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1. Multispecies interactions and the community context of the evolution of virulence

   https://doi.org/10.1098/rspb.2024.0991  

   Evensen, Claire; White, Andrew; Boots, Mike (September 2024, Proceedings of the Royal Society B: Biological Sciences)

   Pairwise host–parasite relationships are typically embedded in broader networks of ecological interactions, which have the potential to shape parasite evolutionary trajectories. Understanding this ‘community context’ of pathogen evolution is vital for wildlife, agricultural and human systems alike, as pathogens typically infect more than one host—and these hosts may have independent ecological relationships. Here, we introduce an eco-evolutionary model examining ecological feedback across a range of host–host interactions. Specifically, we analyse a model of the evolution of virulence of a parasite infecting two hosts exhibiting competitive, mutualistic or exploitative relationships. We first find that parasite specialism is necessary for inter-host interactions to impact parasite evolution. Furthermore, we find generally that increasing competition between hosts leads to higher shared parasite virulence while increasing mutualism leads to lower virulence. In exploitative host–host interactions, the particular form of parasite specialization is critical—for instance, specialization in terms of onward transmission, host tolerance or intra-host pathogen growth rate lead to distinct evolutionary outcomes under the same host–host interactions. Our work provides testable hypotheses for multi-host disease systems, predicts how changing interaction networks may impact virulence evolution and broadly demonstrates the importance of looking beyond pairwise relationships to understand evolution in realistic community contexts. 

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2. 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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3. 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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4. Shoaling guppies evade predation but have deadlier parasites

   https://doi.org/10.1038/s41559-022-01772-5  

   Walsman, Jason C.; Janecka, Mary J.; Clark, David R.; Kramp, Rachael D.; Rovenolt, Faith; Patrick, Regina; Mohammed, Ryan S.; Konczal, Mateusz; Cressler, Clayton E.; Stephenson, Jessica F. (July 2022, Nature Ecology & Evolution)

   Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite. Predators may shift this cost–benefit balance by consuming infected hosts or changing host behaviour, but the strength of these effects remains unclear. Here we use field and lab data on Trinidadian guppies and their Gyrodactylus spp. parasites to show how differential predation pressure influences parasite virulence and transmission. We use an experimentally demonstrated virulence–transmission trade-off to parametrize a mathematical model in which host shoaling (as a means of anti-predator defence), increases contact rates and selects for higher virulence. Then we validate model predictions by collecting parasites from wild, Trinidadian populations; parasites from high-predation populations were more virulent in common gardens than those from low-predation populations. Broadly, our results indicate that reduced social contact selects against parasite virulence. 

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5. The three Ts of virulence evolution during zoonotic emergence

   https://doi.org/10.1098/rspb.2021.0900  

   Visher, Elisa; Evensen, Claire; Guth, Sarah; Lai, Edith; Norfolk, Marina; Rozins, Carly; Sokolov, Nina A.; Sui, Melissa; Boots, Michael (August 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   There is increasing interest in the role that evolution may play in current and future pandemics, but there is often also considerable confusion about the actual evolutionary predictions. This may be, in part, due to a historical separation of evolutionary and medical fields, but there is a large, somewhat nuanced body of evidence-supported theory on the evolution of infectious disease. In this review, we synthesize this evolutionary theory in order to provide a framework for clearer understanding of the key principles. Specifically, we discuss the selection acting on zoonotic pathogens' transmission rates and virulence at spillover and during emergence. We explain how the direction and strength of selection during epidemics of emerging zoonotic disease can be understood by a three Ts framework: trade-offs, transmission, and time scales. Virulence and transmission rate may trade-off, but transmission rate is likely to be favoured by selection early in emergence, particularly if maladapted zoonotic pathogens have ‘no-cost’ transmission rate improving mutations available to them. Additionally, the optimal virulence and transmission rates can shift with the time scale of the epidemic. Predicting pathogen evolution, therefore, depends on understanding both the trade-offs of transmission-improving mutations and the time scales of selection. 

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