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1. Patterns of host–parasite coinvasion promote enemy release and specialist parasite spillover

   https://doi.org/10.1111/1365-2656.13910  

   Schatz, Annakate M. ; Park, Andrew W. ( April 2023 , Journal of Animal Ecology)

   Species invasion and redistribution, driven by climate change and other anthropogenic influences, alter global biodiversity patterns and disrupt ecosystems. As host species move, they can bring their associated parasites with them, potentially infecting resident species, or leave their parasites behind, enhancing their competitive ability in their new ranges. General rules to predict why invading hosts will retain some parasites but not others are relatively unexplored, and the potential predictors are numerous, ranging from parasite life history to host community composition.

   In this study, we focus on the parasite retention process during host invasion. We used the Global Mammal Parasite Database to identify terrestrial mammal hosts sampled for parasites in both native and non‐native ranges. We then selected predictors likely to play a role in parasite retention, such as parasite type, parasite specialism, species composition of the invaded community, and the invading host's phylogenetic or trait‐based similarity to the new community.

   We modelled parasite retention using boosted regression trees, with a suite of 25 predictors describing parasite and host community traits. We further tested the generality of our predictions by cross‐validating models on data for other hosts and invasion locations.

   Our results show that parasite retention is nonrandom and predictable across hosts and invasions. It is broadly shaped by parasite type and parasite specialism, with more specialist parasites that infect many closely related hosts more likely to be retained. This trend is pronounced across parasite types; helminths, however, show a more uniform likelihood of retention regardless of specificity.

   Overall, we see that most parasites are not retained (11% retained), meaning many invasive species may benefit from enemy release. However, species redistribution does have the potential to spread parasites, and this also has great relevance to understanding conservation implications of species invasions. We see that specialist parasites are most likely to coinvade with their hosts, which suggests that species closely related to the invasive hosts are most likely to be affected by parasite spillover.

    

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2. Beyond single host, single parasite interactions: Quantifying competence for complete multi‐host, multi‐parasite communities

   https://doi.org/10.1111/1365-2435.14068  

   Stewart Merrill, Tara E. ; Calhoun, Dana M. ; Johnson, Pieter T. J. ( May 2022 , Functional Ecology)

   Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, ‘competence’, is a critical currency for modelling transmission under community change and for testing diversity–disease theory. Despite the central role of competence in disease ecology, we lack a clear understanding of the factors that generate competence and drive its variation.

   We developed novel conceptual and quantitative approaches to systematically quantify competence for a multi‐host, multi‐parasite community. We applied our framework to an extensive dataset: five amphibian host species exposed to four parasitic trematode species across five ecologically realistic exposure doses. Together, this experimental design captured 20 host–parasite interactions while integrating important information on variation in parasite exposure. Using experimental infection assays, we measured multiple components of the infection process and combined them to produce competence estimates for each interaction.

   With directly estimated competence values, we asked which components of the infection process best explained variation in competence: barrier resistance (the initial fraction of administered parasites blocked from infecting a host), internal clearance (the fraction of established parasites lost over time) or pre‐transmission mortality (the probability of host death prior to transmission). We found that variation in competence among the 20 interactions was best explained by differences in barrier resistance and pre‐transmission mortality, underscoring the importance of host resistance and parasite pathogenicity in shaping competence.

   We also produced dose‐integrated estimates of competence that incorporated natural variation in exposure to address questions on the basis and extent of variation in competence. We found strong signals that host species identity shaped competence variation (as opposed to parasite species identity). While variation in infection outcomes across hosts, parasites, individuals and doses was considerable, individual heterogeneity was limited compared to among‐species differences. This finding highlights the robustness of our competence estimates and suggests that species‐level values may be strong predictors for community‐level transmission in natural systems.

   Competence emerges from distinct underlying processes and can have strong species‐level characteristics; thus, this property has great potential for linking mechanisms of infection to epidemiological patterns.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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3. Disease's hidden death toll: Using parasite aggregation patterns to quantify landscape‐level host mortality in a wildlife system

   https://doi.org/10.1111/1365-2656.13343  

   Wilber, Mark Q. ; Briggs, Cheryl J. ; Johnson, Pieter T. J. ; Cattadori, ed., Isabella ( September 2020 , Journal of Animal Ecology)

   World‐wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease‐induced mortality is likely even greater, but remains notoriously difficult to estimate—especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature.

   Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population‐ and landscape‐level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species.

   We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations.

   Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population‐level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape.

   The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite‐induced mortality can be applied to other host–parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts.

    

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4. The changing ecology of primate parasites: Insights from wild‐captive comparisons

   https://doi.org/10.1002/ajp.22991  

   Herrera, James P. ; Chakraborty, Debapriyo ; Rushmore, Julie ; Altizer, Sonia ; Nunn, Charles ( July 2019 , American Journal of Primatology)

   Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity—a rarely studied yet widespread human‐driven host movement—can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro‐ (helminths and arthropods) and micro‐parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally—including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector‐borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non‐close contact, including through fecal‐oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.

    

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5. Transcriptome assembly and differential gene expression of the invasive avian malaria parasite Plasmodium relictum in Hawaiʻi

   https://doi.org/10.1002/ece3.7401  

   Videvall, Elin ; Paxton, Kristina L. ; Campana, Michael G. ; Cassin‐Sackett, Loren ; Atkinson, Carter T. ; Fleischer, Robert C. ( March 2021 , Ecology and Evolution)

   The malaria parasitePlasmodium relictum(lineage GRW4) was introduced less than a century ago to the native avifauna of Hawaiʻi, where it has since caused major declines of endemic bird populations. One of the native bird species that is frequently infected with GRW4 is the Hawaiʻi ʻamakihi (Chlorodrepanis virens). To achieve a better understanding of the transcriptional activities of this virulent parasite, we performed a controlled challenge experiment of 15 ʻamakihi that were infected with GRW4. Blood samples containing malaria parasites were collected at two time points (intermediate and peak infection stages) from host individuals that were either experimentally infected by mosquitoes or inoculated with infected blood. We then used RNA sequencing to assemble a high‐quality blood transcriptome ofP. relictumGRW4, allowing us to quantify parasite expression levels inside individual birds. We found few significant differences (one to two transcripts) in GRW4 expression levels between host infection stages and between inoculation methods. However, 36 transcripts showed differential expression levels among all host individuals, indicating a potential presence of host‐specific gene regulation across hosts. To reduce the extinction risk of the remaining native bird species in Hawaiʻi, genetic resources of the localPlasmodiumlineage are needed to enable further molecular characterization of this parasite. Our newly built Hawaiian GRW4 transcriptome assembly, together with analyses of the parasite's transcriptional activities inside the blood of Hawaiʻi ʻamakihi, can provide us with important knowledge on how to combat this deadly avian disease in the future.

    

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