Evolution of pathogens towards low R0 in heterogeneous populations

Maximization of the basic reproduction ratio or R0 is widely believed to drive the emergence of novel pathogens. The presence of exploitable heterogeneities in a population, such as high variance in the number of potentially infectious contacts, increases R0 and thus pathogens that can exploit heterogeneities in the contact structure have an advantage over those that do not. However, exploitation of heterogeneities results in a more rapid depletion of the potentially susceptible neighbourhood for an infected host. Here a simple model of pathogen evolution in a heterogeneous environment is developed and placed in the context of HIV transmission. In this model, it is shown that pathogens may evolve towards lower R0, even if this results in pathogen extinction. For sufficiently high transmissibility, two locally stable strategies exist for an evolving pathogen, one that exploits heterogeneities and results in higher R0, and one that does not, and results in lower R0. While the low R0 strategy is never evolutionarily stable, invading strains with higher R0 will also converge to the low R0 strategy if not sufficiently different from the resident strain. Heterogenous transmission is increasingly recognized as fundamental to epidemiological dynamics and the evolution of pathogens; here, it is shown that the ability to exploit heterogeneity is a strategy that can itself evolve.