Metapopulation heterogeneities in host mobility, productivity, and immunocompetency always increase virulence and infectiousness

Sato, M., Dieckmann, U. ORCID: https://orcid.org/0000-0001-7089-0393, & Sasaki, A. (2024). Metapopulation heterogeneities in host mobility, productivity, and immunocompetency always increase virulence and infectiousness. Proceedings of the National Academy of Sciences 121 (52) e2309272121. 10.1073/pnas.2309272121.

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Abstract

The epidemiology and evolution of diseases unfold in populations that are rarely homogeneous. Instead, hosts infected by pathogens often form metapopulations, in which local populations connected by the movement of hosts experience different demographic and epidemiological conditions. Here, we develop a general theory of the evolution of pathogens in heterogeneous metapopulations. We reveal the following key insights into the evolution of pathogen virulence and infectiousness: (1) When the mobility (movement rate), productivity (birth rate and carrying capacity), or immunocompetency (immunity-loss rate) differ among local populations, this variance always increases pathogen virulence and infectiousness (2) The increment of pathogen virulence caused by such heterogeneity is approximately proportional to the variance of the corresponding heterogeneous local conditions (3) This increment can be expressed as the covariance between the local selection pressures and the local reproductive values experienced by the pathogen (4) The reason why heterogeneity always increases pathogen virulence is explained by the positive correlation of local selection pressures with reproductive values (5) Combinations of multiple independent heterogeneities further increase virulence and infectiousness, even more so when their covariances are positive. Our key findings robustly hold for different epidemiological frameworks - including SI, SIS, SIR, and SIRS models, with both density- and frequency-dependent transmission as well as with superinfection. They provide insights into the risks of growing pathogen infectiousness in a world in which heterogeneity - caused, e.g., by the concentration of human populations in urban areas - is rising.

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