Novel infectious diseases, particularly those caused by fungal pathogens, pose considerable risks to global biodiversity. The amphibian chytrid fungus (Batrachochytrium dendrobatidis, Bd) has ...demonstrated the scale of the threat, having caused the greatest recorded loss of vertebrate biodiversity attributable to a pathogen. Despite catastrophic declines on several continents, many affected species have experienced population recoveries after epidemics. However, the potential ongoing threat of endemic Bd in these recovered or recovering populations is still poorly understood. We investigated the threat of endemic Bd to frog populations that recovered after initial precipitous declines, focusing on the endangered rainforest frog Mixophyes fleayi. We conducted extensive field surveys over 4 years at three independent sites in eastern Australia. First, we compared Bd infection prevalence and infection intensities within frog communities to reveal species‐specific infection patterns. Then, we analyzed mark‐recapture data of M. fleayi to estimate the impact of Bd infection intensity on apparent mortality rates and Bd infection dynamics. We found that M. fleayi had lower infection intensities than sympatric frogs across the three sites, and cleared infections at higher rates than they gained infections throughout the study period. By incorporating time‐varying individual infection intensities, we show that healthy M. fleayi populations persist despite increased apparent mortality associated with infrequent high Bd loads. Infection dynamics were influenced by environmental conditions, with Bd prevalence, infection intensity, and rates of gaining infection associated with lower temperatures and increased rainfall. However, mortality remained constant year‐round despite these fluctuations in Bd infections, suggesting major mortality events did not occur over the study period. Together, our results demonstrate that while Bd is still a potential threat to recovered populations of M. fleayi, high rates of clearing infections and generally low average infection loads likely minimize mortality caused by Bd. Our results are consistent with pathogen resistance contributing to the coexistence of M. fleayi with endemic Bd. We emphasize the importance of incorporating infection intensity into disease models rather than infection status alone. Similar population and infection dynamics likely exist within other recovered amphibian‐Bd systems around the globe, promising longer‐term persistence in the face of endemic chytridiomycosis.
Abstract
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.
Changes in species distributions open novel parasite transmission routes at the human–wildlife interface, yet the strength of biotic and biogeographical factors that prevent or facilitate parasite ...host shifting are not well understood. We investigated global patterns of helminth parasite (Nematoda, Cestoda, Trematoda) sharing between mammalian wildlife species and domestic mammal hosts (including humans) using >24,000 unique country‐level records of host–parasite associations. We used hierarchical modelling and species trait data to determine possible drivers of the level of parasite sharing between wildlife species and either humans or domestic animal hosts. We found the diet of wildlife species to be a strong predictor of levels of helminth parasite sharing with humans and domestic animals, followed by a moderate effect of zoogeographical region and minor effects of species’ habitat and climatic niches. Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species (including humans). These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species. If the dietary profile and position in the trophic chain of a wildlife species largely drives its level of helminth parasite sharing with humans/domestic animals, future range shifts of host species that result in novel trophic interactions may likely increase parasite host shifting and have important ramifications for human and animal health.
Changes in species distributions open novel parasite transmission routes at the human–wildlife interface, yet the factors that prevent or facilitate parasite host shifting are not well understood. We investigated global patterns of helminth parasite sharing between mammalian wildlife species and domestic mammal hosts (including humans). Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species. These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species.
The fungal skin disease, chytridiomycosis (caused by
and
), has caused amphibian declines and extinctions globally since its emergence. Characterizing the host immune response to chytridiomycosis has ...been a focus of study with the aim of disease mitigation. However, many aspects of the innate and adaptive arms of this response are still poorly understood, likely due to the wide range of species' responses to infection. In this paper we provide an overview of expected immunological responses (with inference based on amphibian and mammalian immunology), together with a synthesis of current knowledge about these responses for the amphibian-chytridiomycosis system. We structure our review around four key immune stages: (1) the naïve immunocompetent state, (2) immune defenses that are always present (constitutive defenses), (3) mechanisms for recognition of a pathogen threat and innate immune defenses, and (4) adaptive immune responses. We also evaluate the current hot topics of immunosuppression and immunopathology in chytridiomycosis, and discuss their respective roles in pathogenesis. Our synthesis reveals that susceptibility to chytridiomycosis is likely to be multifactorial. Susceptible amphibians appear to have ineffective constitutive and innate defenses, and a late-stage response characterized by immunopathology and Bd-induced suppression of lymphocyte responses. Overall, we identify substantial gaps in current knowledge, particularly concerning the entire innate immune response (mechanisms of initial pathogen detection and possible immunoevasion by Bd, degree of activation and efficacy of the innate immune response, the unexpected absence of innate leukocyte infiltration, and the cause and role of late-stage immunopathology in pathogenesis). There are also gaps concerning most of the adaptive immune system (the relative importance of B and T cell responses for pathogen clearance, the capacity and extent of immunological memory, and specific mechanisms of pathogen-induced immunosuppression). Improving our capacity for amphibian immunological research will require selection of an appropriate Bd-susceptible model species, the development of taxon-specific affinity reagents and cell lines for functional assays, and the application of a suite of conventional and emerging immunological methods. Despite current knowledge gaps, immunological research remains a promising avenue for amphibian conservation management.
Amphibians are among the vertebrate groups suffering great losses of biodiversity due to a variety of causes including diseases, such as chytridiomycosis (caused by the fungal pathogens ...Batrachochytrium dendrobatidis and B. salamandrivorans). The amphibian metamorphic period has been identified as being particularly vulnerable to chytridiomycosis, with dramatic physiological and immunological reorganisation likely contributing to this vulnerability. Here, we overview the processes behind these changes at metamorphosis and then perform a systematic literature review to capture the breadth of empirical research performed over the last two decades on the metamorphic immune response. We found that few studies focused specifically on the immune response during the peri-metamorphic stages of amphibian development and fewer still on the implications of their findings with respect to chytridiomycosis. We recommend future studies consider components of the immune system that are currently under-represented in the literature on amphibian metamorphosis, particularly pathogen recognition pathways. Although logistically challenging, we suggest varying the timing of exposure to Bd across metamorphosis to examine the relative importance of pathogen evasion, suppression or dysregulation of the immune system. We also suggest elucidating the underlying mechanisms of the increased susceptibility to chytridiomycosis at metamorphosis and the associated implications for population persistence. For species that overlap a distribution where Bd/Bsal are now endemic, we recommend a greater focus on management strategies that consider the important peri-metamorphic period.
•Amphibian metamorphosis is a period of extensive immune system restructuring.•Heightened metamorphic vulnerability likely impacts disease dynamics.•More research is needed to understand immunity to chytridiomycosis at metamorphosis.
Amphibian infection tolerance to chytridiomycosis Grogan, Laura F; Mangan, Madelyn J; McCallum, Hamish I
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
07/2023, Letnik:
378, Številka:
1882
Journal Article
Recenzirano
Odprti dostop
Animal defences against infection involve two distinct but complementary mechanisms: tolerance and resistance. Tolerance measures the animal's ability to limit detrimental effects from a given ...infection, whereas resistance is the ability to limit the intensity of that infection. Tolerance is a valuable defence for highly prevalent, persistent or endemic infections where mitigation strategies based on traditional resistance mechanisms are less effective or evolutionarily stable. Selective breeding of amphibians for enhanced tolerance to
spp
has been suggested as a strategy for mitigating the impacts of the fungal disease, chytridiomycosis. Here, we define infection tolerance and resistance in the context of chytridiomycosis, present evidence for variation in tolerance to chytridiomycosis, and explore epidemiological, ecological and evolutionary implications of tolerance to chytridiomycosis. We found that exposure risk and environmental moderation of infection burdens are major confounders of resistance and tolerance, chytridiomycosis is primarily characterized by variation in constitutive rather than adaptive resistance, tolerance is epidemiologically important in driving pathogen spread and maintenance, heterogeneity of tolerance leads to ecological trade-offs, and natural selection for resistance and tolerance is likely to be dilute. Improving our understanding of infection tolerance broadens our capacity for mitigating the ongoing impacts of emerging infectious diseases such as chytridiomycosis. This article is part of the theme issue 'Amphibian immunity: stress, disease and ecoimmunology'.
Pathogen spillover during land conversion Faust, Christina L.; McCallum, Hamish I.; Bloomfield, Laura S. P. ...
Ecology letters,
April 2018, 2018-04-00, 20180401, Letnik:
21, Številka:
4
Journal Article
Recenzirano
Odprti dostop
Pathogen spillover from wildlife to domestic animals and humans, and the reverse, has caused significant epidemics and pandemics worldwide. Although pathogen emergence has been linked to ...anthropogenic land conversion, a general framework to disentangle underlying processes is lacking. We develop a multi‐host model for pathogen transmission between species inhabiting intact and converted habitat. Interspecies contacts and host populations vary with the proportion of land converted; enabling us to quantify infection risk across a changing landscape. In a range of scenarios, the highest spillover risk occurs at intermediate levels of habitat loss, whereas the largest, but rarest, epidemics occur at extremes of land conversion. This framework provides insights into the mechanisms driving disease emergence and spillover during land conversion. The finding that the risk of spillover is highest at intermediate levels of habitat loss provides important guidance for conservation and public health policy.
The amphibian chytrid fungus
Batrachochytrium dendrobatidis
(
Bd
) has caused catastrophic frog declines on several continents, but disease outcome is mediated by a number of factors. Host life stage ...is an important consideration and many studies have highlighted the vulnerability of recently metamorphosed or juvenile frogs compared to adults. The majority of these studies have taken place in a laboratory setting, and there is a general paucity of longitudinal field studies investigating the influence of life stage on disease outcome. In this study, we assessed the effect of endemic
Bd
on juvenile
Mixophyes fleayi
(Fleay’s barred frog) in subtropical eastern Australian rainforest. Using photographic mark-recapture, we made 386 captures of 116 individuals and investigated the effect of
Bd
infection intensity on the apparent mortality rates of frogs using a multievent model correcting for infection state misclassification. We found that neither
Bd
infection status nor infection intensity predicted mortality in juvenile frogs, counter to the expectation that early life stages are more vulnerable to disease, despite average high infection prevalence (0.35, 95% HDPI 0.14, 0.52). Additionally, we found that observed infection prevalence and intensity were somewhat lower for juveniles than adults. Our results indicate that in this
Bd
-recovered species, the realized impacts of chytridiomycosis on juveniles were apparently low, likely resulting in high recruitment contributing to population stability. We highlight the importance of investigating factors relating to disease outcome in a field setting and make recommendations for future studies.
Although cancer rarely acts as an infectious disease, a recently emerged transmissible cancer in Tasmanian devils (Sarcophilus harrisii) is virtually 100% fatal. Devil facial tumour disease (DFTD) ...has swept across nearly the entire species' range, resulting in localized declines exceeding 90% and an overall species decline of more than 80% in less than 20 years. Despite epidemiological models that predict extinction, populations in long-diseased sites persist. Here we report rare genomic evidence of a rapid, parallel evolutionary response to strong selection imposed by a wildlife disease. We identify two genomic regions that contain genes related to immune function or cancer risk in humans that exhibit concordant signatures of selection across three populations. DFTD spreads between hosts by suppressing and evading the immune system, and our results suggest that hosts are evolving immune-modulated resistance that could aid in species persistence in the face of this devastating disease.
Apex predators are important in protecting biodiversity through top‐down influence on food webs. Their loss is linked with competitive release of invasive mesopredators and species extinctions. The ...Tasmanian devil (Sarcophilus harrisii) has experienced severe declines over a 15‐yr period as a novel transmissible cancer has spread across its current geographic range. We surveyed the mammalian community, using hair traps, across the spatial extent of the devil's progressive population decline. We found increased activity of alien invasive species (feral cats, black rats), and reduced small and medium‐sized native prey species in response to the timing of the decline. In areas of long‐term devil decline, invasive species comprised a significantly larger proportion of the community. The results provide evidence that the devil plays a keystone role in Tasmania's ecosystem with their decline linked to a shift toward an invasive state and biodiversity loss in one of Australia's most intact faunal communities.
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