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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. 

Bee declines have been partly attributed to the impacts of invasive or emerging parasite outbreaks. For western honeybees,Apis mellifera, major losses are associated with the virus-vectoring mite,Varroa destructor. In response, beekeepers have focused breeding efforts aimed at conferring resistance to this key parasite. One method of many is survival-based beekeeping where colonies that survive despite significantVarroainfestations produce subsequent colonies. We argue that this ‘hands-off’ approach will not always lead toVarroaresistance evolving but rather tolerance. Tolerance minimizes host fitness costs of parasitism without reducing parasite abundance, whereas resistance either prevents parasitism outright or keeps parasitism intensity low. With clear epidemiological distinctions, and as honeybee disease dynamics impact other wild bees owing to shared pathogens, we discuss why tolerance outcomes in honeybee breeding have important implications for wider pollinator health. Crucially, we argue that unintentional selection for tolerance will not only lead to more spillover from honeybees but may also select for pathogens that are more virulent in wild bees leading to ‘tragedies of tolerance’. These tragedies can be avoided through successful breeding regimes that specifically select for lowVarroa. We emphasize how insights from evolutionary ecology can be applied in ecologically responsible honeybee management. 

Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

COVID-19 infections have underlined that there can be substantial impacts on health after recovery, including elevated mortality. While such post-infection mortality (PIM) is clearly widespread, we do not yet have any understanding of its evolutionary dynamics. To address this gap, we use an eco-evolutionary model to determine conditions where PIM is evolutionarily favoured. Importantly, from a pathogen perspective, there are two potential ‘resources’: never-infected susceptibles and previously infected susceptibles (provided some reinfection is possible), and PIM only occurs in the latter. A key insight is that unlike classic virulence (i.e. during-infection mortality, DIM) PIM is neutral and not selected against in the absence of other trade-offs. However, PIM modulates characteristics of endemicity, and may also vary with other pathogen-specific components. If PIM is only correlated with transmission, recovery or DIM, it simply acts to modulate their impacts on the evolutionary outcome. On the other hand, if PIM trades off with the relative susceptibility to reinfection, there are important evolutionary implications that contrast with DIM. We find settings where a susceptibility–mortality trade-off (i.e. an increase in mortality leads to higher relative susceptibility to reinfection) can select against DIM but favour PIM. This provides a potential explanation for the ubiquity of PIM. Overall, our work illustrates that PIM can readily evolve in certain settings and highlights the importance of considering different sources of mortality. 

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. 

Abstract There is a clear need to understand the effect of human intervention on the evolution of infectious disease. In particular, culling and harvesting of both wildlife and managed livestock populations are carried out in a wide range of management practices, and they have the potential to impact the evolution of a broad range of disease characteristics. Applying eco‐evolutionary theory we show that once culling/harvesting becomes targeted on specific disease classes, the established result that culling selects for higher virulence is only found when sufficient infected individuals are culled. If susceptible or recovered individuals are targeted, selection for lower virulence can occur. An important implication of this result is that when culling to eradicate an infectious disease from a population, while it is optimal to target infected individuals, the consequent evolution can increase the basic reproductive ratio of the infection, , and make parasite eradication more difficult. We show that increases in evolved virulence due to the culling of infected individuals can lead to excess population decline when sustainably harvesting a population. In contrast, culling susceptible or recovered individuals can select for decreased virulence and a reduction in population decline through culling. The implications to the evolution of virulence are typically the same in wildlife populations, that are regulated by the parasite, and livestock populations, that have a constant population size where restocking balances the losses due to mortality. However, the well‐known result that vertical transmission selects for lower virulence and transmission in wildlife populations is less marked in livestock populations for parasites that convey long‐term immunity since restocking can enhance the density of the immune class. Our work emphasizes the importance of understanding the evolutionary consequences of intervention strategies and the different ecological feedbacks that can occur in wildlife and livestock populations. 

The SARS-CoV-2 pandemic has generated a considerable number of infections and associated morbidity and mortality across the world. Recovery from these infections, combined with the onset of large-scale vaccination, have led to rapidly-changing population-level immunological landscapes. In turn, these complexities have highlighted a number of important unknowns related to the breadth and strength of immunity following recovery or vaccination. Using simple mathematical models, we investigate the medium-term impacts of waning immunity against severe disease on immuno-epidemiological dynamics. We find that uncertainties in the duration of severity-blocking immunity (imparted by either infection or vaccination) can lead to a large range of medium-term population-level outcomes (i.e. infection characteristics and immune landscapes). Furthermore, we show that epidemiological dynamics are sensitive to the strength and duration of underlying host immune responses; this implies that determining infection levels from hospitalizations requires accurate estimates of these immune parameters. More durable vaccines both reduce these uncertainties and alleviate the burden of SARS-CoV-2 in pessimistic outcomes. However, heterogeneity in vaccine uptake drastically changes immune landscapes toward larger fractions of individuals with waned severity-blocking immunity. In particular, if hesitancy is substantial, more robust vaccines have almost no effects on population-level immuno-epidemiology, even if vaccination rates are compensatorily high among vaccine-adopters. This pessimistic scenario for vaccination heterogeneity arises because those few individuals that are vaccine-adopters are so readily re-vaccinated that the duration of vaccinal immunity has no appreciable consequences on their immune status. Furthermore, we find that this effect is heightened if vaccine-hesitants have increased transmissibility (e.g. due to riskier behavior). Overall, our results illustrate the necessity to characterize both transmission-blocking and severity-blocking immune time scales. Our findings also underline the importance of developing robust next-generation vaccines with equitable mass vaccine deployment. 

The management of future pandemic risk requires a better understanding of the mechanisms that determine the virulence of emerging zoonotic viruses. Meta-analyses suggest that the virulence of emerging zoonoses is correlated with but not completely predictable from reservoir host phylogeny, indicating that specific characteristics of reservoir host immunology and life history may drive the evolution of viral traits responsible for cross-species virulence. In particular, bats host viruses that cause higher case fatality rates upon spillover to humans than those derived from any other mammal, a phenomenon that cannot be explained by phylogenetic distance alone. In order to disentangle the fundamental drivers of these patterns, we develop a nested modeling framework that highlights mechanisms that underpin the evolution of viral traits in reservoir hosts that cause virulence following cross-species emergence. We apply this framework to generate virulence predictions for viral zoonoses derived from diverse mammalian reservoirs, recapturing trends in virus-induced human mortality rates reported in the literature. Notably, our work offers a mechanistic hypothesis to explain the extreme virulence of bat-borne zoonoses and, more generally, demonstrates how key differences in reservoir host longevity, viral tolerance, and constitutive immunity impact the evolution of viral traits that cause virulence following spillover to humans. Our theoretical framework offers a series of testable questions and predictions designed to stimulate future work comparing cross-species virulence evolution in zoonotic viruses derived from diverse mammalian hosts. 

Infectious diseases may cause some long-term damage to their host, leading to elevated mortality even after recovery. Mortality due to complications from so-called ‘long COVID’ is a stark illustration of this potential, but the impacts of such post-infection mortality (PIM) on epidemic dynamics are not known. Using an epidemiological model that incorporates PIM, we examine the importance of this effect. We find that in contrast to mortality during infection, PIM can induce epidemic cycling. The effect is due to interference between elevated mortality and reinfection through the previously infected susceptible pool. In particular, robust immunity (via decreased susceptibility to reinfection) reduces the likelihood of cycling; on the other hand, disease-induced mortality can interact with weak PIM to generate periodicity. In the absence of PIM, we prove that the unique endemic equilibrium is stable and therefore our key result is that PIM is an overlooked phenomenon that is likely to be destabilizing. Overall, given potentially widespread effects, our findings highlight the importance of characterizing heterogeneity in susceptibility (via both PIM and robustness of host immunity) for accurate epidemiological predictions. In particular, for diseases without robust immunity, such as SARS-CoV-2, PIM may underlie complex epidemiological dynamics especially in the context of seasonal forcing.