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1. Sexual recombination and temporal gene flow maintain host resistance and genetic diversity

   https://doi.org/10.1007/s10682-022-10193-6  

   McLean, Katherine D.; Gowler, Camden D.; Dziuba, Marcin K.; Zamani, Haniyeh; Hall, Spencer R.; Duffy, Meghan A. (January 2022, Evolutionary Ecology)

   Infectious disease can threaten host populations. Hosts can rapidly evolve resistance during epidemics, with this evolution often modulated by fitness trade-offs (e.g., between resistance and fecundity). However, many organisms switch between asexual and sexual reproduction, and this shift in reproductive strategy can also alter how resistance in host populations persists through time. Recombination can shuffle alleles selected for during an asexual phase, uncoupling the combinations of alleles that facilitated resistance to parasites and altering the distribution of resistance phenotypes in populations. Furthermore, in host species that produce diapausing propagules (e.g., seeds, spores, or resting eggs) after sex, accumulation of propagules into and gene flow out of a germ bank introduce allele combinations from past populations. Thus, recombination and gene flow might shift populations away from the trait distribution reached after selection by parasites. To understand how recombination and gene flow alter host population resistance, we tracked the genotypic diversity and resistance distributions of two wild populations of cyclical parthenogens. In one population, resistance and genetic diversity increased after recombination whereas, in the other, recombination did not shift already high resistance and genetic diversity. In both lakes, resistance remained high after temporal gene flow. This observation surprised us: due to costs to resistance imposed by a fecundity-resistance trade-off, we expected that high population resistance would be a transient state that would be eroded through time by recombination and gene flow. Instead, low resistance was the transient state, while recombination and gene flow re-established or maintained high resistance to this virulent parasite. We propose this outcome may have been driven by the joint influence of fitness trade-offs, genetic slippage after recombination, and temporal gene flow via the egg bank. 

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2. 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)

   null (Ed.)

   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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3. Virulence evolution during a naturally occurring parasite outbreak

   https://doi.org/10.1007/s10682-022-10169-6  

   Gowler, Camden D.; Essington, Haley; O’Brien, Bruce; Shaw, Clara L.; Bilich, Rebecca W.; Clay, Patrick A.; Duffy, Meghan A. (January 2022, Evolutionary Ecology)

   Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in the Daphnia - Pasteuria model system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak of Pasteuria ramosa in Daphnia dentifera , where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild. 

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4. 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)

   null (Ed.)

   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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5. The coevolution of parasite virulence and host investment in constitutive and induced defence

   https://doi.org/10.1093/jeb/voaf014  

   Best, Alex; Guth, Sarah; Boots, Mike (April 2025, Journal of Evolutionary Biology)

   Li_Richter, Xiang-Yi; Mullon, Charles (Ed.)

   Abstract Given their ubiquity in nature and their importance to human and agricultural health, it is important to gain a better understanding of the drivers of the evolution of infectious disease. Across vertebrates, invertebrates, and plants, defence mechanisms can be expressed either constitutively (always present and costly) or induced (activated and potentially costly only upon infection). Theory has shown that this distinction has important implications to the evolution of defence due to differences in their impact on both individual fitness and the feedback of the population-level epidemiological outcomes such as prevalence. However, despite the fact that pathogens evolve in response to host immunity and that this can have important implications to the evolution of host defence, the implications of coevolution on constitutive and induced immunity have not been examined. Here we show theoretically how and when incorporating host-parasite coevolution between host defences and parasite growth strategies plays an important role in determining the optimum outcome. A key result is that whether the parasite affects host reproduction critically impacts host-parasite coevolution; when the parasite impacts fecundity, selection on the host is largely geared towards minimizing reproductive costs, through reducing investment in reproductively costly constitutive defence when the parasite prevalence is low, but also by investing in immunity to avoid infection or recover when prevalence is high. Our work emphasizes the importance of coevolution and epidemiological feedbacks to the coevolution of hosts and parasites and provides testable predictions of the determinants of constitutive verses induced defence. 

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