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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. 

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. 

Significance The clear need to mitigate zoonotic risk has fueled increased viral discovery in specific reservoir host taxa. We show that a combination of viral and reservoir traits can predict zoonotic virus virulence and transmissibility in humans, supporting the hypothesis that bats harbor exceptionally virulent zoonoses. However, pandemic prevention requires thinking beyond zoonotic capacity, virulence, and transmissibility to consider collective “burden” on human health. For this, viral discovery targeting specific reservoirs may be inefficient as death burden correlates with viral, not reservoir, traits, and depends on context-specific epidemiological dynamics across and beyond the human–animal interface. These findings suggest that longitudinal studies of viral dynamics in reservoir and spillover host populations may offer the most effective strategy for mitigating zoonotic risk. 

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.