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1. Evolution of intermediate latency strategies in seasonal parasites

   https://doi.org/10.1093/jeb/voae009  

   MacDonald, Hannelore ; Brisson, Dustin ( February 2024 , Journal of Evolutionary Biology)

   Traditional mechanistic trade-offs between transmission and parasite latency period length are foundational for nearly all theories on the evolution of parasite life-history strategies. Prior theoretical studies demonstrate that seasonal host activity can generate a trade-off for obligate-host killer parasites that selects for intermediate latency periods in the absence of a mechanistic trade-off between transmission and latency period lengths. Extensions of these studies predict that host seasonal patterns can lead to evolutionary bistability for obligate-host killer parasites in which two evolutionarily stable strategies, a shorter and longer latency period, are possible. Here we demonstrate that these conclusions from previously published studies hold for non-obligate host killer parasites. That is, seasonal host activity can select for intermediate parasite latency periods for non-obligate killer parasites in the absence of a trade-off between transmission and latency period length and can maintain multiple evolutionarily stable parasite life-history strategies. These results reinforce the hypothesis that host seasonal activity can act as a major selective force on parasite life-history evolution by extending the narrower prior theory to encompass a greater range of disease systems.

    

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2. 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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3. Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes

   https://doi.org/10.1017/S0031182020002048  

   Hawley, Dana M. ; Gibson, Amanda K. ; Townsend, Andrea K. ; Craft, Meggan E. ; Stephenson, Jessica F. ( March 2021 , Parasitology)

   null (Ed.)

   Abstract An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution. 

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4. The evolution of stage-specific virulence: Differential selection of parasites in juveniles

   https://doi.org/10.1002/evl3.105  

   Iritani, Ryosuke ; Visher, Elisa ; Boots, Mike ( April 2019 , Evolution Letters)

   The impact of infectious disease is often very different in juveniles and adults, but theory has focused on the drivers of stage-dependent defense in hosts rather than the potential for stage-dependent virulence evolution in parasites. Stage structure has the potential to be important to the evolution of pathogens because it exposes parasites to heterogeneous environments in terms of both host characteristics and transmission pathways. We develop a stage-structured (juvenile–adult) epidemiological model and examine the evolutionary outcomes of stage-specific virulence under the classic assumption of a transmission-virulence trade-off. We show that selection on virulence against adults remains consistent with the classic theory. However, the evolution of juvenile virulence is sensitive to both demography and transmission pathway with higher virulence against juveniles being favored either when the transmission pathway is assortative (juveniles preferentially interact together) and the juvenile stage is long, or in contrast when the transmission pathway is disassortative and the juvenile stage is short. These results highlight the potentially profound effects of host stage structure on determining parasite virulence in nature. This new perspective may have broad implications for both understanding and managing disease severity.

    

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5. Predation shifts coevolution toward higher host contact rate and parasite virulence

   https://doi.org/10.1098/rspb.2021.2800  

   Walsman, Jason C. ; Cressler, Clayton E. ( July 2022 , Proceedings of the Royal Society B: Biological Sciences)

   Hosts can avoid parasites (and pathogens) by reducing social contact, but such isolation may carry costs, e.g. increased vulnerability to predators. Thus, many predator–host–parasite systems confront hosts with a trade-off between predation and parasitism. Parasites, meanwhile, evolve higher virulence in response to increased host sociality and consequently, increased multiple infections. How does predation shift coevolution of host behaviour and parasite virulence? What if predators are selective, i.e. predators disproportionately capture the sickest hosts? We answer these questions with an eco-coevolutionary model parametrized for a Trinidadian guppy–Gyrodactylusspp. system. Here, increased predation drives host coevolution of higher grouping, which selects for higher virulence. Additionally, higher predator selectivity drives the contact rate higher and virulence lower. Finally, we show how predation and selectivity can have very different impacts on host density and prevalence depending on whether hosts or parasites evolve, or both. For example, higher predator selectivity led to lower prevalence with no evolution or only parasite evolution but higher prevalence with host evolution or coevolution. These findings inform our understanding of diverse systems in which host behavioural responses to predation may lead to increased prevalence and virulence of parasites.

    

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