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1. 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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2. An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds

   https://doi.org/10.1111/1365-2656.13117  

   Fecchio, Alan ; Bell, Jeffrey A. ; Bosholn, Mariane ; Vaughan, Jefferson A. ; Tkach, Vasyl V. ; Lutz, Holly L. ; Cueto, Victor R. ; Gorosito, Cristian A. ; González‐Acuña, Daniel ; Stromlund, Chad ; et al ( October 2019 , Journal of Animal Ecology)

   Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector‐transmitted parasites.

   Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity ofLeucocytozoon(an avian blood parasite) at site and species levels across the New World.

   To explore spatial patterns in infection probability and lineage diversity forLeucocytozoonparasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high‐resolution satellite remote‐sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly.

   Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence ofLeucocytozoonparasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected withLeucocytozoonincreased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes.

   Whereas temperature partially constrainsLeucocytozoondiversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, forLeucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector‐transmitted parasites. Unlike other vector‐transmitted diseases, our results show thatLeucocytozoondiversity and prevalence will likely decrease with warming temperatures.

    

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3. A simulated natural heatwave perturbs bumblebee immunity and resistance to infection

   https://doi.org/10.1111/1365-2656.14041  

   Tobin, Kerrigan B. ; Mandes, Rachel ; Martinez, Abraham ; Sadd, Ben M. ( January 2024 , Journal of Animal Ecology)

   As a consequence of ongoing climate change, heatwaves are predicted to increase in frequency, intensity, and duration in many regions. Such extreme events can shift organisms from thermal optima for physiology and behaviour, with the thermal stress hypothesis predicting reduced performance at temperatures where the maintenance of biological functions is energetically costly. Performance includes the ability to resist biotic stressors, including infectious diseases, with increased exposure to extreme temperatures having the potential to synergise with parasite infection.

   Climate change is a proposed threat to native bee pollinators, directly and through indirect effects on floral resources, but the thermal stress hypothesis, particularly pertaining to infectious disease resistance, has received limited attention. We exposed adultBombus impatiensbumblebee workers to simulated, ecologically relevant heatwave or control thermal regimes and assessed longevity, immunity, and resistance to concurrent or future parasite infections.

   We demonstrate that survival and induced antibacterial immunity are reduced following heatwaves. Supporting that heatwave exposure compromised immunity, the cost of immune activation was thermal regime dependent, with survival costs in control but not heatwave exposed bees. However, in the face of real infections, an inability to mount an optimal immune response will be detrimental, which was reflected by increased trypanosomatid parasite infections following heatwave exposure.

   These results demonstrate interactions between heatwave exposure and bumblebee performance, including immune and infection outcomes. Thus, the health of bumblebee pollinator populations may be affected through altered interactions with parasites and pathogens, in addition to other effects of extreme manifestations of climate change.

    

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4. Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

   https://doi.org/10.1111/1365-2656.13166  

   Becker, Daniel J. ; Albery, Gregory F. ; Kessler, Maureen K. ; Lunn, Tamika J. ; Falvo, Caylee A. ; Czirják, Gábor Á. ; Martin, Lynn B. ; Plowright, Raina K. ; Fenton, ed., Andy ( January 2020 , Journal of Animal Ecology)

   The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre‐empt infectious disease risks, especially in the context of how large‐scale factors such as urbanization affect defence by changing environmental conditions.

   We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large‐scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small‐scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods.

   We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence.

   We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed‐effects models that account for spatial variability while also allowing researchers to account for both individual‐ and habitat‐level covariates.

   We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large‐scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large‐scale field studies with small‐scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta‐analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual‐ to habitat‐level insights about the drivers of immune defence and help predict where environmental change may most alter infectious disease risk.

    

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5. Natural history and ecological effects on the establishment and fate of Florida carpenter ant cadavers infected by the parasitic manipulator Ophiocordyceps camponoti ‐ floridani

   https://doi.org/10.1111/1365-2435.14224  

   Will, Ian ; Linehan, Sara ; Jenkins, David G. ; de Bekker, Charissa ( November 2022 , Functional Ecology)

   Ophiocordycepsfungi manipulate the behaviour of their ant hosts to produce a summit disease phenotype, thereby establishing infected ant cadavers onto vegetation at elevated positions suitable for fungal growth and transmission. Multiple environmental and ecological factors have been proposed to shape the timing, positioning and outcome of these manipulations.

   We conducted a long‐term field study ofOphiocordyceps camponoti‐floridaniinfections ofCamponotus floridanusants—the Florida zombie ants. We propose and refine hypotheses on the factors that shape infection outcomes by tracking the occurrence of and fungal growth from hundreds of ant cadavers. We modelled and report these data in relation to weather, light, vegetation and attack by hyperparasites.

   We investigated environmental factors that could affect the occurrence and location of newly manipulated ant cadavers. New cadaver occurrence was preferentially biased towards epiphyticTillandsiabromeliads, canopy openness and summer weather conditions (an interactive effect of temperature, humidity and precipitation). Furthermore, we suggest that incident light at the individual cadaver level reflects microhabitat choice by manipulated ants or selective pressure on cadaver maintenance for conditions that improve fungal survival.

   We also asked which environmental conditions affect fungal fitness. Continued fungal development of reproductive structures and putative transmission increased with moist weather conditions (interaction of humidity and precipitation) and canopy openness, while being reduced by hyperparasitic mycoparasite infections. Moreover, under the most open canopy conditions, we found an atypicalOphiocordycepsgrowth morphology that could represent a plastic response to conditions influenced by high light levels.

   Taken together, we explore general trends and the effects of various ecological conditions on host and parasite disease outcomes in the Florida zombie ant system. These insights from the field can be used to inform experimental laboratory setups that directly test the effects of biotic and abiotic factors on fungus–ant interactions or aim to uncover underlying molecular mechanisms.

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

    

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