Evolution of pathogens towards low R(0) in heterogeneous populations

Maximization of the basic reproduction ratio or R(0) 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 R(0) 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 R(0), 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 R(0), and one that does not, and results in lower R(0). While the low R(0) strategy is never evolutionarily stable, invading strains with higher R(0) will also converge to the low R(0) 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.