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1. The macroecology and evolution of avian competence for Borrelia burgdorferi

   https://doi.org/10.1111/geb.13256  

   Becker, Daniel J. ; Han, Barbara A. ; Kamath, ed., Pauline ( January 2021 , Global Ecology and Biogeography)

   Prediction of novel reservoirs of zoonotic pathogens would be improved by the identification of interspecific drivers of host competence (i.e., the ability to transmit pathogens to new hosts or vectors). Tick‐borne pathogens can provide a useful model system, because larvae become infected only when feeding on a competent host during their first blood meal. For tick‐borne diseases, competence has been studied best forBorrelia burgdorferisensu lato (Bbsl), which causes Lyme borreliosis. Major reservoirs include several small mammal species, but birds might play an under‐recognized role in human risk given their ability to disperse infected ticks across large spatial scales. Here, we provide a global synthesis of the ecological and evolutionary factors that determine the ability of bird species to infect larval ticks withBbsl.

   Global.

   1983–2019.

   Birds.

   We compiled a dataset ofBbsl competence across 183 bird species and applied meta‐analysis, phylogenetic factorization and boosted regression trees to describe spatial and temporal patterns in competence, characterize its phylogenetic distribution across birds, reconstruct its evolution and evaluate the trait profiles associated with competent avian species.

   Half of the sampled bird species show evidence of competence forBbsl. Competence displays moderate phylogenetic signal, has evolved multiple times across bird species and is pronounced in the genusTurdus. Trait‐based analyses distinguished competent birds with 80% accuracy and showed that such species have low baseline corticosterone, exist on both ends of the pace‐of‐life continuum, breed and winter at high latitudes and have broad migratory movements into their breeding range. We used these trait profiles to predict various likely but unsampled competent species, including novel concentrations of avian reservoirs within the Neotropics.

   Our results can generate new hypotheses for how birds contribute to the dynamics of tick‐borne pathogens and help to prioritize surveillance of likely but unsampled competent birds. Our findings also emphasize that birds display under‐recognized variation in their contributions to enzootic cycles ofBbsl and the broader need to consider competence in ecological and predictive studies of multi‐host pathogens.

    

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2. Ecological Predictors of Zoonotic Vector Status Among Dermacentor Ticks (Acari: Ixodidae): A Trait-Based Approach

   https://doi.org/10.1093/jme/tjac125  

   Martin, Jessica T. ; Fischhoff, Ilya R. ; Castellanos, Adrian A. ; Han, Barbara A. ; Gaff, ed., Holly ( September 2022 , Journal of Medical Entomology)

   Increasing incidence of tick-borne human diseases and geographic range expansion of tick vectors elevates the importance of research on characteristics of tick species that transmit pathogens. Despite their global distribution and role as vectors of pathogens such as Rickettsia spp., ticks in the genus Dermacentor Koch, 1844 (Acari: Ixodidae) have recently received less attention than ticks in the genus Ixodes Latreille, 1795 (Acari: Ixodidae). To address this knowledge gap, we compiled an extensive database of Dermacentor tick traits, including morphological characteristics, host range, and geographic distribution. Zoonotic vector status was determined by compiling information about zoonotic pathogens found in Dermacentor species derived from primary literature and data repositories. We trained a machine learning algorithm on this data set to assess which traits were the most important predictors of zoonotic vector status. Our model successfully classified vector species with ~84% accuracy (mean AUC) and identified two additional Dermacentor species as potential zoonotic vectors. Our results suggest that Dermacentor species that are most likely to be zoonotic vectors are broad ranging, both in terms of the range of hosts they infest and the range of ecoregions across which they are found, and also tend to have large hypostomes and be small-bodied as immature ticks. Beyond the patterns we observed, high spatial and species-level resolution of this new, synthetic dataset has the potential to support future analyses of public health relevance, including species distribution modeling and predictive analytics, to draw attention to emerging or newly identified Dermacentor species that warrant closer monitoring for zoonotic pathogens.

    

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3. Reactivation of latent infections with migration shapes population-level disease dynamics

   https://doi.org/10.1098/rspb.2020.1829  

   Becker, Daniel J. ; Ketterson, Ellen D. ; Hall, Richard J. ( September 2020 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Annual migration is common across animal taxa and can dramatically shape the spatial and temporal patterns of infectious disease. Although migration can decrease infection prevalence in some contexts, these energetically costly long-distance movements can also have immunosuppressive effects that may interact with transmission processes in complex ways. Here, we develop a mechanistic model for the reactivation of latent infections driven by physiological changes or energetic costs associated with migration (i.e. ‘migratory relapse’) and its effects on disease dynamics. We determine conditions under which migratory relapse can amplify or reduce infection prevalence across pathogen and host traits (e.g. infectious periods, virulence, overwinter survival, timing of relapse) and transmission phenologies. We show that relapse at either the start or end of migration can dramatically increase prevalence across the annual cycle and may be crucial for maintaining pathogens with low transmissibility and short infectious periods in migratory populations. Conversely, relapse at the start of migration can reduce the prevalence of highly virulent pathogens by amplifying culling of infected hosts during costly migration, especially for highly transmissible pathogens and those transmitted during migration or the breeding season. Our study provides a mechanistic foundation for understanding the spatio-temporal patterns of relapsing infections in migratory hosts, with implications for zoonotic surveillance and understanding how infection patterns will respond to shifts in migratory propensity associated with environmental change. Further, our work suggests incorporating within-host processes into population-level models of pathogen transmission may be crucial for reconciling the range of migration–infection relationships observed across migratory species. 

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4. Mixed-species assemblages and disease: the importance of differential vector and parasite attraction in transmission dynamics

   https://doi.org/10.1098/rstb.2022.0109  

   Trillo, Paula A. ; Bernal, Ximena E. ; Hall, Richard J. ( June 2023 , Philosophical Transactions of the Royal Society B: Biological Sciences)

   Individuals from multiple species often aggregate at resources, group to facilitate defense and foraging, or are brought together by human activity. While it is well-documented that host-seeking disease vectors and parasites show biases in their responses to cues from different hosts, the influence of mixed-species assemblages on disease dynamics has received limited attention. Here, we synthesize relevant research in host-specific vector and parasite bias. To better understand how vector and parasite biases influence infection, we provide a conceptual framework describing cue-oriented vector and parasite host-seeking behaviour as a two-stage process that encompasses attraction of these enemies to the assemblage and their choice of hosts once at the assemblage. We illustrate this framework, developing a case study of mixed-species frog assemblages, where frog-biting midges transmit trypanosomes. Finally, we present a mathematical model that investigates how host species composition and asymmetries in vector attraction modulate transmission dynamics in mixed-species assemblages. We argue that differential attraction of vectors by hosts can have important consequences for disease transmission within mixed-species assemblages, with implications for wildlife conservation and zoonotic disease. 

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5. 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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