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1. Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns

   https://doi.org/10.3389/fmicb.2020.603046  

   Weiler, Jared ; Zilio, Giacomo ; Zeballos, Nathalie ; Nørgaard, Louise ; Conce Alberto, Winiffer D. ; Krenek, Sascha ; Kaltz, Oliver ; Bright, Lydia ( December 2020 , Frontiers in Microbiology)

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   Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of variation in this trait between strains can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum . We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains, with upper-bound values of broad-sense heritability >0.5 (intraclass correlation coefficients). Strain estimates of resistance were repeatable between laboratories and ranged from total resistance to near-complete susceptibility. Early (1 week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2–3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains ( r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system. 

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2. An experimental test of parasite adaptation to common versus rare host genotypes

   https://doi.org/10.1098/rsbl.2020.0210  

   Gibson, Amanda K. ; White, P. Signe ; Penley, McKenna J. ; de Roode, Jacobus C. ; Morran, Levi T. ( July 2020 , Biology Letters)

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   A core hypothesis in coevolutionary theory proposes that parasites adapt to specifically infect common host genotypes. Under this hypothesis, parasites function as agents of negative frequency-dependent selection, favouring rare host genotypes. This parasite-mediated advantage of rarity is key to the idea that parasites maintain genetic variation and select for outcrossing in host populations. Here, we report the results of an experimental test of parasite adaptation to common versus rare host genotypes. We selected the bacterial parasite Serratia marcescens to kill Caenorhabdiis elegans hosts in uneven mixtures of host genotypes. To examine the effect of commonness itself, independent of host identity, each of four host genotypes was represented as common or rare in experimental host mixtures. After experimental selection, we evaluated a parasite line's change in virulence—the selected fitness trait—on its rare and common host genotypes. Our results were consistent with a slight advantage for rare host genotypes: on average, parasites lost virulence against rare genotypes but not against common genotypes. The response varied substantially, however, with distinct patterns across host genotype mixtures. These findings support the potential for parasites to impose negative frequency-dependent selection, while emphasizing that the cost of being common may vary with host genotype. 

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3. Into the danger zone: How the within‐host distribution of parasites controls virulence

   https://doi.org/10.1111/ele.14352  

   Johnson, Pieter T. J. ; Stewart Merrill, Tara ; Calhoun, Dana M. ; McDevitt‐Galles, Travis ; Hobart, Brendan ( December 2023 , Ecology Letters)

   Despite the importance of virulence in epidemiological theory, the relative contributions of host and parasite to virulence outcomes remain poorly understood. Here, we use reciprocal cross experiments to disentangle the influence of host and parasite on core virulence components—infection and pathology—and understand dramatic differences in parasite‐induced malformations in California amphibians. Surveys across 319 populations revealed that amphibians' malformation risk was 2.7× greater in low‐elevation ponds, even while controlling for trematode infection load. Factorial experiments revealed that parasites from low‐elevation sites induced higher per‐parasite pathology (reduced host survival and growth), whereas there were no effects of host source on resistance or tolerance. Parasite populations also exhibited marked differences in within‐host distribution: ~90% of low‐elevation cysts aggregated around the hind limbs, relative to <60% from high‐elevation. This offers a novel, mechanistic basis for regional variation in parasite‐induced malformations while promoting a framework for partitioning host and parasite contributions to virulence.

    

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4. The evolution of parasite host range in heterogeneous host populations

   https://doi.org/10.1111/jeb.13608  

   Gibson, Amanda K. ; Baffoe‐Bonnie, Helena ; Penley, McKenna J. ; Lin, Julie ; Owens, Raythe ; Khalid, Arooj ; Morran, Levi T. ( March 2020 , Journal of Evolutionary Biology)

   Theory on the evolution of niche width argues that resource heterogeneity selects for niche breadth. For parasites, this theory predicts that parasite populations will evolve, or maintain, broader host ranges when selected in genetically diverse host populations relative to homogeneous host populations. To test this prediction, we selected the bacterial parasiteSerratia marcescensto killCaenorhabditis elegansin populations that were genetically heterogeneous (50% mix of two experimental genotypes) or homogeneous (100% of either genotype). After 20 rounds of selection, we compared the host range of selected parasites by measuring parasite fitness (i.e. virulence, the selected fitness trait) on the two focal host genotypes and on a novel host genotype. As predicted, heterogeneous host populations selected for parasites with a broader host range: these parasite populations gained or maintained virulence on all host genotypes. This result contrasted with selection in homogeneous populations of one host genotype. Here, host range contracted, with parasite populations gaining virulence on the focal host genotype and losing virulence on the novel host genotype. This pattern was not, however, repeated with selection in homogeneous populations of the second host genotype: these parasite populations did not gain virulence on the focal host genotype, nor did they lose virulence on the novel host genotype. Our results indicate that host heterogeneity can maintain broader host ranges in parasite populations. Individual host genotypes, however, vary in the degree to which they select for specialization in parasite populations.

    

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5. Multiple transmission routes sustain high prevalence of a virulent parasite in a butterfly host

   https://doi.org/10.1098/rspb.2019.1630  

   Majewska, Ania A. ; Sims, Stuart ; Schneider, Anna ; Altizer, Sonia ; Hall, Richard J. ( September 2019 , Proceedings of the Royal Society B: Biological Sciences)

   Understanding factors that allow highly virulent parasites to reach high infection prevalence in host populations is important for managing infection risks to human and wildlife health. Multiple transmission routes have been proposed as one mechanism by which virulent pathogens can achieve high prevalence, underscoring the need to investigate this hypothesis through an integrated modelling-empirical framework. Here, we examine a harmful specialist protozoan infecting monarch butterflies that commonly reaches high prevalence (50–100%) in resident populations. We integrate field and modelling work to show that a combination of three empirically-supported transmission routes (vertical, adult transfer and environmental transmission) can produce and sustain high infection prevalence in this system. Although horizontal transmission is necessary for parasite invasion, most new infections post-establishment arise from vertical transmission. Our study predicts that multiple transmission routes, coupled with high parasite virulence, can reduce resident host abundance by up to 50%, suggesting that the protozoan could contribute to declines of North American monarchs. 

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