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1. Pathogen evolution following spillover from a resident to a migrant host population depends on interactions between host pace of life and tolerance to infection

   https://doi.org/10.1111/1365-2656.14075  

   Torstenson, Martha; Shaw, Allison K. (April 2024, Journal of Animal Ecology)

   Abstract Changes to migration routes and phenology create novel contact patterns among hosts and pathogens. These novel contact patterns can lead to pathogens spilling over between resident and migrant populations. Predicting the consequences of such pathogen spillover events requires understanding how pathogen evolution depends on host movement behaviour. Following spillover, pathogens may evolve changes in their transmission rate and virulence phenotypes because different strategies are favoured by resident and migrant host populations. There is conflict in current theoretical predictions about what those differences might be. Some theory predicts lower pathogen virulence and transmission rates in migrant populations because migrants have lower tolerance to infection. Other theoretical work predicts higher pathogen virulence and transmission rates in migrants because migrants have more contacts with susceptible hosts.We aim to understand how differences in tolerance to infection and host pace of life act together to determine the direction of pathogen evolution following pathogen spillover from a resident to a migrant population.We constructed a spatially implicit model in which we investigate how pathogen strategy changes following the addition of a migrant population. We investigate how differences in tolerance to infection and pace of life between residents and migrants determine the effect of spillover on pathogen evolution and host population size.When the paces of life of the migrant and resident hosts are equal, larger costs of infection in the migrants lead to lower pathogen transmission rate and virulence following spillover. When the tolerance to infection in migrant and resident populations is equal, faster migrant paces of life lead to increased transmission rate and virulence following spillover. However, the opposite can also occur: when the migrant population has lower tolerance to infection, faster migrant paces of life can lead to decreases in transmission rate and virulence.Predicting the outcomes of pathogen spillover requires accounting for both differences in tolerance to infection and pace of life between populations. It is also important to consider how movement patterns of populations affect host contact opportunities for pathogens. These results have implications for wildlife conservation, agriculture and human health. 

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2. What Does Tolerance Mean for Animal Disease Dynamics When Pathology Enhances Transmission?

   https://doi.org/10.1093/icb/icz065  

   Henschen, Amberleigh E.; Adelman, James S. (May 2019, Integrative and Comparative Biology)

   Abstract Host competence, or how well an individual transmits pathogens, varies substantially within and among animal populations. As this variation can alter the course of epidemics and epizootics, revealing its underlying causes will help predict and control the spread of disease. One host trait that could drive heterogeneity in competence is host tolerance, which minimizes fitness losses during infection without decreasing pathogen load. In many cases, tolerance should increase competence by extending infectious periods and enabling behaviors that facilitate contact among hosts. However, we argue that the links between tolerance and competence are more varied. Specifically, the different physiological and behavioral mechanisms by which hosts achieve tolerance should have a range of effects on competence, enhancing the ability to transmit pathogens in some circumstances and impeding it in others. Because tissue-based pathology (damage) that reduces host fitness is often critical for pathogen transmission, we focus on two mechanisms that can underlie tolerance at the tissue level: damage-avoidance and damage-repair. As damage-avoidance reduces transmission-enhancing pathology, this mechanism is likely to decrease host competence and pathogen transmission. In contrast, damage-repair does not prevent transmission-relevant pathology from occurring. Rather, damage-repair provides new, healthy tissues that pathogens can exploit, likely extending the infectious period and increasing host competence. We explore these concepts through graphical models and present three disease systems in which damage-avoidance and damage-repair alter host competence in the predicted directions. Finally, we suggest that by incorporating these links, future theoretical studies could provide new insights into infectious disease dynamics and host–pathogen coevolution. 

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3. Rapid adaptation to a novel pathogen through disease tolerance in a wild songbird

   https://doi.org/10.1371/journal.ppat.1011408  

   Henschen, Amberleigh E.; Vinkler, Michal; Langager, Marissa M.; Rowley, Allison A.; Dalloul, Rami A.; Hawley, Dana M.; Adelman, James S. (June 2023, PLOS Pathogens)

   McGraw, Elizabeth A. (Ed.)

   Animal hosts can adapt to emerging infectious disease through both disease resistance, which decreases pathogen numbers, and disease tolerance, which limits damage during infection without limiting pathogen replication. Both resistance and tolerance mechanisms can drive pathogen transmission dynamics. However, it is not well understood how quickly host tolerance evolves in response to novel pathogens or what physiological mechanisms underlie this defense. Using natural populations of house finches ( Haemorhous mexicanus ) across the temporal invasion gradient of a recently emerged bacterial pathogen ( Mycoplasma gallisepticum ), we find rapid evolution of tolerance (<25 years). In particular, populations with a longer history of MG endemism have less pathology but similar pathogen loads compared with populations with a shorter history of MG endemism. Further, gene expression data reveal that more-targeted immune responses early in infection are associated with tolerance. These results suggest an important role for tolerance in host adaptation to emerging infectious diseases, a phenomenon with broad implications for pathogen spread and evolution. 

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4. Within-host priority effects and epidemic timing determine outbreak severity in co-infected populations

   https://doi.org/10.1098/rspb.2020.0046  

   Clay, Patrick A.; Duffy, Meghan A.; Rudolf, Volker H. (March 2020, Proceedings of the Royal Society B: Biological Sciences)

   Co-infections of hosts by multiple pathogen species are ubiquitous, but predicting their impact on disease remains challenging. Interactions between co-infecting pathogens within hosts can alter pathogen transmission, with the impact on transmission typically dependent on the relative arrival order of pathogens within hosts (within-host priority effects). However, it is unclear how these within-host priority effects influence multi-pathogen epidemics, particularly when the arrival order of pathogens at the host-population scale varies. Here, we combined models and experiments with zooplankton and their naturally co-occurring fungal and bacterial pathogens to examine how within-host priority effects influence multi-pathogen epidemics. Epidemiological models parametrized with within-host priority effects measured at the single-host scale predicted that advancing the start date of bacterial epidemics relative to fungal epidemics would decrease the mean bacterial prevalence in a multi-pathogen setting, while models without within-host priority effects predicted the opposite effect. We tested these predictions with experimental multi-pathogen epidemics. Empirical dynamics matched predictions from the model including within-host priority effects, providing evidence that within-host priority effects influenced epidemic dynamics. Overall, within-host priority effects may be a key element of predicting multi-pathogen epidemic dynamics in the future, particularly as shifting disease phenology alters the order of infection within hosts. 

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5. The illusion of personal health decisions for infectious disease management: disease spread in social contact networks

   https://doi.org/10.1098/rsos.221122  

   Michalska-Smith, Matthew; Enns, Eva A.; White, Lauren A.; Gilbertson, Marie L.; Craft, Meggan E. (March 2023, Royal Society Open Science)

   Close contacts between individuals provide opportunities for the transmission of diseases, including COVID-19. While individuals take part in many different types of interactions, including those with classmates, co-workers and household members, it is the conglomeration of all of these interactions that produces the complex social contact network interconnecting individuals across the population. Thus, while an individual might decide their own risk tolerance in response to a threat of infection, the consequences of such decisions are rarely so confined, propagating far beyond any one person. We assess the effect of different population-level risk-tolerance regimes, population structure in the form of age and household-size distributions, and different interaction types on epidemic spread in plausible human contact networks to gain insight into how contact network structure affects pathogen spread through a population. In particular, we find that behavioural changes by vulnerable individuals in isolation are insufficient to reduce those individuals’ infection risk and that population structure can have varied and counteracting effects on epidemic outcomes. The relative impact of each interaction type was contingent on assumptions underlying contact network construction, stressing the importance of empirical validation. Taken together, these results promote a nuanced understanding of disease spread on contact networks, with implications for public health strategies. 

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