysed our results in conjunction with infection intensity data, and the results of a large clinical survival experiment run concurrently with individuals from the same clutches. Here, we show that frogs from an evolutionarily long-exposed and phenotypically more resistant population of the highly susceptible alpine tree frog demonstrate a more robust innate and adaptive immune response at the critical early subclinical stage of infection when compared with two more susceptible populations. These results are consistent with the occurrence of evolution of resistance against chytridiomycosis, help to explain underlying resistance mechanisms, and provide genes of potential interest and sequence data for future research. We recommend further investigation of cell-mediated immunity pathways, the role of interferons and mechanisms of lymphocyte suppression

Red hot frogs:Identifying the Australian frogs most at risk of extinction

More than a third of the world’s amphibian species are listed as Threatened or Extinct, with a recent assessment identifying 45 Australian frogs (18.4% of the currently recognised species) as ‘Threatened’ based on IUCN criteria. We applied structured expert elicitation to 26 frogs assessed as Critically Endangered and Endangered to estimate their probability of extinction by 2040. We also investigated whether participant experience (measured as a self-assigned categorical score, i.e. ‘expert’ or ‘non-expert’) influenced the estimates. Collation and analysis of participant opinion indicated that eight species are at high risk (>50% chance) of becoming extinct by 2040, with the disease chytridiomycosis identified as the primary threat. A further five species are at moderate–high risk (30–50% chance), primarily due to climate change. Fourteen of the 26 frog species are endemic to Queensland, with many species restricted to small geographic ranges that are susceptible to stochastic events (e.g. a severe heatwave or a large bushfire). Experts were more likely to rate extinction probability higher for poorly known species (those with <10 experts), while non-experts were more likely to rate extinction probability higher for better-known species. However, scores converged following discussion, indicating that there was greater consensus in the estimates of extinction probability. Increased resourcing and management intervention are urgently needed to avert future extinctions of Australia’s frogs. Key priorities include developing and supporting captive management and establishing or extending in-situ population refuges to alleviate the impacts of disease and climate change

Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease

Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a 1‐day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the amphibian fungal pathogen Batrachochytrium salamandrivorans. Despite the inevitable uncertainty, experts suggested and discussed several possible strategies. However, their recommendations were undermined by imperfect initial definitions of the objectives and scope of management. This problem is likely to arise in most real‐world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial–temporal scale of mitigation decisions. Managers are commonly under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes

Half of the habitat of Australia\u27s highly imperilled narrow-range species is outside protected areas

Globally, species with small distributions face disproportionate extinction risk, with the impacts of land use change more likely to have catastrophic consequences. Identifying, protecting and managing sites where such species occur is essential for minimising their extinction risk. Yet across Australia, efforts to protect and manage such species\u27 habitats have hitherto been insufficient. Here, we present an example of an analytical and interpretive pathway for the conservation of such species, for a continental-scale case study. We identified 305 Critically Endangered species that have narrow ranges (\u3c20,000 km2), and are distributed in fewer than six discrete patches. We refined existing species\u27 habitat maps with advice from 18 experts via a modified Delphi approach. We assessed how much of each species\u27 habitat is outside protected areas and considered to have agricultural capability, potentially elevating risk of conversion. We identified ∼85,000 km2 of habitat (∼1% of Australia) for these 305 species that must receive protection and management if the nation is going to meet its commitment to halt new extinctions. Approximately half of this habitat is outside the protected area estate, including the entire distribution of 39 species. Approximately 55% of habitat outside of protected areas had at least some agricultural capability. Protecting and managing the habitats of these narrow-range species should be a high priority in state and national conservation policy. Our case study serves as a template for the identification of important habitat for threatened species and could be applied in other regions of the world

Use of micro CHP plants to support the local operation of electric heat pumps

Fig. 1. Global distribution of chytridiomycosis-associated amphibian species declines. Bar plots indicate the number (N) of declined species, grouped by continental area and classified by decline severity. Brazilian species are plotted separately from all other South American species (South America W); Mesoamerica includes Central America, Mexico, and the Caribbean Islands; and Oceania includes Australia and New Zealand. No declines have been reported in Asia. n, total number of declines by region. [Photo credits (clockwise from top left): Anaxyrus boreas, C. Brown, U.S. Geological Survey; Atelopus varius, B.G.; Salamandra salamandra, D. Descouens, Wikimedia Commons; Telmatobius sanborni, I.D.l.R; Cycloramphus boraceiensis, L.F.T.; Cardioglossa melanogaster, M.H.; and Pseudophryne corroboree, C. Doughty